Transcranial electrical stimulation over premotor cortex mimics attentional modulation of visual processing

Abstract

Attentional control over sensory processing has been linked to neural alpha oscillations and related pulsed inhibition of the human 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 premotor cortex are causally involved in top-down regulation of visual cortex responsivity to contrast. We applied intermittent transcranial alternating current stimulation (tACS) over bilateral premotor cortex to manipulate attentional preparation in a visual discrimination task. tACS was applied at 10 Hz (alpha) and controlled with 40 Hz (gamma) and sham stimulation. Importantly, we used a novel linear mixed modeling approach for statistical control of neurosensory side-effects of the electric stimulation. We found a frequency-specific effect of alpha tACS on the slope parameter, leading to enhanced low-contrast perception and decreased perception of high-contrast stimuli. Side-effects affected both threshold and slope parameters, leading to high variability in parameter estimates. Controlling the impact of side-effects on psychometric parameters by linear mixed model analysis reduced variability and clarified the existing effect. We conclude that alpha tACS over premotor cortex mimicked a state of increased endogenous attention potentially by modulation of fronto-occipital connectivity in the alpha band. We speculate that this network modulation allowed for improved sensory readout from visual cortex which led to a decrease in psychometric slope, effectively broadening the dynamic range for contrast perception. Significance statementAttention is fundamental to voluntary control of perception and behavior. Yet, despite extensive scientific efforts, precise underlying neural mechanisms remain elusive. We contribute to this ongoing discussion by providing evidence for a vital role of frontal alpha oscillations in regulating the responsivity of visual cortex. By controlled neuromodulation with intermittent transcranial alternating current stimulation (tACS), we show that alpha tACS modulates psychometric properties of visual contrast perception. This study fills an important gap between work on alpha oscillations in spatial attention and studies on the psychometrics of attention. Furthermore, we pioneered an approach for the statistical control of tACS side-effects with linear mixed modeling and thereby add to the ongoing debate on outcome variability in studies using transcranial neurostimulation methods.