On the effect of remote and proximal distractors on saccadic behavior: A challenge to neural-field models

Abstract

Two proposals have been made to account for the generation of saccadic eye movements. The first assumes that when the eyes move is under the control of a fixation gating system. The second attributes the decisions of both when and where the eyes move to the interplay between short-range excitatory and long-range inhibitory interactions within the motor map of the superior colliculus (SC). To distinguish both views, three behavioral experiments conducted on human participants tested the respective contributions of stimulus eccentricity and interstimulus distance on the effects of remote and proximal distractors on the latency and accuracy of saccades. Experiment 1 showed that the saccade-latency increase that results from the presentation of a remote distractor in the contralateral, nontarget hemifield varies with the ratio of distractor-to-target eccentricity, but not the interstimulus distance in visual or collicular space, thus indicating that the effect is not due to long-range inhibition. Experiments 2a and 2b showed that short-range excitation does not underlie the effect of proximal, ipsilateral distractors. Proximal distractors do not systematically shorten saccade latency, but rather show a range of effects (from a latency increase to no effect and then facilitation) as the ratio of distractor-to-target eccentricity increases, while deviating the eyes to gradually larger extents. The present findings strongly challenge the neural-field account, while suggesting that when a saccade is initiated depends mainly on the activity of a fixation gating system.

How Eye Dominance Strength Modulates the Influence of a Distractor on Saccade Accuracy

“…Thus, the uncertainty of target location was reduced by the hemifield blocked design to minimize the possible contribution to the distractor effect of decisional and strategy-based processes. 11 The order of the blocks was counterbalanced across subjects by alternating target side.…”

“…It is now well established that a distractor being presented close to the target position modifies saccade amplitude by deviating the saccade to an intermediate position between the two stimuli (global effect [GE]), whereas a distractor remote from the target position increases saccade latency (remote distractor effect [RDE]). [10][11][12] Therefore, we hypothesize that a modulation of both effects, depending on the hemifield in which the distractor is displayed, will reflect the influence of eye dominance and of eye dominance strength on saccadic parameters. Indeed, in participants with strong eye dominance the perceptual advantage of the hemifield contralateral to the DE should result in a greater impact of the distractor presented in this hemifield compared to the ipsilateral one on saccade amplitude and latency.…”

Remote distractor effects and saccadic inhibition: Spatial and temporal modulation

“…The RDE is attributed to similar competitive interaction effects operating in the SC, but in this case, it may be a more sustained inhibitory effect. The exact nature of these lateral interactions is not fully understood, and they may operate between populations of neurons encoding the distractor and saccade target (Trappenberg et al, 2001) or between fixation-related and saccade-related activity (Casteau & Vitu, 2012;Findlay & Walker, 1999;Walker et al, 1997). There is, therefore, a possibility that separate, but interacting, inhibitory influences account for the SI and the RDE and that both of these may be observed under certain conditions, such as when a highly predictable target paradigm is used or when the target activity is weak, such as in the delayed and memory-guided paradigms used by Edelman and Xu (2009).…”

“…A visual onset may also result in increased activity of rostral collicular neurons that also serve to inhibit saccade generation. The strength of this activity will depend on the eccentricity of the distractor and target (Casteau & Vitu, 2012;Walker et al, 1997) rather than on the target-distractor spatial separation (Bompas & Sumner, 2011;Trappenberg et al, 2001) and on the level of fixation activity at the time the distractor appears. The competition between the target-related and fixationrelated activity is further influenced over time by sustained endogenous inputs, making this a highly nonlinear process, as noted by Bompas and Sumner (2011).…”

“…More recent studies have shown that fixation neurons are best conceived of as saccade-related neurons that encode small amplitudes (Hafed & Krauzlis, 2012;Krauzlis, Basso, & Wurtz, 1997), and distractors outside the fixation zone may therefore be expected to have qualitatively similar inhibitory effects as those at fixation. Which of these models best accounts for the RDE is controversial (Casteau & Vitu, 2012), and inhibitory influences may not be restricted to the SC alone (Tehovnik, Sommer, Chou, Slocum, & Schiller, 2000). SI has also similarly been attributed to lateral interactions between target and distractor-related activity (Bompas & Sumner, 2011;Buonocore & McIntosh, 2008;Edelman & Xu, 2009;Reingold & Stampe, 2002).…”