Chapter 2 The dynamics of primate retinal ganglion cells

A knowledge of the dynamics (temporal properties) of neuronal populations is essential for an understanding of their function, and is also crucial when one attempts to develop computational or mathematical models of the neurons. Here we review the temporal properties of the receptive fields (RFs) of the two best-studied types of ganglion cells in the primate retina, those that project to the parvocellular (P) and magnocellular (M) layers of the dorsal lateral geniculate nucleus. The center and surround mechanisms of the P RFs are approximately linear, and their impulse responses are very similar, although the surround lags the center by a few milliseconds. The center and surround are chromatically opponent. With the appropriate stimulus, one can find significant nonlinearities in their responses, and also in the interaction between the center and surround. The phase lag between the responses of the center and surround depends on the temporal frequency, so that at high temporal frequency the antagonism between them is reduced or abolished. The temporal responses of M cells are nonlinear, and with increasing contrast they show the effects of a contrast gain control. The different dynamical properties of the two populations suggest that M cells participate in motion analysis, while P cells are used for the analysis of form, texture, and perhaps color.

[1]  J. B. Demb,et al.  Functional Circuitry of the Retinal Ganglion Cell's Nonlinear Receptive Field , 1999, The Journal of Neuroscience.

[2]  C. R. Ingling,et al.  The relationship between spectral sensitivity and spatial sensitivity for the primate r-g X-channel , 1983, Vision Research.

[3]  Joseph J. Atick,et al.  What Does the Retina Know about Natural Scenes? , 1992, Neural Computation.

[4]  W. Paulus,et al.  A new concept of retinal colour coding , 1983, Vision Research.

[5]  John H. R. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

[6]  H. D. L. Dzn Research into the Dynamic Nature of the Human Fovea→Cortex Systems with Intermittent and Modulated Light. II. Phase Shift in Brightness and Delay in Color Perception , 1958 .

[7]  A. Valberg,et al.  Possible contributions of magnocellular- and parvocellular-pathway cells to transient VEPs , 1997, Visual Neuroscience.

[8]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[9]  B. Knight,et al.  Contrast gain control in the primate retina: P cells are not X-like, some M cells are , 1992, Visual Neuroscience.

[10]  Michael S. Landy,et al.  Computational models of visual processing , 1991 .

[11]  L. Croner,et al.  Receptive fields of P and M ganglion cells across the primate retina , 1995, Vision Research.

[12]  V. Casagrande A third parallel visual pathway to primate area V1 , 1994, Trends in Neurosciences.

[13]  D. Tranchina,et al.  Retinal light adaptation—evidence for a feedback mechanism , 1984, Nature.

[14]  R. W. Rodieck,et al.  Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus , 1993, The Journal of comparative neurology.

[15]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[16]  H. D. L. Dzn Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. I. Attenuation characteristics with white and colored light. , 1958 .

[17]  R. Shapley,et al.  Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. , 1976, The Journal of physiology.

[18]  N Milkman,et al.  Superposition of excitatory and inhibitory influences in the retina of Limulus: effect of delayed inhibition. , 1970, Proceedings of the National Academy of Sciences of the United States of America.

[19]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

[20]  D. Hubel,et al.  Specificity of intrinsic connections in primate primary visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  P. Gouras,et al.  Functional properties of ganglion cells of the rhesus monkey retina. , 1975, The Journal of physiology.

[22]  J. Pokorny,et al.  Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. , 1992, The Journal of physiology.

[23]  A Valberg,et al.  Visual evoked potentials and magnocellular and parvocellular segregation , 2000, Visual Neuroscience.

[24]  豊田 順一 The retinal basis of vision , 1999 .

[25]  E. Kaplan,et al.  Dynamics of primate P retinal ganglion cells: responses to chromatic and achromatic stimuli , 1999, The Journal of physiology.

[26]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[27]  R. Shapley,et al.  Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus , 1992, Nature.

[28]  E. Sutter,et al.  M and P Components of the VEP and their Visual Field Distribution , 1997, Vision Research.

[29]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[30]  A. Cowey,et al.  Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey , 1984, Neuroscience.

[31]  Bb Lee,et al.  Nonlinear summation of M- and L-cone inputs to phasic retinal ganglion cells of the macaque , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  R. Shapley,et al.  Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. , 1979, The Journal of physiology.

[33]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[34]  E. Kaplan,et al.  The dynamics of primate M retinal ganglion cells , 1999, Visual Neuroscience.

[35]  P Gouras,et al.  Enchancement of luminance flicker by color-opponent mechanisms. , 1979, Science.

[36]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

[37]  Richard H Masland,et al.  Extreme Diversity among Amacrine Cells: Implications for Function , 1998, Neuron.

[38]  M. Wong-Riley,et al.  Quantitative light and electron microscopic analysis of cytochrome oxidase‐rich zones in the striate cortex of the squirrel monkey , 1984, The Journal of comparative neurology.

[39]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[40]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[41]  D. Dacey Parallel pathways for spectral coding in primate retina. , 2000, Annual review of neuroscience.

[42]  H. Spekreijse,et al.  The “silent substitution” method in visual research , 1982, Vision Research.

[43]  C. Enroth-Cugell,et al.  Suppression of cat retinal ganglion cell responses by moving patterns. , 1980, The Journal of physiology.

[44]  B. Boycott,et al.  The morphological types of ganglion cells of the domestic cat's retina , 1974, The Journal of physiology.

[45]  David J. Calkins,et al.  Evidence that Circuits for Spatial and Color Vision Segregate at the First Retinal Synapse , 1999, Neuron.

[46]  T. Yoshioka,et al.  A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. , 1994, Science.

[47]  R. W. Rodieck,et al.  Parasol and midget ganglion cells of the human retina , 1985, The Journal of comparative neurology.

[48]  S. Shipp,et al.  The functional logic of cortical connections , 1988, Nature.

[49]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Shapley,et al.  The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry , 1984, Vision Research.

[51]  C. Enroth-Cugell,et al.  Spatiotemporal frequency responses of cat retinal ganglion cells , 1987, The Journal of general physiology.

[52]  B. Boycott,et al.  Parallel processing in the mammalian retina: the Proctor Lecture. , 1999, Investigative ophthalmology & visual science.

[53]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[54]  Joel Pokorny,et al.  Responses to pulses and sinusoids in macaque ganglion cells , 1994, Vision Research.

[55]  R. Shapley,et al.  Light adaptation in the primate retina: Analysis of changes in gain and dynamics of monkey retinal ganglion cells , 1990, Visual Neuroscience.

[56]  B. Boycott,et al.  The mosaic of horizontal cells in the macaque monkey retina: With a comment on biplexiform ganglion cells , 2000, Visual Neuroscience.

[57]  Barry B. Lee,et al.  Chapter 7 New views of primate retinal function , 1990 .

[58]  E Kaplan,et al.  Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. , 1979, The Journal of physiology.

[59]  A. Klistorner,et al.  Separate magnocellular and parvocellular contributions from temporal analysis of the multifocal VEP , 1997, Vision Research.

[60]  F. Dodge,et al.  Voltage Noise in Limulus Visual Cells , 1968, Science.

[61]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[62]  B W Knight,et al.  On tuning and amplification by lateral inhibition. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Michael S. Landy,et al.  The Design of Chromatically Opponent Receptive Fields , 1991 .

[64]  C. Enroth-Cugell,et al.  Flux, not retinal illumination, is what cat retinal ganglion cells really care about , 1973, The Journal of physiology.

[65]  J. Victor The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[66]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[67]  P. Gouras Identification of cone mechanisms in monkey ganglion cells , 1968, The Journal of physiology.

[68]  E. Kaplan,et al.  The receptive field of the primate P retinal ganglion cell, II: Nonlinear dynamics , 1997, Visual Neuroscience.

[69]  B. B. Lee,et al.  Amplitude and phase of responses of macaque retinal ganglion cells to flickering stimuli. , 1989, The Journal of physiology.

[70]  B. B. Lee,et al.  Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker. , 1989, The Journal of physiology.

[71]  D. Tranchina,et al.  Light adaptation in the turtle retina: embedding a parametric family of linear models in a single nonlinear model , 1988, Visual Neuroscience.

[72]  R. Shapley,et al.  X and Y cells in the lateral geniculate nucleus of macaque monkeys. , 1982, The Journal of physiology.

[73]  D. Dacey Primate retina: cell types, circuits and color opponency , 1999, Progress in Retinal and Eye Research.

[74]  J. M. Hopkins,et al.  Cone connections of the horizontal cells of the rhesus monkey’s retina , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[75]  J. Victor The dynamics of the cat retinal Y cell subunit. , 1988, The Journal of physiology.