Temporal Limits of Visual Motion Processing: Psychophysics and Neurophysiology

Under optimal conditions, just 3–6 ms of visual stimulation suffices for humans to see motion. Motion perception on this time scale implies that the visual system under these conditions reliably encodes, transmits, and processes neural signals with near-millisecond precision. Motivated by in vitro evidence for high temporal precision of motion signals in the primate retina, we investigated how neuronal and perceptual limits of motion encoding relate. Specifically, we examined the correspondence between the time scale at which cat retinal ganglion cells in vivo represent motion information and temporal thresholds for human motion discrimination. The time scale for motion encoding by ganglion cells ranged from 4.6–91 ms, depended nonlinearly on temporal frequency but not on contrast. Human psychophysics revealed that minimal stimulus durations required for perceiving motion direction were similarly brief, 5.6–65 ms, similarly depended on temporal frequency but, above ~10%, not on contrast. Notably, physiological and psychophysical measurements corresponded closely throughout (r = 0.99), despite more than a 20-fold variation in both human thresholds and optimal time scales for motion encoding in the retina. These results demonstrate that neural circuits for motion vision in cortex can maintain and make use of the high temporal fidelity of the retinal output signals.

[1]  R C Reid,et al.  Efficient Coding of Natural Scenes in the Lateral Geniculate Nucleus: Experimental Test of a Computational Theory , 1996, The Journal of Neuroscience.

[2]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[3]  D. Mastronarde Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. , 1983, Journal of neurophysiology.

[4]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[5]  U. Eysel,et al.  Fluorescent tube light evokes flicker responses in visual neurons , 1984, Vision Research.

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

[7]  Mark C. W. van Rossum,et al.  A Novel Spike Distance , 2001, Neural Computation.

[8]  D. Burr,et al.  Contrast sensitivity at high velocities , 1982, Vision Research.

[9]  B. Knight,et al.  Response variability and timing precision of neuronal spike trains in vivo. , 1997, Journal of neurophysiology.

[10]  M. Wong-Riley,et al.  Primate Visual Cortex , 1994 .

[11]  Randolph Blake,et al.  Fine Temporal Properties of Center–Surround Interactions in Motion Revealed by Reverse Correlation , 2006, The Journal of Neuroscience.

[12]  R. Shapley,et al.  The use of m-sequences in the analysis of visual neurons: Linear receptive field properties , 1997, Visual Neuroscience.

[13]  R. Vautin,et al.  Magnification factor and receptive field size in foveal striate cortex of the monkey , 2004, Experimental Brain Research.

[14]  J. M Zanker,et al.  On temporal hyperacuity in the human visual system , 2002, Vision Research.

[15]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[16]  Michael J. Black,et al.  Visual Orientation and Directional Selectivity through Thalamic Synchrony , 2012, The Journal of Neuroscience.

[17]  K. Nakayama,et al.  Detection and discrimination of sinusoidal grating displacements. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[18]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[19]  A. Watson,et al.  The optimal motion stimulus , 1995, Vision Research.

[20]  R. Reid,et al.  Predicting Every Spike A Model for the Responses of Visual Neurons , 2001, Neuron.

[21]  Alexander Thiele,et al.  Speed skills: measuring the visual speed analyzing properties of primate MT neurons , 2001, Nature Neuroscience.

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

[23]  E. Chichilnisky,et al.  Precision of spike trains in primate retinal ganglion cells. , 2004, Journal of neurophysiology.

[24]  E. Chichilnisky,et al.  Temporal Resolution of Ensemble Visual Motion Signals in Primate Retina , 2003, The Journal of Neuroscience.

[25]  Claude Shannon Information theory in the brain , 2000 .

[26]  Marla B Feller,et al.  Vision and the establishment of direction-selectivity: a tale of two circuits , 2009, Current Opinion in Neurobiology.

[27]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[28]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[29]  C Wehrhahn,et al.  ON- and OFF-pathways form separate neural substrates for motion perception: psychophysical evidence , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Timothy J. Blanche,et al.  Construction of Direction Selectivity through Local Energy Computations in Primary Visual Cortex , 2013, PloS one.

[31]  D. Pollen,et al.  Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. , 1985, The Journal of physiology.

[32]  J J Koenderink,et al.  Influence of contrast on foveal and peripheral detection of coherent motion in moving random-dot patterns. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[33]  B. Fairbank Moving and Nonmoving Visual Stimuli: A Reaction Time Study , 1969, Perceptual and motor skills.

[34]  Valentin Dragoi,et al.  Sensory coding accuracy and perceptual performance are improved during the desynchronized cortical state , 2017, Nature Communications.

[35]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[36]  D. Teller Linking propositions , 1984, Vision Research.

[37]  D. H. Kelly Adaptation effects on spatio-temporal sine-wave thresholds. , 1972, Vision research.

[38]  R. Reid,et al.  Precise Firing Events Are Conserved across Neurons , 2002, The Journal of Neuroscience.

[39]  R. Freeman,et al.  The Derivation of Direction Selectivity in the Striate Cortex , 2004, The Journal of Neuroscience.

[40]  Chun-I Yeh,et al.  Temporal precision in the neural code and the timescales of natural vision , 2007, Nature.

[41]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[42]  S. Nishida,et al.  Contrast Sensitivity of the Motion System , 1996, Vision Research.

[43]  F. Rieke,et al.  Chromatic detection from cone photoreceptors to V1 neurons to behavior in rhesus monkeys. , 2015, Journal of vision.

[44]  T. Albright,et al.  Efficient Discrimination of Temporal Patterns by Motion-Sensitive Neurons in Primate Visual Cortex , 1998, Neuron.

[45]  Duje Tadin,et al.  Increasing stimulus size impairs first- but not second-order motion perception. , 2011, Journal of vision.

[46]  A. Sweet,et al.  Temporal discrimination by the human eye. , 1953, The American journal of psychology.

[47]  Fred Rieke,et al.  Origin and Impact of Phototransduction Noise in Primate Cone Photoreceptors , 2013, Nature Neuroscience.

[48]  Davis M. Glasser,et al.  High temporal precision for perceiving event offsets , 2010, Vision Research.

[49]  E. Chichilnisky,et al.  Functional Asymmetries in ON and OFF Ganglion Cells of Primate Retina , 2002, The Journal of Neuroscience.

[50]  Bart G. Borghuis,et al.  Spike timing precision in the visual front-end , 2003 .

[51]  D. Burr,et al.  Dependency of reaction times to motion onset on luminance and chromatic contrast , 2001, Vision Research.

[52]  Alex M. Kale,et al.  Sex Differences in Visual Motion Processing , 2018, Current Biology.

[53]  K. Purpura,et al.  Response variability in retinal ganglion cells of primates. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Tadin Suppressive mechanisms in visual motion processing: From perception to intelligence , 2015, Vision Research.

[55]  Suzanne P. McKee,et al.  Perception of temporal order in adjacent visual stimuli , 1977, Vision Research.

[56]  Randolph Blake,et al.  Perceptual consequences of centre–surround antagonism in visual motion processing , 2003, Nature.

[57]  D. Mastronarde Interactions between ganglion cells in cat retina. , 1983, Journal of neurophysiology.

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

[59]  E. Chichilnisky,et al.  Fidelity of the ensemble code for visual motion in primate retina. , 2005, Journal of neurophysiology.

[60]  M W Levine,et al.  Common noise in the firing of neighbouring ganglion cells in goldfish retina. , 1984, The Journal of physiology.