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

Tom J Van Grootel,A John Van Opstal,Robert F Van Der Willigen,Markus Lappe

doi:10.1371/journal.pone.0047606

Tom J Van Grootel, A John Van Opstal + Show 2 more

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https://doi.org/10.1371/journal.pone.0047606

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Abstract

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 eye- and head positions rather than relative eye- and head displacements.

Highlights

Saccadic gaze shifts sweep visual images and targets across the retina at high speeds, we perceive the world as stable through a neural process called trans-saccadic integration, or spatial updating
Multiple Linear Regression (MLR) analysis In the model predictions of Figures 8 and 9 we described the data with the ideal model parameters, and concluded that the data can be best described by the dynamic feedback model of Eq 4c, with the strongest discriminative power for the response azimuth components
The present study is the first to show that monkeys update the spatial location of brief visual targets, flashed in midflight of rapid eye-head gaze shifts in darkness

Summary

Introduction

Saccadic gaze shifts sweep visual images and targets across the retina at high speeds, we perceive the world as stable through a neural process called trans-saccadic integration, or spatial updating. The mechanisms underlying spatial updating have been studied extensively with the classical openloop double-step paradigm [2,3,4,5], which requires the programming of two saccades in total darkness in response to brief flashes at different retinal locations. These experiments have shown to invoke adequate spatial updating, as the targeting saccades to the flashed locations are spatially accurate, provided the target flash durations exceed a few ms [6,7]. We have recently argued that the dynamic double-step paradigm could in principle dissociate these different models when considering the inherent variability of saccade responses [5]

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