Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

  1. Thomas Pfeffer  Is a corresponding author
  2. Christian Keitel  Is a corresponding author
  3. Daniel S Kluger
  4. Anne Keitel
  5. Alena Russmann
  6. Gregor Thut
  7. Tobias H Donner
  8. Joachim Gross
  1. Universitat Pompeu Fabra, Spain
  2. University of Stirling, United Kingdom
  3. University of Münster, Germany
  4. University of Dundee, United Kingdom
  5. University Medical Center Hamburg-Eppendorf, Germany
  6. University of Glasgow, United Kingdom
  7. University of Muenster, Germany

Abstract

Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing. Yet, how arousal signals influence cortical population activity in detail has so far only been characterized for a few selected brain regions. Traditional accounts conceptualize arousal as a homogeneous modulator of neural population activity across the cerebral cortex. Recent insights, however, point to a higher specificity of arousal effects on different components of neural activity and across cortical regions. Here, we provide a comprehensive account of the relationships between fluctuations in arousal and neuronal population activity across the human brain. Exploiting the established link between pupil size and central arousal systems, we performed concurrent magnetoencephalographic (MEG) and pupillographic recordings in a large number of participants, pooled across three laboratories. We found a cascade of effects relative to the peak timing of spontaneous pupil dilations: Decreases in low-frequency (2-8 Hz) activity in temporal and lateral frontal cortex, followed by increased high-frequency (>64 Hz) activity in mid-frontal regions, followed by monotonic and inverted-U relationships with intermediate frequency-range activity (8-32 Hz) in occipito-parietal regions. Pupil-linked arousal also coincided with widespread changes in the structure of the aperiodic component of cortical population activity, indicative of changes in the excitation-inhibition balance in underlying microcircuits. Our results provide a novel basis for studying the arousal modulation of cognitive computations in cortical circuits.

Data availability

The ethics protocol(s) disallow sharing raw and preprocessed MEG and MRI data via a public repository. Data may be shared however within the context of a collaboration.No proposal is needed. However, the results presented in the manuscript are based on three separate datasets, collected independently in three different laboratories. As such, in order to obtain the data, an (informal) email to the authors responsible for the respective data sets is required (Hamburg: Thomas Pfeffer, thms.pfffr@gmail.com; Glasgow: Anne Keitel, a.keitel@dundee.ac.uk; Münster: Daniel Kluger, daniel.kluger@wwu.de).The code and data immediately underlying all main and supplementary figures has been made publicly available. Source data has been uploaded to a public repository (https://osf.io/fw4bt), along with MATLAB code that was used to generate the main and supplementary figures.

The following data sets were generated

Article and author information

Author details

  1. Thomas Pfeffer

    Department of Neurophysiology and Pathophysiology, Universitat Pompeu Fabra, Barcelona, Spain
    For correspondence
    thms.pfffr@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9561-3085
  2. Christian Keitel

    Department of Psychology, University of Stirling, Stirling, United Kingdom
    For correspondence
    christian.keitel@stir.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2597-5499
  3. Daniel S Kluger

    Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Münster, Münster, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0691-794X
  4. Anne Keitel

    Department of Psychology, University of Dundee, Dundee, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4498-0146
  5. Alena Russmann

    Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    No competing interests declared.
  6. Gregor Thut

    Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom
    Competing interests
    No competing interests declared.
  7. Tobias H Donner

    Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    Tobias H Donner, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7559-6019
  8. Joachim Gross

    Institute for Biomagnetism and Biosignalanalysis, University of Muenster, Muenster, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3994-1006

Funding

Alexander von Humboldt-Stiftung (Feodor-Lynen Fellowship)

  • Thomas Pfeffer

Interdisciplinary Center for Clinical Research of the Medical Faculty of Münster (Gro3/001/19)

  • Joachim Gross

Deutsche Forschungsgemeinschaft (GR 2024/5-1)

  • Joachim Gross

Wellcome Trust (Senior Investigator Grant #098433)

  • Joachim Gross

Wellcome Trust (Senior Investigator Grant #98434)

  • Gregor Thut

University of Glasgow (BBSRC Flexible Talent Mobility funding (BB/R506576/1))

  • Christian Keitel

Deutsche Forschungsgemeinschaft (DO 1240/3-1)

  • Tobias H Donner

Deutsche Forschungsgemeinschaft (DO 1240/4-1)

  • Tobias H Donner

Deutsche Forschungsgemeinschaft (SFB 936 A7/Z3)

  • Tobias H Donner

Bundesministerium für Bildung und Forschung (01GQ1907)

  • Tobias H Donner

Bundesministerium für Bildung und Forschung (01EW2007B)

  • 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: Human subjects were recruited and participated in the experiments in accordance with the ethics committee responsible for the University Medical Center Hamburg-Eppendorf (Hamburg MEG data) approval number PV4648, the ethics committee of the University of Glasgow, College of Science and Engineering (Glasgow MEG data) approval number 300140078, and the ethics committee of the University of Muenster (Muenster MEG data) approval number 2018-068-f-S. All participants gave written informed consent prior to all experimental procedures and received monetary compensation for their participation.

Reviewing Editor

  1. Ole Jensen, University of Birmingham, United Kingdom

Version history

  1. Preprint posted: June 25, 2021 (view preprint)
  2. Received: July 2, 2021
  3. Accepted: February 4, 2022
  4. Accepted Manuscript published: February 8, 2022 (version 1)
  5. Version of Record published: February 17, 2022 (version 2)
  6. Version of Record updated: May 31, 2022 (version 3)

Copyright

© 2022, Pfeffer 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. Thomas Pfeffer
  2. Christian Keitel
  3. Daniel S Kluger
  4. Anne Keitel
  5. Alena Russmann
  6. Gregor Thut
  7. Tobias H Donner
  8. Joachim Gross
(2022)
Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing
eLife 11:e71890.
https://doi.org/10.7554/eLife.71890

Share this article

https://doi.org/10.7554/eLife.71890

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