Saccadic Suppression Is Embedded Within Extended Oscillatory Modulation of Sensitivity

Abstract

Action and perception are intimately coupled systems. One clear case is saccadic suppression, the reduced visibility around the time of saccades, which is important in mediating visual stability; another is the oscillatory modulation of visibility synchronized with hand action. To suppress effectively the spurious retinal motion generated by the eye movements, it is crucial that saccadic suppression and saccadic onset be temporally synchronous. However, the mechanisms that determine this temporal synchrony are unknown. We investigated the effect of saccades on contrast discrimination sensitivity over a long period stretching over >1 s before and after saccade execution. Human subjects made horizontal saccades at will to two stationary saccadic targets separated by 20°. At a random interval, a brief Gabor patch was displayed between the two fixations in either the upper or lower visual field and the subject had to detect its location. Strong saccadic suppression was measured between -50 and 50 ms from saccadic onset. However, the suppression was systematically embedded in a trough of oscillations of contrast sensitivity that fluctuated rhythmically in the delta range (at ∼3 Hz), commencing ∼1 s before saccade execution and lasting for up to 1 s after the saccade. The results show that saccadic preparation and visual sensitivity oscillations are coupled and the coupling might be instrumental in temporally aligning the initiation of the saccade with the visual suppression. Saccades are known to produce a suppression of contrast sensitivity at saccadic onset and an enhancement after saccadic offset. Here, we show that these dynamics are systematically embedded in visual oscillations of contrast sensitivity that fluctuate rhythmically in the delta range (at ∼3 Hz), commencing ∼1 s before saccade execution and lasting for up to 1 s after the saccade. The results show that saccadic preparation and visual sensitivity oscillations are coupled and the coupling might be instrumental in aligning temporally the initiation of the saccade with the visual suppression.

Sequential hemifield gating of α- and β-behavioral performance oscillations after microsaccades

“…In our experiments, we therefore explored both time-dependent and microsaccade-direction-dependent long-term behavioral fluctuations after the occurrence of microsaccades. Unlike in the large-saccade literature (Benedetto and Morrone 2017;Hogendoorn 2016;Wutz et al 2016), we observed higher frequency oscillations in the ␣and ␤-frequency ranges. This is interesting as it might relate to findings of higher frequency behavioral oscillations in attentional state (Song et al 2014), which is known to be correlated with microsaccades (Engbert and Kliegl 2003;Hafed 2013;Hafed and Clark 2002;Hafed et al 2011;2013;Kliegl et al 2009;Laubrock et al 2005;Peel et al 2016;Tian et al 2016).…”

“…It was also recently found that large voluntary saccades are associated with behavioral performance oscillations like in our results (Benedetto and Morrone 2017;Hogendoorn 2016;Wutz et al 2016). However, an intriguing difference between these observations and ours is that our oscillations were higher in frequency than in these studies.…”

“…Since microsaccades cannot be generally made at such high frequencies (e.g., Fig. 4B), this leads us to hypothesize that microsaccades may "ride" on slow frequency rhythms, as we have recently suggested (Tian et al 2016), and as is the case with the large saccade results of Benedetto and Morrone (2017) and Hogendoorn (2016), but that they reset the phase of higher frequency oscillations. Such resetting could serve the purpose of regularizing visual processing in between two successive movements (Chen and Hafed 2017), particularly with the sequential hemifield pulsing that we observed.…”

“…For example, Benedetto and colleagues have recently found a synchronous relationship between~3.5-and 8-Hz behavioral oscillation rhythms of contrast sensitivity and reaching arm movements (Benedetto et al 2016;Tomassini et al 2015). Moreover, large, voluntary saccades are associated with phase locking of~3-to 4-Hz behavioral oscillations (Benedetto and Morrone 2017;Hogendoorn 2016;Wutz et al 2016), and microsaccades have been shown to reset physiological ␣ rhythms (~10 Hz) in occipital cortex (Gaarder et al 1966).…”

Previewing a face in the periphery reduces the fN170: Combined EEG and eye-tracking suggests two stages of trans-saccadic predictive processes

“…These were trials in which participants kept stable fixation within 2° of screen center, made no saccades before cue onset, and the saccade end point had to be within 2.16° of target face center. If the target had not been presented before fixation onset, due to a delay in saccade detection, the time difference between fixation onset and target onset had to be less than 20 ms (see Figure 1C and Procedure for details), which is largely within the time course of saccadic suppression (Benedetto and Morrone, 2017; Bremmer et al, 2009; Diamond et al, 2000). This restriction was disregarded in Experiment 2 for the preview-locked analysis only, because this analysis focused on the time period before the saccade and disregarding this criterion increased the number of available trials.…”