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The Special Senses
LEARNING OBJECTIVES
Upon completion of this chapter, the student should be able to answer the following questions:
- 1
What is the dark current, and how does the absorption of a photon change it?
- 2
What are the synaptic pathways for the central and surround portions of the receptive field of an on-center bipolar cell? Of an off-center bipolar cell?
- 3
What are the receptive field properties of simple and complex cells in the visual cortex?
- 4
What is the frequency theory of sound encoding? Why is the place theory also required?
- 5
What are the stimuli that are normally transduced by the hair cells in the semicircular canals and otolith organs?
- 6
What are the functional consequences of the differing numbers of different receptor molecules between olfactory and gustatory receptor cells?
The evolution of vertebrates shows a trend called cephalization in which special sensory organs develop in the heads of animals, along with the corresponding development of the brain. These special sensory systems, which include the visual, auditory, vestibular, olfactory, and gustatory systems, detect and analyze light, sound, and chemical signals in the environment, as well as signal the position and movement of the head. The stimuli transduced by these systems are most familiar to humans when they provide conscious awareness of the environment, but they are equally important as the sensory basis for reflexive and subconscious behavior.
The Visual System
Vision is one of the most important special senses in humans and, along with audition, is the basis for most human communication. The visual system detects electromagnetic waves between 400 and 750 nm long as visible light, which enters the eye and affects photoreceptors in a specialized sensory epithelium, the retina.
The photoreceptors, rods and cones, can distinguish two aspects of light: its brightness (or luminance) and its wavelength (or color). Rods have high sensitivity for detecting low-light intensities but do not provide well-defined visual images, nor do they contribute to color vision. Rods operate best under conditions of reduced lighting (scotopic vision). Cones, in contrast, are not as sensitive to light as rods are and thus operate best under daylight conditions (photopic vision). Cones are responsible for high visual acuity and color vision.
The retina is an outgrowth of the thalamus. Information processing within the retina is performed by retinal neurons, and the output signals are carried to the brain by the axons of retinal ganglion cells in the optic nerves. There is a partial crossing of these axons in the optic chiasm that causes all input from one side of the visual space to pass to the opposite side of the brain. Posterior to the optic chiasm, the axons of retinal ganglion cells form the optic tracts and synapse in nuclei of the brain. The main visual pathway in humans targets the lateral geniculate nucleus (LGN) of the thalamus and this nucleus, in turn, projects the visual information to the visual cortex. Other visual pathways project to the superior colliculus, pretectum, and hypothalamus, structures that participate in orientation of the eyes, control of pupil size, and circadian rhythms, respectively.
Structure of the Eye
The wall of the eye is composed of three concentric layers ( Fig. 8.1 ). The outer layer, or the fibrous coat, includes the transparent cornea, with its epithelium, and the opaque sclera. The middle layer, or vascular coat, includes the iris and the choroid. The iris contains both radially and circularly oriented smooth muscle fibers, which make up the pupillary dilator and constrictor muscles, respectively. The choroid is rich in blood vessels that support the outer layers of the retina, and it also contains pigment. The innermost layer of the eye, the retina, is embryologically derived from the diencephalon and therefore is part of the central nervous system (CNS). The functional part of the retina covers the entire posterior aspect of the eye except for the optic nerve head, or optic disc, which is where the optic nerve axons leave the retina. Because there are no receptors at this location, it is often referred to as the anatomical “blind spot” (see Fig. 8.1 ).
A number of functions of the eyes are under muscular control. Externally attached extraocular muscles aim the eyes toward an appropriate visual target (see Chapter 9 ). These muscles are innervated by the oculomotor nerve (cranial nerve [CN] III), the trochlear nerve (CN IV), and the abducens nerve (CN VI). Several muscles are also found within the eye (intraocular muscles). The muscles in the ciliary body control lens shape and thereby the focus of images on the retina. The pupillary dilator and sphincter muscles in the iris control the amount of light entering the eye, in a way similar to that of the diaphragm of a camera. The dilator is activated by the sympathetic nervous system, whereas the sphincter and ciliary muscles are controlled by the parasympathetic nervous system (through the oculomotor nerve; see Chapter 11 ).
Light enters the eye through the cornea and passes through a series of transparent fluids and structures that are collectively called the dioptric media. These fluids and structures consist of the cornea, aqueous humor, lens, and vitreous humor (see Fig. 8.1 ). The aqueous humor (located in the anterior and posterior chambers ) and the vitreous humor (located in the space behind the lens) help maintain the shape of the eye.
Although the geometrical optic axis of the human eye passes through the nodal point of the lens and reaches the retina at a point between the fovea and the optic disc (see Fig. 8.1 ), the eyes are oriented by the oculomotor system to a point, called the fixation point, on the visual target. Light from the fixation point passes through the nodal point of the lens and is focused on the fovea. Light from the remainder of the visual target falls on the retina surrounding the fovea.
Normally, light from a visual target is focused sharply on the retina by the cornea and lens, which bend or refract the light. The cornea is the major refractive element of the eye, with a refractive power of 43 diopters a
a A diopter is a unit of measurement of optical power that is equal to the reciprocal of the focal length measured in meters. Thus it is a unit of reciprocal length, and a 2-D lens would bring parallel rays of light into focus at a distance of 0.5 m.
(D). However, unlike the cornea, the lens can change shape and vary its refractive power between 13 and 26 D, thereby giving the lens the ability to adjust optical focus of the eye. Suspensory ligaments (or zonule fibers ) attach to the wall of the eye at the ciliary body (see Fig. 8.1 ) and hold the lens in place. When the muscles in the ciliary body are relaxed, the tension exerted by the suspensory ligaments flattens the lens. When the ciliary muscles contract, the tension on the suspensory ligaments is reduced; this process allows the somewhat elastic lens to assume a more spherical shape. The ciliary muscles are activated by the parasympathetic nervous system via the oculomotor nerve.
In this way, the lens allows the eye to focus on, or accommodate to, either near or distant objects. For instance, when light from a distant visual target enters a normal eye (one with a relaxed ciliary muscle), the target image is in focus on the retina. However, if the eye is directed at a nearby visual target, the light is initially focused behind the retina (i.e., the image at the retina is blurred) until accommodation occurs; that is, until the ciliary muscle contracts, causing the lens to become more spherical, the increased convexity causes the lens to refract the light waves more strongly, bringing the image into focus on the retina.
Proper imaging of light on the retina depends not only on the lens and cornea but also on the iris, which adjusts the amount of light that can enter the eye through the pupil. In this regard, the pupil is analogous to the aperture in a camera, which also controls the depth of field of the image and the amount of spherical aberration produced by the lens. When the pupil is constricted, the depth of field is increased, and the light is directed through the central part of the lens, where spherical aberration is minimal. Pupillary constriction occurs reflexively when the eye accommodates for near vision or adapts to bright light, or both. Thus, when a person reads or does other fine visual work, the quality of the image is improved by adequate light.
IN THE CLINIC
As an individual ages, the elasticity of the lens gradually declines. As a result, accommodation of the lens for near vision becomes progressively less effective, a condition called presbyopia. A young person can change the power of the lens by as much as 14 D. However, by the time that a person reaches 40 years of age, the amount of accommodation halves, and after 50 years it can decrease to 2 D or less. Presbyopia can be corrected by convex lenses.
Defects in focus can also be caused by a discrepancy between the size of the eye and the refractive power of the dioptric media. For example, in myopia (near-sightedness), the images of distant objects are focused in front of the retina. Concave lenses correct this problem. Conversely, in hypermetropia (far-sightedness), the images of distant objects are focused behind the retina; this problem can be corrected with convex lenses. In astigmatism, an asymmetry exists in the radii of curvature of different meridians of the cornea or lens (or sometimes of the retina). Astigmatism can often be corrected with lenses that possess complementary radii of curvature.
Retina
Layers of the Retina
The 10 layers of the retina are shown in Fig. 8.2 . The outermost portion is the pigmented epithelium (layer 1), which is just inside the choroid. The pigment cells have tentacle-like processes that extend into the photoreceptor layer (layer 2) and surround the outer segments of the rods and cones. These processes prevent transverse scatter of light between photoreceptors. In addition, they serve a mechanical function in maintaining contact between layers 1 and 2 so that the pigmented epithelium can (1) provide nutrients and remove waste from the photoreceptors; (2) phagocytose the ends of the outer segments of the rods, which are continuously shed; and (3) reconvert metabolized visual pigment into a form that can be reused after it is transported back to the photoreceptors.
Retinal glial cells, known as Müller cells, play an important role in maintaining the internal geometry of the retina. Müller cells are oriented radially, parallel to the light path through the retina. The outer ends of Müller cells form tight junctions with the inner segments of the photoreceptors, and these numerous connections have the appearance of a continuous layer, the outer limiting membrane (layer 3 of the retina).
IN THE CLINIC
The junction between layers 1 and 2 of the retina in adults represents the surface of contact between the anterior and posterior walls of the embryonic optic cup during development and is structurally weak. Retinal detachment is the separation at this surface and can cause loss of vision, because there is displacement of the retina from the focal plane of the eye. It can also lead to the death of photoreceptor cells, which are maintained by the blood supply of the choroid (the photoreceptor layer itself is avascular). Deterioration of the pigmented epithelium can also result in macular degeneration, a critical loss of high-acuity central and color vision that does not affect peripheral vision.
Inside the external limiting membrane is the outer nuclear layer (layer 4) that contains the cell bodies and nuclei of the rods and cones. The outer plexiform layer (layer 5) contains synapses between the photoreceptors and retinal interneurons, including bipolar cells and horizontal cells, whose cell bodies are found in the inner nuclear layer (layer 6). This layer also contains the cell bodies of other retinal interneurons (the amacrine and interplexiform cells) and the Müller cells.
The inner plexiform layer (layer 7) contains synapses between the retinal neurons of the inner nuclear layer, including the bipolar and amacrine cells, and the ganglion cells, whose cell bodies lie in the ganglion cell layer (layer 8).As previously mentioned, the ganglion cells are the output cells of the retina; it is their axons that transmit visual information to the brain. These axons form the optic fiber layer (layer 9), pass along the inner surface of the retina while avoiding the fovea, and enter the optic disc, where they leave the eye as the optic nerve. The portions of the ganglion cell axons that are in the optic fiber layer remain unmyelinated, but they become myelinated after they reach the optic disc. The lack of myelin where the axons cross the retina helps permit light to pass through the inner retina with minimal distortion.
The innermost layer of the retina is the inner limiting membrane (layer 10) formed by the end-feet of Müller cells.
Structure of Photoreceptors: Rods and Cones
Each rod or cone photoreceptor cell is composed of a cell body (in layer 4), an inner and an outer segment that extend into layer 2, and a set of synaptic terminals that synapse in layer 5 onto other retinal cells ( Fig. 8.3 ). The outer segments of cones are not as long as those of rods, and they contain stacks of disc membranes formed by infoldings of the plasma membrane. The outer segments of rods are longer, and they contain stacks of membrane discs that float freely in the outer segment, having completely disconnected from the plasma membrane when formed at the base. Both sets of discs are rich in visual pigment molecules, but rods have a greater visual pigment density, which partly accounts for their greater sensitivity to light. A single photon can elicit a rod response, whereas several hundred photons may be required for a cone response.
The outer segments of the photoreceptors are connected by a modified cilium to the inner segments, which contain a number of organelles, including numerous mitochondria. The inner segments are the sites where the visual pigment is synthesized before it is incorporated into the membranes of the outer segment. In rods, the pigment is inserted into new membranous discs, which are then displaced distally until they are eventually shed at the apex of the outer segment, where they undergo phagocytosis by cells of the pigmented epithelium. This process determines the rod-like shape of the outer segments of rods. In cones, the visual pigment is inserted randomly into the membranous folds of the outer segment, and shedding, comparable to that seen in rods, does not take place.
Regional Variations in the Retina
The macula lutea is the area of central vision and is characterized by a slight thickening and a pale color. The thickness is due to the high concentration of photoreceptors and interneurons, which are needed for high-resolution vision. It is pale because both optic nerve fibers and blood vessels are routed around it.
The fovea, which is a depression in the macula lutea, is the region of the retina with the very highest visual resolution and, as noted previously, the light from the fixation point is focused on the fovea. (A major function of eye movements is to bring objects of interest into view on the fovea.) The retinal layers in the foveal region are unusual because several of them appear to be pushed aside into the surrounding macula. Consequently, light can reach the fovealphotoreceptors without having to pass through the inner layers of the retina, and both image distortion and light loss are minimized. The fovea has cones with unusually long and thin outer segments, which allows for high packing density. In fact, cone density is maximal in the fovea, providing for high visual resolution, as well as high quality of the image ( Fig. 8.4 ).
The optic disc, where ganglion cell axons leave the retina, lacks photoreceptors and therefore lacks photosensitivity. This area is a so-called blind spot in the visual surface of the retina (see Figs. 8.4 and 8.9 ). A person is normally unaware of the blind spot because the corresponding part of the visual field can be seen by the contralateral eye and because of the psychological process in which incomplete visual images tend to be completed perceptually.
IN THE CLINIC
As mentioned, the axons of retinal ganglion cells cross the retina in the optic fiber layer (layer 9) to enter the optic nerve at the optic disc. These axons in the optic fiber layer pass around the macula and fovea, as do the blood vessels that supply the inner layers of the retina. The optic disc can be visualized on physical examination with an ophthalmoscope. The normal optic disc has a slight depression in its center. Changes in the appearance of the optic disc are important clinically. For example, the depression may be exaggerated by loss of ganglion cell axons (optic atrophy), or the optic disc may protrude into the vitreous space because of edema (papilledema) that results from increased intracranial pressure.
Visual Transduction
To be detected by the retina, light energy must be absorbed. This is primarily the responsibility of the rods and cones (a small class of ganglion cells are also photosensitive), and is primarily accomplished by visual pigment molecules located in their outer segments. For both rods and cones, the pigment molecule consists of a chromophore, 11- cis retinal, bound to an opsin protein. The visual pigment found in the outer segments of rods is rhodopsin, or visual purple (so named because it has a purple appearance when light has been absorbed). It absorbs light best at a wavelength of 500 nm. Three variants of visual pigment, resulting from the binding of different opsins to retinal, are found in cones (in most species, each cone expresses one of the three cone pigments). The cone pigments absorb best at 419 nm (blue), at 533 nm (green), and at 564 nm (red). However, the absorption spectrum of these visual pigments is broad, so that they overlap considerably ( Fig. 8.5 ).
Despite the differences in spectral sensitivity, the transduction process is similar in rods and cones. The absorption of a photon by a visual pigment molecule leads to the isomerization of 11- cis retinal to all- trans retinal, release of the bond with the opsin, and conversion of retinal to retinol. These changes trigger a second-messenger cascade that leads to a change in the electrical activity of the rod or cone (discussed later in this section).
The separation of all- trans retinal from opsin also causes both the loss of its ability to absorb light and bleaching (i.e., the visual pigment loses its color). In both rods and cones, regeneration of the visual pigment molecule is a multistep process: the all- trans retinal is transported to the retinal pigmented cell layer, where it is reduced to retinol, isomerized, and esterified back to 11- cis retinal. It is then transported back to the photoreceptor layer, taken up by outer segments, and recombined with opsin to regenerate the visual pigment molecule, which can again absorb light. There is evidence that cones also use a second pathway to regenerate visual pigment. This pathway is much more rapid and involves transport of the retinal molecule to and from the Müller cells (see Fig. 8.2 ), rather than the pigmented epithelial cells. The potential importance of this more rapid pathway is discussed later in this chapter in the section “Visual Adaptation.”
Ultimately, the transduction process triggered by absorption of photons causes the photoreceptor to hyperpolarize. To understand this action and its consequences fully, it is necessary to know the baseline state of the photoreceptor in the dark (i.e., before it absorbs a photon). In darkness, photoreceptors are slightly depolarized (≈−40 mV) in relation to most neurons because cyclic guanosine monophosphate (cGMP)-gated cation channels in their outer segments are open ( Fig. 8.6 A ). These channels allow a steady influx of Na + and Ca ++ . The resulting current is known as the dark current, and the depolarization it causes leads to the tonic release of the neurotransmitter glutamate at the photoreceptor’s synapses.
When light is absorbed in a rod (an equivalent sequence happens in cones), photoisomerization of rhodopsin activates a G protein called transducin (see Fig. 8.6 B ). This G protein, in turn, activates cyclic guanosine monophosphate (cGMP) phosphodiesterase, which is associated with the rhodopsin-containing discs, hydrolyzes cGMP to 5′-GMP, and lowers the cGMP concentration in the rod cytoplasm. The reduction in cGMP leads to closing of the cGMP-gated cation channels, hyperpolarization of the rod cell membrane, and a reduction in the release of neurotransmitters. Thus, cGMP acts as a “second messenger” to translate the absorption of a photon by rhodopsin into a change in membrane potential.
In sum, in all photoreceptors (cones undergo a process analogous to that described for rod transduction), capture of light energy leads to (1) hyperpolarization of the photoreceptor and (2) a reduction in the release of neurotransmitters. Because of the very short distance between the site of transduction and the synapse, the modulation of neurotransmitter release is accomplished without the generation of an action potential.
AT THE CELLULAR LEVEL
Rhodopsin contains a chromophore called retinal, which is the aldehyde of retinol, or vitamin A. Retinol is derived from carotenoids, such as β-carotene, the orange pigment found in carrots. Like other vitamins, retinol cannot be synthesized by humans; instead, it is derived from food sources. Individuals with a severe vitamin A deficiency suffer from “night blindness,” a condition in which vision is defective in low-light situations.
The extraordinary sensitivity of rods, which can signal the capture of a single photon, is enhanced by an amplification mechanism in which photoactivation of only one rhodopsin molecule can activate hundreds of transducin molecules. In addition, each phosphodiesterase molecule hydrolyzes thousands of cGMP molecules per second. Similar events occur in cones, but the membrane hyperpolarization occurs much more quickly than in rods and requires thousands of photons.
Visual Adaptation
Adaptation refers to the ability of the retina to adjust its sensitivity according to ambient light. This ability allows the retina to operate efficiently over a wide range of lighting conditions, and it reflects a switching between the use of the cone and rod systems for bright- and low-light conditions, respectively.
Light Adaptation
As described previously, absorption of a photon causes 11- cis retinal to be converted to all- trans retinal, which then splits from the opsin (bleaching). The visual pigments in rods and cones are bleached at a similar rate; however, regeneration of the visual pigment occurs much more rapidly in cones than in rods. This difference is, at least in part, due to the cones’ ability to utilize a second pathway for regeneration (see previous section). This more rapid regeneration of visual pigment prevents cones from becoming unresponsive in bright-light conditions. In contrast, the slowness of the regeneration of rhodopsin molecules means that at light levels not much above those found in evening hours, essentially all of the rhodopsin molecules are bleached. Thus, in bright-light conditions, only the cone system is functioning, and the retina is said to be light-adapted.
When entering a darkened movie theater, a person can observe evidence of the existing light adaptation (decreased light sensitivity in association with the reduced amount of rhodopsin) in the inability to see the empty seats (or much else). The gradual return of the ability to see the seats while the person remains in the theater reflects the slow regeneration of rhodopsin and recovery of function of the rod system, a process known as dark adaptation.
Dark Adaptation
This process refers to the gradual increase in light sensitivity of the retina when in low-light conditions. Rods adapt to darkness slowly as their rhodopsin levels are restored, and indeed, it may take more than 30 minutes for the retina to become fully dark-adapted. In contrast, cones adapt rapidly to darkness, but their adapted threshold is relatively high, so they do not function when the ambient light level is low. Within 10 minutes in a dark room, rod vision is more sensitive than cone vision and becomes the main system for seeing.
In sum, in the dark-adapted state, primarily rod vision is operative, and thus visual acuity is low and colors are not distinguished (this is called scotopic vision ). However, when light levels are higher (e.g., when the movie is projected) and cone function resumes (this is called photopic vision ), visual acuity and color vision are restored. There is an intermediate range of light levels at which rod and cones are both functional (mesopic vision).
Color Vision
The visual pigments in the cone outer segments contain different opsins. As a result of these differences, the three types of cones absorb light best at different wavelengths. Although the cone pigments have maximum efficiency closer to violet, green, and yellow wavelengths, they are referred to as blue, green, and red pigments, respectively (see Fig. 8.5 ). The differences in the cone absorption spectra underlie humans’ ability to see colors, as opposed to only shades of gray.
According to the trichromacy theory, the differences in absorption efficiency of the cone visual pigments are presumed to account for color vision because a suitable mixture of three colors can produce any other color. However, a neural mechanism must also exist for the analysis of color brightness because the amount of light absorbed by a visual pigment, as well as the subsequent response of the cell, depends on both the wavelength and the intensity of the light (see Fig. 8.5 ). Two or three of the cone pigments may absorb a particular wavelength of light, but the amount absorbed by each differs according to its efficiency at that wavelength. If the intensity of the light is increased (or decreased), all will absorb more (or less), but the ratio of absorption among them will remain constant. Consequently, there must be a neural mechanism to compare the absorption of light of different wavelengths by the different types of cones for the visual system to distinguish different colors. At least two different kinds of cones are required for color vision. The presence of three kinds decreases the ambiguity in distinguishing colors when all three absorb light, and it ensures that at least two types of cones will absorb most wavelengths of visible light.
The opponent process theory is based on observations that certain pairs of colors seem to activate opposing neural processes. Green and red are opposed, as are yellow and blue, as well as black and white. For example, if a gray area is surrounded by a green ring, the gray area appears to acquire a reddish color. Furthermore, a greenish red or a bluish yellow color does not exist. These observations are supported by findings that neurons activated by green wavelengths are inhibited by red wavelengths. Similarly, neurons excited by blue wavelengths may be inhibited by yellow wavelengths. Neurons with these characteristics are present both in the retina and at higher levels of the visual pathway and seem to serve to increase the ability to see the contrast between opposing colors.
Retinal Circuitry
A diagram of the basic circuitry of the retina is shown in Fig. 8.7 . Several features of this circuitry are noteworthy: (1) Input to the retina is provided by light striking the photoreceptors. (2) The output is carried by axons of the retinal ganglion cells to the brain. (3) Information is processed within the retina by the interneurons. (4) The most direct pathway through the retina is from a photoreceptor to a bipolar cell and then to a ganglion cell (see Fig. 8.7 ). (5) More indirect pathways that provide for intraretinal signal processing involve photoreceptors, bipolar cells, amacrine cells, and ganglion cells, as well as horizontal cells to provide lateral interactions between adjacent pathways.
IN THE CLINIC
Observations of color blindness are consistent with the trichromacy theory. In color blindness, a genetic defect (sex-linked recessive), one or more cone mechanisms are lost. People with normal color vision are trichromats because they have three cone mechanisms. Individuals who lack one of the cone mechanisms are called dichromats. When the long-wavelength cone mechanism is absent, the resulting condition is called protanopia; absence of the medium-wavelength system causes deuteranopia; and absence of the short-wavelength system causes tritanopia. Monochromats lack two or more cone mechanisms.
Contrasts in Rod and Cone Pathway Functions
Rod and cone pathways have several important functional differences in their phototransduction mechanisms and their retinal circuitry. As described previously, rods have more visual pigment and a better signal amplification system than cones do, and there are many more rods than cones. As a consequence, rods function better in dim light (scotopic vision), and loss of rod function results in night blindness. In addition, all rods contain the same visual pigment, so they cannot signal color differences. Furthermore, many rods converge onto individual bipolar cells and the results are very large receptive fields and low spatial resolution. Finally, in bright light, most rhodopsin is bleached, so that rods no longer function under photopic conditions.
Cones have a higher threshold to light and thus are not activated in dim light after dark adaptation. However, they operate very well in daylight. They provide high-resolution vision because only a few cones converge onto individual bipolar cells in cone pathways. Moreover, no convergence occurs in the fovea, where the cones make one-to-one connections to bipolar cells. As a result of the reduced convergence, cone pathways have very small receptive fields and can resolve stimuli that originate from sources very close to each other. Cones also respond to sequential stimuli with good temporal resolution. Finally, cones have three different visual pigments and therefore provide for color vision. Loss of cone function results in functional blindness; rod vision is not sufficient for normal visual requirements.
Synaptic Interactions and Receptive Field Organization
The receptive field of an individual photoreceptor is circular. Light in the receptive field hyperpolarizes the photoreceptor cell and causes it to release less neurotransmitter. The receptive fields of photoreceptors and retinal interneurons determine the receptive fields of the retinal ganglion cells onto which their activity converges. The characteristics of the receptive fields of retinal ganglion cells constitute an important step in visual information processing because all the information about visual events that is conveyed to the brain is contained in ganglion cell activity.
The bipolar cell, which receives input from a photoreceptor, can have either of two types of receptive fields, as shown in Fig. 8.8 . Both are described as having a center-surround organization in which the light that strikes the central region of the receptive field either excites or inhibits the cell, whereas the light that strikes a region that surrounds the central portion has the converse effect. The receptive field with a centrally located excitatory region surrounded by an inhibitory annulus is called an on-center, off-surround receptive field (see Fig. 8.8 A ). Bipolar cells with such a receptive field are described as “on” bipolar cells. The other type of receptive field has an off-center, on-surround arrangement, which characterizes “off” bipolar cells (see Fig. 8.8 F ).
The center response of a bipolar cell receptive field is due to only the photoreceptors that directly synapse with the bipolar cell. Photoreceptor cells respond to light with hyperpolarization and a decrease in glutamate release and respond to the removal of light with depolarization and increased glutamate release. This implies that the difference in the center responses of “on” and “off” bipolar cells lies in their response to glutamate. In fact, off-center bipolar cells have ionotropic glutamate receptor channels that open in response to glutamate, and thus they are excited by the removal of light stimuli from the center of their receptive field. In contrast, on-center bipolar cells have metabotropic glutamate receptors that close their channels in response to glutamate. They are depolarized by light on the center of their receptive field, because the reduced release of glutamate by the photoreceptors results in more open metabotropic channels. Thus, on-center bipolar cells are excited by light stimulation of the center of their receptive fields.
The antagonistic surround response of bipolar cells is due to photoreceptors that surround those that synapse directly on them. These photoreceptors (which also connect directly with their own bipolar cells) synapse with horizontal cells that participate in complex triadic synapses with many photoreceptors and bipolar cells. The pathway through the horizontal cells results in a response that is opposite in sign to that produced directly by the photoreceptors that mediate the center response. The reason for this is that horizontal cells are depolarized by glutamate released from photoreceptors and thus, like “off” bipolar cells, are hyperpolarized in the light. Moreover, because they are electrically coupled to each other by gap junctions, they have very large receptive fields. Darkness in the periphery of a bipolar cell’s receptive field (such as an annulus that does not affect the photoreceptors to which it is directly connected) causes neighboring photoreceptors and horizontal cells to depolarize. The depolarized horizontal cells release GABA onto central (and peripheral) photoreceptor terminals, reducing their release of glutamate. When darkness surrounds central illumination, there is increased excitation of on-center bipolar cells. There is a complementary effect on off-center bipolar cells when a bright annulus surrounds a central dark spot (see Fig. 8.8 ).
Bipolar cells may not respond to large or diffuse areas of illumination, covering both the receptors that are responsible for the center response and those that cause the surround response because of their opposing actions. Thus, bipolar cells may not signal changes in the intensity of light that strikes a large area of the retina. On the other hand, a small spot of light moving across the receptive field may sequentially alter the activity of the bipolar cell as the light crosses the receptive field from the surround portion to the center and then back again to the surround portion. This demonstrates that bipolar cells respond best to the local contrast of stimuli and function as contrast detectors.
Amacrine cells receive input from different combinations of on-center and off-center bipolar cells, so that Thus their receptive fields are mixtures of on-center and off-center regions. There are many different types of amacrine cells, and they may use at least eight different neurotransmitters. Accordingly, the contributions of amacrine cells to visual processing are complex.
Ganglion cells may receive dominant input from bipolar cells, dominant input from amacrine cells, or mixed input from amacrine and bipolar cells. When amacrine cell input dominates, the receptive fields of ganglion cells tend to be diffuse, and they are either excitatory or inhibitory. Most ganglion cells, however, are dominated by bipolar cell input and have a center-surround organization, similar to that of the bipolar cells that connect to them (see Fig. 8.8 ).
The distances between retinal components are short. Hence, modulation of transmitter release by changes in transmembrane potential and the resulting postsynaptic potentials are sufficient for most of the activity in retinal circuits, and action potentials are not required except for ganglion cells and some amacrine cells, which generate action potentials. It is unclear why amacrine cells have action potentials, but ganglion cells must generate them to transmit information over the relatively long distance from the retina to the brain.
P, M, and W Cells
Experiments have shown that in primates, retinal ganglion cells can be subdivided into three general types called P cells, M cells, and W cells. P and M cells are fairly homogeneous groups, whereas W cells are heterogeneous. P cells are so named because they project to the parvocellular layers of the LGN of the thalamus, whereas M cells project to the magnocellular layers of the LGN. P and M cells have center-surround receptive fields, consistent with being controlled by bipolar cells. W cells have large, diffuse receptive fields and slowly conducting axons. They are probably influenced chiefly through amacrine cell pathways, but less is known about them than about M and P cells.
Several of the physiological differences among these cell types correspond to morphological differences ( Table 8.1 ). For example, P cells have small receptive fields (which corresponds to smaller dendritic trees) and more slowly conducting axons than M cells. In addition, P cells show a linear response in their receptive field; that is, they respond with a sustained, tonic discharge of action potentials in response to maintained light, but do not signal shifts in the pattern of illumination as long as the overall level of illumination is constant. Thus, a small object entering a P cell’s central receptive field will change the cell’s firing, but continued object movement within the field will not be signaled. P cells respond differently to different wavelengths of light. Because there are blue, green, and red cones, many combinations of color properties are possible, but in fact, P cells have been shown to have opposing responses only to red and green or only to blue and yellow (a combination of red and green). These mechanisms can greatly reduce the ambiguity of color detection caused by the overlap in cone color sensitivity and may provide a substrate for the opponency process observations.
TABLE 8.1
Properties of Retinal Ganglion Cells
| Properties | P Cells | M Cells | W Cells |
|---|---|---|---|
| Cell body and axon | Medium sized | Large | Small |
| Dendritic tree | Restricted | Extensive | Extensive |
| Receptive field | |||
| Size | Small | Medium | Large |
| Organization | Center-surround | Center-surround | Diffuse Poorly responsive |
| Adaptation | Tonic | Phasic | |
| Linearity | Linear | Nonlinear | |
| Wavelength | Sensitive | Insensitive | Insensitive |
| Luminance | Insensitive | Sensitive | Sensitive |
M cells, on the other hand, respond with phasic bursts of action potentials to the redistribution of light, such as would be caused by the movement of an object within their large receptive fields. M cells are not sensitive to differences in wavelength, but are more sensitive to luminance than P cells are.
In summary, the output of the retina consists primarily of ganglion cell axons from (1) sustained, linear P cells with small receptive fields that convey information about color, form, and fine details and (2) phasic, nonlinear M cells with larger receptive fields that convey information about illumination and movement. Both exist in on-center and off-center varieties ( Fig. 8.8 ).
The Visual Pathway
Retinal ganglion cells transmit information to the brain by way of the optic nerve, optic chiasm, and optic tract. Fig. 8.9 shows the relationships among a visual target, the retinal images of the target in the two eyes, and the projections of retinal ganglion cells to the two hemispheres of the brain. The eyes and the optic nerves, chiasm, and tract are viewed from above.
The visual target, an arrow, is in the visual fields of both eyes (see Fig. 8.9 ) and, in this case, is so long that it extends into the monocular segments of each retina (i.e., one end of the target can be seen by only one eye and the other end by only the other eye). The shaded circle at the center of the target represents the fixation point. The image of the target on the retinas is reversed by the lens system. The left half of the visual target is imaged on the nasal retina of the left eye and the temporal retina of the right eye; the left visual field is seen by the left nasal retina and the right temporal retina. Similarly, the right half of the visual target is imaged on and seen by the left temporal retina and the right nasal retina. The lens system also causes an inversion in the vertical axis, with the upper visual field imaged on the lower retina and vice versa.
The axons of retinal ganglion cells may or may not cross in the optic chiasm, depending on the location of the ganglion cell in the retina (see Fig. 8.9 ). Axons from the temporal portion of each retina pass through the optic nerve, the lateral side of the optic chiasm, and the ipsilateral optic tract and terminate ipsilaterally in the brain. Axons from the nasal portion of each retina pass through the optic nerve, cross to the opposite side in the optic chiasm, and then pass through the contralateral optic tract to end in the contralateral side of the brain. As a result of this arrangement, objects in the left field of vision are represented in the right side of the brain, and those in the right field of vision are represented in the left side of the brain.
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