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Phasic arousal suppresses suboptimal decision biases in mice and humans

View ORCID ProfileJ. W. de Gee, View ORCID ProfileK. Tsetsos, L. Schwabe, View ORCID ProfileA.E. Urai, D. A. McCormick, M. J. McGinley, View ORCID ProfileT. H. Donner
doi: https://doi.org/10.1101/447656
J. W. de Gee
1Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
2Department of Psychology, University of Amsterdam, Amsterdam, Netherlands
3Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA
4Jan and Dan Duncan Neurological Research Institute, Texas Children’s Hospital, Houston, TX, USA
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  • For correspondence: jwdegee@gmail.com
K. Tsetsos
1Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
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L. Schwabe
5Department of Cognitive Psychology, Institute of Psychology, University of Hamburg, Germany
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A.E. Urai
1Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
2Department of Psychology, University of Amsterdam, Amsterdam, Netherlands
6Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
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D. A. McCormick
7Institute of Neuroscience, University of Oregon, OR, USA
8Department of Neuroscience, Yale University, New Haven, CT, USA
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M. J. McGinley
3Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA
4Jan and Dan Duncan Neurological Research Institute, Texas Children’s Hospital, Houston, TX, USA
8Department of Neuroscience, Yale University, New Haven, CT, USA
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T. H. Donner
1Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
2Department of Psychology, University of Amsterdam, Amsterdam, Netherlands
9Amsterdam Brain & Cognition, University of Amsterdam, Amsterdam, Netherlands
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Abstract

Many difficult decisions are made by accumulating ambiguous evidence over time. The brain’s arousal systems are rapidly activated during such decisions. How do these rapid (“phasic”) boosts in arousal affect the decision process? Here, we have unveiled a general principle of the function of phasic arousal: suppressing suboptimal biases in evidence accumulation. We quantified phasic arousal as rapid dilations of the pupil. Pupil dilations predicted reduced biases in a range of decision-making tasks and different species. In a challenging sound-detection task, both mice and humans were less biased under high arousal. Similar bias suppression occurred when optimal biases were neutral, conservative or liberal, when evidence was accumulated from memory, and for risk-seeking biases in decisions entailing the accumulation of numerical values. In all cases, the smaller behavioral biases were explained by specific changes in evidence accumulation. Thus, phasic arousal calibrates a key computation during decision-making.

Footnotes

  • ↵* shared senior

  • ↵# lead contact

  • We rewrote the manuscript to consistently interpret the pupil response in terms of phasic arousal. We also conducted one new experiment in which we systematically manipulated signal probability, and found that, within the same subjects, phasic arousal flexibly reduces both conservative and liberal accumulation biases in a context-dependent manner. Finally, we replicated the pupil-predicted suppression of biases of both signs in a large sample of human subjects performing a memory task; bringing in yet another mode of decision-making (memory-based decisions) further generalized our claim.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted June 17, 2019.
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Phasic arousal suppresses suboptimal decision biases in mice and humans
J. W. de Gee, K. Tsetsos, L. Schwabe, A.E. Urai, D. A. McCormick, M. J. McGinley, T. H. Donner
bioRxiv 447656; doi: https://doi.org/10.1101/447656
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Phasic arousal suppresses suboptimal decision biases in mice and humans
J. W. de Gee, K. Tsetsos, L. Schwabe, A.E. Urai, D. A. McCormick, M. J. McGinley, T. H. Donner
bioRxiv 447656; doi: https://doi.org/10.1101/447656

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