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.
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 funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
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.
© 2022, Pfeffer et al.
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