The Retina and Vision

CHAPTER 19 The Retina and Vision The visual system is arguably the most important system through which our brain gathers information about our surroundings, and forms one of our most complex phys- iological systems. In vertebrates, light entering the eye through the lens is detected by photosensitive pigment in the photoreceptors, converted to an electrical signal, and passed back through the layers of the retina to the optic nerve, and from there, through the visual nuclei, to the visual cortex of the brain. At each stage, the signal passes through an elaborate system of biochemical and neural feedbacks, the vast majority of which are poorly, if at all, understood. Although there is great variety in detail between the eyes of different species, a number of important features are qualitatively conserved. Perhaps the most striking of these features is the ability of the visual system to adapt to background light. As the background light level increases, the sensitivity of the visual system is decreased, which allows for operation over a huge range of light levels. From a dim starlit night to a bright sunny day, the background light level varies over 10 orders of magnitude (Hood and Finkelstein, 1986), and yet our eyes continue to operate across all these levels without becoming saturated with light. The visual system accomplishes this by ensuring that its sensitivity varies approximately inversely with the background light, a relationship known as Weber’s law (Weber, 1834) and one that we discuss in detail in the next section. Because of this adaptation, the eye is more sensitive to changes in light level than to a steady input. When a space-independent pulse of light is shone on the entire eye, the retina responds with a large-amplitude signal at the beginning followed by a decrease to a lower plateau. Similarly, at the end of the pulse, a large negative transient is followed by a return to a plateau. Response to transients with adaptation in steady conditions is characteristic of inhibitory feedback, or self-inhibition, which occurs at a number 894 19: The Retina and Vision of levels in the retina. Furthermore, the retina is sensitive to particular frequencies of flashing light, with the most sensitive frequency being a function of the background light level. Adaptation is also manifested spatially. When a time-independent strip of light is applied to the retina, the response is greatest at the edges of the pattern. These response variations are known as Mach bands and are due to lateral inhibition, which plays a similar role in space as self-inhibition plays in time. For example, in the interior of a uniformly bright part of the visual field, neurons are inhibited from all sides, while regions near the edge receive little inhibition from their dimly illuminated neighbors and therefore appear brighter. The result is contour enhancement. The effect of lateral inhibition can be seen in the white intersections of Fig. 19.1. In particular, if one looks intently at one of the white intersections, the remaining intersections appear to have a gray or darkened interior, and the center of the white strips appear slightly darkened compared to their edges, because of lateral inhibition. The visual system operates on many levels, ranging from the biochemistry of the photopigments, to the cellular electrophysiology of the individual retinal cells, to the neural pathways responsible for image processing, to the large-scale structure of the visual cortex. Because of this complexity, there is still much debate over the mechanisms of adaptation, and the place where it occurs. Certainly, adaptation occurs in psy- Figure 19.1 Test pattern with which to observe the effects of self-inhibition and lateral inhibition. 19.1: Retinal Light Adaptation 895 chophysical experiments (i.e., with human subjects who report what they detect); one example of this has already been seen in Fig. 19.1. As another example, psychophysical measurement of the threshold-versus-intensity function shows Weber’s law behavior. Plots of the ratio δI/I, where δI is the brightness of the smallest detectable flash superimposed on the background I, shows that δI/I is approximately constant over a range of background light levels. Although relating these psychophysical results to specific mechanisms is not an easy task, it is clear that adaptation occurs at the very lowest level of the visual system, inside the photoreceptors themselves. Obviously, there is insufficient space here for a detailed study of all these aspects of the visual system. Here we concentrate on retinal mechanisms and omit discussion of mechanisms at the level of the visual cortex. The latter questions are better addressed in specialist books on neuroscience. For a more comprehensive view of the visual system, the reader is referred to the excellent book by Nicholls, Martin, and Wallace (1992); other discussions of visual processing can be found in Graham (1989), Blakemore (1990), Landy and Movshon (1991), and Spilmann and Werner (1990). A review of the connection between psychophysical experiments and the underlying physiology is given by Hood (1998), while an excellent earlier review of psychophysical experiments is Barlow (1972). 19.1 Retinal Light Adaptation The first stage of visual processing occurs in the retina, a structure consisting of at least five major neuronal cell types (Fig. 19.2). After entering the eye, light passes through all the cell layers of the retina before being absorbed by photosensitive pigments in the photoreceptors in the final layer of cells. (A functional reason for this arrangement is not known.) Photoreceptors come in two varieties: rods, which operate in conditions of low light, and cones, which operate in bright light conditions and detect color. In the dark, photoreceptors have a resting membrane potential of around −40 mV, and they hyperpolarize in response to light. The light response is graded, with larger light stimuli resulting in larger hyperpolarizations. Note that this is different behavior from typical neurons, in which the action potential is a depolarization and is all-or-nothing, as described in Chapter 5. Photoreceptors make connections to both horizontal cells and bipolar cells. Each horizontal cell makes connections to many photoreceptors (and, often, to bipolar cells), and is coupled to other horizontal cells by gap junctions. The bipolar cells form a more direct pathway, coupling photoreceptor responses to ganglion cells, but this is also a simplification. Amacrine cells connect only to bipolar cells and ganglion cells, and their precise function is unknown. Ganglion cells (which fire action potentials, unlike photoreceptors and horizontal cells) are the output stage of the retina and form the optic nerve. The interconnections among the retinal cells are complex and not well understood; there has been a great deal of work done on how the retina detects features such as moving edges and orientation, while ignoring much of the information presented to it. Here, we describe only the simplest models. 896 19: The Retina and Vision Figure 19.2 Schematic diagram of the layers of the retina. (Nicholls et al., 1992, Chapter 16, Fig. 14, p. 583.) 19.1: Retinal Light Adaptation 897 19.1.1 Weber’s Law and Contrast Detection One of the basic features of the retina is light adaptation, the ability to adapt to varying levels of background light. Over a wide range of light levels, the sensitivity of the retina is observed to be approximately inversely proportional to the background light level. This is an example of Weber’s law, as discussed above, and is sometimes called the Weber–Fechner law. There are three common definitions of sensitivity. It can mean psychophysical sensitivity, defined as 1/threshold, where the threshold is the minimal stimulus necessary to elicit an observable response when superimposed on a given background. Weber’s law describes the fact that in psychophysical experiments the threshold increases as the background light level increases. A second definition of sensitivity is the one used most in this chapter. In response to a small light flash, the membrane potential of a photoreceptor (or horizontal cell) first decreases and then returns to rest (recall that the voltage hyperpolarizes in response to a light flash). If V(I, I0) is the maximum deviation of the membrane potential in response to a light flash of magnitude I on a background of I0, then the peak sensitivity is ∂V S(I0) = . (19.1) ∂I I=I0 In the physiology literature (for example, Fain et al., 2001) the sensitivity is defined as the amplitude of the voltage response to a small flash divided by the intensity of the ∂V(I,I ) ( ) ≈ 0 | = flash (in units of photons per area). Since V I, I0 ∂I I I0 I, these two definitions are equivalent as long as one uses only small flashes. The third definition of sensitivity is the steady-state sensitivity.IfV0(I0) is the steady response as a function of the background light level, then the steady-state sensitivity is defined to be dV0/dI0. Light adaptation serves two fundamentally important purposes. First, it helps the retina handle the wide range of light levels in which the eye must operate. The eye functions in a range of light levels that spans about 10 log units, from a starlit night to bright sunlight. (Light intensities are typically plotted on a dimensionless logarithmic scale. For example, if I0 is a standard unit of light intensity, and the intensity of the light stimulus is I, then log( I ) = log I − log I , so that on a logarithmic scale, the unit I0 0 scale I only shifts log I ). Further, the retina is so sensitive that it can reliably detect 0 I0 as few as 20 photons, and can even, although less reliably, detect single photons.

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