Pupil-Linked Arousal Responds to Unconscious Surprisal

Pupil size under constant illumination reflects brain arousal state, and dilates in response to novel information, or surprisal. Whether this response can be observed regardless of conscious perception is still unknown. In the present study, male and female adult humans performed an implicit learning task across a series of three experiments. We measured pupil and brain-evoked potentials to stimuli that violated transition statistics but were not relevant to the task. We found that pupil size dilated following these surprising events, in the absence of awareness of transition statistics, and only when attention was allocated to the stimulus. These pupil responses correlated with central potentials, evoking an anterior cingulate origin. Arousal response to surprisal outside the scope of conscious perception points to the fundamental relationship between arousal and information processing and indicates that pupil size can be used to track the progression of implicit learning.SIGNIFICANCE STATEMENT Pupil size dilates following increase in mental effort, surprise, or more generally global arousal. However, whether this response arises as a conscious response or reflects a more fundamental mechanism outside the scrutiny of awareness is still unknown. Here, we demonstrate that unexpected changes in the environment, even when processed unconsciously and without being relevant to the task, lead to an increase in arousal levels as reflected by the pupillary response. Further, we show that the concurrent electrophysiological response shares similarities with mismatch negativity, suggesting the involvement of anterior cingulate cortex. All in all, our results establish novel insights about the mechanisms driving global arousal levels, and it provides new possibilities for reliably measuring unconscious processes.