26 Low-Level Visual Processing: The Retina The Photoreceptor Layer Samples the Visual Image The Retina’s Sensitivity Adapts to Changes in Illumination Ocular Optics Limit the Quality of the Retinal Image Light Adaptation Is Apparent in Retinal Processing and Visual Perception There Are Two Types of Photoreceptors: Rods and Cones Multiple Gain Controls Occur Within the Retina Phototransduction Links the Absorption of a Photon to a Light Adaptation Alters Spatial Processing Change in Membrane Conductance An Overall View Light Activates Pigment Molecules in the Photoreceptors Excited Rhodopsin Activates a Phosphodiesterase Through the G Protein Transducin he retina is the brain’s window on the world. Multiple Mechanisms Shut Off the Cascade All visual experience is based on informa- tion processed by this neural circuit in the eye. Defects in Phototransduction Cause Disease T The retina’s output is conveyed to the brain by just Ganglion Cells Transmit Neural Images to the Brain one million optic nerve fibers, and yet almost half of The Two Major Types of Ganglion Cells Are ON Cells the cerebral cortex is used to process these signals. and OFF Cells Visual information lost in the retina—by design or Many Ganglion Cells Respond Strongly to Edges deficiency—can never be recovered. Because retinal in the Image processing sets fundamental limits on what can be The Output of Ganglion Cells Emphasizes Temporal seen, there is great interest in understanding how the Changes in Stimuli retina functions. Retinal Output Emphasizes Moving Objects On the surface the vertebrate eye appears to act much like a camera. The pupil forms a variable dia- Several Ganglion Cell Types Project to the Brain phragm, and the cornea and lens provide the refractive Through Parallel Pathways optics that project a small image of the outside world A Network of Interneurons Shapes the Retinal Output onto the light-sensitive retina lining the back of the eye- Parallel Pathways Originate in Bipolar Cells ball (Figure 26–1). But this is where the analogy ends. Spatial Filtering Is Accomplished by Lateral Inhibition The retina is a thin sheet of neurons, a few hundred micrometers thick, composed of five major cell types Temporal Filtering Occurs in Synapses and Feedback Circuits that are arranged in three cellular layers separated by two synaptic layers (Figure 26–2). Color Vision Begins in Cone-Selective Circuits The photoreceptor cells, in the outermost layer, Congenital Color Blindness Takes Several Forms absorb light and convert it into a neural signal, Rod and Cone Circuits Merge in the Inner Retina an essential process known as phototransduction. 578 Part V / Perception A Refraction of light onto the retina B Focusing of light in the foveaC Packing of photoreceptors in the fovea Ganglion cell Cornea Retina Fixation Light point Foveola 10 µm Fovea Light Lens Photoreceptor Optic nerve Pigment Optic Bipolar epithelium disc cell Pigment epithelium Retina Figure 26–1 The eye projects the visual scene onto the C. A letter from the eye chart for normal visual acuity is pro- retina’s photoreceptors. jected onto the densely packed photoreceptors in the fovea. A. Light from an object in the visual field is refracted by the Although less sharply focused than shown here as a result of cornea and lens and focused onto the retina. diffraction by the eye’s optics, the smallest discernible strokes of the letter are approximately one cone diameter in width. B. In the foveola, corresponding to the very center of gaze, the (Adapted, with permission, from Curcio and Hendrickson 1982.) proximal neurons of the retina are shifted aside so light has direct access to the photoreceptors. These signals are passed synaptically to bipolar cells, In this chapter we discuss in turn the three impor- which in turn connect to retinal ganglion cells in the tant aspects of retinal function: phototransduction, innermost layer. Retinal ganglion cells are the output preprocessing, and adaptation. We will illustrate both neurons of the retina and their axons form the optic the neural mechanisms by which they are achieved nerve. In addition to this vertical pathway from sen- and their consequences for visual perception. sory to output neurons, the retinal circuit includes many lateral connections provided by horizontal cells in the outer synaptic layer and amacrine cells in the The Photoreceptor Layer Samples inner synaptic layer (Figure 26–3). the Visual Image The retinal circuit performs low-level visual processing, the initial stage in the analysis of visual Ocular Optics Limit the Quality images. It extracts from the raw images in the left of the Retinal Image and right eyes certain spatial and temporal features and conveys them to higher visual centers. The rules The sharpness of the retinal image is determined by of this processing are very plastic. In particular, the several factors: diffraction at the pupil’s aperture, retina must adjust its sensitivity to ever-changing refractive errors in the cornea and lens, and scattering conditions of illumination. This adaptation allows due to material in the light path. A point in the out- our vision to remain more or less stable despite the side world is generally focused into a small blurred vast range of light intensities encountered during the circle on the retina. As in other optical devices this course of each day. blur is smallest near the optical axis, where the image Chapter 26 / Low-Level Visual Processing: The Retina 579 quality approaches the limit imposed by diffraction at photoreceptors there is well matched to the size of the the pupil. Away from the axis the image is degraded optical blur circle, and thus samples the image in an ideal significantly owing to aberrations in the cornea and fashion. Light must generally traverse several layers of lens. The image may be degraded further by abnormal cells before reaching the photoreceptors, but in the center conditions such as light-scattering cataracts or refrac- of the fovea, called the foveola, the other cellular layers are tive errors such as myopia. pushed aside to reduce additional blur from light scatter- The area of retina near the optical axis, the fovea, is ing (Figure 26–1B). Finally, the back of the eye is lined by where vision is sharpest and corresponds to the center a black pigment epithelium that absorbs light and keeps of gaze that we direct toward the objects of our attention. it from scattering back into the eye. The density of photoreceptors, bipolar cells, and ganglion The retina contains another special site, the optic cells is highest at the fovea. The spacing between disc, where the axons of retinal ganglion cells converge A Section of retina B Neurons in the retina Cone Outer nuclear layer Rod Outer plexiform layer Midget bipolar Inner Horizontal nuclear Rod layer bipolar Diffuse bipolar Amacrine Inner plexiform layer Ganglion cell layer M ganglion M ganglion P ganglion 50 µm Figure 26–2 The retina comprises five distinct layers of synapses separate these: the outer plexiform layer and the neurons and synapses. inner plexiform layer. (Reproduced, with permission, from A. A perpendicular section of the human retina seen through Boycott and Dowling 1969.) the light microscope. Three layers of cell bodies are evident. B. Neurons in the retina of the macaque monkey based on The outer nuclear layer contains cell bodies of photoreceptors; Golgi staining. The cellular and synaptic layers are aligned with the inner nuclear layer includes horizontal, bipolar, and amacrine the image in part A. (M ganglion, magnocellular ganglion cell; cells; and the ganglion cell layer contains ganglion cells and P ganglion, parvocellular ganglion cell.) (Reproduced, with some displaced amacrine cells. Two layers of fibers and permission, from Polyak 1941.) 580 Part V / Perception A Cone signal circuitry B Rod signal circuitry Cone Cone Rod Cone Photoreceptors Horizontal cells Lateral Inhibition Bipolar Rod cells bipolar Amacrine A�� cells amacrine cell Ganglion cells ON OFF ON OFF Figure 26–3 The retinal circuitry. arrows represent sign-inverting connections through GABA- A. The circuitry for cone signals, highlighting the split into ON ergic, glycinergic, or glutamatergic synapses. and OFF pathways as well as the pathway for lateral inhibition B. Rod signals feed into the cone circuitry through the AII ama- in the outer layer. Red arrows indicate sign-preserving con- crine cell, which serves to split the ON and OFF pathways. nections through electrical or glutamatergic synapses. Gray and extend through the retina to emerge from the back amused biologists for generations. The purpose of this of the eye as the optic nerve. By necessity this area is organization may be to enable the tight apposition of devoid of photoreceptors and thus corresponds to a photoreceptors with the retinal pigment epithelium, blind spot in the visual field of each eye. Because the which plays an essential role in the turnover of retinal disc lies nasal to the fovea of each eye, light coming pigment and recycles photoreceptor membranes by from a single point never falls on both blind spots phagocytosis. simultaneously, and thus normally we are unaware of them. We can experience the blind spot only by There Are Two Types of Photoreceptors: using one eye (Figure 26–4). The blind spot demon- Rods and Cones strates what blind people experience—not blackness, but simply nothing. This explains why damage to the All photoreceptor cells have a common structure with peripheral retina often goes unnoticed. It is usually four functional regions: the outer segment, located at through accidents, such as bumping into an unnoticed the distal surface of the neural retina; the inner seg- object, or through clinical testing that a deficit of sight ment, located more proximally; the cell body; and the is revealed. synaptic terminal (Figure 26–5A).