Motion perception during sinusoidal smooth pursuit eye movements: signal latencies and non-linearities.

Smooth pursuit eye movements add motion to the retinal image. To compensate, the visual system can combine estimates of pursuit velocity and retinal motion to recover motion with respect to the head. Little attention has been paid to the temporal characteristics of this compensation process. Here, we describe how the latency difference between the eye movement signal and the retinal signal can be measured for motion perception during sinusoidal pursuit. In two experiments, observers compared the peak velocity of a motion stimulus presented in pursuit and fixation intervals. Both the pursuit target and the motion stimulus moved with a sinusoidal profile. The phase and amplitude of the motion stimulus were varied systematically in different conditions, along with the amplitude of pursuit. The latency difference between the eye movement signal and the retinal signal was measured by fitting the standard linear model and a non-linear variant to the observed velocity matches. We found that the eye movement signal lagged the retinal signal by a small amount. The non-linear model fitted the velocity matches better than the linear one and this difference increased with pursuit amplitude. The results support previous claims that the visual system estimates eye movement velocity and retinal velocity in a non-linear fashion and that the latency difference between the two signals is small.

[1]  Jan L. Souman,et al.  Perceived motion direction during smooth pursuit eye movements , 2005, Experimental Brain Research.

[2]  Ravi S. Menon,et al.  Interaction of Retinal Image and Eye Velocity in Motion Perception , 2003, Neuron.

[3]  T J Sejnowski,et al.  Motion integration and postdiction in visual awareness. , 2000, Science.

[4]  Christopher C. Pack,et al.  A Neural Model of Smooth Pursuit Control and Motion Perception by Cortical Area MST , 2001, Journal of Cognitive Neuroscience.

[5]  Jan L. Souman,et al.  Vertical object motion during horizontal ocular pursuit: compensation for eye movements increases with presentation duration , 2005, Vision Research.

[6]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[7]  P. Cavanagh,et al.  Illusory spatial offset of a flash relative to a moving stimulus is caused by differential latencies for moving and flashed stimuli , 2000, Vision Research.

[8]  Harold E Bedell,et al.  Differential latencies and the dynamics of the position computation process for moving targets, assessed with the flash-lag effect , 2004, Vision Research.

[9]  Richard A Andersen,et al.  Pursuit Compensation during Self-Motion , 2001, Perception.

[10]  Romi Nijhawan,et al.  Motion extrapolation in catching , 1994, Nature.

[11]  A. Wertheim,et al.  An Acceleration Illusion Caused by Underestimation of Stimulus Velocity during Pursuit Eye Movements: Aubert–Fleischl Revisited , 1990, Perception.

[12]  R. Andersen,et al.  Mechanisms of Heading Perception in Primate Visual Cortex , 1996, Science.

[13]  Eli Brenner,et al.  Smooth eye movements and spatial localisation , 2001, Vision Research.

[14]  Peter Thier,et al.  Modification of the filehne illusion by conditioning visual stimuli , 1996, Vision Research.

[15]  A. Fuchs,et al.  Relationship between eye acceleration and retinal image velocity during foveal smooth pursuit in man and monkey. , 1981, Journal of neurophysiology.

[16]  I. Murakami,et al.  Latency difference, not spatial extrapolation , 1998, Nature Neuroscience.

[17]  J A Crowell,et al.  Extraretinal and retinal amplitude and phase errors during Filehne illusion and path perception , 2000, Perception & psychophysics.

[18]  Edward Herman,et al.  The loss of position constancy during pursuit eye movements , 1978, Vision Research.

[19]  R Nijhawan,et al.  The Flash-Lag Phenomenon: Object Motion and Eye Movements , 2001, Perception.

[20]  Andrew T. Smith,et al.  Visual detection of motion , 1994 .

[21]  A. Wertheim,et al.  Retinal and Extraretinal Information in Movement Perception: How to Invert the Filehne Illusion , 1987, Perception.

[22]  Kathleen A Turano,et al.  Eye movements affect the perceived speed of visual motion , 1999, Vision Research.

[23]  H. Leibowitz,et al.  A revised analysis of the role of efference in motion perception. , 1985, Perception.

[24]  P. Thier,et al.  Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target. , 2003, Journal of neurophysiology.

[25]  E. Holst,et al.  Das Reafferenzprinzip , 2004, Naturwissenschaften.

[26]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[27]  H. Akaike.  A new look at the statistical model identification , 1974 .

[28]  R. Andersen.  Visual and eye movement functions of the posterior parietal cortex. , 1989, Annual review of neuroscience.

[29]  Mark A. Georgeson,et al.  Fixed or variable noise in contrast discrimination? The jury’s still out… , 2006, Vision Research.

[30]  J. Tarnai.  Psychophysical Scaling of Attachment and Loss. , 1983 .

[31]  E. Batschelet.  Circular statistics in biology , 1981 .

[32]  A. A. Skavenski.  Inflow as a source of extraretinal eye position information. , 1972, Vision research.

[33]  J. Vercher,et al.  The role of ocular muscle proprioception in visual localization of targets. , 1990, Science.

[34]  Eli Brenner,et al.  Judging object velocity during smooth pursuit eye movements , 2004, Experimental Brain Research.

[35]  B. Graaf,et al.  The perception of object motion during smooth pursuit eye movements: Adjacency is not a factor contributing to the filehne illusion , 1988, Vision Research.

[36]  Mingsha Zhang,et al.  The proprioceptive representation of eye position in monkey primary somatosensory cortex , 2007, Nature Neuroscience.

[37]  Harold E. Bedell,et al.  Direction and extent of perceived motion smear during pursuit eye movement , 2007, Vision Research.

[38]  Saumil S. Patel,et al.  The attenuation of perceived motion smear during combined eye and head movements , 2006, Vision Research.

[39]  Alexander H. Wertheim,et al.  Motion perception during selfmotion: The direct versus inferential controversy revisited , 1994, Behavioral and Brain Sciences.

[40]  G. Barnes,et al.  Ocular pursuit responses to repeated, single-cycle sinusoids reveal behavior compatible with predictive pursuit. , 2000, Journal of neurophysiology.

[41]  R A Andersen,et al.  Influence of gaze rotation on the visual response of primate MSTd neurons. , 1999, Journal of neurophysiology.

[42]  Magnitude estimation of visual velocity. , 1972, The Journal of psychology.

[43]  David R. Anderson,et al.  Multimodel Inference , 2004 .

[44]  E Herman,et al.  Position Constancy during Pursuit Eye Movement: An Investigation of the Filehne Illusion , 1973, The Quarterly journal of experimental psychology.

[45]  Markus Lappe,et al.  Temporal recruitment along the trajectory of moving objects and the perception of position , 1999, Vision Research.

[46]  Peter Thier,et al.  Optimizing Visual Motion Perception during Eye Movements , 2001, Neuron.

[47]  R. Leigh,et al.  The neurology of eye movements , 2006 .

[48]  Robert W. Massof,et al.  Nonlinear contribution of eye velocity to motion perception , 2001, Vision Research.

[49]  R. M. Siegel,et al.  Neurons of area 7 activated by both visual stimuli and oculomotor behavior , 2004, Experimental Brain Research.

[50]  R. Andersen,et al.  The influence of the angle of gaze upon the excitability of the light- sensitive neurons of the posterior parietal cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  R. Sperry.  Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[52]  T. Mergner,et al.  Role of vestibular and neck inputs for the perception of object motion in space , 2004, Experimental Brain Research.

[53]  P. Thier,et al.  Posterior Parietal Cortex Neurons Encode Target Motion in World-Centered Coordinates , 2004, Neuron.

[54]  S Mateeff,et al.  Localization of brief visual stimuli during pursuit eye movements. , 1981, Acta psychologica.

[55]  A. Crawley,et al.  Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception , 1996, Annals of neurology.

[56]  Terrence J Sejnowski,et al.  Motion signals bias localization judgments: a unified explanation for the flash-lag, flash-drag, flash-jump, and Frohlich illusions. , 2007, Journal of vision.

[57]  Tom C.A. Freeman,et al.  Simultaneous adaptation of retinal and extra-retinal motion signals , 2007, Vision Research.

[58]  R S Kennedy,et al.  Psychophysical scaling of circular vection (CV) produced by optokinetic (OKN) motion: individual differences and effects of practice. , 1996, Journal of vestibular research : equilibrium & orientation.

[59]  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 .

[60]  Jan L. Souman,et al.  Frame of reference transformations in motion perception during smooth pursuit eye movements , 2006, Journal of Computational Neuroscience.

[61]  Martin S. Banks,et al.  Perceived head-centric speed is affected by both extra-retinal and retinal errors , 1998, Vision Research.

[62]  Masaki Tanaka,et al.  Smooth Pursuit Eye Movements , 2018 .

[63]  J. Senders,et al.  Eye Movements and Psychological Processes , 1976 .

[64]  G M Gauthier,et al.  Ocular muscle proprioception and visual localization of targets in man. , 1990, Brain : a journal of neurology.

[65]  E. Holst.  Relations between the central Nervous System and the peripheral organs , 1954 .

[66]  T. Freeman,et al.  Transducer models of head-centred motion perception , 2001, Vision Research.

[67]  Clifford M. Hurvich,et al.  Regression and time series model selection in small samples , 1989 .

[68]  Harold E. Bedell,et al.  Asymmetry of perceived motion smear during head and eye movements: Evidence for a dichotomous neural categorization of retinal image motion , 2005, Vision Research.

[69]  Hiroshi Shono.  Efficiency of the finite correction of Akaike's Information Criteria. , 2000 .

[70]  M. Schlag-Rey,et al.  Through the eye, slowly; Delays and localization errors in the visual system , 2002, Nature Reviews Neuroscience.

[71]  E. Poulton.  Models for biases in judging sensory magnitude. , 1979, Psychological bulletin.