Skip to main content
×
Home
    • Aa
    • Aa

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

  • FRANK S. WERBLIN (a1)
Abstract
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.

Copyright
Corresponding author
*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
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

S.A. Baccus , B.P. Olveczky , M. Manu & M. Meister (2008). A retinal circuit that computes object motion. The Journal of Neuroscience 28, 68076817.

H.B. Barlow & W.R. Levick (1965). The mechanism of directionally selective units in rabbit’s retina. The Journal of Physiology 178, 477504.

J.H. Belgum , D.R. Dvorak & J.S. McReynolds (1982). Light-evoked sustained inhibition in mudpuppy retinal ganglion cells. Vision Research 22, 257260.

J.H. Belgum , D.R. Dvorak , J.S. McReynolds & E. Miyachi (1987). Push-pull effect of surround illumination on excitatory and inhibitory inputs to mudpuppy retinal ganglion cells. The Journal of Physiology 388, 233243.

J.E. Dowling (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, 205228.

J.E. Dowling & B.B. Boycott (1965). Neural connections of the retina: Fine structure of the inner plexiform layer. Cold Spring Harbor Symposia on Quantitative Biology 30, 393402.

J.E. Dowling & B.B. Boycott (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London B: Biological Sciences 166, 80111.

C. Enroth-Cugell & A.W. Freeman (1987). The receptive-field spatial structure of cat retinal Y cells. The Journal of Physiology 384, 4979.

C. Enroth-Cugell & J.G. Robson (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517552.

T. Euler , P.B. Detwiler & W. Denk (2002). Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845852.

S.I. Fried , T.A. Munch & F.S. Werblin (2002). Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411414.

S.I. Fried , T.A. Munch & F.S. Werblin (2005). Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46, 117127.

P. Gaudiano (1994). Simulations of X and Y retinal ganglion cell behavior with a nonlinear push-pull model of spatiotemporal retinal processing. Vision Research 34, 17671784.

D.I. Hamasaki & V.G. Sutija (1979). Classification of cat retinal ganglion cells into X- and Y-cells with a contrast reversal stimulus. Experimental Brain Research 35, 2536.

D.I. Hamasaki , K. Tasaki & H. Suzuki (1979). Properties of X- and Y-cells in the rabbit retina. The Japanese Journal of Physiology 29, 445457.

H.K. Hartline & F. Ratliff (1957). Inhibitory interaction of receptor units in the eye of limulus. The Journal of General Physiology 40, 357376.

S. Haverkamp , U. Muller , K. Harvey , R.J. Harvey , H. Betz & H. Wassle (2003). Diversity of glycine receptors in the mouse retina: Localization of the alpha3 subunit. The Journal of Comparative Neurology 465, 524539.

S. Haverkamp , U. Muller , H.U. Zeilhofer , R.J. Harvey & H. Wassle (2004). Diversity of glycine receptors in the mouse retina: Localization of the alpha2 subunit. The Journal of Comparative Neurology 477, 399411.

R. Heidelberger , W.B. Thoreson & P. Witkovsky (2005). Synaptic transmission at retinal ribbon synapses. Progress in Retinal and Eye Research 24, 682720.

L. Heinze , R.J. Harvey , S. Haverkamp & H. Wassle (2007). Diversity of glycine receptors in the mouse retina: Localization of the alpha4 subunit. The Journal of Comparative Neurology 500, 693707.

J.A. Hirsch (2003). Synaptic physiology and receptive field structure in the early visual pathway of the cat. Cerebral Cortex 13, 6369.

S. Hochstein & R.M. Shapley (1976 a). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. The Journal of Physiology 262, 265284.

S. Hochstein & R.M. Shapley (1976 b). Quantitative analysis of retinal ganglion cell classifications. The Journal of Physiology 262, 237264.

H.A. Hsueh , A. Molnar & F.S. Werblin (2008). Amacrine-to-amacrine cell inhibition in the rabbit retina. Journal of Neurophysiology 100, 20772088.

H.G. Jakiela & C. Enroth-Cugell (1976). Adaptation and dynamics in X-cells and Y-cells of the cat retina. Experimental Brain Research 24, 335342.

B. Katz & R. Miledi (1967). A study of synaptic transmission in the absence of nerve impulses. The Journal of Physiology 192, 407436.

S. Lee & Z.J. Zhou (2006). The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787799.

W.R. Levick (1965). Receptive fields of rabbit retinal ganglion cells. American Journal of Optometry & Archives of American Academy of Optometry 42, 337343.

R.A. Linsenmeier , L.J. Frishman , H.G. Jakiela & C. Enroth-Cugell (1982). Receptive field properties of x and y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 11731183.

M.B. Manookin , D.L. Beaudoin , Z.R. Ernst , L.J. Flagel & J.B. Demb (2008). Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. The Journal of Neuroscience 28, 41364150.

N. Menger , D.V. Pow & H. Wassle (1998). Glycinergic amacrine cells of the rat retina. The Journal of Comparative Neurology 401, 3446.

A. Molnar , H.A. Hsueh , B. Roska & F.S. Werblin (2009). Crossover inhibition in the retina: Circuitry that compensates for nonlinear rectifying synaptic transmission. Journal of Computational Neuroscience 27, 569590.

A. Molnar & F. Werblin (2007). Inhibitory feedback shapes bipolar cell responses in the rabbit retina. Journal of Neurophysiology 98, 34233435.

J.J. Pang , F. Gao & S.M. Wu (2007). Cross-talk between ON and OFF channels in the salamander retina: Indirect bipolar cell inputs to ON-OFF ganglion cells. Vision Research 47, 384392.

K. Rabl , T. Banvolgyi & R. Gabriel (2002). Electrophysiological evidence for push-pull interactions in the inner retina of turtle. Acta Biologica Hungarica 53, 141151.

J. Richter & S. Ullman (1982). A model for the temporal organization of X- and Y-type receptive fields in the primate retina. Biological Cybernetics 43, 127145.

B. Roska , A. Molnar & F.S. Werblin (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, 38103822.

B. Roska & F. Werblin (2001). Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature 410, 583587.

W.B. Thoreson , K. Rabl , E. Townes-Anderson & R. Heidelberger (2004). A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595605.

J. Toyoda , K. Shimbo , H. Kondo & T. Kujiraoka (1992). Push-pull modulation of ganglion cell responses of carp retina by amacrine cells. Neuroscience Letters 142, 4144.

J.B. Troy & C. Enroth-Cugell (1993). X and Y ganglion cells inform the cat’s brain about contrast in the retinal image. Experimental Brain Research 93, 383390.

M. van Wyk , W.R. Taylor & D.I. Vaney (2006). Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina. The Journal of Neuroscience 26, 1325013263.

L. Vitanova , S. Haverkamp & H. Wassle (2004). Immunocytochemical localization of glycine and glycine receptors in the retina of the frog Rana ridibunda. Cell and Tissue Research 317, 227235.

J. Weiss , G.A. O’Sullivan , L. Heinze , H.X. Chen , H. Betz & H. Wassle (2008). Glycinergic input of small-field amacrine cells in the retinas of wildtype and glycine receptor deficient mice. Molecular and Cellular Neurosciences 37, 4055.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords: