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

Abstract

Variations in human behavior correspond to the nervous system's adaptation 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 co-modulated. 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 one minute. 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 approximately 300 ms before the peak of the pupil diameter. In contrast, the minimum alpha-band amplitude was noted to occur about 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 pupil’s diameter.

Significance Statement

Attention is a cognitive process through which an organism selects information based on adaptive behavior. Alpha-band EEG activity and pupil dynamics account for the variations in attention during cognitive tasks. During natural behavior, it is challenging to assess modulations of attention over time solely through EEG signals. Therefore, we explored whether pupillary activity could reflect similar processes. We measured the spontaneous fluctuations of EEG alpha-band activity and pupil diameter and found a robust temporal relationship between the two, suggesting fluctuations in attention.