Oculomotor synchronization of visual responses in modeled populations of retinal ganglion cells.

We have recently shown that fixational eye movements improve discrimination of the orientation of a high spatial frequency grating masked by low-frequency noise, but do not help with a low-frequency grating masked by high-frequency noise (M. Rucci, R. Iovin, M. Poletti, & F. Santini, 2007). In this study, we explored the neural mechanisms responsible for this phenomenon. Models of parvocellular ganglion cells were stimulated by the same visual input experienced by subjects in our psychophysical experiments, i.e., the spatiotemporal signals resulting from viewing stimuli during eye movements. We show that the spatial organization of correlated activity in the model predicts the subjects' performance in the experiments. During viewing of high-frequency gratings, fixational eye movements modulated the responses of modeled neurons in a way that depended on the relative alignment of cell receptive fields. Responses covaried strongly only when receptive fields were aligned parallel to the grating's orientation. Such a dependence on the axis of receptive-field alignment did not occur during viewing of low-frequency gratings. In this case, the responses of cells on the parallel and orthogonal axes were similarly affected by eye movements. These results support a role for oculomotor synchronization of neural activity in the representation of visual information in the retina.

[1]  D. Snodderly,et al.  Response Variability of Neurons in Primary Visual Cortex (V1) of Alert Monkeys , 1997, The Journal of Neuroscience.

[2]  A. Casile,et al.  A Theoretical Analysis of the Influence of Fixational Instability on the Development of Thalamocortical Connectivity , 2006 .

[3]  Victor A. F. Lamme,et al.  Synchrony and covariation of firing rates in the primary visual cortex during contour grouping , 2004, Nature Neuroscience.

[4]  A. A. Skavenski,et al.  Quality of retinal image stabilization during small natural and artificial body rotations in man , 1979, Vision Research.

[5]  G. Edelman,et al.  Modeling LGN Responses during Free-Viewing: A Possible Role of Microscopic Eye Movements in the Refinement of Cortical Orientation Selectivity , 2000, The Journal of Neuroscience.

[6]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

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

[8]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[9]  R. Reid,et al.  Synaptic Interactions between Thalamic Inputs to Simple Cells in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[10]  M. Rucci,et al.  A model of the dynamics of retinal activity during natural visual fixation , 2007, Visual Neuroscience.

[11]  Nikos K. Logothetis,et al.  Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex , 1998, Experimental Brain Research.

[12]  R. Reid,et al.  Synchronous activity in the visual system. , 1999, Annual review of physiology.

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

[14]  A. A. Skavenski,et al.  Miniature eye movement. , 1973, Science.

[15]  Wolf Singer,et al.  Time as coding space? , 1999, Current Opinion in Neurobiology.

[16]  R. K. Simpson.  Nature Neuroscience , 2022 .

[17]  Markus Bongard,et al.  Retinal ganglion cell synchronization by fixational eye movements improves feature estimation , 2002, Nature Neuroscience.

[18]  WH Merigan,et al.  Chromatic and achromatic vision of macaques: role of the P pathway , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  C. Gray.  The Temporal Correlation Hypothesis of Visual Feature Integration Still Alive and Well , 1999, Neuron.

[20]  D. Snodderly,et al.  Selective activation of visual cortex neurons by fixational eye movements: Implications for neural coding , 2001, Visual Neuroscience.

[21]  D. Hubel,et al.  The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  L. Arend.  Spatial differential and integral operations in human vision: implications of stabilized retinal image fading. , 1973, Psychological review.

[23]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[24]  J. Changeux,et al.  Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks , 1976, Nature.

[25]  Patrick Cavanagh,et al.  A jitter after-effect reveals motion-based stabilization of vision , 1998, Nature.

[26]  J. Bendat,et al.  Random Data: Analysis and Measurement Procedures , 1987 .

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

[28]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

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

[30]  R. W. DITCHBURN,et al.  Vision with a Stabilized Retinal Image , 1952, Nature.

[31]  Michele Rucci,et al.  Decorrelation of neural activity during fixational instability: Possible implications for the refinement of V1 receptive fields , 2004, Visual Neuroscience.

[32]  F. W. Weymouth,et al.  Visual perception and the retinal mosaic. II. The influence of eye-movements on the displacement threshold. , 1925 .

[33]  Michele Rucci,et al.  EyeRIS: A general-purpose system for eye-movement-contingent display control , 2007, Behavior research methods.

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

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

[36]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[37]  F. Attneave.  Some informational aspects of visual perception. , 1954, Psychological review.

[38]  A. L. I︠A︡rbus.  Eye Movements and Vision , 1967 .

[39]  E. Kaplan,et al.  The receptive field of the primate P retinal ganglion cell, I: Linear dynamics , 1997, Visual Neuroscience.

[40]  L. Riggs,et al.  Involuntary motions of the eye during monocular fixation. , 1950, Journal of experimental psychology.

[41]  D J Field,et al.  Relations between the statistics of natural images and the response properties of cortical cells. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[42]  Martina Poletti,et al.  Miniature eye movements enhance fine spatial detail , 2007, Nature.

[43]  R. Reid,et al.  Precisely correlated firing in cells of the lateral geniculate nucleus , 1996, Nature.

[44]  R. Steinman,et al.  The role of eye movement in the detection of contrast and spatial detail. , 1990, Reviews of oculomotor research.

[45]  Eileen Kowler.  Eye movements and their role in visual and cognitive processes. , 1990, Reviews of oculomotor research.

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

[47]  Ehud Ahissar,et al.  Figuring Space by Time , 2001, Neuron.

[48]  Nicole C. Rust,et al.  Do We Know What the Early Visual System Does? , 2005, The Journal of Neuroscience.

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

[50]  Steinman Rm,et al.  The role of eye movement in the detection of contrast and spatial detail. , 1990 .

[51]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[52]  Michele Rucci,et al.  Fixational instability and natural image statistics: Implications for early visual representations , 2005, Network.