Transcranial alternating current stimulation over frontal eye fields mimics attentional modulation of visual processing

Abstract

Attentional control over sensory processing has been linked to neural alpha oscillations and related inhibition of cerebral cortex. Despite the wide consensus on the functional relevance of alpha oscillations for attention, precise neural mechanisms of how alpha oscillations shape perception and how this top-down modulation is implemented in cortical networks remain unclear. Here, we tested the hypothesis that alpha oscillations in frontal eye fields (FEF) are causally involved in the top-down regulation of visual processing in humans (male and female). We applied sham-controlled, intermittent transcranial alternating current stimulation (tACS) over bilateral FEF at either 10 Hz (alpha) or 40 Hz (gamma) to manipulate attentional preparation in a visual discrimination task. Under each stimulation condition, we measured psychometric functions for contrast perception and introduced a novel linear mixed modeling approach for statistical control of neurosensory side effects of the electric stimulation. TACS at alpha frequency reduced the slope of the psychometric function, resulting in improved sub-threshold and impaired super-threshold contrast perception. Side effects on the psychometric functions were complex and showed large interindividual variability. Controlling for the impact of side effects on the psychometric parameters by using covariates in the linear mixed model analysis reduced this variability and strengthened the perceptual effect. We propose that alpha tACS over FEF mimicked a state of endogenous attention by strengthening a fronto-occipitoparietal network in the alpha band. We speculate that this network modulation enhanced phasic gating in occipitoparietal cortex leading to increased variability of single-trial psychometric thresholds, measurable as a reduction of psychometric slope.Significance statement Attention is fundamental to the voluntary control of perception and behavior. Yet, precise underlying neural mechanisms remain unclear. Here, we provide evidence for a vital role of frontal alpha oscillations in the regulation of gating of visual information by using intermittent transcranial alternating current stimulation (tACS). We show that modulation of frontal alpha oscillations affected the slope of psychometric functions of visual contrast perception, leading to contrast-dependent improvement and impairment of perception. Our data adds to work on alpha oscillations in spatial attention and studies on the psychometrics of attention. Furthermore, we introduce a novel approach for the statistical control of tACS side effects and thereby contribute to the ongoing debate on outcome variability in studies using transcranial neurostimulation methods.