Consequences of the Oculomotor Cycle for the Dynamics of Perception

Much evidence indicates that humans and other species process large-scale visual information before fine spatial detail. Neurophysiological data obtained with paralyzed eyes suggest that this coarse-to-fine sequence results from spatiotemporal filtering by neurons in the early visual pathway. However, the eyes are normally never stationary: rapid gaze shifts (saccades) incessantly alternate with slow fixational movements. To investigate the consequences of this oculomotor cycle on the dynamics of perception, we combined spectral analysis of visual input signals, neural modeling, and gaze-contingent control of retinal stimulation in humans. We show that the saccade/fixation cycle reformats the flow impinging on the retina in a way that initiates coarse-to-fine processing at each fixation. This finding reveals that the visual system uses oculomotor-induced temporal modulations to sequentially encode different spatial components and suggests that, rather than initiating coarse-to-fine processing, spatiotemporal coupling in the early visual pathway builds on the information dynamics of the oculomotor cycle.

[1]  R. Watt Scanning from coarse to fine spatial scales in the human visual system after the onset of a stimulus. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[2]  Martina Poletti,et al.  Control and Functions of Fixational Eye Movements. , 2015, Annual review of vision science.

[3]  Bruno Breitmeyer,et al.  The role of on and off transients in determining the psychophysical spatial frequency response , 1975, Vision Research.

[4]  H. Collewijn,et al.  The significance of microsaccades for vision and oculomotor control. , 2008, Journal of vision.

[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]  M. Bar,et al.  Magnocellular Projections as the Trigger of Top-Down Facilitation in Recognition , 2007, The Journal of Neuroscience.

[7]  Dario L Ringach,et al.  Dynamics of receptive field size in primary visual cortex. , 2007, Journal of neurophysiology.

[8]  Maria Concetta Morrone,et al.  Spatiotopic coding and remapping in humans , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  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.

[10]  D. Snodderly,et al.  Saccades and drifts differentially modulate neuronal activity in V1: effects of retinal image motion, position, and extraretinal influences. , 2008, Journal of vision.

[11]  D. Burr,et al.  Changes in visual perception at the time of saccades , 2001, Trends in Neurosciences.

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

[13]  Martina Poletti,et al.  Head-Eye Coordination at a Microscopic Scale , 2015, Current Biology.

[14]  J. Robson Spatial and Temporal Contrast-Sensitivity Functions of the Visual System , 1966 .

[15]  M. Rucci,et al.  Contributions of fixational eye movements to the discrimination of briefly presented stimuli. , 2003, Journal of vision.

[16]  Temporal sensitivity of the human visual system to sinusoidal gratings. , 1980, Journal of the Optical Society of America.

[17]  D. Ringach,et al.  Dynamics of Spatial Frequency Tuning in Macaque V1 , 2002, The Journal of Neuroscience.

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

[19]  M. M. Taylor,et al.  PEST: Efficient Estimates on Probability Functions , 1967 .

[20]  Eileen Kowler Eye movements: The past 25years , 2011, Vision Research.

[21]  Felix Wichmann,et al.  The psychometric function: II. Bootstrap-based confidence intervals and sampling , 2001, Perception & psychophysics.

[22]  D. Burr Temporal summation of moving images by the human visual system , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[24]  Peter Neri,et al.  Coarse to fine dynamics of monocular and binocular processing in human pattern vision , 2011, Proceedings of the National Academy of Sciences.

[25]  J. L. Hall Hybrid adaptive procedure for estimation of psychometric functions. , 1980, The Journal of the Acoustical Society of America.

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

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

[28]  K. Fujii,et al.  Visualization for the analysis of fluid motion , 2005, J. Vis..

[29]  Nikos K Logothetis,et al.  The color-opponent and broad-band channels of the primate visual system , 1990, Trends in Neurosciences.

[30]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.

[31]  M. Webster,et al.  Contrast adaptation and the spatial structure of natural images. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[33]  C W Tyler,et al.  Colour bit-stealing to enhance the luminance resolution of digital displays on a single pixel basis. , 1997, Spatial vision.

[34]  David Burr,et al.  Suppression of the magnocellular pathway during saccades , 1996, Behavioural Brain Research.

[35]  J. Victor,et al.  The unsteady eye: an information-processing stage, not a bug , 2015, Trends in Neurosciences.

[36]  Rémy Allard,et al.  The noisy-bit method for digital displays: Converting a 256 luminance resolution into a continuous resolution , 2008, Behavior research methods.

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

[38]  M. Ibbotson,et al.  Visual perception and saccadic eye movements , 2011, Current Opinion in Neurobiology.

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

[40]  A. Derrington The lateral geniculate nucleus , 2001, Current Biology.

[41]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[42]  Martina Poletti,et al.  A compact field guide to the study of microsaccades: Challenges and functions , 2016, Vision Research.

[43]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[44]  Martina Poletti,et al.  Eye movements under various conditions of image fading. , 2010, Journal of vision.

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

[46]  Martina Poletti,et al.  Microscopic Eye Movements Compensate for Nonhomogeneous Vision within the Fovea , 2013, Current Biology.

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

[48]  P. H. Schiller,et al.  Spatial frequency and orientation tuning dynamics in area V1 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Nathan J Hall,et al.  Remapping for visual stability , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  Joseph L. Mundy,et al.  Change Detection , 2014, Computer Vision, A Reference Guide.

[51]  J. Victor,et al.  Temporal Encoding of Spatial Information during Active Visual Fixation , 2012, Current Biology.

[52]  J. P. Jones,et al.  An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[53]  Michele Rucci,et al.  The Visual Input to the Retina during Natural Head-Free Fixation , 2014, The Journal of Neuroscience.

[54]  R. Wurtz Neuronal mechanisms of visual stability , 2008, Vision Research.

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

[56]  A. Oliva,et al.  From Blobs to Boundary Edges: Evidence for Time- and Spatial-Scale-Dependent Scene Recognition , 1994 .

[57]  J. Hegdé Time course of visual perception: Coarse-to-fine processing and beyond , 2008, Progress in Neurobiology.