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Responses of Bipolar Cells Each Bipolar Cell Receives Its Direct Input Either from Rods Or Cones

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Responses of Bipolar Cells Each Bipolar Cell Receives Its Direct Input Either from Rods Or Cones Transduction and Transmission in the Retina 423 Free vesicle FIGURE 20.18 Molecular Components of Tethered vesicle Ribbon Synapses. The electron-dense body of the ribbon is made up largely of the Ribeye (CtBP2) protein, with contributions from CtBP1/ BARS and KIF3A. Piccolo and Rab3-interact- ing molecule 1 (RIM1) are ribbon-associated Ribeye Piccolo proteins. L-type calcium channels cluster in RIM1 the plasma membrane beneath the ribbon and associate with Bassoon, RIM2, Munc13-1, and Presynaptic RIM2 membrane ERC2/CAST1 proteins. Metabotropic (mGluR) Bassoon and ionotropic (iGluR) glutamate receptors Munc13-1 are located in the postsynaptic membranes of bipolar and horizontal cell. (After Dieck and ERC2/CAST1 Brandstatter, 2006.) Ca2+ channel α mGluR 1 subunit iGluR Postsynaptic membranes long before intracellular electrodes were inserted into individual retinal neurons. Although a product of necessity, beginning with the output signal was nonetheless an excellent start- ing point for analyzing retinal processing. Two important features were established by such recordings. The first was that the receptive field of a retinal ganglion cell is organized in a circular, center-surround manner. That is, light in the receptive field surround area produces an opposite effect to that in the center (see Figure 2.5). The second essential feature obtained from ganglion cell recordings was that some retinal ganglion cells were excited by light in their receptive field center, the on retinal ganglion cells; in contrast, other ganglion cells were inhibited by light in their receptive field center, the off retinal ganglion cells. This dichotomy of on and off pathways is now known to be a fundamental property of all vertebrate retinas and establishes an organizing principle for higher visual centers.56 From these recordings of retinal ganglion cells, it is clear that the eye tells the brain about patterns of light and dark. Since photoreceptors can only report light intensity, it must fall to retinal interneurons to provide the analytical steps leading to the more structured retinal output. Responses of Bipolar Cells Each bipolar cell receives its direct input either from rods or cones. Rod bipolar cells are typically supplied by 15 to 45 receptors. One type of cone bipolar, the midget bipolar, re- ceives its input from a single cone. As one might expect, midget bipolar cells are found in the through-line from the fovea, where acuity is highest. They end on specialized ganglion cells. Other bipolar cells are supplied by a convergent input from 5 to 20 adjacent cones. H bipolar cells, like photoreceptors, are hyperpolarized by an increase in light. However, D bipolar cells are depolarized by light, laying the basis for the off and on output carried by retinal ganglion cells. The responses and receptive fields of bipolar cells depend on two mechanisms. First, the continuous release of glutamate from photoreceptors in the dark keeps some bipolar cells depolarized and others hyperpolarized, depending on whether the cells have excitatory or inhibitory glutamate receptors. Second, light causes photoreceptors to be hyperpolarized, thereby reducing glutamate release. Accordingly, decreased tonic release from illuminated photoreceptors will reduce excitation of bipolar cells with excitatory (i.e., sign preserving) 73 Kaneko, A., and Hashimoto, H. 1969. Vision receptors, giving rise to hyperpolarization.73 These are called H (hyperpolarizing) bipolar Res. 9: 37–55. ©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 424 Chapter 20 (A) Central illumination cells (Figure 20.19). Conversely, decreased tonic release from illuminated photoreceptors will give rise to depolarization of Light bipolar cells with inhibitory (i.e., sign reversing) glutamate 10 receptors. These are D (depolarizing) bipolar cells. D bipolar cells constitute one of the few cell types in which glutamate has mV 0 been shown to have an inhibitory action (see Chapter 14). Thus, a fundamental property of the visual system, on and off responses 0 0.4 0.8 1 mm to light, originates in the differential response of bipolar cells to Time (s) glutamate, determined by each cell’s glutamate receptors. (B) Annular illumination H bipolar cells have α-amino-3-hydroxy-5-methyl-4-isoxazole Light propionic acid (AMPA) or kainate-type cation-selective ionotropic 74 10 glutamate receptors. Depolarized by glutamate released from photoreceptors in the dark, H bipolar cells hyperpolarize when light mV reduces glutamate release. In contrast, as Kaneko, his colleagues and 0 others have shown, the hyperpolarizing transmission to D bipolar 0 0.4 0.8 cells in the dark is mediated by mGluR6 metabotropic glutamate Time (s) receptors that act through G proteins and second messengers.75,76 FIGURE 20.19 Receptive Field Organization of a Hyperpolar- These close a TRP melastatin 1 (TRPM1) cation channel, which 77,78 izing (H) Bipolar Cell. (A) Records made from the bipolar cell in the opens with light to depolarize the D bipolar cell. goldfish retina show a hyperpolarization in response to illumination of the center of the receptive field. Annular illumination causes the cell to respond with a depolarization (B). Diffuse light would have little effect Receptive Field Organization of Bipolar Cells on the cell. For a D bipolar cell, illumination of the center would pro- The receptive field of a hyperpolarizing bipolar cell is shown in duce depolarization, while the annulus would produce hyperpolariza- Figure 20.19. A small spot of light shone onto the central part of tion. (After Kaneko, 1970.) the field causes a sustained hyperpolarization. Illumination by an annulus, leaving the center dark, causes depolarization. Thus, the central area, driven directly by photoreceptors, is enveloped by an antagonistic surround. The H bipolar cell of Figure 20.19 can be described as having an off-center receptive field, since it is depolarized when the spot of light goes off. D bipolar cells have similarly shaped concentric fields, except that illumination of the center causes depolarization and illumination of the surround causes hyperpolarization. Because it is depolarized when the light goes on, the D bipolar cell has an on-center receptive field. The terminology of on and off responses is used extensively to describe receptive field properties at successive levels of the visual system. An important principle is that a single photoreceptor can contribute to the receptive field centers of both on and off bipolar cells and to the surrounds of others. Rod Bipolar Cells Rod bipolar cells depart from the straightforward pattern described for cone bipolar cells. All rod bipolar cells are on type, expressing sign-reversing inhibitory mGluR6 metabotropic 79 74 glutamate receptors. Rather than contacting retinal ganglion cells directly, rod bipolar cells DeVries, S. H. 2000. Neuron 28: 847–856. 80 75 Kikkawa, S. et al. 1993. Biochem. Biophys. synapse onto AII amacrine cells. Each AII amacrine cell depolarizes due to the summed Res. Commun. 195: 374–379. input of many rod bipolar cells, and in turn forms synapses onto the axon terminals of cone 76 Masu, M. et al. 1995. Cell 80: 757–765. bipolar cells to influence the activity of retinal ganglion cells.81 It has been suggested that 77 Nakanishi, S. et al. 1998. Brain Res. Brain this indirect arrangement results from the later evolutionary arrival of rod photoreceptors Res. Rev. 26: 230–235. to the vertebrate retina, piggybacking onto the preexisting cone circuitry.82 AII amacrine 78 Koike, C. et al. 2010. Cell Calcium 48: 95–101. cells collect input from large numbers of rod photoreceptors, and they form electrical 79 Nomura, A. et al. 1994. Cell 77: 361–369. synapses onto the synaptic pedicle of on cone bipolars and make inhibitory glycinergic 80 Famiglietti, E. V., Jr., and Kolb, H. 1975. synapses with off cone bipolars.80 This connectivity suggests that rods provide a wide-field Brain Res. 84: 293–300. measure of background light levels.81 The retinal processing of rod photoreception is an 81 Wässle, H. 2004. Nat. Rev. Neurosci. 5: 83 747–757. emerging story, since there is now evidence for electrical synapses of rods with cones 84,85 82 Lamb, T. D. 2009. Philos. Trans. R. Soc. and for glutamatergic synapses of rods and cones onto some of the same bipolar cells. Lond. B, Biol. Sci. 364: 2911–2924. 83 Deans, M. R. et al. 2002. Neuron 36: 703–712. Horizontal Cells and Surround Inhibition 84 Pang, J. J. et al. 2010 Proc. Natl. Acad. Sci. USA 107: 395–400. Rods and cones make synapses with bipolar cells and horizontal cells. The responses of D and 85 Soucy, E. et al. 1998. Neuron 21: 481–493. H bipolar cells to surround illumination are mediated by horizontal cells. Each horizontal cell ©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher..
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