Wink or blush? Pupil-linked brain arousal signals both change and uncertainty during assessment of changing environmental regularities

Abstract

One main cornerstone of adaptive behavior is belief updating, whereby new and unexpected observations lead to the updating of learned associations between events, behaviors and outcomes. This process necessitates the detection of changed environmental contingencies which in turn leads to uncertainty about the environmental regularities. Change and uncertainty are thus inherently linked, and both constructs have been linked to pupil size changes, which might reflect activity in neural networks underlying belief updating. Thus, in our study, we aimed to disentangle the effects of change and uncertainty on pupil-linked brain arousal. We used a probabilistic reversal learning task, where participants had to act according to changing preferences of a fictional character, and used specific cues to independently manipulate the level of change and uncertainty (e.g. the fictional character winked for signalizing change, or his face was blushed to indicate uncertainty). We found that when the cues triggered the same amount of uncertainty, larger levels of change in beliefs led to a transient increase in pupil size during cue processing. In contrast, when the cues signalized a similar amount of change, then increased belief uncertainty was associated with a sustained increase in pupil size, extending in time beyond cue processing. Thus, change and uncertainty exerted independent influence on pupil-linked brain arousal, suggesting the activity of different neural networks, and highlighting the need to disentangle the effects of these overlapping but distinct theoretical constructs.