Dynamic modulation of decision biases by brainstem arousal systems

  1. Jan Willem de Gee  Is a corresponding author
  2. Olympia Colizoli
  3. Niels A Kloosterman
  4. Tomas Knapen
  5. Sander Nieuwenhuis
  6. Tobias H Donner  Is a corresponding author
  1. University Medical Center Hamburg-Eppendorf, Germany
  2. University of Amsterdam, Netherlands
  3. Vrije Universiteit Amsterdam, Netherlands
  4. Leiden University, Netherlands

Abstract

Decision-makers often arrive at different choices when faced with repeated presentations of the same evidence. Variability of behavior is commonly attributed to noise in the brain's decision-making machinery. We hypothesized that phasic responses of brainstem arousal systems are a significant source of this variability. We tracked pupil responses (a proxy of phasic arousal) during sensory-motor decisions in humans, across different sensory modalities and task protocols. Large pupil responses generally predicted a reduction in decision bias. Using fMRI, we showed that the pupil-linked bias reduction was (i) accompanied by a modulation of choice-encoding pattern signals in parietal and prefrontal cortex and (ii) predicted by phasic, pupil-linked responses of a number of neuromodulatory brainstem centers involved in the control of cortical arousal state, including the noradrenergic locus coeruleus. We conclude that phasic arousal suppresses decision bias on a trial-by-trial basis, thus accounting for a significant component of the variability of choice behavior.

Data availability

The following previously published data sets were used

Article and author information

Author details

  1. Jan Willem de Gee

    Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    For correspondence
    jwdegee@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5875-8282
  2. Olympia Colizoli

    Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Niels A Kloosterman

    Department of Psychology, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Tomas Knapen

    Department of Experimental and Applied Psychology, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Sander Nieuwenhuis

    Institute of Psychology, Leiden University, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2418-3879
  6. Tobias H Donner

    Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    For correspondence
    t.donner@uke.de
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (SFB 936/Z1)

  • Tobias H Donner

Deutsche Forschungsgemeinschaft (DO1240/3-1)

  • Tobias H Donner

Seventh Framework Programme (604102)

  • Tobias H Donner

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

Ethics

Human subjects: All subjects gave written informed consent, and consent to publish. The ethics committee of the Psychology Department of the University of Amsterdam approved the experiments (Id's: 2014-BC-3406; 2015-BC-4613; 2016-BC-6842).

Reviewing Editor

  1. Klaas Enno Stephan, University of Zurich and ETH Zurich, Switzerland

Publication history

  1. Received: November 14, 2016
  2. Accepted: March 17, 2017
  3. Accepted Manuscript published: April 6, 2017 (version 1)
  4. Accepted Manuscript updated: April 11, 2017 (version 2)
  5. Version of Record published: April 28, 2017 (version 3)
  6. Version of Record updated: May 22, 2017 (version 4)

Copyright

© 2017, de Gee et al.

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.

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  1. Jan Willem de Gee
  2. Olympia Colizoli
  3. Niels A Kloosterman
  4. Tomas Knapen
  5. Sander Nieuwenhuis
  6. Tobias H Donner
(2017)
Dynamic modulation of decision biases by brainstem arousal systems
eLife 6:e23232.
https://doi.org/10.7554/eLife.23232
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