20.1 Introduction

The ability of an animal to acquire information about the internal state of its body, the movement of its body, and the interaction of its body with the external environment is critical for survival. The acquisition and processing of sensory information help animals make decisions and responses that are appropriate for a given situation. These decisions and responses to stimuli are often highly influenced by the particular sensory information acquired by an animal. For example, sensing an internal state of hunger and the subsequent use of various sensory systems like vision and olfaction are often required to locate a food source. Sensory information on the internal state of the body and monitoring variables like blood pressure and volume, blood chemistry, and temperature allow our body to respond appropriately in order to maintain homeostasis. Thus, nearly every bodily function and behavior is triggered or modulated by the acquisition of information.

In order to acquire information from both internal and external sources, the vertebrate body relies on sensory receptors. A sensory receptor is responsible for the conversion of a given stimulus (often a specific type) into a neural signal that can be transmitted along a neuron to the central nervous system. The conversion of the sensory stimulus into a neural signal is called transduction. The specific transduction mechanism is highly dependent on the type of sensory receptor and the type of stimulus being transduced. Regardless of sensor type, transduction results in the depolarization (a change in the membrane potential to a more positive value) of the sensory receptor; if the stimulus is of a great enough intensity, the depolarization will reach a threshold that triggers the firing of an action potential. However, vertebrates are not aware of each piece of information being sensed at every moment. For example, we can assume that no person reading this book has ever been keenly aware of their specific blood pH level at any given moment. Differently, the feeling of pain is often a stimulus that is hard to ignore. Thus, it is important to distinguish the difference between sensation and perception. Sensation is the acquisition of information, while perception is the conscious awareness of that sensation.

Sensory receptors can be classified according to the origin of the stimulus (inside or outside the vertebrate body), the modality of the stimulus they transduce (e.g., pain, temperature, mechanosensation, among others), or the concentration of sensory receptors used to detect a certain stimulus. Receptors that sense stimuli outside the body can be referred to as exteroceptors. Two examples of exteroceptors include the receptors responsible for vision and touch, as both types of stimuli (light and the interaction of the body with a physical stimulus) originate from outside the body. Receptors that sense stimuli inside the body can be referred to as interoceptors. An example of interoceptors includes the receptors responsible for sensing stimuli associated with internal organs (e.g., blood pressure, blood chemistry, and bladder fullness).

Stimulus modality, or the type of stimulus capable of generating a response in a given receptor, is another method for classifying sensory receptors. In other words, many types of receptors only respond to a specific type(s) of stimuli. Thermoreceptors respond to changes in temperature. Mechanoreceptors respond to the deformation of the cell or a tissue due to the application of physical force, which can include touch and pressure of the skin from an external stimulus or an internal stimulus like bladder or blood pressure. Chemoreceptors respond to chemicals and include receptors responsible for taste and smell as well as those responsible for sensing internal body chemistry like blood sugar level. Nociceptors are responsible for sensing pain and tissue damage. Finally, radiation receptors respond to electromagnetic radiation, which includes visible light and radiation of other wavelengths. Over evolutionary time, these receptors have diversified and undergone specializations to facilitate additional but related sensory capabilities that will be discussed throughout the chapter. It is important to note that these classifications are not mutually exclusive, and the categorization of receptors by stimulus origin and modality can be combined to describe a receptor. For example, the receptor used to sense the pressure required for you to effectively hold a glass cup can be referred to as both a mechanosensor and an exteroceptor, while the receptor used to sense the pressure and volume of urine within the mammalian urinary bladder can be referred to as both a mechanosensor and an interoceptor.

It is also possible to classify sensory receptors based on the density of their distribution in the vertebrate body. This classification generally falls into two groups: general and specialized sensation. General sensation refers to senses that rely on the wide distribution of the sensory receptors across the body. General sensation can include both interoceptors and exteroceptors that could be distributed across the skin, muscles, tendons, joints, and organs. The senses involve receptors capable of mechanosensation, nociception, chemosensation, and thermosensation. In contrast, special sensation refers to sensory capabilities that typically rely on a more complex sensory organ. A sensory organ is composed of a high density of individual sensory receptors supported by other tissue types (as opposed to single receptors distributed across the body). A prime example of a special sensation and a sensory organ is the vertebrate eye. Indeed, many of these specialized and complex sensory organs used in special sensation are associated with the head, and interestingly, the enlargement of specialized sensory organs associated with the head is a trait that evolved incredibly early in the evolutionary history of vertebrates.

Sensory receptors are capable of coding different features of a stimulus that include stimulus location, intensity (and rate of change), and duration. The location of a given stimulus is determined by the receptive field of a sensory receptor, which is the specific area of the body or the relative location in the surrounding environment where a given receptor can detect a stimulus. Similarly, the neural pathway that transmits this signal to the central nervous system and the specific region of the central nervous system that receives the signal are highly organized, allowing the body location of the stimulus to maintain its identity.

Stimulus duration, or the duration in which a stimulus is being detected by a sensor, can be encoded both by a single receptor and groups of receptors. A single sensory receptor can encode information on the duration of a stimulus in two ways, which are dependent on the type of the receptor. Receptors can respond to stimuli in different ways. Rapidly adapting sensors typically fire a burst of action potentials at the onset and, often, offset of a stimulus. Thus, calculating the time difference between these two bursts of action potentials reveals information on stimulus duration. Differently, slowly adapting sensors typically respond to a stimulus throughout the duration a stimulus is being detected, and the rate of action potential firing frequency often decreases over the duration of the stimulus. The use of both slowly and rapidly adapting fibers, which are often found working together, therefore provides two overlapping mechanisms for encoding features of stimulus duration.

Stimulus intensity, which is the magnitude of the stimulus being applied, as well as changes in stimulus intensity, can also be encoded through changes in receptor firing rate. For example, as stimulus intensity increases, the firing frequency of slowly adapting sensors can also increase over the entire stimulus duration. Similarly, as stimulus intensity increases, rapidly adapting sensors can increase both the burst duration and the frequency of action potentials over the duration of the burst, providing two additional means of encoding stimulus intensity. Relative changes in burst duration and firing frequency of rapidly adapting sensors are also known to encode information on the rate at which a stimulus intensity changes while it is being applied. In other words, rapidly adapting sensors encode how fast or slow a stimulus intensity is changing over time (e.g., flipping a light switch versus using a dimmer to slowly increase the brightness in a room).

Ultimately, it is the integration of the information sensed by various sensory receptors that allows vertebrates to perceive the complex stimuli around the body. This is referred to as multimodal sensory integration and is a powerful mechanism that helps vertebrates generate the correct behavioral output in response to a variety of stimuli being experienced at the same time. Here, we will go through these different sensory modalities and types of sensory receptors.

20.2 Sense: Radiation Reception

All vertebrates are continuously exposed to electromagnetic radiation (ER). ER is a form of energy that travels in the form of waves, lying on a continuum often characterized by its wavelength or frequency (Figure 20.1). You are probably familiar with ER, as humans have been able to harness different wavelengths of ER for various purposes, like sending information in the form of radio waves, quickly heating your favorite brand of ramen noodles using microwaves, visualizing the inside of the vertebrate body using X-rays, and lighting your room at night with visible light to help you read your favorite anatomy textbook. ER is also a form of energy that naturally occurs in our universe and is constantly being emitted from solar objects like our sun. Given these various artificial and natural sources of ER and the ways they interact with natural objects in our world, it is not surprising that vertebrates (and other organisms) have evolved different ways to detect this energy to help acquire information about the world around them.

Across vertebrates, species have evolved different sensory structures to sense different but limited ranges of the ER spectrum. While the most notable and widely utilized ER sensor is the vertebrate eye, which is capable of transducing visible light into neural signals, other sensors have evolved in select species to sense UV light and infrared radiation. In this section we will consider these different radiation receptors that have evolved and the corresponding sensory capabilities they have unlocked.

Vision

Vision is the perception of objects in the environment by detecting the visible light an object emits or reflects. Light is naturally produced in a few specialized organs that have independently evolved in various organisms like fireflies and angler fish. However, most objects in our environment cannot emit light. Instead, we rely on the detection of light that is reflected by an object in the environment. This is why, for humans and some other vertebrates that have not evolved specific adaptations, it is so difficult to see at night, as there is not much light reflecting from the objects in our environment.

The vertebrate eye is a sensory organ that has evolved to facilitate the transduction of visible light into neural signals using a set of sensors called photoreceptors. Yet due to the physical properties of light, other structures have also evolved in the vertebrate eye to help facilitate the focus of this light on the photoreceptors. Therefore, the vertebrate eye performs two primary functions: to capture and focus light and subsequently transduce that light into a neural signal that can be sent to the brain.

The Anatomy of the Vertebrate Eye

The anatomy of the eye is surprisingly conserved across vertebrates. Thus, as is often customary when studying the eye, we will begin our investigation with a mammalian (or human) perspective, as it is a good representation of the general condition found across vertebrates with few adaptations. During this initial investigation of the mammalian eye, we highlight some key differences between the mammalian condition and the condition found in other major vertebrate clades, and we will follow our investigation of the mammalian eye by examining additional differences between the mammalian condition and the condition found in other major vertebrate lineages.

The eye of all gnathostomes is approximately spherical in shape and composed of three distinct layers. These layers (in order of superficial to deep) are the superficial fibrous layer (sometimes referred to as the tunica fibrosa or even incorrectly simply as the sclera) and the uvea (i.e., the tunica vasculosa), and the deepest layer is often referred to as the retina (but can also be titled the tunica interna, especially in a human anatomy course).

The Tunica Fibrosa

The superficial fibrous layer of the eye is divided into two functionally distinct regions, the sclera and the cornea. The cornea is the anterior transparent portion of the fibrous tunic through which all light entering the spherical eye must first pass. In all directions surrounding the cornea, the adjacent fibrous layer is referred to as the sclera. The transition between the cornea and the sclera is referred to as the limbus and is quite distinct in most mammals because the scleral tissues in mammals possess a distinct white color. Indeed, in a human anatomy textbook, the sclera is often referred to as the white of the eye. However, it is noteworthy that the white coloration of the mammalian sclera is a derived trait; the sclera is nearly transparent in some other extant vertebrate lineages, which is likely reminiscent of the ancestral condition.

The sclera is a tough fibrous layer composed mostly of a dense connective tissue with collagen fibers running in multiple directions. The sclera provides structure and protection, and because of the irregular arrangement of the collagen fibers, it is appropriate for resisting the internal pressures of the eye that are experienced in all directions. Indeed, the sclera is a wonderful demonstration of the structure-function relationship at the tissue level. The sclera not only resists internal forces and provides the eye with structure; it also serves as the attachment point for the extraocular eye muscles, which are responsible for moving the eyeball. The sclera is nearly devoid of cells and the metabolic needs of the sclera are so low that no direct blood supply is required. The vasculature that is found in the sclera is therefore not supplying the scleral tissue but rather passing through the superficial layer of the eye en route to the deeper uvea layer. Finally, in some vertebrates, the sclera is further reinforced by the presence of bony sheets known as scleral ossicles. The next time you are at a natural history museum, examine the orbits of skeletons on display (e.g., dinosaurs) and see if these scleral bones were included in the display.

The cornea itself is composed of three layers. The middle layer of the cornea, the substantia propria, is the thickest corneal layer and composed of multiple layers of regularly arranged collagen fibers. The substantia propria is sandwiched between epithelial tissue on both the superficial and deep surfaces. The deep epithelial layer is composed of simple squamous epithelium, while the superficial epithelium is composed of nonkeratinized stratified squamous epithelium that is actually continuous with the epithelia of the conjunctiva that lines the inner surface of the eyelids. The cornea is completely avascular, which is a critical feature of the eye, as any blood vessels traversing the corneal surface would obstruct your field of view. Although the cornea is avascular, it is densely innervated by sensory endings for pain and touch; it is these sensory endings that provide the sensory feedback that initiates the blink reflex (and make it so difficult to withstand the puff of air that is a common component of a routine eye exam).

The Uvea (Tunica Vasculosa)

The uvea is the layer of the vertebrate eye just deep to the fibrous tunic. The uvea is closely associated with the sclera throughout the inside of the posterior five-sixths of the eye sphere but remains separated from the cornea anteriorly. The uvea is composed of three different regions: the choroid, the ciliary body, and the iris.

The choroid is the largest region of the uvea found sandwiched between the deep-laying retina and superficial sclera. The uvea is both highly vascularized and pigmented. The vascularity found in the choroid provides a source of nutrition for the surrounding ocular tissues, especially the highly metabolic retinal cells. In diurnal species, the pigmentation of the choroid can help prevent internal reflections of light and reduce the unintended entrance of light through the eye wall. However, in some nocturnal vertebrates, the choroid actually includes the tapetum lucidum, which is a reflective tissue that functions to reflect the minimal light entering the eye at night to further stimulate the photoreceptors of the retina. It is the tapetum lucidum that is responsible for the “eye shine” you can observe when a light is shined on the eyes of some nocturnal vertebrates—a pet cat is a great example.

The choroid continues toward the corneal surface of the eye and transitions to become the ciliary body, which is predominantly composed of smooth muscle called the ciliary muscle. The ciliary muscle forms a ring of smooth muscle surrounding the lens of the eye. The contraction of the ciliary muscle, in mammals, can modulate the shape of the lens to help focus on objects at different distances (see below), and it is attached to the lens by the suspensory ligament. The ciliary body is also associated with the secretion of one of the intraocular fluids filling the internal cavity of the eye (see the subhead The Chambers and Intraocular Fluids of the Mammalian Eye).

The ciliary body also supports the iris, which is a thin layer of smooth muscle and pigmented epithelium. The iris is situated in the space between the cornea and the lens. The smooth muscle acts as an adjustable diaphragm that can expand and contract to regulate the amount of light entering the eye. The central opening of the iris is what is referred to as the pupil. However, the pupil is not a true structure of the eye, as it is formed from the opening of the iris. The smooth muscle of the iris is sandwiched between two pigmented layers. The corneal-facing (anterior in mammals) layer contains melanocytes, which produce the pigments that give the iris different colors. The general function of these pigmented layers is to reduce stray light from entering the eye anywhere adjacent to the pupil. The double layer is critical in reducing the entrance of stray light, as the translucent cornea is often larger in diameter than the pupil aperture of the iris.

The Retina (Tunica Interna)

The third, and deepest, layer of the eye consists of the cup-shaped retina and the genesis of the optic nerve (CN II). The retina is the photosensitive layer of the eye and is responsible for transduction of light into neural signals. The retina is composed of three cell layers. The most superficial retinal cell layer at the back of the eye (and just deep to the choroid) is composed of photoreceptors. Vertebrate photoreceptors belong to two classes: rods and cones. Rods are generally responsible for night vision and do not sense color, therefore producing a gray-scale image. Cones are generally responsible for bright light and color vision. In humans, there are three types of cones, providing trichromatic vision. Cones and the evolution of color vision will be discussed more later.

The rods and cones synapse with bipolar cells, which are the cells of the second retinal cell layer. Also found associated with this cell layer are horizontal cells, which make horizontal connections through synapses with adjacent photoreceptors.

Bipolar cells in turn synapse with ganglion cells. Ganglion cells are at the front of the retina and compose the deepest retinal cell layer. The axons of the ganglion cells ultimately converge to form the optic nerve (CN II). Some ganglion cells are themselves photoreceptive but do not contribute to image formation; instead, the photoreceptive capacity of ganglion cells functions to sense light intensity that can influence the pupillary reflex as well as broad patterns of day-night cycles that can influence the circadian rhythm of the body. Also included in this layer are amacrine cells, which synapse to create horizontal connections between adjacent ganglion cells.

There are fewer bipolar cells than there are rods and cones, and there are fewer ganglion cells than there are bipolar cells. Thus, a single ganglion cell often synapses with multiple bipolar cells, and a single bipolar cell often synapses with more than one photoreceptor; this results in neural signal integration along this pathway from the point of transduction in the photoreceptor to the optic nerve (CN II).

It is important to note that the arrangement of the retinal cell layers means that light must first pass through the deeper, corneal-facing layers of the retina (ganglion cells and bipolar cells) before reaching the photoreceptors at the back of the eye.

The Chambers and Intraocular Fluids of the Mammalian Eye

In gnathostomes, the three layers of the eye and the connections between their associated structures result in the presence of three chambers that are each filled with a type of intraocular fluid. Two chambers are present between the lens and the cornea of the eye. The more anterior of these chambers is appropriately named the anterior chamber and is the space between the cornea of the tunica fibrosa and the iris of the tunica vasculosa. Posteriorly, in the space between the iris and the lens, is the posterior chamber. Finally, the third chamber, known as the vitreous (or vitreal) chamber, is the space between the lens and cup-shaped tunica interna on the interior (deep) surface of the back of the eye.

All three chambers are filled with an intraocular fluid. The anterior and posterior chambers are both filled with a minimally viscous serous fluid secreted by epithelial cells of the tunica vasculosa layer. This watery serous fluid is often referred to as the aqueous humor. In comparison to the anterior and posterior chambers, the third chamber, the vitreous chamber, is filled with a relatively more viscous (jellylike) fluid called the vitreous humor.

Optical Components and Pathway of Light Through the Eye

As the retina, which contains the cells that transduce light into neural signals, is located on the deep surface of the posterior side of the eye, all light that hits the retina must pass through several structures. The eye structures that light penetrates en route to the retina are often referred to as the optical components of the eye and function to not only admit light but also bend (refract) and appropriately focus the light on the retina. The pathway of light through the eye occurs in the following order: the cornea, the aqueous humor of the anterior chamber, the pupil (however, this is simply a space of variable diameter determined by the contractile state of the muscles of the iris), the aqueous humor of the posterior chamber, the lens, and finally, the vitreous humor of the vitreous chamber.

It is relevant to mention this pathway, as the refraction (or bending) of light can occur to different degrees as it passes through each of these different structures or media. Ultimately, the formation of an (crisp and clear) image depends on the appropriate bending of light as it passes through the optical structures of the eye. The ability of a structure or a medium to bend light is quantified by its refractive index, and the bending or refraction of light occurs when it passes from one structure or media to another that has a different refractive index. The larger the difference in the refractive index between two sequential structures or media, the more the light will bend. You can observe this phenomenon yourself if you place a pencil in a glass that is half full of water—the piece of the pencil outside of the water appears offset from the piece of the pencil contained within the water. Thus, you can probably already start imagining that the refraction of light must pose different challenges to animals that are fully terrestrial, fully aquatic, or in extreme cases, living at the interface of water and land.

The optical component of the eye that plays the most significant role in focusing light on the retina is strongly dependent on the habitat of the animal. In most fully terrestrial vertebrates, the cornea is responsible for the majority (~66%) of the total refraction of light entering the eye. The refractive power of the cornea is so great in terrestrial vertebrates because of the relatively large difference between the corneal refractive index and that of the air that light passes through before reaching the corneal surface. In terrestrial vertebrates, the remaining refraction is primarily accomplished by the lens, which functions to focus the light precisely on the photoreceptors of the retina. Indeed, individuals who rely on corrective lenses (i.e., glasses or contact lenses) to see clearly are using these lenses to properly focus (or bend) light so that it directly hits the retina; in humans, the cause of improper focus is usually related to differences in eye size, where an elongated eyeball causes the light to focus anterior to the retina and a flattened eyeball causes the light to focus posterior to the retina.

In fully aquatic vertebrates, the lens plays the most significant role in focusing light on the retina. The refractive index of water is nearly identical to that of the cornea and the aqueous humor filling the chambers between the cornea and lens. Thus, in fully aquatic vertebrates, it is the lens that provides the primary refractive power and is responsible for nearly 100% of the focus of light on the retina.

Accommodation and the Diversity of Accommodation Mechanisms Across Vertebrates

In order to focus on objects located at different distances within an individual’s visual field, an animal usually needs to dynamically change the magnitude of light refraction in the eye. This process is known as accommodation. In gnathostomes, accommodation results from changes in the placement or shape of the lens, changes in the shape of the cornea, or some combination of these mechanisms. In gnathostomes, these accommodation mechanisms are generated by the contraction of muscles contained within the eye itself, while the lamprey (a jawless vertebrate) relies on extraocular eye muscles to accomplish accommodation. Interestingly, despite the generalized anatomy of the eye being well conserved across vertebrates, the mechanisms (and associated morphology) of accommodation are relatively diverse in comparison. Here, we will review this diversity in accommodation mechanism and morphology within each major vertebrate clade.

Before we continue it is important to note that not all vertebrates have a significant requirement for accommodation. The ability of the eye to focus on objects at different distances within the visual field is inversely proportional to the axial length of the eye. Therefore, vertebrates with very small eyes have little need for accommodation. In addition, vertebrates living in low light levels also have a low necessity for accommodation. Species living or behaving exclusively at low light levels usually have poor visual resolution, and that negates the need for any additional focus, as it would not significantly enhance the clarity of the image. Finally, animals that routinely transition between aquatic and terrestrial environments on a daily basis rely on accommodation to counteract the gain and loss of the refractive power of the cornea on land and underwater, respectively.

Lamprey

The lampreys are a lineage of vertebrates in which the mechanism of accommodation is not well studied. Thus, here, we will review what is currently known about lamprey accommodation mechanisms. Lamprey accommodation has been best studied in the genus Petromyzon. Interestingly, lampreys are the only currently known vertebrate lineage that relies on extraocular eye muscles to mediate accommodation. In at least two species of Petromyzon, an extraocular muscle, the cornealis muscle, attaches to the superficial aspect of the cornea. The contraction of the cornealis muscle mediates the formation of lateral tension in the eyeball, causing the corneal surface to get pulled into a flatter state, and thus the front of the cornea is now positioned more posteriorly. As the corneal surface is flattened to lay more posteriorly, the corneal disposition subsequently makes contact with and pushes the lens closer to the retina (a more posterior position). The posterior movement of the lens closer to the retina allows lampreys to focus on more distant objects. In contrast, the relaxation of the cornealis muscle ultimately results in the movement of the lens to a more anterior position that is farther from the retina. Thus, just as you move the lens closer and farther from a microscope slide when focusing your microscope in general biology, some species of lamprey can move and control the position of the lens relative to the retina in order to focus on more objects at different distances.

Interestingly, it is not clear whether or not all lamprey species have the ability to undergo visual accommodation. For example, P. marinus does not possess the extraocular cornealis muscle. However, it has also been suggested that the simultaneous co-contraction of all six extraocular eye muscles results in the squeezing or compression of the eyeball around the equator separating the anterior and posterior halves. In this situation, the long axis of the eye between the anterior cornea and the posterior retina will elongate; the elongation of the long axis of the eye, which is the pathway light takes, will naturally lead to a mechanism of accommodation by increasing the distances between the cornea, lens, and retina. In other words, the eye goes from a spherical shape to become more of an egg-like shape with the apexes of the eggs being aligned with the anterior-posterior path of light. It will be interesting to see further research explore this hypothesis and whether this mechanism is reminiscent of the ancestral state of vertebrate accommodation methods.

Chondrichthyans and Most Teleosts

The mechanism and morphology of accommodation are generally similar in most chondrichthyans and teleost fishes. In both groups, the lens of the eye is displaced to mediate accommodation. In chondrichthyans, the lens is generally displaced anteriorly toward the cornea to focus on objects that are closer in the field of view. In teleosts, the lens is generally displaced posteriorly toward the retina to focus on objects that are farther or most distant in the field of view. The lens is generally spherical in both chondrichthyans and most teleosts. In both groups, the lens is supported dorsally by a suspensory ligament that runs between the ciliary body and the lens. Ventrally, the lens is supported and actuated by a lentis muscle. In chondrichthyans, the muscle is called the protractor lentis muscle, as it moves the lens anteriorly, and in teleosts, the muscle is called the retractor lentis muscle, as it moves the lens posteriorly. However, in some teleost species, the stimulation of the retractor lentis muscle results in oblique or vertical movements of the lens. Furthermore, an additional muscle within the choroid layer is also present in some teleost species (e.g., deep-sea fishes) that could function to modulate corneal shape and also contribute to accommodation. It is likely that accommodation is far more variable and complicated across fishes than is currently understood. Finally, while chondrichthyans do have the ability to accommodate, studies suggest that this ability is relatively limited.

Amphibians

The two primary extant clades within amphibians, Anura (frogs) and Urodela (salamanders), rely on similar mechanisms of accommodation. Similar to the chondrichthyans, both of these groups rely on the anterior/forward displacement of the lens toward the retina in order to focus on closer objects within the field of view. In Urodela, accommodation is accomplished by the contraction of a single, ventrally located protractor lentis muscle, while the dorsal side of the lens is supported by a suspensory ligament. In Anura, anterior lens displacement is accomplished by the combined action of both a dorsal and a ventral protractor muscle; the ventral protractor muscle is prominent, however. In addition to the attachment to the lens, the lentis muscles of both Anura and Urodela also attach to the ciliary body.

Reptiles (Including Birds)

Across the group that includes turtles, birds, and other modern “reptiles,” the method of accommodation relies on a change of shape to the lens, cornea, or both. The mechanisms are too diverse to cover in full detail here, but published journal articles review these methods in grave detail. Here, we will provide a few interesting highlights.

In birds, the ciliary muscle is subdivided into anterior and posterior divisions. The anterior division of the ciliary muscle attaches to both the sclera (which is thickened in birds due to the presence of scleral ossicles) and the cornea. The contraction of the anterior division of the ciliary muscle flattens the cornea and can have a significant impact on the refractive power of the cornea. Additional accommodation in birds occurs through the posterior division of the ciliary muscle, which can contract to modulate the shape of the lens. The contraction of the posterior division indirectly modulates lens shape in birds, as the shape change is mediated through the ciliary body and circumferential muscle fibers of the iris. Ultimately, contraction of the posterior division of the ciliary muscle results in the anterior portion of the lens being squeezed and distended in the anterior direction.

Lizards and Snakes

The mechanisms and morphology of accommodation have not been recently studied in lizards or snakes and warrant reevaluation in both groups. However, in lizards, all historical accounts suggest a process that is very similar to birds in that accommodation is accomplished through the modulation of both corneal and lens shape using a similar morphological mechanism to birds. In snakes, there is some evidence that the corneal shape can be modulated for accommodation. However, most historical accounts in snakes suggest the forward displacement of the lens is the primary mechanism of accommodation in most snakes. The mechanism for lens displacement in snakes is poorly understood. The interspecific differences in snake eye accommodation might correlate with interspecific differences in ecology, and the evolutionary history of the different snake clades might be a significant driver in the differences across species.

Mammals

The mammalian accommodation mechanism and morphology are best studied in primates. In primates, the primary means of accommodation is through the modulation of lens shape. Lens shape is accomplished through the contraction of the ciliary muscle. The ciliary muscle of primates is attached to the lens through the suspensory ligament. The contraction of the ciliary muscle reduces tension in these ligaments, allowing the lens to form a more spherical shape, which occurs due to the inherent elasticity of the lens. The subsequent relaxation of the ciliary muscle results in the formation of tension in the suspensory ligaments and the flattening of the lens.

It is likely that variation in the magnitude of accommodation ability and mechanism exists across mammals. For example, many mammals are nocturnal, and accommodation rarely occurs in nocturnal animals, as it does not improve visual focus. Furthermore, many mammals possess small eyes where, again, accommodation is sometimes not needed due to the small eye size (see above). Indeed, rats and mice likely do not possess the ability to accommodate and do not seem to have the necessary morphology. Some mammals might also rely on the displacement of the lens for accommodation, as has been suggested in cats and sea otters.

The Photoreceptors of the Retina

The retina of most vertebrates contains two classes of photoreceptors: rods and cones. Rods are not able to discriminate between different colors but are very sensitive to light, enabling vision in dim and dark conditions. Cones are the photoreceptors responsible for color vision but are less sensitive than rods and function primarily in bright conditions. The retina of all vertebrate eyes (to our knowledge) contains rods, and most contain cones (with few exceptions, see below). Both rods and cones contain a class of pigment called opsins, which are responsible for absorbing light. Through downstream connections to a series of intracellular molecules, opsins are responsible for the transduction of light into a neural signal that ultimately travels along the optic nerve (CN II).

In cones, different subtypes of opsins exist and are directly related to differences in the color vision capacity across vertebrates. Recall that visible light ranges in wavelength, and across the spectrum of visible light, different wavelengths are directly related to different colors. The ability to sense and discriminate colors occurs because different opsin subtypes are maximally sensitive to different wavelengths of visible light (and thus different colors).

Color vision is likely to have evolved early in the history of vertebrates and since diversified significantly over evolutionary time. Across vertebrates, at least four different types of cones are known to exist and respond to different ranges of the visible light spectrum, but the specific opsins sensitive to specific wavelengths have been lost and reevolved over evolutionary time. Further, clear and colored oil droplets, which can function to increase sensitivity to a particular wavelength, have also been incorporated into and lost from cones over evolutionary time. Thus, since the evolutionary history of color vision is complicated, we will here report major transitions and general color vision capabilities in the major vertebrate groups.

It is possible that ancient vertebrates possessed four different types of cones and were able to finely discriminate color. In support of this hypothesis, extant vertebrates belonging to ancient clades that branched early in vertebrate evolutionary history (lamprey, some chondrichthyans that have not lost color vision, and many actinopterygians) all possess four different cone types. In order of increasing wavelength, these cone types are sensitive to violet, blue, green, and orange, respectively. Many extant turtles, birds, and other reptiles maintain the presence of four cones in their retinas. Most mammals, however, only possess two cone types and have lost the cones sensitive to blue and green light. If this is hard for you to believe, given your (the reader’s) ability to discriminate color, you are right to be skeptical. Humans and some other primates independently reevolved a cone type that contains an opsin allowing the perception of orange color. Thus, the capacity of color vision is quite different between humans and the majority of the pets we keep in our home (e.g., a fish or turtle, which can discriminate more colors than a human, or a cat or dog, which can distinguish fewer colors than a human).

Regardless of the number and ratio of different photoreceptors, light (and therefore images and color) is only sensed and transduced by retinal photoreceptors; it is not until those neural signals reach the brain that light is perceived. The evolution and diversification of the vertebrate brain itself are quite extensive, and thus it is difficult to succinctly review the different pathways and locations these neural signals are sent to from the retina after being carried by the optic nerve (CN II). However, in most vertebrates, multiple synapses occur in the relay of the neural signals carrying visual information en route to the various visual processing centers. In most amniotes, the first synapse in this relay usually occurs in the thalamus, which you might recall contains nuclei relaying much of the incoming sensory information from the periphery.

Anatomical Adaptations to Dark Environments

The evolution of nocturnality and the ability to see in dark, low-light environments has evolved independently multiple times across vertebrates. In each instance, many analogous solutions have evolved. One aspect of nocturnal vision that is generally true across all nocturnal animals is its association with poor visual acuity (image clarity). This is why nocturnal species often have a reduced capacity for visual accommodation. Here, we will review a few of the most common solutions that have evolved to enable low-light vision. Note that these different adaptations for nocturnal vision are far from mutually exclusive.

One of the simplest solutions to low light is the evolution of a maximum pupil size that is large relative to the size of the eye, which results in a brighter image because proportionally more light is able to enter the eye. However, the position and size of each optical component of the eye are incredibly sensitive and tuned to others, which results in many other corresponding changes to eye and corneal shape, lens position, and relative intraocular compartment size necessary to balance the relatively larger pupil size.

A second solution that has repeatedly evolved in response to nocturnality is an increase in the ratio of rods to cones as well as an increase in the total number and density of rods within the retina. While a retina entirely composed of rods is exceedingly rare (e.g., some species of deep-sea fishes, bats, armadillos, lizards, and snakes), a significant increase in the ratio of rods to cones is quite common. In addition, rod shape often evolves to become long and slender, which results in a higher density of rods per unit of retinal area. Ultimately, a high density of rods results in a greater degree of summation between the rods and the bipolar (and ganglion) cells, which increases sensitivity to light at the expense of visual acuity.

Interestingly, while the vertical slit pupil is regularly associated with nocturnality, the possession of a slit pupil alone does not increase light sensitivity. The slit pupil actually evolved as a mechanism needed to ensure the full and adequate closure of the pupil. The retina and photoreceptors of nocturnal animals are so sensitive to light that they must also evolve a mechanism to protect the retina from excess light (for example, when your cat decides to hang out with you during the day). A round pupil changes diameter through the contraction of circular, ring-shaped pupillary muscles, but these muscles are unable to shorten to a significant enough distance that entirely closes the pupil. However, the muscles that control pupil size in a slit-shaped pupil are arranged in a way that allows the pupil to be closed adequately to not overstimulate the highly sensitive retinal cells. Thus, the evolution of the slit pupil itself does not directly improve vision in low-light situations. Rather, the evolution of the slit pupil is an adaptation associated with nocturnality that helps protect the highly sensitive photoreceptors by allowing the pupil to fully close in comparison to a round pupil.

Finally, the repeated and independent evolution of a tapetum is another common mechanism that helps facilitate nocturnal vision. The tapetum lucidum is the general term we provide for a variety of reflective structures that have evolved to reflect light after it reaches the back of the eye and enhance the stimulation of the photoreceptors. It is the tapetum lucidum that is responsible for the eye shine we observe when a bright light, like the headlights of a car, is reflected from the eyes of nocturnal vertebrates. However, the tapetum lucidum has evolved independently numerous times and as such has taken multiple different forms. Most commonly, the tapetum lucidum is incorporated into the choroid layer of the eye and sits just behind the retina. Here, it has evolved in at least two ways. One way is through the evolution of a fibrous, tendinous connective tissue that sits on the posterior surface of the choroid. The shiny, tendinous layer of tissue is then able to reflect light, which might not be too surprising if you have ever observed the shiny surface of a tendinous sheet or aponeurosis while dissecting your favorite species in a vertebrate anatomy lab. A different evolution of a choroid-based tapetum lucidum occurs by adding reflective inclusions (often guanin crystal) to the cytoplasm of epithelial cells within the choroid. Similarly, a reflective tapetum lucidum has also evolved directly within the retina through the inclusion of reflective particles inside the cytoplasm of retinal epithelial cells.

Other Types of Radiation Receptors

Pineal Gland and Eye

The pineal complex of vertebrates is another system that, at least ancestrally and in a handful of extant vertebrates, also has photoreceptive capabilities. The pineal complex is a group of one or more organs associated with the diencephalon of the vertebrate brain. The two most common organs of the pineal complex found across extant vertebrates are the epiphysis and the parietal organ (also known as the parietal or third eye). Ancestrally, it is most likely that the parietal organ (i.e., parietal eye) was used as a third eye that had photosensitive capabilities that were accessory to the paired eyes that also evolved early in vertebrate history. However, over the course of vertebrate history, this complex has evolved incredible variation. A pineal complex that includes a photosensitive organ (usually the parietal eye but sometimes the epiphysis) is still found in extant vertebrates including lampreys, frogs, and many reptiles. However, in other species it has been lost or transformed entirely into an endocrine organ. For example, in mammals and birds, only the epiphysis remains and is used entirely as an endocrine organ that secretes the hormone melatonin, which helps regulate the internal clock and circadian rhythm of the animal. In these cases, the epiphysis is usually referred to as the pineal organ. Thus, despite no longer having photoreceptive capabilities in some clades, it still retains a connection to daily cycles of light and dark.

UV Receptors

Some vertebrate species also contain retinal photoreceptors that respond to ultraviolet (UV) radiation. There is no clear phylogenetic signal behind the distribution of retinal UV receptors, but they can be found in most major vertebrate clades other than Mammalia. The functional significance of UV reception is not clear, but in terrestrial vertebrates, it might be related to tracking prey. For example, animal urine reflects UV light, which you might have experienced when using a black light to find dog or cat urine in the carpet of your home. Similarly, one functional purpose of this might be related to predators that possess UV receptors tracking the urine of their mammalian prey.

Infrared Receptors

Receptors sensitive to infrared (IR) radiation have evolved independently at least three times across vertebrates. IR receptors have independently evolved in vampire bats (Desmodus rotundus), the snake families Boidae and Pythonidae, and a different clade of snakes consisting of the pit vipers (Crotalinae within the family Viperidae). In all cases, the ability to detect IR radiation aids in the detection of prey, particularly in low light levels at night. IR radiation is naturally emitted from the bodies of all living animals and therefore will also be emitted at night even when there is no visible light source able to reflect off the body. Thus, the ability to sense the emitted IR radiation from a nearby prey item provides a significant advantage to a nocturnal species (or even a diurnal species that has poor vision) in locating its prey.

Developmental Origins of the Eye and Associated Structures

Paired eye development in vertebrates begins when the forebrain (diencephalon) evaginates (bulges outward) and protrudes toward the surface during the early part of neurulation (Figure 20.5). This evagination begins with a singular eye field that later splits into two paired capsules, called optic vesicles, on either side of the head and within the neuroectoderm. This process requires the expression of a gene called cyclops—if cyclops function is lost, a single midline eye results and the ventral forebrain fails to form. As the optic vesicles are forming, the surface ectoderm also begins to thicken into an overlying layer called the lens placode. The next stage of eye development consists of an invagination of the lens placode to form a pit that deepens into a lens vesicle, which will go on to differentiate into the lens. Lens fiber differentiation begins with expression of several crystallin genes, which trigger the elongation of the posterior cells of the lens vesicle and the loss of organelles like the nucleus, mitochondria, and endoplasmic reticulum. After the lens buds off from the surface ectoderm, the remaining ectodermal cells are invaded by nearby neural crest cells, and together they form the cornea.

While the lens and cornea develop, the superficial portion of the optic vesicles extends toward the surface and invaginates to form the optic cup, while the deeper portion thins to form the optic stalk. The optic cup then consists of outer and inner cell layers, which at their junction form the ciliary body and iris. The outer layer then goes on to give rise to the retinal pigment epithelium, and the inner layer forms the photoreceptors and the neural retina (which later extends into the brain as the optic nerve [CN II]). The first type of retinal cell to form is retinal ganglion cells, then rod photoreceptors, then Müller glial cells (this is well conserved in vertebrates, with some variation). Retinal cells differentiate starting in a ventral patch near the optic stalk/future optic nerve (CN II) and then progress outward first toward the nasal capsule, then dorsally, and finally posteriorly.

20.3 Sense: Chemosensation

We see it in every cartoon—a pie is left on a windowsill to cool. A tendril of smell emanates from the pie and winds its way to the nose of a dozing, mischievous character. They float along the smell tendril, following the scent to the cooling pie. They steal the pie and take a bite, sighing in satisfaction as they taste their stolen sweets. Although silly and corny, this is not too far off from the way vertebrates use chemosensation—the detection of chemicals in the environment. They detect long-range chemicals using their olfactory system (their sense of smell), following their nose. Once they’ve gotten close to the source of the smell, they can use their gustatory system (their sense of taste) to detect close-range chemicals using their mouth and tongue.

Chemosensation goes beyond finding food. It allows vertebrates to avoid predator chemical cues, use pheromones to attract mates, identify conspecifics, return to their natal grounds, and care for their young. Different chemicals stimulate the olfactory system and the gustatory system. Why some chemicals stimulate one system versus the other is still unclear. Chemicals are separated out by their volatility and solubility—how well they readily vaporize and dissolve in water—and the different chemosensory systems are generally tuned to detect different chemical categories. When chemicals are detected by these systems, the chemical stimulus from the environment is transduced into a neurological signal, which can be interpreted by the animal, allowing them to make decisions based on the type of chemicals they are detecting.

Chemosensation—Olfaction

Olfaction is commonly referred to as the sense of smell. During olfaction, the nose detects chemicals and sends this information to the brain via the olfactory nerves. Most vertebrates have two types of olfactory systems: the main olfactory system (MOS) and the accessory olfactory system (AOS). Typically, the MOS, which detects airborne odorants, is what normally comes to mind when we think about the sense of smell. The AOS, also called the vomeronasal system in tetrapods, responds to water-soluble stimuli such as pheromones and is highly tied to the sense of taste. You can blame your vomeronasal system when a stuffy nose makes your food taste funny. This delineation between the MOS and AOS becomes blurry when we think about aquatic vertebrates (like fish and amphibians), but we’ll talk about that in the Aquatic Chemosensation section.

Anatomy of Vertebrate Nose

The vertebrate nose is a sensory organ that houses both the MOS and AOS. The nose has evolved to facilitate the transport of chemicals to their specific sensors called olfactory receptor neurons (ORNs). The anatomy of the nose is just as diverse as the animals who have them. As you learned in Chapter 14 on the respiratory system, during the evolutionary shift from water to land, vertebrates adapted to terrestrial life by developing the ability to breathe air. This is also the point in evolutionary history where olfaction and respiration are first tied. Fishes, for example, have separate olfactory and respiratory systems (more on this in the Aquatic Chemosensation section). In most tetrapods, air is brought in through the nose during respiration, allowing airborne odorants to travel into the nasal cavity along with each breath. Respiratory-tied olfaction also allows for sniffing—the active sampling of odors through intakes of air through the nose.

Airflow through the nose differs greatly across air-smelling vertebrates. Humans, for example, breathe in and out through the same cavity, causing airflow to change directions. On the other hand, air flows through dog noses in a unidirectional pathway, flowing in through the center of the nostril (or naris) and out through the outer regions of the naris, where you see the little slit on a dog’s nose. In dogs, the airflow pattern helps with their keen sniffing ability—odorants are deposited in different parts of the nose based on their solubility. The ORNs in that area of the nose are sensitive to the particular class of odorants deposited there. So the airflow helps match the chemical to the right type of sensor, increasing the efficiency of the dog olfactory system.

Main Olfactory System (MOS)

In tetrapods, air travels into the paired nasal cavities through the external incurrent nares. Tetrapods also possess internal, incurrent nares, called choanae, which connect the nasal cavity to the buccal cavity. The nasal cavities are partially lined with olfactory epithelium—where olfaction takes place. The rest of the nose is covered in respiratory epithelium. Nasal epithelium often covers one or more conchae—thin, turbinate bones on the side of the nasal cavity. These conchae increase surface area for odorant detection and help humidify the air passing through. It is hypothesized that conchae also play a role in warming the air in endotherms.

Within the olfactory epithelium there is the sensory epithelium, which houses the ORNs, and the nonsensory epithelium, without ORNs. Both tissues have supporting cells, mucus-producing cells, and basal cells. ORNs are bipolar neurons, meaning they have a dendrite on one side of the soma (cell body) and an axon on the other. The dendritic end of these ORNs extends to the olfactory epithelium, coming in direct contact with the chemical-containing air moving through the nose. ORNs are the only part of the nervous system that comes in direct contact with the external environment! The ORN dendrites terminate in cilia and/or microvilli within the sensory epithelium. The sensory epithelium is covered by a mucus layer, which is produced by Bowman’s glands or olfactory glands. While runny noses may be annoying, mucus production is vital to olfaction. Chemicals in the air are caught by the mucus and are spread by diffusion to the ORNs.

The axons of ORNs project from the olfactory epithelium into the lamina propria, the connective tissue beneath that contains blood vessels and the Bowman’s glands. These axons of the ORNs run together to form an olfactory nerve, which projects to the olfactory bulb. Here, the axons synapse onto mitral cells to form glomeruli. Afferent axons leaving the olfactory bulb form the olfactory tract or cranial nerve I (CN I), which projects to the pallium of the telencephalon.

Accessory Olfactory System (AOS)

The vomeronasal system is classified as a specialized accessory olfactory system based on its anatomy and the types of odorants it responds to, although the delineation between the two olfactory systems is still muddy. The vomeronasal organ, also sometimes called the Jacobson’s organ, varies anatomically among tetrapod groups. In amphibians, the vomeronasal organ is an offshoot of the main nasal cavity. In amniotes, it is a more distinct separate organ, either connected directly to the nasal or buccal cavity or indirectly connected to both by the nasopalatine duct. The vomeronasal organ is secondarily lost in some taxa like birds.

The sensory epithelium of the vomeronasal organ is similar to olfactory sensory epithelium. One major difference is that the dendritic ends of the vomeronasal receptor neurons exclusively terminate in microvilli. The axons of these receptors terminate in the accessory olfactory bulb, which is distinct from the main olfactory bulb. The afferent axons from the accessory olfactory bulb unite with those from the main olfactory bulb to form CN I. However, the vomeronasal system’s projections terminate in different areas of the brain than the main olfactory system.

The tie between nonvolatile odorants (compounds that do not easily evaporate) and the vomeronasal system is supported behaviorally. Think of a snake flicking its tongue in and out—this is a nonvolatile odorant sampling technique! Squamates transfer odorants from the environment to their vomeronasal organ on their tongue. Mammals use the flehmen response—which we see horses and cats do commonly. They curl back their front lips to expose their teeth, inhale with their nostrils closed, and hold the position, allowing nonvolatile chemicals to be more directly sampled by their vomeronasal organ. Elephants have an even more direct way to sample the nonvolatile pheromones of conspecifics. Elephants will dip their trunks into the urine of other elephants and transfer it directly to their vomeronasal organs. Elephants can learn a lot from urine, like the reproductive stages of potential mates. A study on African elephants suggested that by scenting urine trails, they may be able to determine the age and maturity of the individuals who made that trail, cluing them in to who they may encounter in their environment.

Developmental Origins of the Vertebrate Olfactory System

The olfactory organs of the paired nasal epithelia in vertebrates develop from both cranial neural crest cells and ectodermal olfactory placodes located ventrally on the developing face. The olfactory placode emerges through a process of convergence and thickening of migrating epithelial cells. The placode contains a mixture of columnar cells, undifferentiated cells, and spindle-shaped cells, which serve as precursors to olfactory receptor neurons. Once established, the placode then invaginates anteriorly and dorsally and deepens into a nasal pit, which will give rise to the olfactory epithelium. Axons extend from bases of the sensory cells, making up the center of the nasal pit, collect into fascicles, and perforate the basement membrane to make connections with the olfactory bulb extending from the anterior part of the telencephalon. Surrounding each bundle of olfactory axons are specialized glial cells called olfactory ensheathing cells, which develop from migratory neural crest cells. At the opposite end of each receptor cell, dendrites begin to grow toward the surface of the epithelium, branch out, and sprout multiple cilia. These dendrites will then receive the odorant molecules that identify each smell.

Olfactory development across jawed vertebrates seems to be relatively conserved. However, a major difference arises in the origin of the single median nostril of cyclostomes. An additional placode that typically gives rise to the hypothalamus and anterior pituitary gland, the adenohypophyseal placode, forms as a separate thickening of cells in the midline of the head in gnathostomes but combines with the olfactory placode in cyclostomes to form the nasohypophyseal placode. This placode then goes on to develop into a midline nasal sac.

Another difference in olfactory development across vertebrates concerns the vomeronasal organ, which is present in reptiles and amphibians, as well as some mammals. The vomeronasal organ forms through a secondary medial invagination of the developing nasal pit into a separate cavity within the olfactory opening. After the formation of this groove, several populations of migratory neurons colonize the vomeronasal epithelium, and the groove deepens into a well that separates from the olfactory pit completely. In many vertebrates, even those that lack a vomeronasal organ in adulthood, a temporary vomeronasal anlage forms during development and then is lost, supporting a more ancestral origin of this structure in early jawed vertebrates.

Chemosensation—Gustation

Gustation, colloquially referred to as taste, is the detection of chemicals within the oral cavity through taste buds. During gustation, taste buds on the tongue, roof of the mouth, and upper esophagus detect chemicals brought in through the drinking of liquid, licking of a substance, or the mastication of solid food. The taste buds detect these chemicals and send taste information to the brain through a suite of cranial nerves. Aquatic animals are freed from the constraint of mouth-housed taste buds. We see proliferation of extraoral taste buds not just on their heads but on their limbs (see Aquatic Chemosensation section).

The tongue is the main location for taste buds across vertebrates. Beyond being used to manipulate food (see digestion chapter, Chapter 13, for more on this), the tongue determines the palatability of a substance, a.k.a. the tastiness. The tongue can also test possible food via licking, checking if something is edible before it enters the oral cavity. It is still unknown why some chemicals stimulate the gustatory system and not the vomeronasal system (and vice versa). Generally, the gustatory system responds to compounds that are dissolved in fluids and do not significantly become airborne.

Taste Receptors

The functional unit of the gustatory system is the taste bud. Taste buds are made up of taste receptor cells, supporting cells, and basal cells. In most tetrapods, the receptors are sunken into the tongue. Chemicals reach the receptor via a mucus-filled pit or pore. The taste bud’s gustatory hairs stick out into the pore. Taste buds rapidly regenerate (every 8–12 days in humans!).

Taste buds are innervated by thin, dendritic sensory endings projecting from specific brain neurons, unlike the centrally projecting axons we see in the olfactory system. They are also not all innervated by one cranial nerve, like CN I for the olfactory system. In humans, the anterior part of our tongue is innervated by the facial nerve (CN VII) and the posterior tongue by the glossopharyngeal nerve (CN IX). The taste receptors on the roof of our mouth and beginning of our esophagus are innervated by the vagus nerve (CN X). Despite this array of innervation pathways, gustatory nerve fibers all terminate in the same nuclear complex in the medulla.

The human tongue is covered in papillae—the majority of which are not taste buds. These filiform papillae are small projections arranged in rows covering most of the front of the tongue. The papillae that do contain taste buds are categorized based on their shape. Humans have three different types of taste bud papillae, which are concentrated in specific areas of our tongue. Circumvallate taste bud papillae are larger and shaped like an upside-down V. These are concentrated in the posterior section of the tongue. Fungiform taste buds, as their name implies, are mushroom shaped and located in the anterior section of our tongue. Continuing with the nature-nomenclature, foliate taste bud papillae are leaf shaped and concentrated on the lateral portion of our tongue.

In mammals, taste bud cells have been classified into types, which are distinguished by both their morphology and cellular expression. While we have some hypotheses over which cell types respond to which types of tastes, we do not definitively know this correlation. Type I are glial-like cells and hypothesized to respond to salty tastes. These are the most frequent and exhibit a spindle shape with brush-like, long microvilli extending into the taste pit. Type II are receptor cells that express G-protein coupled receptors, which respond to bitter, sweet, and savory tastes. They are fusiform shaped and mostly occur on the periphery of the taste bud. Type II cells also secrete ATP and ACh neurotransmitters. Type III cells are presynaptic cells, which sense sour taste and secrete serotonin, GABA, and norepinephrine neurotransmitters. They have unbranched apical processes, each with a single large microvillus. Type IV cells are basal, nonpolarized cells whose taste specificity is unknown. They are small cells at the base of the taste bud. Finally, Type V cells are marginal cells that are hypothesized to be taste bud stem cells that express non–taste receptor proteins.

The link between taste bud types and the types of taste they respond to is still under investigation. The majority of research in this area also primarily revolves around humans and how we identify tastes. Some functional links between taste repertoire and function are understood. Bitter taste receptors, for example, are important for identifying toxins.

Interestingly, snakes lack taste buds on their tongue. While their tongue is still a chemosensory organ, it is responsible for transport of chemicals to the vomeronasal organ, not direct detection of those chemicals. Most snakes do have taste buds; they’re just in their oral cavity—namely, by the jaws. In some snakes, taste buds are elevated on papillae that also have mechanoreceptors, forming a taste/touch sensory complex that helps with the identification and manipulation of food items inside the mouth.

Developmental Origins of the Vertebrate Gustatory System

Taste buds and gustatory receptors form from sheets of epithelial cells that cover the developing tongue and differentiate first into taste placodes and then into fully formed taste buds. Unlike other sensory systems, there is good evidence that there is no neural crest contribution to taste buds in fish, amphibians, birds, or mammals. Taste bud development is broadly similar across different vertebrate groups. In mice, the taste placodes consist of a cluster of columnar cells and begin to differentiate after sensory nerve fibers arrive and make contact with the placode cells. As the cells of the taste bud itself undergo morphogenesis, the surrounding epithelial sheets invaginate down into the mesenchyme to form the papillae that house the taste buds.

In zebrafish, taste bud primordia develop within the surface epithelium, as in mammals, where they are initially covered by layers of epithelial cells. As development proceeds, a taste pore forms between the cells, exposing the developing taste buds to the environment. However, the timing of development of gustatory receptors in zebrafish differs with location on the body. The first taste buds to differentiate are those on the lips and gill arches (3–4 days postfertilization; dpf), while taste buds inside the mouth cavity appear later (4–5 dpf), and those on the head form even later (12 dpf).

Two main models of taste bud development have been proposed: the neural induction model and the early specification model. The neural induction model states that innervation of each taste bud with a protrusion from either the facial, glossopharyngeal, or vagus nerves is required to induce differentiation of lingual papillae and eventually taste bud primordia. The early specification model suggests that patterning of taste buds is specified earlier on in development and that cell-cell interactions within the lingual epithelium, and not neural input, are the driving factors of differentiation. Despite a correlation between the appearance of sensory nerves at taste placodes, experiments in axolotls have shown that taste papillae and primordia can be induced to form without innervation. Additionally, rodent tongues cultured in a dish develop taste buds that are similar in number and size to those of control animals, suggesting that taste buds and the surrounding epithelia have their own inherent molecular signals that control their development.

Aquatic Chemosensation

Aquatic vertebrates detect chemicals in the water.

Fish

Fish are the most diverse vertebrate group, and their noses are diverse as well—far beyond the scope of what we are able to cover in this chapter. Instead, we will cover the general arrangement of the olfactory system in fish while highlighting some interesting oddballs along the way. Cyclostomes (hagfishes and lampreys) have one naris on the dorsal part of their head, which leads to one nasal chamber. The nasal chamber also connects to the pharynx via a nasopharyngeal duct. Holocephalans (a Chondrichthyan group that includes chimeras and ratfish) have a pair of forward-facing nares on the tip of their rostrum. They also have an internal nose-to-mouth connection, which allows them to irrigate their nose through buccal pumping, much like the choana we see arise later in tetrapods. Most other fish have two sets of nares on either side of their head: an incurrent and excurrent naris, which allows for unidirectional water flow through their olfactory organ. Water flows into the olfactory chamber via the incurrent naris. Within the chamber, water travels through the incurrent canal and back out of the excurrent naris through the excurrent canal. Within the olfactory chamber is the olfactory rosette, so named because of its floral-like arrangement. The “petals” of this rosette are the olfactory lamellae, sheets of olfactory tissue containing both sensory and nonsensory olfactory epithelium. Rosettes vary in size and shape. Chimeras, for example, have radially arranged rosettes where the lamellae are connected like the petals of a daisy. Sharks, in particular, have elongated rosettes with paired lamellae on either side of a connecting tube called the raphe. Shark rosettes range in lamellar count from 26 (in the Japanese angel shark) to 718 (in the winghead shark). On the opposite end, some teleosts have as few as one or two lamellae, which are attached directly to the olfactory chamber. Of course, there are plenty of weirdos in the bunch. For example, tetraodontids, like the blackspotted puffer, have no nostrils at all. Instead, their olfactory organ is located on tentacle-like growths on their rostrum, whose inner cavities are covered by olfactory epithelium. Fish lack Bowman’s glands but still rely on mucus (secreted from goblet cells) for chemical detection.

Fish also do not possess a distinct and separate vomeronasal system. However, the olfactory epithelium of teleosts is a hybrid olfactory and vomeronasal epithelium expressing both genes for olfactory and vomeronasal receptor neurons. These two neuron groups also project to different regions of the olfactory bulb. Speaking of the olfactory bulb, unlike most tetrapods, fish olfactory bulbs are not in direct contact with the telencephalon. Instead, fish olfactory bulbs are projected forward, connected to the olfactory rosettes. The olfactory bulb is connected to the telencephalon via the olfactory tracts or peduncles. The length of the olfactory tracts varies among species and is dependent on how far the olfactory bulb is from the telencephalon. Hammerhead sharks, for example, have long, thin olfactory tracts running from their olfactory bulbs on the distal ends of their elongated heads to their telencephalon.

Gustation-wise, fish have taste buds in their oral cavities as well as in their gills, gular region (i.e., what we would colloquially call their chin), barbels, and even fins. The abundance of extraoral taste buds highlights the issue with separating gustation from olfaction in the aquatic environment. Some fish, like the yellow bullhead, have more than 175,000 taste buds on the entire surface of their body. Typically, the facial nerve (CN VII) innervates the extraoral taste buds in fish. In some fish, like catfish, the extraoral and oral gustatory systems are two functionally separated systems—the extraoral taste buds detect chemical stimuli at a distance, while the oral taste buds are used in close stimuli detection and are used in discriminating palatable versus unpalatable foods. Adding further confusion to the delineation between olfaction and gustation in fish—both systems respond to similar chemical types at comparable concentrations.

Amphibians

Because of their dramatic life history change from aquatic larvae to terrestrial adults, amphibians are a fascinating subject for the evolution and development of chemosensation. While there is a large diversity in chemosensory morphology within amphibians, here we will lay out the general trends. Larval frogs and salamanders have a specialized olfactory organ associated with a small mouth. By contrast, caecilians have relatively simple, triangular olfactory organs. The external naris is connected to the nasal sac through a nonsensory vestibule. The choana is guarded by a valve that is hypothesized to stop the backflow of water and allow for unidirectional water flow through the olfactory system. The vomeronasal organ forms as a pocket off the nasal sac. Taste buds form on papillae throughout the oral epithelium.

During metamorphosis, the chemosensory system goes through an extreme makeover. Instead of the previous unidirectional water flow, metamorphosized amphibian olfactory systems allow for bidirectional airflow. Keeping their mouth closed, they oscillate their buccal floor—bring air in and out of their excurrent nares. This new bidirectional olfactory flow eliminates the need for stopping backflow, and the choanal valve is lost. The vestibule between the external naris and the nasal sac is either reduced or completely lost along with the choanal valve. The choana normally shifts significantly in position, and the vomeronasal organ connects to the mouth. This change in positioning with a newly terrestrial lifestyle may allow for odorants to be deposited separately between the olfactory and vomeronasal organs based on their volatility. Physiological research on salamanders shows a change in the responsiveness of their olfactory epithelium with decreased sensitivity to dissolved odorants and increased sensitivity to volatile odorants.

After metamorphosis, amphibians develop the nasolacrimal duct, which connects the eyes to the nose, allowing for the reabsorption of excess lacrimal fluid (a.k.a. tears). Metamorphosis also cues the increased presence and function of Bowman’s glands. In their new terrestrial lives, many amphibians develop the ability to close their external nares to help with lung inflation. Anurans, for example, close their nares during lung inflation via a specialized mechanism using their lower jaw and submentalis muscle.

The amphibian gustatory system also goes through a morphological change after metamorphosis. They develop a fleshy tongue, and their taste buds are replaced by taste discs. Taste discs are made up of an epithelium similar to that of the olfactory and vomeronasal systems. Taste discs are lauded as the largest gustatory organ in all vertebrates and have a variety of different epithelial cells, chemoreceptive surface types, and neuro-epithelial systems.

Despite this shift to a more typical terrestrial olfactory system, many amphibians retain the ability to smell underwater. Frogs and salamanders can still detect pheromones in the water. In one behavioral study, blinded tiger salamanders would tap their noses and bite at bags of earthworms underwater but stopped this behavior when their noses were plugged.

Aquatic Mammals

Mammals have the largest olfactory gene repertoire of any animal group, suggesting that olfaction is incredibly important for the majority of mammals. So what about aquatic mammals? Platypuses have very small olfactory bulbs and few olfactory turbinates in their nasal cavities. Their closest relative, the short-beaked echidna, has large olfactory bulbs and organs and as many as seven olfactory turbinates. Platypuses do have a vomeronasal organ. For marine mammals we see similar reductions in olfactory morphology. Some, like the sirenians and most cetaceans, lack a vomeronasal organ altogether.

While underwater olfaction is assumed to be absent in mammals, there are two mammals that employ “underwater sniffing”—the star-nosed mole and water shrew. These two will exhale air bubbles onto objects or into scent trails. They then sniff back up the bubble, allowing the chemicals to travel back into the nose and olfactory system.

While marine mammals may not smell underwater, there is evidence they still use their chemosensory systems. Baleen whale blowholes act as nares. One study found a correlation between baleen nare morphology and their level of zooplanktivory. Why does this matter? Plankton release dimethyl sulfide (DMS), a chemical cue shown to assist in seabirds’ abilities to locate prey. It’s hypothesized that nares are best suited for stereo-olfaction—the ability to compare differences in chemical signal strength between two nares. Bowhead whales in particular have complex and large (for a whale) olfactory bulbs, and 51% of their olfactory gene repertoire is intact, characteristics that could be linked with their ability to find krill aggregations.

The aquatic mammal gustatory system is severely understudied, but we have some interesting findings in bottlenose dolphins. Not only can dolphins recognize different individuals based on signature whistles, but they can also use urine signals. In this study, dolphins used their gustatory system to differentiate water from urine samples. Furthermore, they differentiated between urine from familiar and unfamiliar individuals. Dolphins were able to recognize individuals by gustation and were able to integrate both the acoustic signal of the signature whistle and the gustatory signal of the urine sample when they were presented together.

The Human Connection—COVID-19 and the Chemosensory System

One of the most commonly shared side effects of COVID-19 infection is a loss of smell and/or taste. While this was commonly brushed off as insignificant, by now we hope you have realized that disruption of these chemosensory systems is more than a minor inconvenience—it’s a shutdown of two of the five human senses! This is a direct, observable, and widespread neurological impact and sensory impairment. Why does this happen? The research is still not conclusive. Here’s what we do know.

Lingual epithelial cells, such as taste buds, serve as a hotspot for SARS-CoV-2, the virus that causes COVID-19. SARS-Cov-2 replicates within taste buds, contributing to one of the most famous COVID-19 symptoms: ageusia (loss of taste) and dysgeusia (persistent sensation of foul tastes). On the olfactory side, experts believe that while the SARS-CoV-2 virus is not affecting the olfactory receptors or nerves directly, the evidence suggests that the virus injures the supporting cells. If these supporting cells are not able to “support” by providing nutrition and structure to the olfactory nerves, the nerves may become secondarily injured.

Additionally, early-stage COVID-19 begins with nasal congestion. Stuffy noses and sinus blockages narrow the passageways for airflow, making it more difficult for odorants to make it to the olfactory sensory epithelium. A common treatment method for congestion is nasal sprays. Nasal decongestant sprays constrict the blood vessels in nasal passages to reduce swelling. The same can be achieved by corticosteroid sprays, which reduce nasal inflammation by reducing the production of the inflammatory chemicals that cause congestion. Alternatively, saline-based sprays work by moisturizing dry nasal passages and thinning nasal mucus.

20.4 Sense: Mechanosensation

Mechanosensation is the transduction of small changes in the mechanical force applied to a tissue into a neural signal. We will broadly refer to any sensory cell capable of transducing a mechanical signal as a mechanoreceptor. Due to the generality of mechanosensation, many different senses rely on mechanoreceptors. Indeed, mechanoreceptors are involved in the sensation of stimuli, including touch, pressure, proprioception, balance, and hearing.

Somatosensation

Somatosensation is a general sense that includes multiple stimuli, including touch, pressure, pain, temperature, and proprioception. In comparison to most of the senses you will learn about in this chapter, the sensors associated with somatosensation are distributed across the body and can be associated with a variety of different organ systems. Many somatosensory sensors are found in the skin, but other locations include muscles, tendons, and direct association with organs. Consequently, somatosensation is used to sense both internal and external stimuli. For example, receptors used to sense pressure can be found in the skin of your fingers, which helps you regulate the magnitude of pressure you need to apply to a glass in order to keep it from slipping from your hand and ensuring that you don’t squeeze the glass too hard so that it breaks. In contrast, a different type of pressure receptor can also be associated with arteries inside the body to monitor the pressure of blood. Thus, somatosensation is an incredibly versatile system that facilitates the sensation of many different types of stimuli from both inside and outside the vertebrate body.

Touch, Pressure, Pain, and Surface Temperature

The sensation of touch, pressure, pain, and temperature due to the interaction between the body and external stimuli results from the response of a suite of sensory receptors distributed in the skin. The external mechanical stimuli (i.e., objects and surfaces) the vertebrate body interacts with on a regular basis are incredibly complex. Simply think of an ice cube and the different variables associated with it. To do so, imagine you are blindfolded and handed an object that is relatively small, generally cube shaped; it is likely to be slippery and certain to be cold. It is likely you will be able to quickly guess the object you were handed despite being blindfolded. However, your ability to do so relied on sensing each of these different variables. Therefore, it shouldn’t be surprising that the vertebrate body is outfitted with so many different types of sensors and that each of these sensors is responsible for sensing different ranges and specific stimuli associated with these external stimuli.

The different types of sensory endings (a term often used interchangeably with sensory receptors) responsible for somatosensation have been best studied in mammals (particularly humans). Thus, we will begin our investigation of these different types of sensory endings from a mammalian perspective (Table 20.1). To do so, we will briefly cover each sensory ending and its general function in the mammalian system. Many of these receptors might be familiar, as you might have already heard of them during your exploration of the integumentary system.

Free nerve endings associated with the skin are generally responsible for the sensation of pain and temperature. Free nerve endings are sensory neurons with a receptive end that lacks any kind of specialization. Free nerve endings responsible for sensing pain are often referred to as nociceptors, and sensors responsible for sensing temperature are often referred to as thermoreceptors. Thermoreceptors embedded in the skin are usually activated in response to changes in surface temperature relative to internal body temperature. There is a wide range of thermoreceptors that respond to specific changes in temperature like increasing versus decreasing temperature. Nociceptors respond to stimuli of an intensity that surpasses a given threshold. Painful stimuli can include mechanical, thermal, or chemical. For example, stubbing your toe is a mechanical stimulus that can elicit a painful sensation, whereas eating a spicy pepper is a chemical stimulus that can elicit a painful burning sensation. In both examples, nociceptors are activated. Finally, the root of the hairs embedded in the skin of mammals is also wrapped by a free nerve ending, which provides mammals an additional sensory structure. Mammals use hair to sense a range of stimuli including wind or body movement while running or swimming through an environment and light touch associated with an animal (e.g., an insect) crawling across the body. Free nerve endings also contribute to the sensory endings associated with the whiskers of mammals (in addition to other endings like tactile discs). Free nerve endings are believed to be present in extant representative species of all major vertebrate clades. However, the specific functional capabilities of these sensors have not been evaluated in every species and therefore could vary across the phylogeny.

Table 20.1—Mechanoreceptors responsible for general somatosensation

Touch, pressure, and vibration are sensed by a suite of receptors that are either encapsulated or unencapsulated. These sensors are generally located in the skin, and each is tuned to sense a specific feature or range of features associated with mechanical stimuli. The specific range of stimulus features or intensity acquired by each type of sensory receptor is heavily influenced by whether the sensor is or is not encapsulated as well as the depth of the sensor in the skin of the animal. Unencapsulated sensory receptors are receptor endings that are not covered by any additional tissue surrounding the receptive ending of the neuron and include free nerve endings and tactile discs. Encapsulated sensory receptors are receptor endings that are covered in an additional tissue (often connective) or membrane of a nearby glial cell. The encapsulation of the sensory receptor can help to either augment the responsivity of the sensor by increasing receptor sensitivity or filter the stimuli so the receptor is tuned to only respond to a very select type of stimulus or a narrow range of stimulus intensity.

Tactile discs are unencapsulated sensory receptors located in the integument of vertebrates that generally respond to light touch, help encode features of objects like shape and edge detection, and are capable of providing information about texture by being sensitive to low-frequency vibrations.

Bulbous corpuscles are slowly adapting encapsulated sensory receptors found in the deep layers of the integument as well as in joint capsules. Bulbous corpuscles respond to the stretch of the integument, movements at joints, and at least in mammals, deep pressure applied to the skin. The role of bulbous corpuscles in sensing joint movements should not be surprising given these receptors are often found in high densities within the vertebrate joint capsule. Further, the ability of these receptors to sense skin distortion and joint movements enables these receptors to also contribute to the sense of proprioception.

Tactile corpuscles are rapidly adapting encapsulated sensory receptors found in the superficial dermis of the integument. These receptors are primarily responsible for sensing light touch and some features of texture by responding to relatively low-frequency vibrations of the integument.

Lamellated corpuscles are rapidly adapting encapsulated sensory receptors in the dermis of the integument. Lamellated corpuscles respond to deep pressure and high-frequency vibrations.

The suite of sensory receptors responsible for general somatosensation is not well characterized across all vertebrates. However, it is likely that most vertebrates have at least similar mechanosensors that overlap in functional capability. For example, actinopterygians have the ability to sense texture using the sensory receptors embedded in their fins, and the fins of Chondrichthyes have sensory receptors capable of sensing pressure. Similarly, investigations have also revealed the presence of analogous joint receptors in at least one species of all major vertebrate clades. Further investigation will be required to reveal the homology and evolutionary history of these receptors across vertebrate clades.

Proprioception

Proprioception is defined as the ability to sense the movement and position of one’s own body axis and one’s appendages relative to the trunk. For example, even after you fully close your eyes, many of you will be capable of touching the tip of your nose with your finger. In theme with somatosensation, proprioception itself relies on a variety of different mechanoreceptors distributed throughout the body.

Proprioceptors of the Skin

Many mechanoreceptors distributed throughout the skin are also used to sense proprioceptive stimuli. For example, in many tetrapods, the mechanoreceptors responsible for sensing skin distortion (bulbous corpuscles), especially at joints, provide complimentary proprioceptive feedback. Further, the fins of actinopterygians and chondrichthyans are also outfitted with a variety of mechanoreceptors embedded in the tissues of the skin and the fin rays, and these sensors are consistently found to encode proprioceptive information like fin ray position, bending magnitude, and bending rate. The sensory endings found in the skin and fins of actinopterygians and chondrichthyans have not been studied in enough detail to reveal their homology with the different sensory receptors that have been well described in mammalian systems.

Tendon Organs

Tendon organs are stretch receptors embedded in the tendons of skeletal muscle. These tendons respond to tendon stretch and ultimately are capable of encoding the tension or strain developed in a tendon. Thus, tendon organs are also one of the prominent vertebrate proprioceptors. The precise homology and evolutionary history of tendon organs is not clear across all vertebrates. However, analogous sensory receptors associated with muscle tendons that are capable of sensing tension of the tendon are present in at least a representative species of all major gnathostome clades.

Muscle Spindles

Muscle spindles are a proprioceptive sensory receptor that encodes details of muscle length and, therefore, changes in muscle length. You can find more details about muscle spindles within the chapter focused on muscle tissues (Chapter 11). Briefly, muscle spindles are ultimately stretch receptors found within the belly of skeletal muscle. A muscle spindle is composed of a fibrous capsule that contains a small number of muscle fibers, called intrafusal fibers, inside the capsule. Both the capsule and the intrafusal fibers are aligned in the same orientation as the rest of the muscle fibers found outside the capsule, which are referred to as extrafusal fibers. Nerve endings wrap and surround the intrafusal fibers within the capsule and respond to the stretch of the fibers, allowing muscle length to be encoded.

Muscle spindles are most likely only found in tetrapods. However, one study suggested the presence of muscle spindles in the jaw musculature of an actinopterygian fish, but this work has never been duplicated or confirmed, despite attempts. Thus, we conservatively suggest that muscle spindles are traits that first evolved in early tetrapods sometime around the vertebrate water-to-land transition.

Finally, it is important to note that proprioceptive feedback is not unique to limbed vertebrates, and undulatory locomotion using the body axis also relies heavily on proprioceptive feedback. In these cases, mechanosensory receptors are located along the entirety of the body axis. Animals undergoing undulatory locomotion rely on the sensation of the various stimuli discussed above to encode information on myotomal muscle contraction and force, as well as the magnitude, location, and direction of body axis undulation.

The Neuromast Organ

The neuromast organ is a specialized sensory organ (composed of many individual receptors) contributing to mechanosensation in a variety of vertebrate sensory systems. The neuromast organ, or a modified version of it, is the primary sensory organ of the auditory system, vestibular system, lateral line system, and electroreception. Therefore, before the anatomy of each of these systems is examined, it is important to understand the anatomy of the neuromast organ.

The neuromast organ is a collection of mechanosensitive hair cells, supporting cells, and the afferent sensory neurons responsible for carrying the neural impulses transduced by the hair cells toward the central nervous system. A neuromast organ is also often surrounded by a cupula, which is a gelatinous membrane that embeds the underlying hair cells. In a neuromast organ, each individual hair cell is ultimately the mechanosensory receptor, and the cupula helps tune, filter, and enhance the mechanical stimulus being transduced by the hair cells.

The primary sensory receptor of a neuromast organ is the hair cell. Oddly, hair cells are not neurons but actually specialized epithelial cells. These epithelial cells are called hair cells due to the presence of numerous stereocilia projecting from the apical cell surface. Stereocilia are nonmobile cylindrical fingerlike projections of the apical surface cell membrane and structurally are more similar to large microvilli than they are to cilia. These stereocilia are of unequal length and typically arranged in order of height along the apical cell surface, so they almost appear as a steep staircase. The edge of the cell surface with the tallest stereocilia is bordered by a single large, modified cilium called a kinocilium. Again, a neuromast organ is formed when multiple individual hair cells (with each cell possessing many apical surface stereocilia) are clustered together with supporting cells and surrounded by the gelatinous cupula. Thus, a neuromast organ fits the requirements of an organ, as it contains multiple tissue types working together to produce a function.

Hair cells respond to and transduce mechanical stimuli due to the physical deflection of the apical stereocilia. The bending of the stereocilia results in the opening (or closing) of mechanically gated ion channels embedded in the cell membrane, ultimately resulting in changes in cell electrical potential. Hair cells are usually highly directionally sensitive and only respond to mechanical stimuli applied in a single direction. Deflection in one direction, often along the apical surface in the direction of increasing stereocilia height, results in cell excitation, whereas deflection in the opposite direction results in cell inhibition. However, as hair cells are indeed epithelial cells, they do not have an axon directly associated with the cell. Instead, hair cells synapse (either chemically or physically) with a supporting neuron. It is the associated neuron that will ultimately carry the neural signal to the central nervous system.

Vestibular System

The vertebrate vestibular apparatus allows animals to maintain positional equilibrium, which includes the body position, orientation, and movement in three-dimensional space. Thus, the vestibular apparatus is critical for maintaining balance. All vertebrates possess a vestibular apparatus that includes the same basic components, although there is variation across species and clades. The common components of the vestibular apparatus include at least one semicircular canal and two associated vestibular chambers called the saccule and the utricle. The interconnected canal(s) and chambers are all filled with a viscous fluid known as endolymph. The vestibular apparatus is a bilaterally symmetrical structure found on both the right and left sides of the vertebrate head. Indeed, it is often the comparison of sensory information acquired by the right and left vestibular apparatus that allows the brain to decode the complex stimuli associated with body position, orientation, and linear and angular accelerations.

The saccule and utricle contain a sensory receptor named the macula, which responds to changes in orientation on the vestibular apparatus. The macula (or otolith receptor) is a modified neuromast organ where calcium carbonate protein granules called otoliths (or otoconia) are embedded in the gelatinous copula surrounding the patch of hair cells. The macula of the utricle and saccule detect changes in orientation of the head because the otoliths are subjected to gravitational forces and therefore bend in response to movements of the head. For example, as the head is tilted, the otoliths cause the otolith-occupied cupula to bend and ultimately stimulate the hair cells. The macula is also capable of sensing changes in linear acceleration due to the inertia of the otoliths suspended in the cupula of the macula. Imagine riding a roller coaster (or even driving a car); as you accelerate, the mass of your body is deflected in a given direction. The same concept applies to the macula within the utricle and saccule, where linear accelerations result in the displacement of the cupula of the macula that stimulates the hair cells.

The semicircular canal(s) of the vestibular apparatus senses changes in angular acceleration. A semicircular canal is a semicircular duct filled with endolymph that contains a dilated sac at its end called an ampulla. Enlarged neuromasts, called cristae, are found within the ampulla of the semicircular canal and are the sensory receptors responsible for sensing changes in angular acceleration. Due to the viscosity, and therefore interior properties, of the endolymph contained in the semicircular canals, accelerations of the vestibular apparatus result in the movement of the circulating endolymph lagging behind the physical movement of the vestibular apparatus. The delayed movement of the endolymph contained within the semicircular canal ultimately results in the deflection of the cristae contained within the ampulla, thereby stimulating the hair cells. The magnitude of the acceleration will result in differences in the magnitude and timing of endolymph movement, thereby providing a means to encode angular acceleration. All extant gnathostomes have three semicircular canals (on each side of the head) that are generally oriented to capture acceleration around each of the three body axes. Thus, extant gnathostomes can generally sense acceleration associated with body pitch, yaw, and roll. However, species of lamprey are only known to have two semicircular canals, and species of hagfish are only known to have a single semicircular canal, thereby limiting the different rotational angles lampreys and hagfishes are capable of sensing.

Vestibular Development

Vertebrate vestibular and auditory systems begin their development as one structure with the emergence of the otic placode. The otic placode is a thickened region of ectoderm that sits adjacent to rhombomeres four through six in the embryonic hindbrain. As development proceeds, the otic placode invaginates to form an otic pit, which then closes to form a vesicle that is lined by pseudostratified epithelial cells. While the otic pit is closing, ventromedial cells detach from their epithelial layer and extend toward the neural tube to form the vestibulocochlear ganglion, which later differentiates into separate vestibular and cochlear ganglia. The cells of the otic vesicle then proliferate and differentiate to form an otocyst, which includes primordia of the semicircular canals, cochlea (in mammals), and endolymphatic duct. Genes expressed in the nearby hindbrain influence the patterning and morphogenesis of different cell types in the ear.

The development of the semicircular canals varies slightly across vertebrates. In amniotes, the canal primordia emerge as anterior, posterior, and lateral bulging epithelial plates. The plates then fuse and the supporting tissue surrounding the canals is resorbed, leaving the canals themselves behind. In fishes and frogs, rather than forming as fusion plates, the semicircular canals begin as cylindrical projections of the epithelium that extend into the lumen of the otic vesicle. The projections meet corresponding bulges on the opposite sides of the vesicle and fuse to form pillars of tissue that will differentiate into the semicircular canals.

Auditory System

The auditory system is present in most major vertebrate lineages and enables the ability to sense sound, which humans often refer to as hearing. The auditory system is inherently connected to the vestibular system, and in some species, a clear separation of function of certain structures is not fully distinct. Common to both systems, mechanosensitive neuromast organs are used to transduce the stimulus. The portion of the vestibular apparatus that is typically utilized for sound transduction is known broadly as the lagena, which can mostly simply and inclusively be considered a fluid-filled chamber. This chamber can range in size and shape from that of a small sphere resembling the saccule and utricle of the vestibular apparatus (e.g., many fishes) to that of a lengthened and coiled tube, which is found in most mammals and sometimes referred to as the cochlea. Across all vertebrates that possess a specialized or shared (with the vestibular apparatus) organ for sound transduction, the components of the vestibular apparatus and the lagena are together referred to as the inner ear and usually embedded within the skeletal component of the skull. Similar to the chambers of the vestibular apparatus, the primary chamber(s) responsible for sound transduction is also filled with endolymph. In addition, in most vertebrate lineages, other fluid-filled canals are also contained within the inner ear and contain perilymph and can be broadly referred to as the perilymphatic canals (also referred to as the scala vestibuli and the scala tympani in amniotes).

Interestingly, one of the most variable components of the vertebrate auditory system is how sound is transmitted from the external environment to the component of the inner ear responsible for sound transduction. The routes for sound transmission can include other chambers often referred to as the middle and external ear.

In this section, we will begin our study of the vertebrate auditory system by considering the anatomy of the inner ear and then add on the additional structures used for sound transmission that evolved in each major vertebrate lineage.

Actinopterygii

The auditory system of actinopterygian fishes generally lacks any structure associated with the vestibular apparatus that is specialized for auditory transduction. Studies find that the saccule of the vestibular apparatus is the primary auditory chamber used for sound wave transduction in most fishes. However, in other species, the lagena as well as the utricle have also been identified as contributing to auditory transduction. Regardless of the specific chamber, transduction relies on the deformation of the mechanosensitive macula (modified neuromast organs) for sound transduction. The sound waves propagated to the chamber result in the vibration of the macula at the frequency of the propagating sound waves. The mechanical stimulation of the macula from sound waves is therefore distinct from the unidirectional bending that occurs during equilibrium sensation. Thus, the macula can contribute to both vestibular and auditory sensation.

Actinopterygian fishes do not possess any specialized structures that can be associated with the middle or external ear. Instead, in the vast majority of fish species, because the bodies of vertebrates are primarily composed of water, the sound waves received by fishes are easily propagated from the surrounding water and through the body to stimulate the macula. Other mechanisms might also contribute to sound transmission in fishes. For example, in some species, the air-filled swim bladder includes extensions that directly contact the chambers of the inner ear. In other species, a chain of three to four tiny ossicles helps propagate sound waves from the swim bladder to the saccule for transduction. The role of the swim bladder in propagating sound waves could help enhance sound detection by increasing the sensitivity of the system.

Amphibia

The auditory system of amphibians is best studied in frogs (Anura) and will be the basis of this section. Additional notes will be included for hearing in the other two main amphibian lineages, salamanders (Urodela) and caecilians (Apoda).

Two distinct auditory receptors are found in the amphibian inner ear. The amphibian papilla is an auditory receptor unique to amphibians and generally common across all species of amphibians. The amphibian papilla is located in a small recess in the medial portion of the saccule. Here, a modified neuromast organ is suspended from the roof of this recess. Thus, it is the motion of the fluid moving across the suspended neuromast organ that results in the mechanical deformation of the hair cells.

The other auditory receptor found in the amphibian inner ear is the basilar papilla. The basilar papilla is not present in every amphibian species and it is possible that it independently and convergently evolved in each major amphibian lineage. In Anura the basilar papilla is also found within the saccule, but it is found within the lagena of Urodela and the utriculus of Apoda. The basilar papilla is also stationary and deforms in response to fluid movement.

The movement of the inner ear fluid occurs in response to the reception and propagation of external sound waves, but these sound waves need amplification in order to reach and then subsequently stimulate the fluid contained within the inner ear. This amplification is necessary because the fluid contained within the inner ear is of higher viscosity than the air of the surrounding terrestrial environment. The energy of the sound waves needs to be amplified in order to produce movement of the fluid of the inner ear. Thus, terrestrial vertebrates evolved additional structures to concentrate, amplify, and deliver sound waves traveling through the air to the inner ear. Tetrapods initially solve this problem by evolving the middle ear cavity. Later, in mammals and birds, the external ear also evolves to further aid in this endeavor.

The structures contained within the middle ear cavity aid in the amplification of sound from the external environment. The middle ear consists of a tympanum (also referred to as the eardrum), which is set in vibration by the reception of external sound waves. These sound waves are then transmitted from the tympanum to the inner ear by way of one or more middle ear ossicles (or bones). One middle ear ossicle common to most amniotes is the columella (or stapes). The stapes is homologous to the hyomandibula, which is a bone that first evolved in early gnathostomes and is involved in jaw suspension. In species that possess more than one middle ear ossicle, the columella is always the bone that is closest to the inner ear and the bone that is therefore responsible for the final propagation of sound waves to the middle ear. The vibrating columella is capable of initiating the movement of the fluid of the inner ear through the oval window (fenestra ovalis). The surface of the columella that initiates the movement of the inner fluid is often expanded to fit snugly into the oval window and secured via a ligament. Finally, other structures of the middle ear cavity include the eustachian tube, which is a tube that forms continuity between the cavity of the middle ear and the pharynx. Indeed, it is the presence of the eustachian tube that allows you (and other tetrapods) the ability to equalize pressure within the middle ear cavity, which is a process you might be familiar with if you have ever flown on an airplane, participated in scuba diving, or even changed elevation in a vehicle.

In amphibians, there are at least two mechanisms of sound propagation from the external environment to the inner ear. One occurs through the tympanum, which in many amphibians is directly on the outside surface of the head. The vibration of the tympanum then sets in motion the bones traversing the middle ear cavity. In amphibians, there are usually two in-series middle ear ossicles, the tympanum-facing extracolumella and oval window–facing columella. The tympanum–columella route is the primary mechanism of propagating high-frequency airborne sounds, which are primarily transduced by the basilar papilla auditory receptor. However, seismic waves, or sounds initiating from the vibration of the ground, can be delivered to the inner ear through a different mechanism. Interestingly, in amphibians, the oval window is also partly covered by a third bone, the operculum, which is not in series with the columella. A small muscle, the opercularis, is found traversing the space between the operculum and the pectoral girdle. Thus, ground-based sounds and vibrations can be transferred to the inner ear through the series consisting of the ground-facing forelimb bones, pectoral girdle, opercularis muscle, and operculum. The operculum will then transfer vibrations directly to the fluid of the inner ear. The operculum route is the primary mechanism for propagating low-frequency ground-based sounds, which are primarily transduced by the amphibian papilla sound receptor.

Amniotes

The inner ear and its connection to the middle ear cavity are generally similar across most lineages of amniotes. The middle ear cavity of amniotes is similar to that of amphibians; however, the structures associated with the middle ear do diversify across amniotes. Thus, we will introduce the general structure of the inner ear here and in the following subsections highlight key differences of the middle and inner ear that exist between major vertebrate lineages. The inner ear of amniotes is again categorized by a series of tubes within the skeleton. The skeletal tube that is typically associated with hearing is generally referred to as the cochlea (or lagena) in amniotes and is an extension from the chambers of the vestibular apparatus. Contained within the cochlea are three fluid-filled tubes separated by membranes. Two tubes found within the cochlea in amniotes are the scala vestibuli and the scala tympani, which both contain perilymph and reside adjacent to the skeleton. Sandwiched between the scala vestibuli and the scala tympani is the cochlear duct (or scala media), which is filled with endolymph. A vestibular membrane (formerly Reissner’s membrane) separates the scala media from the scala vestibuli, and the basilar membrane separates the scala media from the scala tympani. It is the basilar membrane that supports the auditory receptor, which we generally refer to as the auditory organ (formerly the Organ of Corti and still referred to as the spiral organ in some human anatomy textbooks). However, we make note of additional naming conventions specific to each vertebrate lineage below. The auditory organ is a series of neuromast organs along the length of the basilar membrane that transduces sound waves and are connected to the brain via the auditory nerve (CN VIII). One interesting difference in comparison to nonamniote vertebrates is that in amniotes, fluid movement through the cochlea results in the movement of the basilar membrane (and the subsequent stimulation of the supported neuromast organs).

The movement of the basilar membrane occurs in response to the movement of the inner ear fluids. The sound waves approaching the ear will ultimately generate the movement of the tympanum, which through a series of middle ear ossicles (ending in the columella) transmit these sound waves to the inner ear fluids through the oval window. The oval window is a window in the region of the scala vestibuli. The perilymphatic fluid within the inner ear is not compressible, and thus, the movement of the fluid through the scala vestibuli results in the subsequent downward movement of the following structures (in order): the vestibular membrane, endolymph contained within the cochlear duct, the basilar membrane, and finally, the perilymphatic fluid within the scala tympani. After the sound wave is removed from the tympanic membrane, the exact same series of events will occur in reverse. Thus, the basilar membrane will oscillate up and down at the frequency of the propagating sound waves. Because the perilymphatic fluid is not compressible, a second small region of the tube must also be mobile or elastic in order to yield to the moving perilymphatic fluid, or else the basilar membrane would not oscillate. In most amniotes, the yielding structure is the membrane covering the round window. The round window sits between the scala tympani and the middle ear cavity. The round window is covered by a thin, elastic membrane and is free to oscillate with the fluid because the middle ear cavity is hollow and filled with air. Finally, in most amniotes the hair cells of the neuromast organs along the basilar membrane (i.e., the acoustic organ) are covered by the tectorial membrane, which is firm and does not oscillate in response to inner ear fluid movement. Thus, the vibration of the basilar membrane results in the deflection of hair cells against the stationary tectorial membrane. Typically, different regions of the basilar membrane respond differently to different frequencies of sound waves resulting in the ability to discriminate between sound waves of different frequencies (tones). However, across vertebrates, several different mechanisms have evolved in order to discriminate between tones.

Nonavian Reptiles

The inner ear of most species of reptile follows the general condition of other amniotes. Here, we classify reptiles for the purpose of this section as any species of amniote that does not belong to either Aves or Mammalia. In most reptiles, the bones (or middle ear ossicles) traversing the middle ear cavity responsible for sound wave propagation between the tympanum and the oval window of the inner ear are the extracolumella and the columella (stapes). These bones are homologous and arranged in the same order as those referred to previously in the amphibian section. The inner ear of most species is consistent with the general amniotic condition. The lagena is slightly expanded in most reptilians. The reptilian acoustic organ, which likely evolved in early reptiles, is often referred to as the auditory papilla within reptiles. The auditory papilla is anchored directly to the surface of the basilar membrane found bordering the scala media (or cochlear duct). The apical surface of individual hair cells is roofed with the tectorial membrane.

Finally, the movement of fluid within the inner ear is variable across species of reptiles, as not every species has evolved a round window. Instead, in some reptilian lineages (e.g., turtles and snakes) displacement of the incompressible fluids of the inner ear are able to be mobilized due to the evolution of an open circuit where fluid flow from the scala tympani is pushed into the scala vestibuli. Thus, the same volume of fluid within the scala vestibuli displaced by the movement of the columella on the oval window is returned to the starting point from the scala tympani.

Aves

The auditory system of birds is generally similar across Aves. In birds, the primary chamber of the inner ear associated with hearing is the lagena (i.e., cochlea). In birds, the cochlea is of significantly greater length in comparison to the lineages we consider reptiles above. The cochlea of birds is also slightly curved, and this curvature is most pronounced in owls. The auditory organ is distributed along the now lengthened basilar membrane traversing through the cochlear duct. Again, the apical surface of individual hair cells is roofed with the tectorial membrane.

The middle ear cavity of birds is similar to that described in reptiles and amphibians. The two middle ear ossicles responsible for propagating sound waves between the tympanum and the oval window are again the extracolumella and the columella (stapes), which are arranged in the same order.

Birds also evolved a true external ear. In birds, the external ear, characterized as a short canal, runs from the tympanic membrane toward the external surface of the head. This canal, referred to as the external auditory meatus (but also known as the external auditory canal, external acoustic meatus/canal), is analogous to convergent evolution of the similar structure in mammals. Birds have not evolved a true outer ear, which in mammals is a skin-covered, cartilaginous structure referred to as the pinna or the auricle (usually in human anatomy). Instead, in birds, the facial feathers surrounding the opening of the external auditory meatus are sometimes raised to provide similar functionality to the mammalian pinna (discussed below).

Mammals

The mammalian inner ear is characterized by a highly elongated and (to different degrees) coiled cochlea. In mammals, this elongated and coiled chamber is almost exclusively referred to as the cochlea. In monotremes, the cochlea is only slightly coiled, and the degree of cochlear coiling ranges from one to four total coils across therian mammals. The inside of the cochlea follows the same condition described above in the introduction to hearing in amniotes. However, the number (and rows) of hair cells is significantly greater than in other vertebrate lineages, thereby increasing sensitivity and the ability to discriminate different tones. Sadly, for the humans reading this chapter, the range of tones that mammals are capable of transducing is limited in humans in comparison to many other mammalian species (especially bats and dolphins).

Mammals also evolved modification of the middle ear that contributes to their auditory sensitivity. While other tetrapods utilize the two-structure chain composed of the extracolumella and the columella to propagate sound waves from the tympanum to the oval window of the inner ear, mammals utilize three middle ear ossicles. In mammals (in order from the tympanum to the oval window), these three middle ear ossicles are the malleus, incus, and stapes. The stapes is indeed homologous to the columella of other amniotes. The malleus and incus are actually homologous to two bones that constitute the bones of the jaw joint in other vertebrates, the articular and the quadrate. Over evolutionary times, these two bones were freed from use at the jaw joint and migrated toward the middle ear cavity in mammals.

Finally, mammals also rely on an external auditory meatus that runs from the tympanum toward the external surface of the head. In addition, most mammals (all but monotremes) possess the pinna (or auricle), which is the visually noticeable external feature that humans often consider “the ear.” The pinna, which has different degrees of mobility across mammals (compare the mobility of the pinna of your pet cat to that of your own pinna in humans), functions to help direct sound into the external auditory meatus, improving the ability of an animal to localize the source of the sound.

Ear Development

As described above, development of the auditory system begins with the emergence of the otic placode. The placode formation stage is similar across all vertebrate groups, but in zebrafish no otic cup or pit forms; rather, the placode thickens into a solid sphere of cells. These cells then become polarized, with their nuclei moving to more superficial positions within the cells, and an elongated hollow cavity appears in the center of the sphere to form the lumen of the otic vesicle. This lumen then expands to quickly enlarge the otic vesicle, and the cells sink into the lumen to form the different chambers of the ear.

The ears of zebrafish, like most other fishes, also include otoliths, which develop in an interesting way. Within the otic vesicle, small seeding particles are bound by the kinocilia of early forming tether hair cells. Other cilia within the vesicle beat to move additional seeding particles around to prevent them from clumping up prematurely. When these particles contact those already bound to the tether, they aggregate, and the otoliths increase in size.

Lateral Line System

The lateral line is an aquatic mechanosensory system that allows fish and amphibians to “feel the flow” around them. Picture a bait ball of schooling silvery fish. A swordfish dives through and a hole opens up in the shimmering sphere. This interaction is mediated by the lateral line system: The baitfish school closely together without crashing into each other by utilizing their lateral line. The swordfish senses the vibrations of the bait ball in the water using its lateral line. The baitfish dodge out of the way in time thanks to their lateral line feeling the water pressure wave created by the plunging swordfish.

The sensor of the lateral line system is the neuromast organ (discussed above). Each hair cell has a single kinocilium as well as several stereocilia. As water passes over the neuromasts, their cupulas are deflected, and the hair cells embedded in the cupula are deflected with it. Because neuromasts are morphologically asymmetrical, the way that the stereocilia are deflected impacts relays directional information to the rest of the animal. In other words, the directional response of the hair cell is determined by the bending of the stereocilia toward the kinocilium, resulting in depolarization of the cell. If the stereocilia bend away from the kinocilium, it causes hyperpolarization of the cell.

Neuromasts are distributed both on the skin (superficial neuromasts) and in fluid-filled canals (canal neuromasts). These two types of neuromasts have slightly different functions. Superficial neuromasts respond to direct fluid flows. Canal neuromasts respond to water flows indirectly, instead sensing the pressure difference between the pores of the canals they sit in. Simply, superficial neuromasts are velocimeters and canal neuromasts are accelerometers. Canal neuromasts are oriented in the direction of their canal. However, superficial neuromasts can be oriented in lots of directions, but mostly they are oriented parallel or perpendicular to axes of their neighboring canals.

While the lateral line is most well known in fish, most amphibian larvae and some adult amphibians possess a lateral line system. In amphibians, neuromasts are mostly superficial, but some more basal amphibians have recessed neuromasts in canals or grooves, like the canal neuromasts seen in fish. Studies on the effects of metamorphosis on the lateral line have shown that larval neuromasts are very similar to those found in adults. They change slightly in shape (adult neuromasts are longer and more slender), which is attributed to the thickening of the epidermis during metamorphosis.

The Acousticlateralis System: The Historical Overlap Between Sound and Touch

The lateral line was originally lumped in with the acoustic system as the “acousticlateralis” system. This is because (1) they share a similar developmental pathway via dorsolateral placodes, (2) they both project to similar parts of the hindbrain, and (3) they use the same functional unit: the hair cell. Both systems respond to low frequencies, but the lateral line responds to lower frequencies of 0–200 Hz. Although they are both responding to mechanosensory stimuli, we now know they’re two separate systems thanks to physiological and morphological studies. That’s not to say that they’re not related. Some fish have portions of their lateral line adapted to sensing sound pressure. This is mediated by their close association with compressible gas cavities. If you’re interested in a thorough history of the lateral line and personal histories of leaders in the field, check out Coombs and Bleckmann, 2014; Bleckmann, 2023; and Webb, 2023.

Lateral Line Development

The lateral line system is widely distributed along the head and body of fishes and amphibians and consists of mechanosensory neuromasts and their afferent neurons. Anteriorly, the lateral line develops from anterodorsal and anteroventral lateral line placodes, through proliferation and differentiation of a combination of migratory embryonic cells and stationary progenitors. The posterior lateral line develops from separate lateral line placodes located just posterior to the otic vesicle and gives rise to a set of sensory primordial cells. This cluster of migratory cells deposits neuromasts at intervals as it moves along the body and induces overlying epidermal cells to form a ringlike pore around each neuromast. Posteriorly, the posterior lateral line placode generates a line of seven or eight neuromasts during embryonic development, while three more lateral lines form during larval development.

Electroreception

Electroreception, or the ability to sense electrical stimuli, can be separated into passive and active. Passive electroreception is when organisms detect electric fields already present in the environment, from both abiotic and biotic sources. Alternatively, active electroreception is when an organism generates and senses its own electrical fields or those generated by other actively electroreceptive organisms.

Passive Electroreception

Passively electroreceptive fish are able to sense both abiotic and biotic electric fields. Abiotic electric fields are things like the electric fields produced by the Earth’s magnetic field or even those produced by strong water currents due to water being a polar molecule. Biotic electric fields are produced by other animals, such as the electrical signal of contracting muscles or the ion imbalance between an animal’s internal and external environment. This is how hammerhead sharks, for example, can sense a stingray buried in the sand.

Electrosensory receptors, or ampullary receptors, are named for their shape. Elasmobranchs are probably the most famous passively electroreceptive animals, but 16% of fish are passively electroreceptive. Elasmobranchs have the famous ampullae of Lorenzini, first described by Lorenzini in 1678. Ampullary receptors are modified neuromasts and share many of the morphological characteristics discussed already in this section. Pores in the skin connect to an ampullary organ via jelly-filled canals, which are lined with tightly packed cells providing a high resistance barrier and stopping electrical leakage. The jelly found in the ampullae of Lorenzini is actually the most conductive naturally occurring material on Earth. The ampullary organs at the end of the canals are made up of electrically excitable sensory cells, which are “always on,” a.k.a. tonically active. These cells are constantly producing neurotransmitters, and their membrane potential differences change based on external electrical stimuli. Fish don’t have all the electric fun—some amphibians have passive electrosensory systems as well that are similar in morphology, function, development, and evolutionary origins.

Some aquatic mammals are also passively electroreceptive. Platypuses use their bills to sense electrical fields via modified mucus or serous glands. Their close cousins, the short-beaked and western long-beaked echidnas, also have electroreceptors despite being fully terrestrial. They use their electrosensory abilities when they snuffle around with their snouts underwater. Guiana dolphins are also electroreceptive. Their electroreceptive sensors are suspected to be their vibrissal crypts—the empty pores formally filled by vibrissae (whiskers) during neoteny. These crypts are similar morphologically to the ampullary organs seen in platypuses and fish. While other dolphins have similar crypts, electrical sensitivity has yet to be shown in other species.

Active Electroreception

Actively electroreceptive animals can generate their own electric fields and sense both their own and that of conspecifics. This cool sensory modality is most famous in electric fish. Strongly electric fish use powerful electric discharges to stun prey, while weakly electric fish mostly use their generated electrical fields for intraspecific communication. The electric organ of these fish is made of modified muscle cells called electrocytes. They have a smooth side, which is innervated, and a rough side, which is not, causing an unequal voltage distribution. Much like a battery, they have a positive end and a negative end, maintained by an Na⁺/K⁺ ion pump, keeping Na⁺ excluded from the cell and keeping K⁺ inside. When the nerve is stimulated, Na⁺ rushes out much faster than K⁺ rushes in, causing a sharp increase in electrical potential difference. These cells are stacked positive end to negative end (once again, think of batteries in a remote) to generate larger voltages, forming an electrical field around their body.

Weakly electric fish, like knife fish or elephant fish, generate weak electric discharges. They can create pulses of electric fields that extend around their body via variation in the arrangement of these electrocytes. They can modulate this field based on habitat, behavior, navigational need, or motivational state. Socially, they can use these fields to defend territories or advertise to mates. They sense these fields via tuberous receptors, which can sense fields up to 1 kHz. Like ampullary organs, they are named for their shape. Each tuberous receptor sits in a tuber-shaped capsule in the epidermis. At the base of the capsule sit the electrosensitive sensory cells, which are different from those in ampullary organs. These sensory cells are covered in microvilli, which are hypothesized to act as a high-pass filter for the system.

Electroreceptor Development—Ampullary Organs

Most of our current knowledge of the development of electrosensory ampullary organs in vertebrates comes from axolotls, nonteleost actinopterygians, and chondrichthyans, with little data coming from teleost fishes, since those that are known to have electroreceptors are not commonly used as developmental models. Cell lineage tracing studies have shown in all three groups mentioned previously that ampullary organs, like neuromasts, develop from the lateral line placodes but are confined to just the head. Numerous small lateral line placodes covering the head first elongate into ridges, and then ampullary organs form deep within the epidermis and then open to the surface on the lateral sides of the ridges.

20.5 Summary

You have learned how the different vertebrate sensory systems are made up of specialized structures that facilitate perception and enable animals to interact with their environment. Each of the discussed sensory systems has receptors that respond to stimuli in the environment—converting physical stimuli into neural signals, specialized anatomy to help the stimuli reach their intended receptors, and a network of neural pathways to carry the sensory neural outputs to the brain.

It’s important to remember that these specialized systems do not work in isolation—animals integrate sensory information to navigate their world. It’s easy to forget this, especially when we think of animals who are lauded as having a particularly good sense (a shark’s sense of smell or a bat’s ability to hear, for example.) While in these cases other senses may be reduced, it’s vital to think about the whole suite of sensory systems, not just the “famous” one.

The way sensory systems are integrated can also change over time. Sensory adaptation, for example, occurs when the sensitivity to a constant stimulus decreases over time. Think about entering a bakery: When you walk in, you’re initially overwhelmed with the smell of cookies and pastries, but the longer you wait in line to purchase your sweets, you will become “nose blind” to the smell, no longer noticing the aromas. Sensory systems can also experience cross-modal interactions where one sensory modality impacts another. A famous example of this is the McGurk effect, which impacts how we hear speech. When we watch someone speak, our visual cues (the speaker’s lip movements) impact our auditory perception.

Studying sensory systems across vertebrate groups gives great insight into the pressures that have driven vertebrate evolution and radiation. Sensory systems evolved as vertebrates survived by adapting to diverse ecological niches. Studying sensory system anatomy gives us insights into not only how these systems work but how they have evolved. The exploration of vertebrate sensory anatomy deepens our understanding of basic biological functions, the evolution of these systems, and the complexity of sensory system integration. We hope that after this quick tour through vertebrate sensory systems, you have learned to appreciate the intricacies that underlie the sensory experiences that allow us to interact with the world.

20.6 Further Reading

1. Aiello, Brett R., M. Saad Bhamla, Jeff Gau, John G. L. Morris, Kenji Bomar, Shashwati da Cunha, Harrison Fu, et al. “The origin of blinking in both mudskippers and tetrapods is linked to life on land.” Proceedings of the National Academy of Sciences U.S.A. 120 (2023): e2220404120.
2. Baldwin, Maude W., and Meng-Ching Ko. “Functional evolution of vertebrate sensory receptors.” Hormones and Behavior 124 (2020): 104771.
3. Oteiza, Pablo and Baldwin, Maude W. “Evolution of sensory systems” Current Opinion in Neurobiology 71 (2021): 52–59.
4. Policarpo, Maxime, et al. “Diversity and evolution of the vertebrate chemoreceptor gene repertoire.” Nature Communications 15.1 (2024): 1421.
5. Poncelet, Guillaume, and Sebastian M. Shimeld. “The evolutionary origins of the vertebrate olfactory system.” Open biology 10.12 (2020): 200330.
6. Valencia-Montoya, Wendy A., Naomi E. Pierce, and Nicholas W. Bellono. “Evolution of sensory receptors.” Annual Review of Cell and Developmental Biology 40 (2024).

20.7 References

1. Aiello, Brett R., M. Saad Bhamla, Jeff Gau, John GL Morris, Kenji Bomar, Shashwati da Cunha, Harrison Fu et al. “The origin of blinking in both mudskippers and tetrapods is linked to life on land.” Proceedings of the National Academy of Sciences U.S.A. 120 (2023): e2220404120.
2. Aiello, Brett R., Thomas A. Stewart, and Melina E. Hale. “Mechanosensation in an adipose fin.” Proceedings of the Royal Society B: Biological Sciences 283 (2016): 20152794.
3. Aiello, Brett. R., Mark W. Westneat, and Melina E. Hale. “Mechanosensation is evolutionarily tuned to locomotor mechanics.” Proceedings of the National Academy of Sciences U.S.A. 114 (2017): 4459–4464.
4. Aiello, Brett R., Adam R. Hardy, Mark W. Westneat, and Melina E. Hale (2018). “Fins as mechanosensors for movement and touch-related behaviors.” Integrative and Comparative Biology 58 (2018): 844–859.
5. Allen, Connie R. B., Lauren J. N. Brent, Thatayaone Motsentwa, and Darren P. Croft. “Field evidence supporting monitoring of chemical information on pathways by male African elephants.” Animal Behaviour 176 (2021): 193–206.
6. Arzt, Adam H., Wayne L. Silver, J. Russell Mason, and Larry Clark. “Olfactory responses of aquatic and terrestrial tiger salamanders to airborne and waterborne stimuli.” Journal of Comparative Physiology A 158 (1986): 479–487.
7. Baker, Clare V. H., Melinda S. Modrell, and J. Andrew Gillis. “The evolution and development of vertebrate lateral line electroreceptors.” Journal of Experimental Biology 216 (2013): 2515–2522.
8. Barlow, Linda A. “Progress and renewal in gustation: New insights into taste bud development.” Development 142 (2015): 3620–3629.
9. Bigiani, Albertino, Valeria Ghiaroni, and Francesca Fieni. (2003). “Channels as taste receptors in vertebrates.” Progress in Biophysics and Molecular Biology 83(2003): 193–225.
10. Bleckmann, Horst. “Life along the fish lateral line and beyond.” Journal of the Acoustical Society of America 154 (2023): 1274–1286.
11. Bodznick, David, and John C. Montgomery. “The physiology of low-frequency electrosensory systems.” In Electroreception, edited by Theodore H. Bullock, Carl D. Hopkins, Arthur N. Popper, and Richard R. Fay, pp. 132–153. New York: Springer, 2005.
12. Bradbury, J. W., and Sandra L. Vehrencamp. Principles of Animal Communication, Vol. 132. Sunderland: Sinauer Associates, 1998.
13. Bradshaw, Sarah N., and W. Ted Allison. “Hagfish to illuminate the developmental and evolutionary origins of the vertebrate retina.” Frontiers in Cell and Developmental Biology 10 (2022): 822358.
14. Bruck, Jason N., Sam F. Walmsley, and Vincent M. Janik. “Cross-modal perception of identity by sound and taste in bottlenose dolphins.” Science Advances 8 (2022): eabm7684.
15. Cao, Yanxiang, Byran C. Oh, and Lubert Stryer. “Cloning and localization of two multigene receptor families in goldfish olfactory epithelium.” Proceedings of the National Academy of Sciences U.S.A. 95 (1998): 11987–11992.
16. Catania, Kenneth C. “Underwater ‘sniffing’ by semi-aquatic mammals.” Nature 444 (2006), 1024–1025.
17. Chow, Robert L., and Richard A. Lang. “Early eye development in vertebrates.” Annual Reviews in Cell and Developmental Biology 17 (2003): 255–296.
18. Collin, H. Barry, Julian Ratcliffe, and Shaun P. Collin. “The functional anatomy of the cornea and anterior chamber in lampreys: Insights from the pouched lamprey, Geotria australis (Geotriidae, Agnatha).” Frontiers in Neuroanatomy 15 (2021): 786729.
19. Coombs, Sheryl, John Janssen, and Jacqueline F. Webb. “Diversity of lateral line systems: Evolutionary and functional considerations.” In Sensory Biology of Aquatic Animals, edited by Jelle Atema, Richard R. Fay, Arthur N. Popper, and William N. Tavolga, 553–593. New York: Springer, 1988.
20. Coombs, Sheryl, and Horst Bleckmann. “The gems of the past: A brief history of lateral line research in the context of the hearing sciences.” In The Lateral Line System, edited by Sheryl Coombs, Horst Bleckmann, Richard R. Fay, and Arthur N. Popper, 1–16. New York: Springer, 2014.
21. Cronin, Thomas W. and Bok, Michael J. “Photoreception and vision in the ultraviolet.” J Exp Biol 15 (2016); 219 (18): 2790–2801.
22. Derby, Charles D., and John Caprio. “What are olfaction and gustation, and do all animals have them?.” Chemical Senses 49 (2024): bjae009.
23. Drozdzik, Agnieszka, and Marek Drozdzik. “Oral pathology in COVID-19 and SARS-CoV-2 infection—Molecular aspects.” International Journal of Molecular Sciences 23 (2022): 1431.
24. Dusenbery, David B. Sensory Ecology: How Organisms Acquire and Respond to Information. New York: WH Freeman, 1992.
25. England, Sam J., and Daniel Robert. “The ecology of electricity and electroreception.” Biological Reviews 97 (2022): 383–413.
26. Farbman, Albert I. “Prenatal development of olfactory receptor cells.” Chemical Senses 11 (1986): 3–18.
27. Fritzsch, Bernd, Kate F. Barald, and Margaret I. Lomax. “Early embryology of the vertebrate ear.” In Development of the Auditory System, edited by Edwin W. Rubel, Arthur N. Popper, and Richard R. Fay, 80–145. New York: Springer, 1998.
28. Fritzsch, B., and K. W. Beisel. “Evolution and development of the vertebrate ear.” Brain Research Bulletin 55 (2001): 711–721.
29. Godfrey, Stephen J., Jonathan Geisler, and Erich M. Fitzgerald. “On the olfactory anatomy in an archaic whale (Protocetidae, Cetacea) and the minke whale Balaenoptera acutorostrata (Balaenopteridae, Cetacea).” Anatomical Record 296 (2013): 257–272.
30. Graw, Jochen. “Eye development.” Current Topics in Developmental Biology 90 (2010): 343–386.
31. Gruber, Samuel. “The visual system of sharks: Adaptations and capability.” American Zoologist 17 (1977): 453–469.
32. Haddon, Catherine, and Julian Lewis. “Early ear development in the embryo of the zebrafish, Danio rerio.” Journal of Comparative Neurology 365 (1996): 113–128.
33. Hale, Melina E. “Evolution of touch and proprioception of the limbs: Insights from fish and humans.” Current Opinion in Neurobiology 71 (2021) 37–43.
34. Hansen, Anne, and Eckert Zeiske. “Development of the olfactory organ in the zebrafish, Brachydanio rerio.” Journal of Comparative Neurology 333 (1993): 289–300.
35. Hansen, Anne, Klaus Reutter, and Eckert Zeiske, E. “Taste bud development in the zebrafish, Danio rerio.” Developmental Dynamics 223 (2002): 483–496.
36. Hansen, Anne, Shane H. Rolen, Karl Anderson, Yasuhiro Morita, John Caprio and Thomas E. Finger. “Correlation between olfactory receptor cell type and function in the channel catfish.” Journal of Neuroscience 23 (2003): 9328–9339.
37. Hansen, Anne, Karl T. Anderson, and Thomas E. Finger. “Differential distribution of olfactory receptor neurons in goldfish: Structural and molecular correlates.” Journal of Comparative Neurology 477 (2004): 347–359.
38. Hansen, Anne, Shane H. Rolen, Karl Anderson, Yasuhiro Morita, John Caprio and Thomas E. Finger. “Olfactory receptor neurons in fish: Structural, molecular and functional correlates.” Chemical Senses 30, Suppl. 1 (2005): i311–i311.
39. Hara, Toshiaki J. “Olfaction and gustation in fish: An overview.” Acta Physiologica Scandinavica 152 (1994): 207–217.
40. Hara, Toshiaki J., and Barbara Zielinski. “Structural and functional development of the olfactory organ in teleosts.” Transactions of the American Fisheries Society 118 (1989): 183–194.
41. Hardy, Adam R., and Melina E. Hale. “Extraoral taste buds on the paired fins of damselfishes.” Integrative Organismal Biology 4 (2022): obac035.
42. Hardy, Adam R., Bailey M. Steinworth, and Melina E. Hale. “Touch sensation by pectoral fins of the catfish Pimelodus pictus.” Proceedings of the Royal Society B: Biological Sciences 283 (2016): 20152652.
43. Holmes, William M., Ross Cotton, Viet Bui Xuan, Alex D. Rygg, Brent A. Craven, Richard L. Abel, Robert Slack, and Jonathan P. L. Cox. “Three-dimensional structure of the nasal passageway of a hagfish and its implications for olfaction.” Anatomical Record 294 (2011): 1045–1056.
44. Jungblut, Lucas D., Andre G. Pozzi, and Dante A. Paz. “Larval development and metamorphosis of the olfactory and vomeronasal organs in the toad Rhinella (Bufo) arenarum (Hensel, 1867).” Acta Zoologica 92 (2011): 305–315.
45. Kasumyan, A. O. “The olfactory system in fish: Structure, function, and role in behavior.” Journal of Ichthyology 44 (2004): S180.
46. Katreddi, Raghu R., and Paulo E. Forni. “Mechanisms underlying pre- and postnatal development of the vomeronasal organ.” Cellular and Molecular Life Sciences 78 (2021): 5069–5082.
47. Lancet, Doron. “Vertebrate olfactory reception.” Annual Review of Neuroscience 9 (1986): 329–355.
48. Lipovsek, Marcela, and Ana Belén Elgoyhen. “The evolutionary tuning of hearing.” Trends in Neurosciences 46 (2023): 110–123.
49. Mombaerts, Peter. “Genes and ligands for odorant, vomeronasal and taste receptors.” Nature Reviews Neuroscience 5 (2004): 263–278.
50. Naito, Takayuki, Yutaka Saito, Jun Yamamoto, Yuko Nozaki, Keiko Tomura, Masaaki Hazama, Shigetada Nakanishi, and Sydney Brenner. “Putative pheromone receptors related to the Ca2+-sensing receptor in Fugu.” Proceedings of the National Academy of Sciences U.S.A. 95 (1998): 5178–5181.
51. Nicholas, J. S. The reactions of Amblystoma tigrinum to olfactory stimuli. Journal of Experimental Zoology 35 (1922): 257–281.
52. Nishida, Yasutaka, Sumio Yoshie, and Tsuneo Fujita. “Oral sensory papillae, chemo-and mechano-receptors, in the snake, Elaphe quadrivirgata. A light and electron microscopic study.” Archives of Histology and Cytology 63 (2000): 55–70.
53. Northcutt, R. Glenn. “Taste buds: Development and evolution.” Brain, Behavior, and Evolution 64 (2004): 198–206.
54. Newton, Kyle C., Andrew B. Gill, and Stephen M. Kajiura. “Electroreception in marine fishes: Chondrichthyans.” Journal of Fish Biology 95 (2019): 135–154.
55. Ollivier, F. J., D. A. Samuelson, D. E. Brooks, P. A. Lewis, M. E. Kallberg, and A. M. Komáromy. “Comparative morphology of the tapetum lucidum (among selected species).” Veterinary Ophthalmology 7 (2004): 11–22.
56. Osculati, Francesco, and Andrea A. Sbarbati. “The frog taste disc: A prototype of the vertebrate gustatory organ.” Progress in Neurobiology 46 (1995): 351–399.
57. Ott, Matthias. “Visual accommodation in vertebrates: Mechanisms, physiological response and stimuli.” Journal of Comparative Physiology A 192 (2006) 97–111.
58. Russell, I. J. Amphibian lateral line receptors. Frog Neurobiology: A Handbook, edited by Rodolfo Llinás and Wolfgang Precht, 513–550. New York: Springer, 1976.
59. Ryan, Conor, Maria C. I. Martins, Kevin Healy, Lars Bejder, et al. “Morphology of nares associated with stereo-olfaction in baleen whales.” Biology Letters 20 (2024): 20230479.
60. Sapède, Dora, Nicolas Gompel, Christine Dambly-Chaudière, and Alain Ghysen. “Cell migration in the postembryonic development of the fish lateral line.” Development 129 (2002): 605–615.
61. Sato, Yuki, Nobuhiko Miyasaka, and Yoshihiro Yoshihara. “Mutually exclusive glomerular innervation by two distinct types of olfactory sensory neurons revealed in transgenic zebrafish.” Journal of Neuroscience 25 (2005): 4889–4897.
62. Schlosser, Gerhard. “A short history of nearly every sense—the evolutionary history of vertebrate sensory cell types.” Integrative and Comparative Biology 58 (2018): 301–316.
63. Simonitis, Lauren E., Miasara Andrew, Tatyana Brewer-Tinsley, Aubree Jones, Peyton Thomas, Sabrina Van Ecyk and Amani Webber-Schultz. “Fields of elasmobranch anatomy and physiology.” In Minorities in Shark Sciences: Diverse Voices in Shark Research, edited by Jasmin Graham, Camila Caceres, and Deborah Santos de Azevedo Menna, 71–116. Boca Raton: CRC Press, 2022.
64. Simonitis, Lauren E., and Christopher D. Marshall. “Microstructure of the bonnethead shark (Sphyrna tiburo) olfactory rosette.” Integrative Organismal Biology 4 (2022): obac027.
65. Simonitis, Lauren E., Aubrey E. Clark, Elizaveta Barskaya, Gabriella Castillo, Marianne Porter, and Tricia Meredith. “Getting nosy: Olfactory rosette morphology and lamellar microstructure of two chondrichthyan species.” Integrative and Comparative Biology 64, no. 2 (2024): 441–458.
66. Sinn, Rebecca, and Joachim Wittbrodt. “An eye on eye development.” Mechanisms of Development 130 (2013): 347–358.
67. Smith, C. U. M. Biology of Sensory Systems, 2nd ed. Hoboken: John Wiley & Sons, 2008.
68. Srinivasan, Mithily, and Thankham Thyvalikakath. “Oral cavity and COVID-19: Clinical manifestations, pathology, and dental profession.” In Textbook of SARS-CoV-2 and COVID-19: Epidemiology, Etiopathogenesis, Immunology, Clinical Manifestations, Treatment, Complications and Preventive Measures, edited by Subramani Mani and Jorn-Hendrik Weitkamp, 173–190. Amsterdam: Elsevier Health Sciences, 2022.
69. Stenkamp, Deborah L. “Development of the vertebrate eye and retina.” Molecular Biology and Translational Science 134 (2015): 397–414.
70. Spors, Hartwig, Dinu Florin Albeanu, Venkatesh N. Murthy, Dmitry Rinberg, Naoshige Uchida, Matt Wachowiak and Rainer W. Friedrich. “Illuminating vertebrate olfactory processing.” Journal of Neuroscience 32 (2012): 14102–14108a.
71. Torres, Miguel, and Fernando Giraldez. “The development of the vertebrate inner ear.” Mechanisms of Development 71 (1998): 5–21.
72. Thewissen, J. G. M., and Sirpa Nummela, S., Eds. Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates. Berkeley: University of California Press, 2008.
73. Thewissen, J. G. M., John George, Cheryl Rosa, and Takushi Kishida. “Olfaction and brain size in the bowhead whale (Balaena mysticetus).” Marine Mammal Science 27 (2011): 282–294.
74. Thomas, Eric D., Ivan A. Cruz, Dale W. Hailey, and David W. Raible “There and back again: Development and regeneration of the zebrafish lateral line system.” WIREs Developmental Biology 4 (2015): 1–16.
75. van Bergeijk, William A. (1967). “The evolution of vertebrate hearing.” Contributions to Sensory Physiology 2 (1967): 1–49.
76. Walls, Gordon Lynn. The Vertebrate Eye and its Adaptive Radiation. New York: Hafner Publishing Company, 1944.
77. Webb, Jacqueline F. “Structural and functional evolution of the mechanosensory lateral line system of fishes.” Journal of the Acoustical Society of America 154 (2023): 3526–3542.
78. Wever, Ernest Glen. “The evolution of vertebrate hearing.” In Auditory System: Anatomy Physiology (ear), edited by Wolf D. Keidel and William D. Neff, 423–454. New York: Springer-Verlag, 1974.
79. Wever, Ernest Glen. “Origin and evolution of the ear of vertebrates.” In Evolution of Brain and Behavior in Vertebrates, edited by R. B. Masterton, M. E. Bitterman, C. B. G. Campbell, and Nicholas Hotton, 89–105. London: Routledge, 1976.
80. Williams IV, Richard, Nicole Neubarth, and Melina E. Hale. “The function of fin rays as proprioceptive sensors in fish.” Nature Communications 4 (2013): 1729.
81. Witt, Martin, and Klaus Reutter. “Anatomy of the tongue and taste buds.” In Handbook of Olfaction and Gustation, edited by Richard L. Doty, 637–664. Hoboken: John Wiley & Sons, 2015.
82. Wyart, Claire, and Martin Carbo-Tano. “Design of mechanosensory feedback during undulatory locomotion to enhance speed and stability.” Current Opinion in Neurobiology 83 (2023): 102777.
83. Yu, Wenxin, Zhonghou Wang, Brett Marshall, Yuta Yoshida, et al. “Taste buds are not derived from neural crest in mouse, chicken, and zebrafish.” Developmental Biology 471 (2021): 76–88.
84. Zeiske, Eckert, and Anne Hansen. “Development and evolution of the olfactory organ in gnathostome fish.” In Fish Chemosenses, edited by Klaus Reutter and B. G. Kapoor, 1–29. London: Routledge, 2005.