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Molecular Biology of Retinal Ganglion Cells

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Molecular Biology of Retinal Ganglion Cells Proc. Natl. Acad. Sci. USA Vol. 93, pp. 596-601, January 1996 Colloquium Paper This paper was presented at a coUloquium entitled "Vision: From Photon to Perception, " organized by John Dowling, Lubert Stryer (chair), and Torsten Wiesel, held May 20-22, 1995, at the National Academy of Sciences in Irvine, CA. Molecular biology of retinal ganglion cells MENGQING XIANG*t, HAO ZHOU*, AND JEREMY NATHANS*t#§ Departments of *Molecular Biology and Genetics, tNeuroscience, §Ophthalmology, tHoward Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21205 ABSTRACT Retinal ganglion cells are the output neurons the image by emphasizing spatial contrast. This type of spa- that encode and transmit information from the eye to the tially antagonistic filtering had been predicted in the 19th brain. Their diverse physiologic and anatomic properties have century by both Hering and Mach (4, 5) on psychophysical been intensively studied and appear to account well for a grounds, and it accounts for the illusory black dots seen in the number of psychophysical phenomena such as lateral inhibi- Hermann grid in Fig. 2. In the retinas of old world primates, tion and chromatic opponency. In this paper, we summarize many ganglion cells also relay chromatic information by re- our current view of retinal ganglion cell properties and pose porting either the difference between red and green cone a number of questions regarding underlying molecular mech- inputs or the difference between blue cone input and a sum of anisms. As an example of one approach to understanding red and green (= yellow) cone inputs. For reasons that are not molecular mechanisms, we describe recent work on several obvious, most ganglion cells of the red vs. green type have both POU domain transcription factors that are expressed in chromatically and spatially opponent receptive fields, whereas subsets ofretinal ganglion cells and that appear to be involved most ganglion cells of the blue vs. red + green type have nearly in ganglion cell development. coextensive excitatory and inhibitory zones and therefore a much smaller degree of spatial opponency (6). The channeling of This paper reviews our current knowledge of retinal ganglion chromatic information into two pathways with red vs. green and cell structure and function with an emphasis on those areas in blue vs. yellow color opponent organization was deduced on which molecular biological approaches may be expected to psychophysical grounds by Hering (4). It accounts for the chro- provide new insights. We begin with an overview of the matic afterimages generated by selective desensitization of one or physiological, anatomical, and psychophysical experiments another limb of the opponent processing system (Fig. that have revealed the diversity of ganglion cell properties and 2). the significance of that diversity for visual perception. Al- Hartline's original recordings showed that in some ganglion though little is currently known about the molecular basis of cells a prolonged light stimulus evoked a steady response, this diversity, it is likely that many of the relevant molecules whereas in others it evoked a transient (i.e., nonlinear) re- will be identified in the near future. As an illustration of one sponse (Fig. 1). The latter type of response filters the image by area in which significant progress seems likely, we conclude emphasizing temporal changes. Beginning in the mid-1960s, with a description of recent work on transcription factors in this distinction was systematically investigated in both cat and retinal ganglion cells. monkey retinas (reviewed in refs. 6 and 7). In the cat two major ganglion cell types were identified and termed X and Y, the Physiological Properties of Retinal Ganglion Cells former responding both spatially and temporally in a linear manner and the latter responding nonlinearly (8). In primates, Ganglion cells are the output units of the retina. Because their a similar dichotomy was found in temporal response proper- cell bodies and axons are relatively accessible, they were among ties, with one class, now referred to as parvocellular or P-type the first vertebrate neurons for which single unit responses ganglion cells, responding linearly, and a second class, now were determined. In 1938 Hartline (1) recorded from individ- referred to as magnocellular or M-type ganglion cells, respond- ual axons at the vitreal surface of the frog retina while ing nonlinearly (9). P- and M-type cells have been found to stimulating the retina with a spot of light. These seminal differ in a number of properties. In general terms, P cells are experiments introduced the concept of a receptive field, defined characterized by relatively slow conduction velocities, insen- by Hartline as the region of the retina that must be illuminated sitivity to small changes in luminance contrast, and high spatial in order to obtain a response in a given fiber. As shown in Fig. 1, resolution, especially near the fovea. Most P cells have a these experiments also revealed a multiplicity of response prop- chromatically opponent receptive field organization as de- erties among retinal ganglion cells, including both activation and scribed above. By contrast, M cells are characterized by inhibition: "This diversity of response among fibers from closely relatively fast conduction velocities, sensitivity to small adjacent regions of the same retina is extreme and unmistakable; changes in luminance contrast, and low spatial resolution. M it does not depend upon local conditions of stimulation or cells have achromatic center-surround receptive fields and adaptation, but appears to be an inherent property of the therefore detect luminance but not chromatic contrast. The individual ganglion cells themselves" (1). distinction drawn between cat X and Y cells in spatial response In 1953 Barlow and Kuffler (2, 3) independently discovered properties does not appear to carry over to the primate P/M that many ganglion cells have an antagonistic spatial organi- as all zation in which either an excitatory center is paired with an system P-type and most M-type ganglion cells show linear inhibitory surround or an inhibitory center is paired with an spatial summation (10). The distinct P and M systems appear excitatory surround. The center-surround organization filters Abbreviations: IPL, inner plexiform layer; LGN, lateral geniculate nucleus. The publication costs of this article were defrayed in part by page charge ITo whom reprint requests should be addressed at: 805 Preclinical payment. This article must therefore be hereby marked "advertisement" in Teaching Building, 725 North Wolfe Street, Johns Hopkins Univer- accordance with 18 U.S.C. §1734 solely to indicate this fact. sity School of Medicine, Baltimore, MD 21205. 596 Downloaded by guest on September 29, 2021 Colloquium Paper: Xiang et al. Proc. Natl. Acad. Sci. USA 93 (1996) 597 FIG. 1. Light responses obtained from isolated ganglion cell axons in the frog retina (reproduced from ref. 1). The interval between the regular marks at the bottom of each trace correspond to 0.2 sec. The duration of illumination is indicated by the blackened portion of the strip near the bottom of each trace. The three cells reveal responses to the onset of illumination, the cessation of illumination, steady illumination, or various combinations of these. (Note: in trace A the apparent activity following cessation of illumination is from another cell.) to represent a critical point at which the image is divided into These are likely to be related, at least in part, to the segregation separate and parallel streams. of chromatic inputs. In one well characterized example, the blue ON/yellow OFF color opponent type of ganglion cell has Morphologic and Anatomic Properties of Retinal Ganglion been shown to be bistratified (17). One dendritic tree is located Cells at that level in the inner part of the IPL where the processes of blue cone bipolar cells terminate, and the second dendritic From the earliest histologic studies of the vertebrate retina it tree is located in the outer part of the IPL where it presumably has been apparent that each major class of cells- receives inhibitory signals from bipolar cells driven by red and photoreceptor, bipolar, horizontal, amacrine, and ganglion- green cones. contains within it morphologically distinct subtypes (11). A A third structure-function correlation can be seen in the major theme during the past century of retina research has different projections made by retinal ganglion cells, with the been the identification of functional correlates for these mor- result that distinct aspects of the retinal image are delivered to phologic differences (12). Among ganglion cells, one correla- different destinations in the brain (reviewed in refs. 6 and 7). tion that is now well established (and is perhaps not surprising) The two principal projections from the retina are to the is between the area of the dendritic field and the area of the midbrain and to the dorsal lateral geniculate nucleus (LGN) of receptive field, the former appearing to coincide with and to the thalamus, the latter projecting to the primary visual cortex. determine the extent of the latter. Both dendritic field size and In amphibia and other lower vertebrates the midbrain projec- cell body size differ markedly between physiologically distinct tion (the retinotectal pathway) constitutes the major output ganglion cell types. For example, in the cat, X and Y cells pathway from the retina and mediates simple visually guided correspond, respectively, to the medium (,B) and large (a) cell behaviors. In primates, the analogous pathway is devoted types, and in the monkey, P- and M-type cells correspond, principally to the control of eye and head movements. Many respectively, to the small (midget) and large (parasol) cell types ganglion cells that project to the midbrain exhibit receptive (reviewed in refs. 6 and 13). For P and M cells, both dendritic fields with a high degree of selectivity-for example, to field and soma size increase progressively with increasing movement in a particular direction.
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