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

Pfeffer, T., Keitel, C. , Kluger, D. S., Keitel, A. , Russmann, A., Thut, G. , Donner, T. H. and Gross, J. (2022) Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing. eLife, 11, e71890. (doi: 10.7554/elife.71890) (PMID:35133276) (PMCID:PMC8853659)

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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.

Item Type:Articles
Keywords:Neuroscience, arousal, locus coeruleus, noradrenaline, acetylcholine, cortical state, pupil.
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Thut, Professor Gregor and Keitel, Dr Christian and Gross, Professor Joachim and Donner, Professor Tobias and Keitel, Dr Anne
Authors: Pfeffer, T., Keitel, C., Kluger, D. S., Keitel, A., Russmann, A., Thut, G., Donner, T. H., and Gross, J.
College/School:College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
Journal Name:eLife
Publisher:eLife Sciences Publications
ISSN:2050-084X
ISSN (Online):2050-084X
Copyright Holders:Copyright © 2022 Pfeffer et al.
First Published:First published in eLife 11:e71890
Publisher Policy:Reproduced under a Creative Commons licence

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
167204Natural and modulated neural communication: State-dependent decoding and driving of human Brain Oscillations.Joachim GrossWellcome Trust (WELLCOTR)098433/Z/12/ZCentre for Cognitive Neuroimaging
167201Natural and modulated neural communication: State-dependent decoding and driving of human Brain OscillationsGregor ThutWellcome Trust (WELLCOTR)098434/Z/12/ZCentre for Cognitive Neuroimaging
302024Flexible Talent Mobility AccountsCarl GoodyearBiotechnology and Biological Sciences Research Council (BBSRC)BB/R506576/1III - Immunology