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).

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.

Metrics

  • 5,888
    views
  • 1,086
    downloads
  • 246
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.23232

Further reading

    1. Neuroscience
    Lisa Reisinger, Gianpaolo Demarchi ... Nathan Weisz
    Research Article

    Phantom perceptions like tinnitus occur without any identifiable environmental or bodily source. The mechanisms and key drivers behind tinnitus are poorly understood. The dominant framework, suggesting that tinnitus results from neural hyperactivity in the auditory pathway following hearing damage, has been difficult to investigate in humans and has reached explanatory limits. As a result, researchers have tried to explain perceptual and potential neural aberrations in tinnitus within a more parsimonious predictive-coding framework. In two independent magnetoencephalography studies, participants passively listened to sequences of pure tones with varying levels of regularity (i.e. predictability) ranging from random to ordered. Aside from being a replication of the first study, the pre-registered second study, including 80 participants, ensured rigorous matching of hearing status, as well as age, sex, and hearing loss, between individuals with and without tinnitus. Despite some changes in the details of the paradigm, both studies equivalently reveal a group difference in neural representation, based on multivariate pattern analysis, of upcoming stimuli before their onset. These data strongly suggest that individuals with tinnitus engage anticipatory auditory predictions differently to controls. While the observation of different predictive processes is robust and replicable, the precise neurocognitive mechanism underlying it calls for further, ideally longitudinal, studies to establish its role as a potential contributor to, and/or consequence of, tinnitus.

    1. Neuroscience
    Rongxin Fang, Aaron Halpern ... Xiaowei Zhuang
    Tools and Resources

    Multiplexed error-robust fluorescence in situ hybridization (MERFISH) allows genome-scale imaging of RNAs in individual cells in intact tissues. To date, MERFISH has been applied to image thin-tissue samples of ~10 µm thickness. Here, we present a thick-tissue three-dimensional (3D) MERFISH imaging method, which uses confocal microscopy for optical sectioning, deep learning for increasing imaging speed and quality, as well as sample preparation and imaging protocol optimized for thick samples. We demonstrated 3D MERFISH on mouse brain tissue sections of up to 200 µm thickness with high detection efficiency and accuracy. We anticipate that 3D thick-tissue MERFISH imaging will broaden the scope of questions that can be addressed by spatial genomics.