Alpha EEG Activity and Pupil Diameter Coupling during Inactive Wakefulness in Humans

Variations in human behavior correspond to the adaptation of the nervous system to different internal and environmental demands. Attention, a cognitive process for weighing environmental demands, changes over time. Pupillary activity, which is affected by fluctuating levels of cognitive processing, appears to identify neural dynamics that relate to different states of attention. In mice, for example, pupil dynamics directly correlate with brain state fluctuations. Although, in humans, alpha-band activity is associated with inhibitory processes in cortical networks during visual processing, and its amplitude is modulated by attention, conclusive evidence linking this narrowband activity to pupil changes in time remains sparse. We hypothesize that, as alpha activity and pupil diameter indicate attentional variations over time, these two measures should be comodulated. In this work, we recorded the electroencephalographic (EEG) and pupillary activity of 16 human subjects who had their eyes fixed on a gray screen for 1 min. Our study revealed that the alpha-band amplitude and the high-frequency component of the pupil diameter covariate spontaneously. Specifically, the maximum alpha-band amplitude was observed to occur ∼300 ms before the peak of the pupil diameter. In contrast, the minimum alpha-band amplitude was noted to occur ∼350 ms before the trough of the pupil diameter. The consistent temporal coincidence of these two measurements strongly suggests that the subject's state of attention, as indicated by the EEG alpha amplitude, is changing moment to moment and can be monitored by measuring EEG together with the diameter pupil.