Phasic modulation of visual representations during sustained attention

van Es, Mats W.J.; Marshall, Tom R.; Spaak, Eelke; Jensen, Ole; Schoffelen, Jan-Mathijs · 2020 · Crossref

DOI: 10.1101/2020.09.04.282715

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Summary

This study investigates whether sustained visual attention modulates the strength of visual representations in the brain in a discrete, rhythmic manner, challenging the traditional view of continuous attentional processing. Motivated by prior evidence linking behavioral fluctuations to theta/alpha (7–10 Hz) oscillatory phases, the authors sought to determine if the decodability of visual stimulus orientation from magnetoencephalographic (MEG) signals fluctuates periodically with the phase of spontaneous brain activity. Specifically, they tested whether these phasic modulations originate in early visual cortex or in the fronto-parietal attention network. Ten healthy participants performed a covert spatial attention task while undergoing MEG recording. Subjects fixated on a central cross and attended to one of two drifting sinusoidal gratings presented in the left or right visual hemifield, indicated by a spatial cue. They reported the rotation direction of the cued grating. The researchers used multivariate pattern analysis, specifically support vector machines (SVM), to decode the orientation (clockwise vs. counter-clockwise) of the attended stimulus from MEG data recorded 400–1000 ms after stimulus onset, excluding early event-related fields. To assess phasic modulation, decoding performance was analyzed as a function of the instantaneous phase of ongoing theta/alpha activity in various brain regions, including visual cortex and the fronto-parietal network (frontal eye fields and parietal cortex). Control analyses ensured that decoding accuracy was not driven by eye movements or gaze biases. The results demonstrated that stimulus orientation could be reliably decoded from MEG signals with approximately 70% accuracy, significantly above chance. Crucially, the phase of ongoing theta/alpha activity in the visual cortex did not modulate decoding performance. However, the theta/alpha phase of activity in the frontal eye fields (FEF) and parietal cortex, specifically contralateral to the attended stimulus, significantly modulated the strength of the visual representation. This indicates that the periodic fluctuations in visual processing are not driven by local sensory rhythms but by top-down signals from the attention network. These findings suggest that sustained attention operates through discrete, rhythmic sampling governed by theta/alpha oscillations in the fronto-parietal attention network. The study provides neural evidence that top-down attentional mechanisms impose a phasic structure on visual representations, supporting theoretical accounts where oscillatory phases gate sensory input. This implies that the efficiency of visual perception is not constant but fluctuates rhythmically based on the state of fronto-parietal circuits, offering a mechanistic explanation for the discrete nature of attentional sampling.

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