Top-down control of saccades requires inhibition of suddenly appearing stimuli

Abstract

Humans scan their visual environment using saccade eye movements. Where we look is influenced by bottom-up salience and top-down factors, like value. For reactive saccades in response to suddenly appearing stimuli, it has been shown that short-latency saccades are biased towards salience, and that top-down control increases with increasing latency. Here, we show, in a series of six experiments, that this transition towards top-down control is not determined by the time it takes to integrate value information into the saccade plan, but by the time it takes to inhibit suddenly appearing salient stimuli. Participants made consecutive saccades to three fixation crosses and a vertical bar consisting of a high-salient and a rewarded low-salient region. Endpoints on the bar were biased towards salience whenever it appeared or reappeared shortly before the last saccade was initiated. This was also true when the eye movement was already planned. When the location of the suddenly appearing salient region was predictable, saccades were aimed in the opposite direction to nullify this sudden onset effect. Successfully inhibiting salience, however, could only be achieved by previewing the target. These findings highlight the importance of inhibition for top-down eye-movement control.

Salient objects dominate the central fixation bias when orienting toward images

“…A similar temporal dependency of saccade endpoints has been observed for saccades in response to a single spatially extended target that contained a high-salient region and a low-salient region, when the low-salient region was associated with a reward ( Schütz et al, 2012 ; Wolf & Lappe, 2020 ). Early saccades were biased toward high salience and only later saccades could be governed by voluntary control and successfully landed in the rewarded region (see also Ludwig & Gilchrist, 2002 ; van Zoest et al, 2004 ; van Heusden et al, 2021 ).…”

Vision as oculomotor reward: cognitive contributions to the dynamic control of saccadic eye movements

“…This dynamic transition from bottom-up to top-down oculomotor control could either depend on the time it takes to integrate value information into the saccade plan (Schütz et al 2012 ) or by the time it takes to inhibit the orienting response caused by the suddenly appearing salient stimulus. Recent evidence supports the latter option (Wolf and Lappe 2020 ): Saccade endpoints were temporally biased towards salience whenever a salient item suddenly appeared or re-appeared close to a designated and rewarded saccade target. This onset bias was found even when a saccade to the rewarded target had been pre-planned and the onset was fully predictable.…”

“…When looking at the temporal dynamics of oculomotor selection among two competing targets or target regions, then short-latency saccades are typically guided by physical salience whereas long-latency saccades are driven by top-down aspects like the prospect of reward (Ludwig and Gilchrist 2002 ; Markowitz et al 2011 ; Schütz et al 2012 ; van Zoest et al 2004 ; Wolf and Lappe 2020 ). This dynamic transition from bottom-up to top-down oculomotor control could either depend on the time it takes to integrate value information into the saccade plan (Schütz et al 2012 ) or by the time it takes to inhibit the orienting response caused by the suddenly appearing salient stimulus.…”

“…This onset bias was found even when a saccade to the rewarded target had been pre-planned and the onset was fully predictable. Successfully selecting the rewarded target could only be achieved by pre-viewing the salient stimulus in the periphery (Wolf and Lappe 2020 ). These temporal dynamics share characteristics with the global effect, i.e.…”

“…In contrast, the encoding of reward-related distractors was reduced although their presence increased reaction times, highlighting that reward does not per se enhance the representation of reward-related objects, but that they need to be actively suppressed (Gaspelin et al 2015 ; Hickey and Peelen 2015 ). This active suppression of salient or reward-related distractors was related to dopaminergic midbrain activity (Hickey and Peelen 2015 ) and is presumably also reflected in the time course of saccade endpoints when a distractor and a target compete for overt visual selection (Arkesteijn et al 2020 ; Coëffé and O’Regan 1987 ; Ottes et al 1985 ; Wolf and Lappe 2020 ).…”