Eye movement accuracy determines natural interception strategies.

Eye movements aid visual perception and guide actions such as reaching or grasping. Most previous work on eye-hand coordination has focused on saccadic eye movements. Here we show that smooth pursuit eye movement accuracy strongly predicts both interception accuracy and the strategy used to intercept a moving object. We developed a naturalistic task in which participants (n = 42 varsity baseball players) intercepted a moving dot (a "2D fly ball") with their index finger in a designated "hit zone." Participants were instructed to track the ball with their eyes, but were only shown its initial launch (100-300 ms). Better smooth pursuit resulted in more accurate interceptions and determined the strategy used for interception, i.e., whether interception was early or late in the hit zone. Even though early and late interceptors showed equally accurate interceptions, they may have relied on distinct tactics: early interceptors used cognitive heuristics, whereas late interceptors' performance was best predicted by pursuit accuracy. Late interception may be beneficial in real-world tasks as it provides more time for decision and adjustment. Supporting this view, baseball players who were more senior were more likely to be late interceptors. Our findings suggest that interception strategies are optimally adapted to the proficiency of the pursuit system.

[1]  Eun Jung Hwang,et al.  Spatial and Temporal Eye–Hand Coordination Relies on the Parietal Reach Region , 2014, The Journal of Neuroscience.

[2]  Francesco Lacquaniti,et al.  Gaze Behavior in One-Handed Catching and Its Relation with Interceptive Performance: What the Eyes Can't Tell , 2015, PloS one.

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

[4]  M. Land Eye movements and the control of actions in everyday life , 2006, Progress in Retinal and Eye Research.

[5]  K. Hoffmann,et al.  Influence of arm movements on saccades in humans , 2000, The European journal of neuroscience.

[6]  L H Snyder,et al.  Saccade-related activity in the parietal reach region. , 2000, Journal of neurophysiology.

[7]  A. Terry Bahill,et al.  Predicting a Baseball’s Path , 2005 .

[8]  Jacqueline Gottlieb,et al.  Functional Significance of Nonspatial Information in Monkey Lateral Intraparietal Area , 2009, The Journal of Neuroscience.

[9]  William H. Warren,et al.  On-line and model-based approaches to the visual control of action , 2015, Vision Research.

[10]  B. Abernethy,et al.  The Head Tracks and Gaze Predicts: How the World’s Best Batters Hit a Ball , 2013, PloS one.

[11]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus biases target choice for smooth pursuit, saccades, and button press responses. , 2010, Journal of neurophysiology.

[12]  Heiko Hecht,et al.  Eye movements influence estimation of time-to-contact in prediction motion , 2010, Experimental Brain Research.

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

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

[15]  J. F. Soechting,et al.  Extrapolation of visual motion for manual interception. , 2008, Journal of neurophysiology.

[16]  Mary Hayhoe,et al.  Saccades to future ball location reveal memory-based prediction in a virtual-reality interception task. , 2013, Journal of vision.

[17]  Miles C. Bowman,et al.  Control strategies in object manipulation tasks , 2006, Current Opinion in Neurobiology.

[18]  D. Ballard,et al.  Goal-directed arm movements change eye-head coordination , 1996, Experimental Brain Research.

[19]  Joo-Hyun Song,et al.  Deficits in reach target selection during inactivation of the midbrain superior colliculus , 2011, Proceedings of the National Academy of Sciences.

[20]  J. F. Soechting,et al.  Target Interception: Hand–Eye Coordination and Strategies , 2007, The Journal of Neuroscience.

[21]  Peter Comninos,et al.  Three-Dimensional Transformations , 2006 .

[22]  R. Johansson,et al.  Eye–Hand Coordination during Learning of a Novel Visuomotor Task , 2005, The Journal of Neuroscience.

[23]  Robert G. Watts,et al.  The lateral force on a spinning sphere: Aerodynamics of a curveball , 1987 .

[24]  S. Lisberger,et al.  Properties of visual inputs that initiate horizontal smooth pursuit eye movements in monkeys , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  R. Johansson,et al.  Eye–Hand Coordination in Object Manipulation , 2001, The Journal of Neuroscience.

[26]  Miriam Spering,et al.  Acting without seeing: eye movements reveal visual processing without awareness , 2015, Trends in Neurosciences.

[27]  Jing Chen,et al.  LRP predicts smooth pursuit eye movement onset during the ocular tracking of self-generated movements. , 2016, Journal of neurophysiology.

[28]  Eli Brenner,et al.  Continuous visual control of interception. , 2011, Human movement science.

[29]  D. Ballard,et al.  Eye movements in natural behavior , 2005, Trends in Cognitive Sciences.

[30]  M. Missal,et al.  What triggers catch-up saccades during visual tracking? , 2002, Journal of Neurophysiology.

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

[32]  Francesco Lacquaniti,et al.  Catching What We Can't See: Manual Interception of Occluded Fly-Ball Trajectories , 2012, PloS one.

[33]  H. Collewijn,et al.  Gaze-shift dynamics in two kinds of sequential looking tasks , 1997, Vision Research.

[34]  A. Montagnini,et al.  Do we track what we see? Common versus independent processing for motion perception and smooth pursuit eye movements: A review , 2011, Vision Research.

[35]  Eli Brenner,et al.  How people achieve their amazing temporal precision in interception. , 2015, Journal of vision.

[36]  Li Li,et al.  Manual tracking enhances smooth pursuit eye movements. , 2015, Journal of vision.

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

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

[39]  Philippe Lefèvre,et al.  The saccadic system does not compensate for the immaturity of the smooth pursuit system during visual tracking in children. , 2013, Journal of neurophysiology.

[40]  John F Soechting,et al.  Models for the extrapolation of target motion for manual interception. , 2009, Journal of neurophysiology.

[41]  A P Batista,et al.  Reach plans in eye-centered coordinates. , 1999, Science.

[42]  Chantal Bard,et al.  Stabilization of head and eyes on target as a factor in successful basketball shooting , 1986 .

[43]  Robert M. McPeek,et al.  Deficits in saccade target selection after inactivation of superior colliculus , 2004, Nature Neuroscience.

[44]  H. Bekkering,et al.  Ocular gaze is anchored to the target of an ongoing pointing movement. , 2000, Journal of neurophysiology.

[45]  R. Gellman,et al.  The contribution of retinal and extraretinal signals to manual tracking movements , 2004, Experimental Brain Research.

[46]  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.

[47]  Stefan Everling,et al.  Hand-eye coordination for rapid pointing movements , 2002, Experimental Brain Research.

[48]  Andy Liaw,et al.  Classification and Regression by randomForest , 2007 .

[49]  Jean-Jacques Orban de Xivry,et al.  Kalman Filtering Naturally Accounts for Visually Guided and Predictive Smooth Pursuit Dynamics , 2013, The Journal of Neuroscience.

[50]  Anthony R. Dickinson,et al.  Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. , 2002, Journal of neurophysiology.

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

[52]  W Pieter Medendorp,et al.  Three-dimensional transformations for goal-directed action. , 2011, Annual review of neuroscience.

[53]  Stephen G Lisberger,et al.  Visual Guidance of Smooth Pursuit Eye Movements. , 2015, Annual review of vision science.

[54]  Jean-Jacques Orban de Xivry,et al.  Saccades and pursuit: two outcomes of a single sensorimotor process , 2007, The Journal of physiology.

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

[56]  Eli Brenner,et al.  How the required precision influences the way we intercept a moving object , 2013, Experimental Brain Research.

[57]  Eric A. Yttri,et al.  Lesions of cortical area LIP affect reach onset only when the reach is accompanied by a saccade, revealing an active eye–hand coordination circuit , 2013, Proceedings of the National Academy of Sciences.

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

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

[60]  Christopher D. Carello,et al.  Manipulating Intent Evidence for a Causal Role of the Superior Colliculus in Target Selection , 2004, Neuron.

[61]  A. Bahill,et al.  Why can't batters keep their eyes on the ball? , 1984 .

[62]  D H Ballard,et al.  Hand-eye coordination during sequential tasks. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  Bijan Pesaran,et al.  Reaction Time Correlations during Eye–Hand Coordination: Behavior and Modeling , 2011, The Journal of Neuroscience.

[64]  Martin V. Butz,et al.  It's in the eyes: Planning precise manual actions before execution. , 2016, Journal of vision.

[65]  Dinesh K. Pai,et al.  Eyecatch: simulating visuomotor coordination for object interception , 2012, ACM Trans. Graph..