Specialization in the retina - University of Minnesota Specialization.pdf · Specialization in the retina ... J. Y. LETTVIN,‡ H. R. MATURANA, ... separate temporal channels is to

Specialization in the retina• Review of photoreceptor adaptation

• Retinal Ganglion Cells

• Center-surround organization

• Horizontal cells

• Bipolar cells/ ON and OFF pathways

• Contrast encoding

• Neuronal diversity in the retina

• Fast contrast adaptation

• flash lag effect and motion anticipation

Wednesday, January 27, 2010

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Reprinted from: “The Mind: Biological Approaches to its Functions” Editors: William C. Corning, Martin Balaban, 1968, pp 233-258.

CHAPTER 7

WHAT THE FROG'S EYE TELLSTHE FROG'S BRAIN * †

J. Y. LETTVIN,‡ H. R. MATURANA,§W. S. McCULLOCH,‡ AND W. H. PITTS‡

I. INTRODUCTION

A. Behavior of a FrogA frog hunts on land by vision. He escapes enemies mainly by

seeing them. His eyes do not move, as do ours, to follow prey, attendsuspicious events, or search for things of interest. If his body changesits position with respect to gravity or the whole visual world isrotated about him, then he shows compensatory eye movements.These movements enter his hunting and evading habits only, e.g., ashe sits on a rocking lily pad. Thus his eyes are actively stabilized. Hehas no fovea, or region of greatest acuity in vision, upon which hemust center a part of the image. He has only a single visual system,retina to colliculus, not a double one such as ours where the retinasends fibers not only to colliculus but to the lateral geniculate bodywhich relays to cerebral cortex. Thus, we chose to work on the frogbecause of the uniformity of his retina, the normal lack of eye andhead movements except for those which stabilize the

* This paper originally appeared in the Proc. Inst. Radio Engr. 1959, vol. 47pages 1940-1951. Reprinted by permission of Dr. Lettvin and the Institute ofElectrical and Electronics Engineers, Inc.† This work supported in part by the U. S. Army (Signal Corps), the U. S. AirForce (Office of Sci. Res., Air Res. and Dev. Command), and the U. S. Navy(Office of Naval Res.), and in part by Bell Telephone Labs, Inc.‡ Research Laboratory of Electronics, Massachusetts Institute of Technology.§ On leave from the University of Chile, Santiago, Chile.

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This combination of a short-wavelength cone and one ormore long-wavelength cones is avirtually universal feature ofmammalian retinas14. At onetime, many mammals werethought to lack color vision, and

indeed an animal with only these two visual pigments is adichromat—in everyday language, red–green ‘color blind.’ Butthe phrase is misleading; the distance between the peak sensi-tivities of the short and long opsins spans the wavelengthsreflected by important objects in the natural world, and an ani-mal with only those opsins has a strong form of color vision.If any doubt exists on this point, one should remember thatroughly 5% of humans inherit this form of dichromacy, butmany learn of it only during adulthood, when first confront-ed by tests designed to reveal variations in color vision.

The pathway from rods to ganglion cellsMost amacrine cells and all ganglion cells receive their main bipo-lar cell synapses from cone bipolars, but retinas work in starlightas well as daylight, and this range is created by a division of laborbetween cones (for bright light) and rods (for dim light). Signalsoriginating in rod photoreceptors reach the retinal ganglion cellsvia an indirect route using as its final path the axon terminals ofthe cone bipolar cells34–37.

That a single set of ganglion cells is used for both starlightand sunlight represents an obvious efficiency, long known fromelectrophysiological findings. However, it was not obvious a pri-

Fig. 3. The connections with cones and axonalstratification of different types of bipolar cells.Five different types of bipolar cells are illus-trated. Two of them are diffuse (chromaticallynonselective) ON bipolar cells terminating inthe inner half of the inner plexiform layer. Twoare diffuse OFF bipolar cells terminating in theouter half. Each samples indiscriminately fromthe spectral classes of cones. The blue conebipolar, however, contacts only blue cones andthus is spectrally tuned to short wavelengths.Within the ON or OFF sublayer, axons of thebipolar cells terminate at different levels, indi-cating that they contact different sets of postsy-naptic partners. After refs. 9 and 17.

Fig. 2. The bipolar cell pathways ofmammalian retinas, assembled fromindividual components. This diagramis intended to emphasize the overallorganization of the parallel channels,and much detail is omitted. Many pri-mate retinas have midget bipolar andganglion cells, but only a few have aseparate red and green channels.Rods are not as clumped as would besuggested here. For visual clarity,cones are shown contacting only asingle bipolar cell each; in fact, allcones contact several bipolar cells, asshown in Figs. 3, 4 and 6. For thedetailed synaptology of the rod path-way, see refs. 36, 37, 125.

Early in evolution, two cone opsins diverged, one with max-imal absorption at long wavelengths and one with maximalabsorption at short wavelengths12–14. Because an individual conecontains only a single spectral type of opsin, this creates two typesof cones, one reporting on long wavelengths and one on short;by comparing their outputs, the retina can create a single signalthat reflects the spectral composition of the stimulus.

The short-wavelength-sensitive cone, familiarly termed the‘blue cone,’ occupies a distinct and simple position in the arrayof retinal circuitry: blue cones synapse on their own specializedtype of bipolar cell, which in turn synapses on a dedicated class ofretinal ganglion cells32,33. Blue cones generally make up less than15% of all cones. The retina thus contains many long-wavelengthcones, which communicate to ganglion cells via a variety of bipo-lar cells, a single type of blue cone, and a single type of blue cone-driven bipolar cell (Figs. 2d and 3).

The synaptic connections of the inner retina are arrangedso that the outputs of some ganglion cells compare the respons-es of the blue cones with those of the long-wavelength cones.For example, the ganglion cell may be excited by short-wave-length stimuli and inhibited by long wavelengths. This repre-sents an economy; a single signal tells the brain where alongthe spectrum from blue to yellow thestimulus lies.

review

nature neuroscience • volume 4 no 9 • september 2001 879

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Bipolar cell diversity

878 nature neuroscience • volume 4 no 9 • september 2001

and this confines their possiblesynaptic partners to cells withprocesses that occupy thosesame levels. Second, differenttypes of bipolar cells have dif-ferent numbers and distribu-tions of synapses, without agradation of intermediate formsbetween the types. The conclu-sion reflects more than neu-roanatomical anecdote; a formalcluster analysis showed thatcone bipolars segregate into dis-crete groups based on synapsenumber and distribution16,19.Third, individual bipolar celltypes have characteristic sets ofneurotransmitter receptors andcalcium-binding proteins20–22.These molecular distinctionsreflect different modes of intra-cellular signaling and differenttypes of excitatory and inhibito-ry inputs from other retinalneurons, either at their inputsfrom cones or from amacrinecells that synapse on their axonterminals. At the cone synapses,different glutamate receptors arepresent. At their axon terminals,different bipolar cells canreceive inhibitory glycinergic orGABAergic input via one of twodifferent kinds of GABA recep-tors. The different receptors andtheir channels have differing affinities and rates of activationand inactivation, which give the cells different postsynapticresponsiveness22–25.

How are these differences manifested physiologically? First,the output of the cone photoreceptors is separated into ON andOFF signals (Fig. 2b). All cone synapses release glutamate, butbipolar cell types respond to glutamate differently. Some bipo-lar cells have ionotropic glutamate receptors: glutamate opens acation channel, and the cell depolarizes. Other bipolar cells havea sign-inverting synapse mediated by metabotropic glutamatereceptors, mainly mGluR6; these bipolar cells hyperpolarize inresponse to glutamate26,27. As it happens, photoreceptor cellswork ‘backward’ (they hyperpolarize when excited by light,causing their synapses to release less glutamate), but the ensu-ing series of sign-reversals is not important for present pur-poses. When the retina is stimulated by light, one type of bipolarcell hyperpolarizes, and the other type depolarizes. OFF andON bipolar cells occur in approximately equal numbers. Thedistinction, created at the first retinal synapse, is propagatedthroughout the visual system.

The classes of ON and OFF bipolars are each further subdivid-ed; there are three to five distinct types of ON and three to five typesof OFF bipolars (Figs. 2c and 3). The purpose of the subdivisionis, at least in part, to provide separate channels for high-frequency(transient) and low-frequency (sustained) information. Thus, thereare separate ON-transient, ON-sustained, OFF-transient and OFF-sustained bipolar cells28–30. An elegant series of experiments showsthat the distinction is caused by different glutamate receptors on

the respective OFF bipolar cells; they recover from desensitizationquickly in the transient cells and more slowly in the sustained cells31.

An often-cited reason for splitting the output of the cones intoseparate temporal channels is to expand the overall bandwidth ofthe system. However, this would imply that the frequency band-width present at the output of a cone is too broad for transmis-sion through the cone-to-bipolar synapse, which is uncertain giventhe many modes of synaptic transmission available. An alterna-tive is that fractionating the temporal domain facilitates the cre-ation of temporally distinct types of ganglion cells (Fig. 4).

An important point here is that there are no dedicatedcones—cones that provide input, say, only to ON bipolars oronly to OFF bipolars (as shown for simplicity in Fig. 2).Instead, the output of each cone is tapped by several bipolarcell types to provide many parallel channels, each communi-cating a different version of the cone’s output to the inner reti-na (Figs. 3, 4 and 6).

The foundations of color visionThe bipolar cells discussed so far are not chromatically selective,and this would prevent the retina from discriminating amongwavelengths. A single type of cone, no matter how narrow itsspectral tuning, cannot create color vision. A cone’s synaptic out-put is a single signal, which can vary only in magnitude. For thatreason, a cone’s signal to the brain is inevitably ambiguous; thereare many combinations of wavelength and intensity that willevoke the same output from the cone. To specify the wavelengthof a stimulus, the outputs of at least two cones must be compared.

review

Fig. 1. The major cell types of a typical mammalian retina. From the top row to the bottom, photoreceptors,horizontal cells, bipolar cells, amacrine cells and ganglion cells. Amacrine cells, the most diverse class, havebeen studied most systematically in the rabbit3,4, and the illustration is based primarily on work in the rabbit.Most of the cells are also seen in a variety of mammalian species. The bipolar cells are from work in the rat39;similar ones have been observed in the rabbit, cat16 and monkey17. For steric reasons, only a subset of thewide-field amacrine cells is shown.©

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Masland, 2001Wednesday, January 27, 2010

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Documents

Specialization in the retina - University of Minnesota Specialization.pdf · Specialization in the retina ... J. Y. LETTVIN,‡ H. R. MATURANA, ... separate temporal channels is to