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Countermanding Eye-Head Gaze Shifts in Humans: Marching Orders Are Delivered to the Head First

Department of Physiology and Pharmacology and Psychology, University of Western Ontario, London, Ontario, Canada

Submitted 11 November 2004; accepted in final form 19 February 2005

The countermanding task requires subjects to cancel a planned movement on appearance of a stop signal, providing insights into response generation and suppression. Here, we studied human eye-head gaze shifts in a countermanding task with targets located beyond the horizontal oculomotor range. Consistent with head-restrained saccadic countermanding studies, the proportion of gaze shifts on STOP trials increased the longer the stop signal was delayed after target presentation, and gaze shift stop-signal reaction times (SSRTs: a derived statistic measuring how long it takes to cancel a movement) averaged 120 ms across seven subjects. We also observed a marked proportion of trials (13% of all STOP trials) during which gaze remained stable but the head moved toward the target. Such head movements were more common at intermediate stop signal delays. We never observed the converse sequence wherein gaze moved while the head remained stable. SSRTs for head movements averaged 190 ms or 70–75 ms longer than gaze SSRTs. Although our findings are inconsistent with a single race to threshold as proposed for controlling saccadic eye movements, movement parameters on STOP trials attested to interactions consistent with a race model architecture. To explain our data, we tested two extensions to the saccadic race model. The first assumed that gaze shifts and head movements are controlled by parallel but independent races. The second model assumed that gaze shifts and head movements are controlled by a single race, preceded by terminal ballistic intervals not under inhibitory control, and that the head-movement branch is activated at a lower threshold. Although simulations of both models produced acceptable fits to the empirical data, we favor the second alternative as it is more parsimonious with recent findings in the oculomotor system. Using the second model, estimates for gaze and head ballistic intervals were 25 and 90 ms, respectively, consistent with the known physiology of the final motor paths. Further, the threshold of the head movement branch was estimated to be 85% of that required to activate gaze shifts. From these results, we conclude that a commitment to a head movement is made in advance of gaze shifts and that the comparative SSRT differences result primarily from biomechanical differences inherent to eye and head motion.

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