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Six different roles for crossover inhibition in the retina: Correcting the nonlinearities of synaptic transmission

Published online by Cambridge University Press:  15 April 2010

FRANK S. WERBLIN
FRANK S. WERBLIN*
Affiliation:
Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, California
*
*Address correspondence and reprint requests to: Frank S. Weblin,Department of Molecular and Cell Biology, Division of Neurobiology UC Berkeley, Berkeley, CA 94720. E-mail: werblin@berkeley.edu
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Abstract

Early retinal studies categorized ganglion cell behavior as either linear or nonlinear and rectifying as represented by the familiar X- and Y-type ganglion cells in cat. Nonlinear behavior is in large part a consequence of the rectifying nonlinearities inherent in synaptic transmission. These nonlinear signals underlie many special functions in retinal processing, including motion detection, motion in motion, and local edge detection. But linear behavior is also required for some visual processing tasks. For these tasks, the inherently nonlinear signals are “linearized” by “crossover inhibition.” Linearization utilizes a circuitry whereby nonlinear ON inhibition adds with nonlinear OFF excitation or ON excitation adds with OFF inhibition to generate a more linear postsynaptic voltage response. Crossover inhibition has now been measured in most bipolar, amacrine, and ganglion cells. Functionally crossover inhibition enhances edge detection, allows ganglion cells to recognize luminance-neutral patterns with their receptive fields, permits ganglion cells to distinguish contrast from luminance, and maintains a more constant conductance during the light response. In some cases, crossover extends the operating range of cone-driven OFF ganglion cells into the scotopic levels. Crossover inhibition is also found in neurons of the lateral geniculate nucleus and V1.

Keywords

RetinaInhibitionAmacrine cellsVisual signals
Type
Review Article
Information
Visual Neuroscience , Volume 27 , Issue 1-2 , March 2010 , pp. 1 - 8
Copyright
Copyright © Cambridge University Press 2010

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References

Anderson, J.S., Carandini, M. & Ferster, D. (2000). Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. Journal of Neurophysiology 84, 909–926.CrossRefGoogle ScholarPubMed
Arkin, M.S. & Miller, R.F. (1988). Bipolar origin of synaptic inputs to sustained OFF-ganglion cells in the mudpuppy retina. Journal of Neurophysiology 60, 1122–1142.CrossRefGoogle ScholarPubMed
Baccus, S.A., Olveczky, B.P., Manu, M. & Meister, M. (2008). A retinal circuit that computes object motion. The Journal of Neuroscience 28, 6807–6817.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit’s retina. The Journal of Physiology 178, 477–504.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1982). Light-evoked sustained inhibition in mudpuppy retinal ganglion cells. Vision Research 22, 257–260.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R., McReynolds, J.S. & Miyachi, E. (1987). Push-pull effect of surround illumination on excitatory and inhibitory inputs to mudpuppy retinal ganglion cells. The Journal of Physiology 388, 233–243.CrossRefGoogle ScholarPubMed
Demb, J.B., Haarsma, L., Freed, M.A. & Sterling, P. (1999). Functional circuitry of the retinal ganglion cell’s nonlinear receptive field. The Journal of Neuroscience 19, 9756–9767.CrossRefGoogle ScholarPubMed
Demb, J.B., Zaghloul, K., Haarsma, L. & Sterling, P. (2001). Bipolar cells contribute to nonlinear spatial summation in the brisk-transient (Y) ganglion cell in mammalian retina. The Journal of Neuroscience 21, 7447–7454.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1968). Synaptic organization of the frog retina: An electron microscopic analysis comparing the retinas of frogs and primates. Proceedings of the Royal Society of London B: Biological Sciences 170, 205–228.Google ScholarPubMed
Dowling, J.E. (1970 a). Organization of the vertebrate retina. Nippon Seirigaku Zasshi. Journal of the Physiological Society of Japan 32, 546–547.Google ScholarPubMed
Dowling, J.E. (1970 b). Organization of vertebrate retinas. Investigative Ophthalmology 9, 655–680.Google ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1965). Neural connections of the retina: Fine structure of the inner plexiform layer. Cold Spring Harbor Symposia on Quantitative Biology 30, 393–402.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London B: Biological Sciences 166, 80–111.Google ScholarPubMed
Enroth-Cugell, C. & Freeman, A.W. (1987). The receptive-field spatial structure of cat retinal Y cells. The Journal of Physiology 384, 49–79.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1984). Functional characteristics and diversity of cat retinal ganglion cells. Basic characteristics and quantitative description. Investigative Ophthalmology & Visual Science 25, 250–267.Google ScholarPubMed
Euler, T., Detwiler, P.B. & Denk, W. (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852.CrossRefGoogle ScholarPubMed
Fried, S.I., Munch, T.A. & Werblin, F.S. (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414.CrossRefGoogle ScholarPubMed
Fried, S.I., Munch, T.A. & Werblin, F.S. (2005). Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46, 117–127.CrossRefGoogle ScholarPubMed
Gaudiano, P. (1994). Simulations of X and Y retinal ganglion cell behavior with a nonlinear push-pull model of spatiotemporal retinal processing. Vision Research 34, 1767–1784.CrossRefGoogle ScholarPubMed
Hamasaki, D.I. & Sutija, V.G. (1979). Classification of cat retinal ganglion cells into X- and Y-cells with a contrast reversal stimulus. Experimental Brain Research 35, 25–36.CrossRefGoogle ScholarPubMed
Hamasaki, D.I., Tasaki, K. & Suzuki, H. (1979). Properties of X- and Y-cells in the rabbit retina. The Japanese Journal of Physiology 29, 445–457.CrossRefGoogle ScholarPubMed
Hartline, H.K. & Ratliff, F. (1957). Inhibitory interaction of receptor units in the eye of limulus. The Journal of General Physiology 40, 357–376.CrossRefGoogle ScholarPubMed
Haverkamp, S., Muller, U., Harvey, K., Harvey, R.J., Betz, H. & Wassle, H. (2003). Diversity of glycine receptors in the mouse retina: Localization of the alpha3 subunit. The Journal of Comparative Neurology 465, 524–539.CrossRefGoogle ScholarPubMed
Haverkamp, S., Muller, U., Zeilhofer, H.U., Harvey, R.J. & Wassle, H. (2004). Diversity of glycine receptors in the mouse retina: Localization of the alpha2 subunit. The Journal of Comparative Neurology 477, 399–411.CrossRefGoogle ScholarPubMed
Heidelberger, R., Thoreson, W.B. & Witkovsky, P. (2005). Synaptic transmission at retinal ribbon synapses. Progress in Retinal and Eye Research 24, 682–720.CrossRefGoogle ScholarPubMed
Heinze, L., Harvey, R.J., Haverkamp, S. & Wassle, H. (2007). Diversity of glycine receptors in the mouse retina: Localization of the alpha4 subunit. The Journal of Comparative Neurology 500, 693–707.CrossRefGoogle ScholarPubMed
Hirsch, J.A. (2003). Synaptic physiology and receptive field structure in the early visual pathway of the cat. Cerebral Cortex 13, 63–69.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976 a). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. The Journal of Physiology 262, 265–284.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976 b). Quantitative analysis of retinal ganglion cell classifications. The Journal of Physiology 262, 237–264.CrossRefGoogle ScholarPubMed
Hsueh, H.A., Molnar, A. & Werblin, F.S. (2008). Amacrine-to-amacrine cell inhibition in the rabbit retina. Journal of Neurophysiology 100, 2077–2088.CrossRefGoogle ScholarPubMed
Jakiela, H.G. & Enroth-Cugell, C. (1976). Adaptation and dynamics in X-cells and Y-cells of the cat retina. Experimental Brain Research 24, 335–342.CrossRefGoogle ScholarPubMed
Katz, B. & Miledi, R. (1967). A study of synaptic transmission in the absence of nerve impulses. The Journal of Physiology 192, 407–436.CrossRefGoogle ScholarPubMed
Lauritzen, T.Z. & Miller, K.D. (2003). Different roles for simple-cell and complex-cell inhibition in V1. The Journal of Neuroscience 23, 10201–10213.CrossRefGoogle ScholarPubMed
Lee, S. & Zhou, Z.J. (2006). The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787–799.CrossRefGoogle ScholarPubMed
Levick, W.R. (1965). Receptive fields of rabbit retinal ganglion cells. American Journal of Optometry & Archives of American Academy of Optometry 42, 337–343.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, C. (1982). Receptive field properties of x and y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 1173–1183.CrossRefGoogle ScholarPubMed
Manookin, M.B., Beaudoin, D.L., Ernst, Z.R., Flagel, L.J. & Demb, J.B. (2008). Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. The Journal of Neuroscience 28, 4136–4150.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. The Journal of Neuroscience 6, 907–918.CrossRefGoogle ScholarPubMed
Menger, N., Pow, D.V. & Wassle, H. (1998). Glycinergic amacrine cells of the rat retina. The Journal of Comparative Neurology 401, 34–46.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Molnar, A., Hsueh, H.A., Roska, B. & Werblin, F.S. (2009). Crossover inhibition in the retina: Circuitry that compensates for nonlinear rectifying synaptic transmission. Journal of Computational Neuroscience 27, 569–590.CrossRefGoogle ScholarPubMed
Molnar, A. & Werblin, F. (2007). Inhibitory feedback shapes bipolar cell responses in the rabbit retina. Journal of Neurophysiology 98, 3423–3435.CrossRefGoogle ScholarPubMed
Pang, J.J., Gao, F. & Wu, S.M. (2003). Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. The Journal of Neuroscience 23, 6063–6073.CrossRefGoogle Scholar
Pang, J.J., Gao, F. & Wu, S.M. (2007). Cross-talk between ON and OFF channels in the salamander retina: Indirect bipolar cell inputs to ON-OFF ganglion cells. Vision Research 47, 384–392.CrossRefGoogle ScholarPubMed
Rabl, K., Banvolgyi, T. & Gabriel, R. (2002). Electrophysiological evidence for push-pull interactions in the inner retina of turtle. Acta Biologica Hungarica 53, 141–151.CrossRefGoogle ScholarPubMed
Richter, J. & Ullman, S. (1982). A model for the temporal organization of X- and Y-type receptive fields in the primate retina. Biological Cybernetics 43, 127–145.CrossRefGoogle Scholar
Roska, B., Molnar, A. & Werblin, F.S. (2006). Parallel processing in retinal ganglion cells: How integration of space-time patterns of excitation and inhibition form the spiking output. Journal of Neurophysiology 95, 3810–3822.CrossRefGoogle ScholarPubMed
Roska, B. & Werblin, F. (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583–587.CrossRefGoogle ScholarPubMed
Thoreson, W.B., Rabl, K., Townes-Anderson, E. & Heidelberger, R. (2004). A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595–605.CrossRefGoogle ScholarPubMed
Toyoda, J., Shimbo, K., Kondo, H. & Kujiraoka, T. (1992). Push-pull modulation of ganglion cell responses of carp retina by amacrine cells. Neuroscience Letters 142, 41–44.CrossRefGoogle ScholarPubMed
Troy, J.B. & Enroth-Cugell, C. (1993). X and Y ganglion cells inform the cat’s brain about contrast in the retinal image. Experimental Brain Research 93, 383–390.CrossRefGoogle ScholarPubMed
van Wyk, M., Taylor, W.R. & Vaney, D.I. (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 13250–13263.CrossRefGoogle ScholarPubMed
Vitanova, L., Haverkamp, S. & Wassle, H. (2004). Immunocytochemical localization of glycine and glycine receptors in the retina of the frog Rana ridibunda. Cell and Tissue Research 317, 227–235.CrossRefGoogle ScholarPubMed
Wassle, H., Schafer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. The Journal of Neuroscience 6, 594–604.CrossRefGoogle ScholarPubMed
Weiss, J., O’Sullivan, G.A., Heinze, L., Chen, H.X., Betz, H. & Wassle, H. (2008). Glycinergic input of small-field amacrine cells in the retinas of wildtype and glycine receptor deficient mice. Molecular and Cellular Neurosciences 37, 40–55.CrossRefGoogle ScholarPubMed
Zaghloul, K.A., Boahen, K. & Demb, J.B. (2003). Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. The Journal of Neuroscience 23, 2645–2654.CrossRefGoogle ScholarPubMed