Strength of low-frequency EEG phase entrainment to external stimuli is associated with fluctuations in the brain's internal state

Abstract

The brain attends to environmental rhythms by aligning the phase of internal oscillations. However, the factors underlying fluctuations in the strength of this phase entrainment remain largely unknown. In the present study we examined whether the strength of low-frequency EEG phase entrainment to rhythmic stimulus sequences varied with pupil size and posterior alpha-band power, thought to reflect arousal level and excitability of posterior cortical brain areas, respectively. We recorded pupil size and scalp EEG while participants carried out an intermodal selective attention task, in which they were instructed to attend to a rhythmic sequence of visual or auditory stimuli and ignore the other perceptual modality. As expected, intertrial phase coherence (ITC), a measure of entrainment strength, was larger for the task-relevant than for the task-irrelevant modality. Across the experiment, pupil size and posterior alpha power were strongly linked with each other. Interestingly, ITC tracked both variables: larger pupil size was associated with a selective increase in entrainment to the task-relevant stimulus sequence, whereas larger posterior alpha power was associated with a decrease in phase entrainment to both the task-relevant and task-irrelevant stimulus sequences. Exploratory analyses showed that a temporal relation between ITC and posterior alpha power emerged in the time periods around pupil maxima and pupil minima. These results indicate that endogenous sources contribute distinctly to the fluctuations of EEG phase entrainment. Significance statementFluctuations in cortical state powerfully shape the perception of external stimuli. Understanding the physiological signatures of cortical state fluctuations is crucial to understand how the brain selectively attends and switches between internal and external content. Here we studied how two signatures of attentional state, pupil-linked arousal and power in the alpha band, shape the entrainment of brain activity to low-frequency rhythmic stimuli. Our results reveal common and dissociable influences of these signatures at slow time scales. Furthermore, measuring and including pupil size and posterior alpha power as covariates in statistical models can help increase statistical power in studies focusing on EEG phase entrainment. Our study provides new evidence on a direct influence of cortical state on the perception of rhythmic stimuli.