Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing
- Universitat Pompeu Fabra, Spain
- University of Stirling, United Kingdom
- University of Münster, Germany
- University of Dundee, United Kingdom
- University Medical Center Hamburg-Eppendorf, Germany
- University of Glasgow, United Kingdom
- 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.
Article and author information
Author details
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.
Reviewing Editor
- Ole Jensen, University of Birmingham, United Kingdom
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.
Version history
- Preprint posted: June 25, 2021 (view preprint)
- Received: July 2, 2021
- Accepted: February 4, 2022
- Accepted Manuscript published: February 8, 2022 (version 1)
- Version of Record published: February 17, 2022 (version 2)
- 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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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
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