Dynamic interaction between retinal and extraretinal signals in motion integration for smooth pursuit.

Due to the aperture problem, the initial direction of tracking responses to a translating bar is biased towards the direction orthogonal to the bar. This observation offers a powerful way to explore the interactions between retinal and extraretinal signals in controlling our actions. We conducted two experiments to probe these interactions by briefly (200 and 400 ms) blanking the moving target (45° or 135° tilted bar) during steady state (Experiment 1) and at different moments during the early phase of pursuit (Experiment 2). In Experiment 1, we found a marginal but statistically significant directional bias on target reappearance for all subjects in at least one blank condition (200 or 400 ms). In Experiment 2, no systematic significant directional bias was observed at target reappearance after a blank. These results suggest that the weighting of retinal and extraretinal signals is dynamically modulated during the different phases of pursuit. Based on our previous theoretical work on motion integration, we propose a new closed-loop two-stage recurrent Bayesian model where retinal and extraretinal signals are dynamically weighted based on their respective reliabilities and combined to compute the visuomotor drive. With a single free parameter, the model reproduces many aspects of smooth pursuit observed across subjects during and immediately after target blanking. It provides a new theoretical framework to understand how different signals are dynamically combined based on their relative reliability to adaptively control our actions. Overall, the model and behavioral results suggest that human subjects rely more strongly on prediction during the early phase than in the steady state phase of pursuit.

[1]  J. L. Gordon,et al.  A model of the smooth pursuit eye movement system , 1986, Biological Cybernetics.

[2]  Simon J Bennett,et al.  Predictive smooth ocular pursuit during the transient disappearance of a visual target. , 2004, Journal of neurophysiology.

[3]  Philippe Lefèvre,et al.  A dynamic representation of target motion drives predictive smooth pursuit during target blanking. , 2008, Journal of vision.

[4]  Stephen G Lisberger,et al.  Visual Guidance of Smooth-Pursuit Eye Movements: Sensation, Action, and What Happens in Between , 2010, Neuron.

[5]  Stephen G. Lisberger,et al.  A model of visually-guided smooth pursuit eye movements based on behavioral observations , 1994, Journal of Computational Neuroscience.

[6]  Miriam Spering,et al.  Combining 1D visual motion and 2D predictive signals to control smooth pursuit eye movements , 2010 .

[7]  T. Başar,et al.  A New Approach to Linear Filtering and Prediction Problems , 2001 .

[8]  Vincent P. Ferrera,et al.  Estimating invisible target speed from neuronal activity in monkey frontal eye field , 2003, Nature Neuroscience.

[9]  M. Missal,et al.  Supplementary eye fields stimulation facilitates anticipatory pursuit. , 2004, Journal of neurophysiology.

[10]  Guillaume S Masson,et al.  Object motion computation for the initiation of smooth pursuit eye movements in humans. , 2005, Journal of neurophysiology.

[11]  Anna Montagnini,et al.  When the Brain Meets the Eye: Tracking Object Motion , 2009 .

[12]  A. Fuchs,et al.  Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target , 2004, Experimental Brain Research.

[13]  L. Mitrani,et al.  Pursuit eye movements of a disappearing moving target , 1978, Vision Research.

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

[15]  Vincent P Ferrera,et al.  Modulation of visual responses in macaque frontal eye field during covert tracking of invisible targets. , 2006, Cerebral cortex.

[16]  Pascal Mamassian,et al.  Predicting and computing 2D target motion for smooth-pursuit eye movements in macaque monkeys , 2010 .

[17]  Guillaume S. Masson,et al.  The behavioral receptive field underlying motion integration for primate tracking eye movements , 2012, Neuroscience & Biobehavioral Reviews.

[18]  Peter Thier,et al.  The neural basis of smooth pursuit eye movements in the rhesus monkey brain , 2008, Brain and Cognition.

[19]  Eric Castet,et al.  Parallel Motion Processing for the Initiation of Short-Latency Ocular Following in Humans , 2002, The Journal of Neuroscience.

[20]  Carlos R. Ponce,et al.  Temporal evolution of 2-dimensional direction signals used to guide eye movements. , 2005, Journal of neurophysiology.

[21]  S. G. Lisberger,et al.  A Control Systems Model of Smooth Pursuit Eye Movements with Realistic Emergent Properties , 1989, Neural Computation.

[22]  S. Lisberger,et al.  Evidence for object permanence in the smooth-pursuit eye movements of monkeys. , 2003, Journal of neurophysiology.

[23]  R. Krauzlis,et al.  Effects of learning on smooth pursuit during transient disappearance of a visual target. , 2003, Journal of neurophysiology.

[24]  G R Barnes,et al.  Evidence for a link between the extra-retinal component of random-onset pursuit and the anticipatory pursuit of predictable object motion. , 2008, Journal of neurophysiology.

[25]  G. DeAngelis,et al.  A Normalization Model of Multisensory Integration , 2011, Nature Neuroscience.

[26]  Christopher C. Pack,et al.  Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain , 2001, Nature.

[27]  E. Todorov.  Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[28]  P. Kornprobst,et al.  Modelling the dynamics of motion integration with a new luminance-gated diffusion mechanism , 2010, Vision Research.

[29]  Miriam Spering,et al.  Predicting 2D target velocity cannot help 2D motion integration for smooth pursuit initiation. , 2006, Journal of neurophysiology.

[30]  G. Barnes,et al.  Human ocular pursuit during the transient disappearance of a visual target. , 2003, Journal of neurophysiology.

[31]  Paul A. Warren,et al.  A Bayesian Model of Perceived Head-Centered Velocity during Smooth Pursuit Eye Movement , 2010, Current Biology.

[32]  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.

[33]  A. Yuille,et al.  Object perception as Bayesian inference. , 2004, Annual review of psychology.

[34]  Guillaume S. Masson,et al.  Dynamics of distributed 1D and 2D motion representations for short-latency ocular following , 2008, Vision Research.

[35]  Pascal Mamassian,et al.  Pursuing motion illusions: A realistic oculomotor framework for Bayesian inference , 2011, Vision Research.

[36]  Uwe J Ilg,et al.  Commentary: smooth pursuit eye movements: from low-level to high-level vision. , 2002, Progress in brain research.

[37]  H. J. Wyatt,et al.  Offset dynamics of human smooth pursuit eye movements: Effects of target presence and subject attention , 1997, Vision Research.

[38]  K. Fukushima,et al.  Predictive responses of periarcuate pursuit neurons to visual target motion , 2002, Experimental Brain Research.

[39]  Edward H. Adelson,et al.  Motion illusions as optimal percepts , 2002, Nature Neuroscience.

[40]  C. Rashbass,et al.  The relationship between saccadic and smooth tracking eye movements , 1961, The Journal of physiology.

[41]  L. Stone,et al.  From following edges to pursuing objects. , 2002, Journal of neurophysiology.

[42]  Eero P. Simoncelli,et al.  Noise characteristics and prior expectations in human visual speed perception , 2006, Nature Neuroscience.

[43]  F A Miles,et al.  Initiation of saccades during fixation or pursuit: evidence in humans for a single mechanism. , 1996, Journal of neurophysiology.

[44]  S G Lisberger,et al.  Effect of changing feedback delay on spontaneous oscillations in smooth pursuit eye movements of monkeys. , 1992, Journal of neurophysiology.

[45]  F A Miles,et al.  Transitions between pursuit eye movements and fixation in the monkey: dependence on context. , 1996, Journal of neurophysiology.

[46]  William Bialek,et al.  Time Course of Precision in Smooth-Pursuit Eye Movements of Monkeys , 2007, The Journal of Neuroscience.

[47]  S. Yasui,et al.  On the predictive control of foveal eye tracking and slow phases of optokinetic and vestibular nystagmus. , 1984, The Journal of physiology.

[48]  Christopher R Fetsch,et al.  Neural correlates of reliability-based cue weighting during multisensory integration , 2011, Nature Neuroscience.

[49]  G R Barnes,et al.  The influence of briefly presented randomized target motion on the extraretinal component of ocular pursuit. , 2008, Journal of neurophysiology.

[50]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[51]  Pascal Mamassian,et al.  Bayesian modeling of dynamic motion integration , 2007, Journal of Physiology-Paris.

[52]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[53]  R. Krauzlis,et al.  Tracking with the mind’s eye , 1999, Trends in Neurosciences.

[54]  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.

[55]  Guillaume S. Masson,et al.  From 1D to 2D via 3D: dynamics of surface motion segmentation for ocular tracking in primates , 2004, Journal of Physiology-Paris.

[56]  Simon J. Bennett,et al.  Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control , 2006, Experimental Brain Research.

[57]  Philippe Lefèvre,et al.  Neuronal Bases of Directional Expectation and Anticipatory Pursuit , 2008, The Journal of Neuroscience.

[58]  M. Carandini,et al.  Testing the Bayesian model of perceived speed , 2002, Vision Research.