Temporal Integration Windows in Neural Processing and Perception Aligned to Saccadic Eye Movements

Abstract

SummaryWhen processing dynamic input, the brain balances the opposing needs of temporal integration and sensitivity to change. We hypothesized that the visual system might resolve this challenge by aligning integration windows to the onset of newly arriving sensory samples. In a series of experiments, human participants observed the same sequence of two displays separated by a brief blank delay when performing either an integration or segregation task. First, using magneto-encephalography (MEG), we found a shift in the stimulus-evoked time courses by a 150-ms time window between task signals. After stimulus onset, multivariate pattern analysis (MVPA) decoding of task in occipital-parietal sources remained above chance for almost 1 s, and the task-decoding pattern interacted with task outcome. In the pre-stimulus period, the oscillatory phase in the theta frequency band was informative about both task processing and behavioral outcome for each task separately, suggesting that the post-stimulus effects were caused by a theta-band phase shift. Second, when aligning stimulus presentation to the onset of eye fixations, there was a similar phase shift in behavioral performance according to task demands. In both MEG and behavioral measures, task processing was optimal first for segregation and then integration, with opposite phase in the theta frequency range (3–5 Hz). The best fit to neurophysiological and behavioral data was given by a dampened 3-Hz oscillation from stimulus or eye fixation onset. The alignment of temporal integration windows to input changes found here may serve to actively organize the temporal processing of continuous sensory input.

Saccadic Suppression Is Embedded Within Extended Oscillatory Modulation of Sensitivity

“…Both suppression and enhancement are independent of stimulus eccentricity (Knöll et al, 2011) and thus are unlikely generated by spatial attention, which shifts from fixation to saccadic target very early, ϳ300 ms before saccadic onset (Kowler et al, 1995;Deubel and Schneider, 1996;Rolfs and Carrasco, 2012). The perisaccadic suppression and the subsequent enhancement form a cycle of an oscillation at ϳ3 Hz, suggesting that they might be part of a more prolonged oscillation linked to saccadic preparation, similarly to the visual oscillation demonstrated in preparation of an hand action (Tomassini et al, 2015;Benedetto et al, 2016).…”

“…Brain oscillations might be important in binding and integrating sensorimotor information (Engel et al, 2001) via a shared internal oscillator that coordinates the two systems. Recent experiments have shown that voluntary movements can synchronize oscillations of visual performance (Tomassini et al, 2015;Benedetto et al, 2016). Therefore, action not only interferes with perception through a single transient suppression at around movement time (a phenomenon called "motorinduced suppression"), but rhythmically interacting long before and after action execution.…”

“…However, we do not know whether it is a temporally punctual signal informing vision about the incoming saccades or if it is a sluggish signal that builds up during the preparation of the saccade. Many voluntary action onsets are preceded by a readiness potential that have a gradual buildup over 500 ms or more (Deecke et al, 1969;Libet et al, 1983;Ball et al, 1999;Toma et al, 2002;Bozzacchi et al, 2012). It is likely that, for saccades as well, there is a long buildup of the corollary discharge signal.…”

How to test for phasic modulation of neural and behavioural responses

“…the null distribution). This distribution can, for instance, be constructed by repeatedly shuffling performance labels (e.g., "hits" vs "misses") and re-running the original analysis on the permuted datasets (Busch et al, 2009;Dugué et al, 2011;Hanslmayr et al, 2013;Ng et al, 2012;Ronconi et al, 2017;Strauß et al, 2015;ten Oever and Sack, 2015;Wutz et al, 2016).…”

Prefrontal attentional saccades explore space rhythmically

“…However, recent experimental 18 work provides a completely different perspective onto selective attention, suggesting that spatial 19 attention samples the visual scene rhythmically [20][21][22][23][24][25][26] . These studies report that target detection 20 performance at an attended location fluctuates rhythmically very much like overt sampling processes, such 21 as eye exploration in primates [27][28][29] or whisking in rodents 30,31 . The neural processes at the origin of this 22 rhythmic sampling of space by attention are still poorly understood.…”