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

Christian Keitel,Thomas Pfeffer,Tobias H Donner,Daniel S Kluger,Joachim Gross,Gregor Thut,Anne Keitel,Alena Russmann

doi:10.7554/elife.71890

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.

Highlights

Variations in cortical state profoundly shape information processing and, cognition (Busse et al, 2017; Fu et al, 2014; Zagha et al, 2013)
We comprehensively show how this structural and molecular heterogeneity translates into a multitude of arousal effects on neuronal population activity across the human cortex
We found evidence for a inverted-U relationship between pupil-linked arousal and band-limited cortical activity that was confined to the classical alpha/beta frequency band

Summary

Introduction

Variations in cortical state profoundly shape information processing and, cognition (Busse et al, 2017; Fu et al, 2014; Zagha et al, 2013). Uniform controller of cortical state (Aston-Jones & Cohen, 2005; Harris & Thiele, 2011; Leopold et al, 2003; Turchi et al, 2018) This view has been challenged: Several neuronal subpopulations with distinct projection targets have been found in both the LC and BF (Chandler et al, 2013, 2019; Sarter et al, 2009; Schwarz & Luo, 2015; Totah et al, 2018; Zaborszky et al, 2015; Záborszky et al, 2018). We comprehensively show how this structural and molecular heterogeneity translates into a multitude of arousal effects on neuronal population activity across the human cortex

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