Pupil diameter encodes the idiosyncratic, cognitive complexity of belief updating

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Abstract

Pupils tend to dilate in response to surprising events, but it is not known whether these responses are primarily stimulus driven or instead reflect a more nuanced relationship between pupil-linked arousal systems and cognitive expectations. Using an auditory adaptive decision-making task, we show that evoked pupil diameter is more parsimoniously described as signaling violations of learned, top-down expectations than 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 idiosyncratic cognitive processing in how arousal systems respond to new inputs and, via our complexity-based analyses, offer a potential framework for understanding these effects in terms of both inference processes aimed to reduce belief uncertainty and more traditional notions of mental effort.

Data availability

All data that support the findings in this article are available at https://osf.io/4ahkx/wiki/home/. All code used in the preparation of this article can be found at https://osf.io/4ahkx/wiki/home/ and https://github.com/TheGoldLab/Analysis_Filipowicz_Glaze_etal_Audio_2AFC .

Article and author information

Author details

Alexandre L S Filipowicz

Department of Neuroscience, University of Pennsylvania, Philadelphia, United States

For correspondence
alsfilip@pennmedicine.upenn.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-1311-386X
Christopher M Glaze

Department of Neuroscience, University of Pennsylvania, Philadelphia, United States

Competing interests
No competing interests declared.
Joseph W Kable

Department of Psychology, University of Pennsylvania, Philadelphia, United States

Competing interests
No competing interests declared.
Joshua I Gold

Department of Neuroscience, University of Pennsylvania, Philadelphia, United States

Competing interests
Joshua I Gold, Senior editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0002-6018-0483

Funding

NSF (NSF-NCS 1533623)

Joseph W Kable
Joshua I Gold

NIBIB (R01 EB026945)

Joshua I Gold

NIMH (F32 MH117924)

Alexandre L S Filipowicz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: The study protocol was reviewed and approved by the University of Pennsylvania's Institutional Review Board. All subjects provided written informed consent prior to participating in the study. (IRB Protocol # 816727).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.