Gcl

Figure 17.1. Radial section through monkey retina about 5 mm (~25°) from the fovea. The synaptic layers span only 60 mm. Cone and rod inner segments are easily distinguished from each other, as are their terminals in the outer plexiform layer. Pigmented cells of the choroid layer (Ch) convert vitamin A to its photoactive form and return it to the outer segments. Pigmented cells also phagocytose membrane discs that are shed daily from the outer segment tips. OS, outer segment; IS, inner segment; ONL, outer nuclear layer; CT, cone terminal; RT, rod terminal; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer; B, bipolar cell; M, Müller cell; H, horizontal cell; A, amacrine cell; ME, Müller end feet; GON and GOFF, ganglion cells. (Light micrograph by N. Vardi; modified from Sterling, 1998.)

Figure 17.2. The basic circuits that relay rod and cone signals through the retina to ganglion cells are known. Cone signals modulate ON and OFF cone bipolar cells (CB) that excite ON and OFF ganglion cells (GC). Rod signals modulate cone terminals via electrical synapse and relay single-photon signals via a private rod bipolar cell (RB) that excites the AII amacrine cell. The AII is bifunctional, inhibiting the OFF ganglion cell with glycine and exciting the ON ganglion cell via electrical synapse to the ON bipolar terminal. IPL, inner plexiform layer. (Modified from Sterling, 1998.)

Figure 17.2. The basic circuits that relay rod and cone signals through the retina to ganglion cells are known. Cone signals modulate ON and OFF cone bipolar cells (CB) that excite ON and OFF ganglion cells (GC). Rod signals modulate cone terminals via electrical synapse and relay single-photon signals via a private rod has clearly hit the wall. And where several physical constraints conflict, neural design must reflect their compromise. In short, where actual performance approaches "ideal" performance calculated from physical limits, there is a genuine opportunity to address the "why" of a design. Although for most brain regions this is a distant goal, for mammalian retina such questions can now be addressed, and they provide the framework for this overview.

Consider that in nature the visual system operates near threshold. This is easily forgotten living under artificially bright light and viewing mostly high-contrast images, such as newsprint or the computer screen. But go bird watching or hunting (heaven forbid!), and you are quickly reminded that our ancestors strained to see the finest detail at the lowest contrast in the poorest light. To maximize sensitivity their eyes were selected to make each stage—from the optical image to the ganglion cell spike train—as efficient bipolar cell (RB) that excites the AII amacrine cell. The AII is bifunctional, inhibiting the OFF ganglion cell with glycine and exciting the ON ganglion cell via electrical synapse to the ON bipolar terminal. IPL, inner plexiform layer. (Modified from Sterling, 1998.)

as possible. Thus each stage should approach the limits set by physical laws and by compromises required by the organism's "niche." Thus every stage is a potential "bottleneck," and the purpose at each stage must be to staunch the loss of information up to the physical limit. This hypothesis sets a framework for interpreting the functional architecture.

The central idea of this chapter is that the retina evolved to maximally extract information from the natural spatiotemporal distribution of photons and to convey this information centrally, with minimal loss. Upon this broad goal there are functional constraints: cover a wide range of intensities (1010); respond to very low contrasts (~1%); integrate for short times (~0.1 second); keep tissue thin (~0.2 mm); and maintain the metabolic rate no higher. There are also basic constraints on biological computation: signal amplitude and velocities are set by properties of biological membranes and

Figure 17.3. Only the visual sense requires neural processing at the site of transduction. The mammalian cone (upper left) requires lateral integration at its output (horizontal cells [H]), followed by 8 to 10 parallel circuits for a second stage (cone bipolar cells [CB]). Then, it requires more lateral integration (amacrine cells [A]) and finally, 10 to 20 parallel lines (four are shown; ganglion cells [G]) to carry action potentials to the brain. This chapter considers why photoreceptors require such extensive integration and so many parallel circuits before projecting centrally.

Figure 17.3. Only the visual sense requires neural processing at the site of transduction. The mammalian cone (upper left) requires lateral integration at its output (horizontal cells [H]), followed by 8 to 10 parallel circuits for a second stage (cone bipolar cells [CB]). Then, it requires more lateral integration (amacrine cells [A]) and finally, 10 to 20 parallel lines (four are shown; ganglion cells [G]) to carry action potentials to the brain. This chapter considers why photoreceptors require such extensive integration and so many parallel circuits before projecting centrally.

the speed of aqueous diffusion; accuracy and reliability of synaptic transmission are constrained by its quantal and Poisson nature. The retina's functional architecture reflects numerous compromises shaped by the interplay of these major factors as they contribute to the organism's overall success in its environment.

Why Natural Images Need Lots of Light Both prey and predators try to merge with the background, so in nature contrast for significant objects tends to be low. Consider the bighorn sheep among the cottonwoods (Fig. 17.4A). The retinal image is represented as peaks and troughs of intensity that differ from the local mean by only ~20%, and much fine structure exhibits far lower contrast, only a few percent (Fig. 17.4B). This range is common in nature (Laughlin, 1994; Srinivasan et al., 1982), and thus our visual threshold for a small stimulus, such as one spanning a single ganglion cell dendritic field, is ~3% contrast (Watson et al., 1983; Dhingra et al., 2003).

To create an optical image at low contrast requires many photons (Rose, 1973; Snyder et al., 1977). Because light is quantized, a small difference from the mean, say 1%, implies that the mean itself must contain at least 100 photons. But photons at each image point arrive randomly in time (Poisson distribution). So even when an image is perfectly still on the retina, the intensity at every point varies temporally, with a standard deviation equal to the square root of the mean. Because the minimum detectable contrast (An) must differ from the mean by at least one standard deviation, the ability to detect a contrast of 1% implies a mean of at least 10,000 photons:

This root-mean-square fluctuation (Vn) is termed "photon noise."

One might think that daylight would provide plenty of photons to represent any scene. But this depends on the extent of photon integration: fine spatial detail implies limited spatial pooling and thus relatively large fluctuations from photon noise (Fig. 17.5A). This might be avoided by increasing temporal integration, but because mammals move swiftly, prolonged integration would blur the spatial image. Thus temporal integration is constrained to ~ 100 msec (Schneeweis and Schnapf, 1995). Although daylight contains enough photons/100 msec to cast a fine image on the cornea, the excess is not large, nor does it extend to even slightly dimmer situations, for example, when a cloud obscures the sun. The need for intense light to register fine detail at low contrast partly explains why athletes, bird watchers, and the like do not wear sunglasses (Sterling et al., 1992).

Mammalian photoreceptor mosaic

The Need for Two Types of Detector The photoreceptor mosaic is optimized to cover the full range of environmental light intensities (1010). This design specification requires two types of detector with different sensitivities, the rod and the cone (see Figs. 17.1, 17.5, and 17.6).1 The rod serves under starlight where photons are so sparse that over 0.2 second (the rod integration time), they cause only ~1 photoisomerization (R*)/10,000 rods. Consequently, under starlight and for 3 log units brighter, a rod must give a binary response, reporting over each integration time the

1 Of course, insects cover the same intensity range with a single type of photoreceptor, but they differ in many respects, including basic optical design, regeneration of rhodopsin, and use of an entirely different transduction cascade. When insect phototransduction is finally worked out, we may understand better how it manages to compress the full intensity range into a single cell type.

STERLING: RETINAL CIRCUITS AND VISUAL INFORMATION

Was this article helpful?

0 0

Post a comment