Pupil diameter encodes the idiosyncratic, cognitive complexity of belief updating

Abstract

Pupils tend to dilate in response to surprising events, but whether these responses are primarily stimulus driven or instead reflect a more nuanced relationship between pupillinked arousal systems and cognitive expectations is not known. Using an auditory adaptive decision-making task, we show that evoked pupil diameter is modulated more strongly by violations of learned, top-down expectations than by changes in low-level stimulus properties. We further show that both baseline and evoked pupil diameter is modulated by the degree to which individual subjects use these violations to update their subsequent expectations, as reflected in the complexity of their updating strategy. Together these results demonstrate a central role for cognitive processing in how arousal systems respond to new inputs and, via our complexity-based analyses, provide a unified framework for understanding these effects in terms of both inference processes aimed to reduce belief uncertainty and more traditional notions of mental effort.

Behavioral, physiological, and neural signatures of surprise during naturalistic sports viewing

“…The angular gyrus also strongly aligned with subjective boundary agreement (r = 0.21, p = 0.005), in line with previous accounts 18,33 . Previous accounts have linked event segmentation and surprise with pupil dilation [19][20][21][22][23] , which we investigated next. There are challenges analyzing pupil dilation with video stimuli, as pupil area measurements with conventional eye trackers differ by the gaze location of the eye 37 , decrease with global and local visual luminance 38 , and increase with salient sounds 39 .…”

“…Violations of these predictions (i.e., surprises) are thought to create event boundaries, which are reflected by subjective segmentation of continuous perception 16 , pronounced shifts in neural states 18 , and physiological changes such as pupil dilations [19][20][21][22][23] . Here, we investigated how surprise relates to these measurements.…”

Pupil diameter tracked during motor adaptation in humans

“…One novel finding that has not been well documented in the previous studies is the rapid reduction of surprise/uncertainty-like pupillary responses at force field change points across repeated exposures (experiment 2). We have called this meta-habituation, which may indicate the dynamic partitioning of uncertainty into expected vs. unexpected sources over the course of task experience, presumably through the interaction between bottom-up and top-down processes in assessing environmental uncertainty and surprise about observations (Filipowicz et al, 2020;Joshi and Gold, 2020). In other words, acquisition of higher-level knowledge about the task structure (i.e., the presence of change points) might have made the sudden increase in motor errors no longer surprising, but somehow "expected".…”

Pupil dilation and the slow wave ERP reflect surprise about choice outcome resulting from intrinsic variability in decision confidence

“…Pupil dilation at constant luminance has been related to deviant (unexpected) stimuli (Alamia et al, 2019;Bianco et al, 2020;Kamp & Donchin, 2015a;Kloosterman et al, 2015;Knapen et al, 2016;Liao et al, 2018;Murphy, Vandekerckhove, et al, 2014;Raisig et al, 2010;Van Slooten et al, 2018;Wetzel et al, 2016;Zhao et al, 2019), behavioral error awareness (Critchley, 2005;Maier et al, 2019;Murphy et al, 2016) and to key computational variables such as "uncertainty" about the state the world and/or the right course of action and subsequent "surprise" after finding out (Colizoli et al, 2018;De Berker et al, 2016;Filipowicz et al, 2020;Findling et al, 2019;Krishnamurthy et al, 2017;Lempert et al, 2015;Murphy et al, 2020;Nassar et al, 2012;O'Reilly et al, 2013;Preuschoff et al, 2011;Richer & Beatty, 1987;Urai et al, 2017;Van Slooten et al, 2018;Vincent et al, 2019). Pupil size closely tracks fluctuations in the cortical arousal state mediated by subcortical neuromodulatory systems like the noradrenergic locus coeruleus and the cholinergic basal forebrain (Aston-Jones & Joshi & Gold, 2020;Larsen & Waters, 2018;McGinley et al, 2015).…”