Experimental Test of Spatial Updating Models for Monkey Eye-Head Gaze Shifts

How the brain maintains an accurate and stable representation of visual target locations despite the occurrence of saccadic gaze shifts is a classical problem in oculomotor research. Here we test and dissociate the predictions of different conceptual models for head-unrestrained gaze-localization behavior of macaque monkeys. We adopted the double-step paradigm with rapid eye-head gaze shifts to measure localization accuracy in response to flashed visual stimuli in darkness. We presented the second target flash either before (static), or during (dynamic) the first gaze displacement. In the dynamic case the brief visual flash induced a small retinal streak of up to about 20 deg at an unpredictable moment and retinal location during the eye-head gaze shift, which provides serious challenges for the gaze-control system. However, for both stimulus conditions, monkeys localized the flashed targets with accurate gaze shifts, which rules out several models of visuomotor control. First, these findings exclude the possibility that gaze-shift programming relies on retinal inputs only. Instead, they support the notion that accurate eye-head motor feedback updates the gaze-saccade coordinates. Second, in dynamic trials the visuomotor system cannot rely on the coordinates of the planned first eye-head saccade either, which rules out remapping on the basis of a predictive corollary gaze-displacement signal. Finally, because gaze-related head movements were also goal-directed, requiring continuous access to eye-in-head position, we propose that our results best support a dynamic feedback scheme for spatial updating in which visuomotor control incorporates accurate signals about instantaneous eyeand head positions rather than relative eyeand head displacements. Citation: Van Grootel TJ, Van der Willigen RF, Van Opstal AJ (2012) Experimental Test of Spatial Updating Models for Monkey Eye-Head Gaze Shifts. PLoS ONE 7(10): e47606. doi:10.1371/journal.pone.0047606 Editor: Markus Lappe, University of Muenster, Germany Received April 16, 2012; Accepted September 13, 2012; Published October 31, 2012 Copyright: 2012 Van Grootel et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported by the Earth and Life Sciences (ALW) section of the Netherlands Organization for Scientific Research (NWO-ALW/VICI 865.05.003; AJVO, TJVG, RFVDW), and the Radboud University Nijmegen (AJVO). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected]