Saccades to future ball location reveal memory-based prediction in a virtual-reality interception task.

Despite general agreement that prediction is a central aspect of perception, there is relatively little evidence concerning the basis on which visual predictions are made. Although both saccadic and pursuit eye-movements reveal knowledge of the future position of a moving visual target, in many of these studies targets move along simple trajectories through a fronto-parallel plane. Here, using a naturalistic and racquet-based interception task in a virtual environment, we demonstrate that subjects make accurate predictions of visual target motion, even when targets follow trajectories determined by the complex dynamics of physical interactions and the head and body are unrestrained. Furthermore, we found that, following a change in ball elasticity, subjects were able to accurately adjust their prebounce predictions of the ball's post-bounce trajectory. This suggests that prediction is guided by experience-based models of how information in the visual image will change over time.

[1]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.

[2]  John M. Findlay,et al.  Spatial and temporal factors in the predictive generation of saccadic eye movements , 1981, Vision Research.

[3]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[4]  H. Helmholtz Helmholtz's Treatise on Physiological Optics , 1963 .

[5]  J. F. Soechting,et al.  Predicting curvilinear target motion through an occlusion , 2007, Experimental Brain Research.

[6]  M F Land,et al.  The knowledge base of the oculomotor system. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[7]  J. Saunders,et al.  Humans use continuous visual feedback from the hand to control fast reaching movements , 2003, Experimental Brain Research.

[8]  D. Wolpert,et al.  The cerebellum is involved in predicting the sensory consequences of action , 1999, Neuroreport.

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

[10]  Michael S Landy,et al.  Combining Priors and Noisy Visual Cues in a Rapid Pointing Task , 2006, The Journal of Neuroscience.

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

[12]  R. Gregory Perceptions as hypotheses. , 1980, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[13]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[14]  Hunter A. Murphy,et al.  3-D eye movement analysis , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[15]  Kikuro Fukushima,et al.  The vestibular-related frontal cortex and its role in smooth-pursuit eye movements and vestibular-pursuit interactions. , 2006, Journal of vestibular research : equilibrium & orientation.

[16]  Eileen Kowler,et al.  The effect of expectations on slow oculomotor control—IV. Anticipatory smooth eye movements depend on prior target motions , 1984, Vision Research.

[17]  Michael F. Land,et al.  From eye movements to actions: how batsmen hit the ball , 2000, Nature Neuroscience.

[18]  C. Colby,et al.  Trans-saccadic perception , 2008, Trends in Cognitive Sciences.

[19]  F. Lacquaniti,et al.  Visuo-motor coordination and internal models for object interception , 2009, Experimental Brain Research.

[20]  Tim K Marks,et al.  SUN: A Bayesian framework for saliency using natural statistics. , 2008, Journal of vision.

[21]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

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

[23]  Thomas Nyffeler,et al.  Involvement of the Supplementary Eye Field in Oculomotor Predictive Behavior , 2008, Journal of Cognitive Neuroscience.

[24]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[25]  Kikuro Fukushima,et al.  Memory and Decision Making in the Frontal Cortex during Visual Motion Processing for Smooth Pursuit Eye Movements , 2009, Neuron.

[26]  Joan López-Moliner,et al.  People Favour Imperfect Catching by Assuming a Stable World , 2012, PloS one.

[27]  Vincent P Ferrera,et al.  Internally Generated Error Signals in Monkey Frontal Eye Field during an Inferred Motion Task , 2010, The Journal of Neuroscience.

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

[29]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[30]  W H Warren,et al.  The Way the Ball Bounces: Visual and Auditory Perception of Elasticity and Control of the Bounce Pass , 1987, Perception.

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

[32]  C. Genovese,et al.  Remapping in human visual cortex. , 2007, Journal of neurophysiology.

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

[34]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[35]  J. Enns,et al.  What's next? New evidence for prediction in human vision , 2008, Trends in Cognitive Sciences.

[36]  Anne-Marie Brouwer,et al.  Perception of acceleration with short presentation times: Can acceleration be used in interception? , 2001, Perception & psychophysics.

[37]  Kenji Kawano,et al.  Preparation for smooth pursuit eye movement based on expectation in humans , 2007, Systems and Computers in Japan.

[38]  Simon J. Bennett,et al.  Combined smooth and saccadic ocular pursuit during the transient occlusion of a moving visual object , 2005, Experimental Brain Research.

[39]  Karl R Gegenfurtner,et al.  Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion. , 2011, Journal of neurophysiology.

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

[41]  Christof Koch,et al.  Learning a saliency map using fixated locations in natural scenes. , 2011, Journal of vision.

[42]  Eileen Kowler Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit , 1989, Vision Research.

[43]  Philippe Lefèvre,et al.  Evidence for synergy between saccades and smooth pursuit during transient target disappearance. , 2006, Journal of neurophysiology.

[44]  Philippe Lefèvre,et al.  Target acceleration can be extracted and represented within the predictive drive to ocular pursuit. , 2007, Journal of neurophysiology.

[45]  P J Cordo,et al.  Kinesthetic and visual control of a bimanual task: specification of direction and amplitude , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[47]  C. Pierrot-Deseilligny,et al.  The Role of the Human Dorsolateral Prefrontal Cortex in Ocular Motor Behavior , 2005, Annals of the New York Academy of Sciences.

[48]  D. Wolpert,et al.  Internal models in the cerebellum , 1998, Trends in Cognitive Sciences.

[49]  J. Maunsell,et al.  Neuronal correlates of inferred motion in primate posterior parietal cortex , 1995, Nature.

[50]  Mary Hayhoe,et al.  The role of internal models and prediction in catching balls , 2005, AAAI 2005.

[51]  G. Barnes,et al.  Predicting the duration of ocular pursuit in humans , 2004, Experimental Brain Research.

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

[53]  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.

[54]  Mark Shelhamer,et al.  Saccades exhibit abrupt transition between reactive and predictive; predictive saccade sequences have long-term correlations. , 2003, Journal of neurophysiology.

[55]  L. Fautrelle,et al.  Catching falling objects: the role of the cerebellum in processing sensory–motor errors that may influence updating of feedforward commands. An fMRI study , 2011, Neuroscience.

[56]  J. Krakauer,et al.  Error correction, sensory prediction, and adaptation in motor control. , 2010, Annual review of neuroscience.

[57]  L. Simo,et al.  Functional neuroanatomy of anticipatory behavior: dissociation between sensory-driven and memory-driven systems. , 2005, Cerebral cortex.

[58]  Jeff B. Pelz,et al.  Predictive eye movements in natural vision , 2011, Experimental Brain Research.

[59]  J. T. Massey,et al.  Spatial trajectories and reaction times of aimed movements: effects of practice, uncertainty, and change in target location. , 1981, Journal of neurophysiology.

[60]  Paul R. Schrater,et al.  Auxiliary object knowledge influences visually-guided interception behavior , 2005, APGV '05.

[61]  W. H. Warren The dynamics of perception and action. , 2006, Psychological review.