Voluntary Saccadic Eye Movements Ride the Attentional Rhythm

Abstract

Visual perception seems continuous, but recent evidence suggests that the underlying perceptual mechanisms are in fact periodic-particularly visual attention. Because visual attention is closely linked to the preparation of saccadic eye movements, the question arises how periodic attentional processes interact with the preparation and execution of voluntary saccades. In two experiments, human observers made voluntary saccades between two placeholders, monitoring each one for the presentation of a threshold-level target. Detection performance was evaluated as a function of latency with respect to saccade landing. The time course of detection performance revealed oscillations at around 4 Hz both before the saccade at the saccade origin and after the saccade at the saccade destination. Furthermore, oscillations before and after the saccade were in phase, meaning that the saccade did not disrupt or reset the ongoing attentional rhythm. Instead, it seems that voluntary saccades are executed as part of an ongoing attentional rhythm, with the eyes in flight during the troughs of the attentional wave. This finding for the first time demonstrates that periodic attentional mechanisms affect not only perception but also overt motor behavior.

Temporal dynamics of saccades explained by a self-paced process

“…However, in what seems to be inconsistent with the central role of environmental factors, saccade-timings are rhythmically modulated. This rhythmic modulation cannot be trivially explained by environmental factors, which do not necessarily have a periodic influence, and has led some to suggest that there is a central oscillator modulating saccade generation 14, 26, 28–30 , along the influences of task and stimulation. The present findings provide an alternative parsimonious solution to the apparent contradiction between the rhythmicity of saccades and their modulation by environmental factors.…”

“…The “communication through coherence” (CTC) model suggests that neural theta rhythm reflects the periodic termination of attentional engagement and shifts of attention from one attended target to another 3, 54, 57, 58 . This theta rhythm was suggested to drive both performance fluctuations and rhythmic sensory sampling behaviors, including saccades 26, 30 . Indeed, visual cortical oscillations at this frequency are highly synchronized with the occurrences of saccades 26, 28, 59–61 .…”

“…Environmental and volitional influences are typically non-periodic and therefore cannot trivially explain this rhythmicity. The observed saccadic rhythmicity has led some to the speculate the existence of an oscillating generation process, possibly located in the motor cortex 27 , which was also thought to govern visual attention 26, 28–30 . According to this view, human saccades are modulated by the activity of autonomous oscillatory generators, similarly to exploration behaviors in rodents.…”

Oscillatory Mechanisms of Stimulus Processing and Selection in the Visual and Auditory Systems: State-of-the-Art, Speculations and Suggestions

“…However, we emphasize that saccades are initiated by the brain: The timing of incoming information is thus known in advance—e.g., via feedback from the motor system. Therefore, we argue that, in the visual system, it might not be necessary to adapt stimulus processing to the input per se , but rather to the (rather irregular) scanning of the environment introduced by eye movements: Indeed, there is evidence that the oscillatory phase and eye movements are linked (Hogendoorn, 2016; McLelland et al, 2016). Moreover, as the visual input “changes” every ~300–500 ms (induced by a saccade) but is rather stable within this time interval, it is not essential to process (or sample) the input at the moment of the saccade (it can be processed anytime within the ~300–500 ms interval).…”

Active information sampling varies across the cardiac cycle

“…Based on findings of facilitated processing for visual stimuli (Azevedo et al, 2018(Azevedo et al, , 2017Garfinkel et al, 2014;Pramme, Larra, Schächinger, & Frings, 2014, 2016 and increased oculomotor activity (Ohl et al, 2016) during early phases of the cardiac cycle, we here hypothesized that active information sampling (i.e., self-initiated action toward a visual stimulus) shows periodic variations with the phase of our heartbeat. To investigate perception and action within a comprehensive framework of mind-brain-body interactions, we studied cardiac-related sensorimotor processing in a self-paced visual sampling paradigm, in which participants decide when to press a key to see a task-relevant visual stimulus.…”