Eye–hand coordination while pointing rapidly under risk

Humans make rapid, goal-directed movements to interact with their environment. Saccadic eye movements usually accompany rapid hand movements, suggesting neural coupling, although it remains unclear what determines the strength of the coupling. Here, we present evidence that humans can alter eye–hand coordination in response to risk associated with endpoint variability. We used a paradigm in which human participants were forced to point rapidly under risk and were penalized or rewarded depending on the hand movement outcome. A separate reward schedule was employed for relative saccadic endpoint position. Participants received a monetary reward proportional to points won. We present a model that defines optimality of eye–hand coordination for this task depending on where the hand lands relative to the eye. A comparison of the results and model predictions showed that participants could optimize performance to maximize gain in some conditions, but not others. Participants produced near-optimal results when no feedback was given about relative saccade location and when negative feedback was provided for large distances between the saccade and hand. Participants were sub-optimal when given negative feedback for saccades very close to the hand endpoint. Our results suggest that eye–hand coordination is flexible when pointing rapidly under risk, but final eye position remains correlated with finger location.

[1]  A. Fuchs,et al.  Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. , 1969, Vision research.

[2]  Suzanne P. McKee,et al.  Initial visual information determines endpoint precision for rapid pointing , 2006, Vision Research.

[3]  M. Landy,et al.  Optimal Compensation for Changes in Task-Relevant Movement Variability , 2005, The Journal of Neuroscience.

[4]  Michael S Landy,et al.  Statistical decision theory and the selection of rapid, goal-directed movements. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[6]  J. Kohno,et al.  Visualization of the tidal flow in Sasebo and Oomura Bays , 2002 .

[7]  Julia Trommershäuser,et al.  Eye movements during rapid pointing under risk , 2007, Vision Research.

[8]  Christiane,et al.  World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. , 2004, Journal international de bioethique = International journal of bioethics.

[9]  M. Landy,et al.  Statistical decision theory and trade-offs in the control of motor response. , 2003, Spatial vision.

[10]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[11]  M. Landy,et al.  Decision making, movement planning and statistical decision theory , 2008, Trends in Cognitive Sciences.

[12]  Mary M Hayhoe,et al.  Spatial memory and saccadic targeting in a natural task. , 2005, Journal of vision.

[13]  J. T. Enright,et al.  The non-visual impact of eye orientation on eye—hand coordination , 1995, Vision Research.

[14]  M. Hayhoe,et al.  Look-ahead fixations: anticipatory eye movements in natural tasks , 2007, Experimental Brain Research.

[15]  D. Levi,et al.  Spatial localization without visual references , 1992, Vision Research.

[16]  S. McKee,et al.  The imprecision of stereopsis , 1990, Vision Research.

[17]  T. Vilis,et al.  Gaze-Centered Updating of Visual Space in Human Parietal Cortex , 2003, The Journal of Neuroscience.

[18]  Anna Ma-Wyatt,et al.  Seeing and ballistic pointing at perisaccadic targets. , 2005, Journal of vision.

[19]  J. D. Crawford,et al.  Coordinate transformations for hand-guided saccades , 2009, Experimental Brain Research.

[20]  Philip N. Sabes,et al.  Multisensory Integration during Motor Planning , 2003, The Journal of Neuroscience.

[21]  Anna Ma-Wyatt,et al.  Saccades actively maintain perceptual continuity , 2004, Nature Neuroscience.

[22]  D. Robinson,et al.  Saccadic undershoot is not inevitable: Saccades can be accurate , 1986, Vision Research.

[23]  C. Prablanc,et al.  Neural control of on-line guidance of hand reaching movements. , 2003, Progress in brain research.

[24]  Ferdinando A Mussa-Ivaldi,et al.  Interaction of visual and proprioceptive feedback during adaptation of human reaching movements. , 2005, Journal of neurophysiology.

[25]  Heiner Deubel,et al.  Deployment of visual attention before sequences of goal-directed hand movements , 2006, Vision Research.

[26]  H. Collewijn,et al.  The function of visual search and memory in sequential looking tasks , 1995, Vision Research.

[27]  Jitendra Malik,et al.  An Information Maximization Model of Eye Movements , 2004, NIPS.

[28]  DAVID WHITAKER,et al.  Centroid Analysis Predicts Visual Localization of First- and Second-order Stimuli , 1996, Vision Research.

[29]  J. Crawford,et al.  Gaze-Centered Remapping of Remembered Visual Space in an Open-Loop Pointing Task , 1998, The Journal of Neuroscience.

[30]  M. Land,et al.  The Roles of Vision and Eye Movements in the Control of Activities of Daily Living , 1998, Perception.

[31]  M. Hayhoe,et al.  The coordination of eye, head, and hand movements in a natural task , 2001, Experimental Brain Research.

[32]  David Whitaker,et al.  The effect of suprathreshold contrast on stimulus centroid and its implications for the perceived location of objects , 1998, Vision Research.

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

[34]  S. McKee,et al.  Spatial configurations for visual hyperacuity , 1977, Vision Research.

[35]  J D Crawford,et al.  Proprioceptive guidance of saccades in eye-hand coordination. , 2006, Journal of neurophysiology.

[36]  Aarlenne Z. Khan,et al.  Coordinating one hand with two eyes: optimizing for field of view in a pointing task , 2003, Vision Research.

[37]  Otmar Bock,et al.  Localization of objects in the peripheral visual field , 1993, Behavioural Brain Research.

[38]  H. Basford,et al.  Optimal eye movement strategies in visual search , 2005 .