A common stochastic accumulator with effector-dependent noise can explain eye-hand coordination.

The computational architecture that enables the flexible coupling between otherwise independent eye and hand effector systems is not understood. By using a drift diffusion framework, in which variability of the reaction time (RT) distribution scales with mean RT, we tested the ability of a common stochastic accumulator to explain eye-hand coordination. Using a combination of behavior, computational modeling and electromyography, we show how a single stochastic accumulator to threshold, followed by noisy effector-dependent delays, explains eye-hand RT distributions and their correlation, while an alternate independent, interactive eye and hand accumulator model does not. Interestingly, the common accumulator model did not explain the RT distributions of the same subjects when they made eye and hand movements in isolation. Taken together, these data suggest that a dedicated circuit underlies coordinated eye-hand planning.

[1]  Frederick Verbruggen,et al.  Response Suppression by Automatic Retrieval of Stimulus–Stop Association: Evidence from Transcranial Magnetic Stimulation , 2012, Journal of Cognitive Neuroscience.

[2]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[3]  James L. McClelland,et al.  The time course of perceptual choice: the leaky, competing accumulator model. , 2001, Psychological review.

[4]  Z. Hasan,et al.  Timing and magnitude of electromyographic activity for two-joint arm movements in different directions. , 1991, Journal of neurophysiology.

[5]  U. Sailer,et al.  Spatial and temporal aspects of eye-hand coordination across different tasks , 2000, Experimental Brain Research.

[6]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[7]  M. Jeannerod,et al.  The coordination of eye, head, and arm movements during reaching at a single visual target , 2004, Experimental Brain Research.

[8]  Jos J. Adam,et al.  Reaction time latencies of eye and hand movements in single- and dual-task conditions , 2004, Experimental Brain Research.

[9]  M Straschill,et al.  Eye movements evoked by focal stimulation of the cat's superior colliculus. , 1973, Brain research.

[10]  Scott D. Brown,et al.  On the linear relation between the mean and the standard deviation of a response time distribution. , 2007, Psychological review.

[11]  Otmar Bock,et al.  Coordination of arm and eye movements in tracking of sinusoidally moving targets , 1987, Behavioural Brain Research.

[12]  E. Bizzi,et al.  Eye-Head Coordination in Monkeys: Evidence for Centrally Patterned Organization , 1971, Science.

[13]  J. D. Fisk,et al.  The organization of eye and limb movements during unrestricted reaching to targets in contralateral and ipsilateral visual space , 2004, Experimental Brain Research.

[14]  A. Murthy,et al.  Programming of double-step saccade sequences: Modulation by cognitive control , 2004, Vision Research.

[15]  B. Fischer,et al.  Reaction times of the eye and the hand of the monkey in a visual reach task , 1985, Neuroscience Letters.

[16]  M. Segraves,et al.  The relationship of monkey frontal eye field activity to saccade dynamics. , 1993, Journal of neurophysiology.

[17]  R. Carpenter,et al.  The influence of urgency on decision time , 2000, Nature Neuroscience.

[18]  Jeffrey D. Schall,et al.  Neural Mechanisms of Selection and Control of Visually Guided Eye Movements , 1998 .

[19]  R. Duncan Luce,et al.  Response Times: Their Role in Inferring Elementary Mental Organization , 1986 .

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

[21]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[22]  Ruth Maulucci,et al.  Visually triggered eye-arm movements in man , 2004, Experimental Brain Research.

[23]  Ausaf A Farooqui,et al.  Impaired conflict monitoring in Parkinson’s disease patients during an oculomotor redirect task , 2010, Experimental Brain Research.

[24]  R. H. S. Carpenter,et al.  Neural computation of log likelihood in control of saccadic eye movements , 1995, Nature.

[25]  R. Ratcliff,et al.  Diffusion model for one-choice reaction-time tasks and the cognitive effects of sleep deprivation , 2011, Proceedings of the National Academy of Sciences.

[26]  B A J Reddi,et al.  Accuracy, information, and response time in a saccadic decision task. , 2003, Journal of neurophysiology.

[27]  Jennifer A. Mather,et al.  Orienting to Targets by Looking and Pointing: Parallels and Interactions in Ocular and Manual Performance , 1985 .

[28]  P. Schiller,et al.  Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. , 1972, Journal of neurophysiology.

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

[30]  Aditya Murthy,et al.  Voluntary control of multisaccade gaze shifts during movement preparation and execution. , 2010, Journal of neurophysiology.

[31]  C. C. A. M. Gielen,et al.  Coordination of fast eye and arm movements in a tracking task , 2004, Experimental Brain Research.

[32]  Roger Ratcliff,et al.  A Theory of Memory Retrieval. , 1978 .

[33]  Peter C. M. Molenaar,et al.  On the relation between the mean and the variance of a diffusion model response time distribution , 2005 .

[34]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

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

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