Vision: from Photon to Perception
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Proc. Natl. Acad. Sci. USA Vol. 93, pp. 557-559, January 1996 Colloquium Paper This paper serves as an introduction to the foUlowing papers, which were presented at a colloquium 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. Vision: From photon to perception LUBERT STRYER Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305 A National Academy of Sciences colloquium entitled "Vision: vation pathway. A rich harvest is being reaped from the From Photon to Perception" was held at the Beckman Center concerted use of electrophysiological and molecular genetic of the Academy in Irvine, California, on May 20-22, 1995. The techniques. meeting was organized by John Dowling, Lubert Stryer (chair), A workshop entitled "Amplification in Phototransduction," and Torsten Wiesel. The aim of the colloquium was to bring chaired by Trevor Lamb, further explored the cyclic GMP together leading scientists and students from different disci- cascade of vertebrate vision. Lamb (2) presented a stochastic plines ofvision research ranging from physics to psychology to simulation of the photoactivation of the cyclic GMP phos- define and explore the most challenging questions in the field. phodiesterase. The simulated rising phase of the photocurrent One hundred forty scientists participated in the colloquium. agrees closely with the response of intact rods as measured We are indebted to Silicon Graphics, Inc., and the Ruth and electrophysiologically. This modeling approach will be useful Milton Steinbach Fund, Inc., for generous grants that helped in testing our emerging grasp ofhow the cascade is deactivated. bring graduate students to the meeting. New experimental methods too are enriching our understand- The major topics discussed were as follows. ing of the early events in vision. Minh Vuong (3) demonstrated (i) How is light converted into a nerve signal? a highly sensitive microcalorimetric technique for measuring (ii) How are the outputs of rod and cone cells processed by the heat released by cyclic GMP hydrolysis. This approach the retina? provides a window on the kinetics and gain of the initial steps (iii) How does the visual system develop and how did it in phototransduction. Joe Noel (4) vividly displayed the three- evolve? dimensional structure of the a subunit of transducin, the first (iv) How do we perceive color, depth, and motion? amplified intermediate in vision. The colloquium began with a spirited opening lecture by Invertebrate vision too begins with the activation of a G David Hubel on the process of discovery in vision research. protein by photoexcited rhodopsin. As was discussed by The first session, "From Photon to Nerve Signal" (chaired by Charles Zuker (5), the cascades of vertebrates and inverte- Lubert Stryer), focused on transduction processes in verte- brates then diverge. In Drosophila, the activated G protein brate and invertebrate photoreceptor cells. The second ses- stimulates a phospholipase C rather than a cyclic GMP phos- sion, "Development and Circuitry" (chaired by John Dowling), phodiesterase. Another major difference is that, in Drosophila, dealt with the development of the retina and lateral geniculate light opens channels and depolarizes the photoreceptor mem- nucleus and with signal processing. Higher-order processes brane. How does phospholipase C activation lead to channel occurring in the visual cortex were considered in the third opening? Inositol trisphosphate, calcium, and cyclic GMP have session, "Representation and Perception" (chaired by Francis been implicated in the process but the actual messenger has Crick). Torsten Wiesel gave a reflective closing lecture on the eluded detection. Zuker outlined three genetic approaches pursuit of knowledge and the future of research in neurobi- that have led to the identification of more than 50 genes in ology. phototransduction. Electrophysiological studies of mutants Denis Baylor (1) began the first session by providing an generated by these approaches and laser scanning confocal account of how the absorption of a photon by a retinal rod or microscopic studies of photoreceptor cells show that localized cone cell leads to the generation of an amplified neural signal. changes in the calcium level play a key role in switching off the Photoexcited rhodopsin triggers the activation of transducin, a photoresponse. The major task now is to complete the mo- G protein, which in turn stimulates a cyclic GMP phospho- lecular characterization of the light-sensitive channel and, diesterase. The consequent hydrolysis of cyclic GMP directly most important, to learn how it is gated. closes cation-specific channels in the plasma membrane. The Gerald Jacobs (6) reviewed recent advances in our under- resulting hyperpolarization is sensed at the synapse, where it standing of color vision in primates and discussed their evo- decreases the rate of transmitter release. This light-triggered lutionary implications. The number of dimensions of color cyclic GMP cascade is one of the best understood signal vision as determined by perceptual color matching tests is transduction processes in nature. The challenge now is to usually the same as the number of types of cone visual elucidate the molecular events mediating recovery of the dark pigments in the retina of a primate. Four patterns of primate state and adaptation to background light. The remarkable color vision are evident. Old World monkeys, apes, and reproducibility of the single-photon response also needs to be humans are trichromatic. New World monkeys were once understood in molecular terms. Investigators are now focusing thought to be dichromatic, but the actual situation is more on the negative feedback actions of the light-induced fall in the complex and interesting. Males are always dichromatic, cytosolic calcium level. Baylor presented several incisive recent whereas females can be either dichromatic or trichromatic experiments comparing phototransduction in normal and depending on whether their X chromosomes contain the same transgenic mouse rods harboring mutant genes in the deacti- or different alleles of the long-wavelength pigment gene. This potential polymorphism is absent in diurnal prosimians, who The publication costs of this article were defrayed in part by page charge are uniformly dichromatic. The situation is even simpler in payment. This article must therefore be hereby marked "advertisement" in nocturnal primates, who are monochromatic because they accordance with 18 U.S.C. §1734 solely to indicate this fact. possess only one functional cone pigment. These findings pose 557 Downloaded by guest on September 24, 2021 558 Colloquium Paper: Stryer Proc. Natl. Acad. Sci. USA 93 (1996) two intriguing questions: (a) What were the selective pressures utero before vision is operative but requires ganglion cell underlying the evolution of partial trichromacy in the New signaling. How is this accomplished? Spontaneous action World lineage and uniform trichromacy in the Old World potentials arising from as many as 100 ganglion cells were lineage? (b) How did the retinal circuitry for color vision simultaneously recorded by use of a multielectrode array. The coevolve with the establishment of a second visual pigment surprising finding was that neighboring cells fired in a con- locus on the X chromosome in the emergence of trichromacy certed manner. Their action potentials occurred within 5 sec in Old World monkeys? of each other, followed by a silent period of up to 2 min before The next set of papers dealt with the circuitry and devel- firing resumed. The ganglion cell activity comprised a wave opment of the retina. Human color vision begins with signals that swept across the retina. Optical recordings monitoring from three types of cones that combine antagonistically to changes in intracellular calcium levels suggested that amacrine form blue-yellow and red-green opponent pathways. Dennis cells and ganglion cells act together in generating spontaneous Dacey (7) showed how the circuits underlying opponency are synchronous activity in the developing retina. Shatz proposed being deciphered. The macaque monkey retina can be studied that activity-dependent wiring may be generally used in the in vitro, and photoresponses can be recorded from cells developing nervous system to help refine early neural connec- identified by their morphology and binding of specific fluo- tions. rescent markers. Blue-yellow opponency is mediated by a The optic nerve is a severe bottleneck in visual signaling. All small bistratified ganglion cell that receives depolarizing inputs information captured by 125 million photoreceptor cells in from a blue-sensitive "on" bipolar cell and a summed red and humans is carried into the brain by only 1 million ganglion cell green-sensitive "off' bipolar cell. A different kind of circuitry axons. How does the retina generate a highly efficient repre- underlies red-green opponency, which is signaled by midget sentation of the visual scene? Markus Meister (11) described ganglion cells. Dacey proposed that the receptive field centers recent experiments suggesting that the retina employs of these cells get a simple cone input (either maximally red- or multineuronal coding to compress a large number of distinct maximally green-sensitive), whereas the surround gets both visual messages into a relatively small number of optic nerve types.