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

TY - JOUR

T1 - Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

AU - Pfeffer, Thomas

AU - Keitel, Christian

AU - Kluger, Daniel S.

AU - Keitel, Anne

AU - Russmann, Alena

AU - Thut, Gregor

AU - Donner, Tobias H.

AU - Gross, Joachim

N1 - Copyright: © 2022 Pfeffer et al.

PY - 2022/2/8

Y1 - 2022/2/8

N2 - 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.

AB - 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.

KW - acetylcholine

KW - arousal

KW - cortical state

KW - human

KW - locus coeruleus

KW - neuroscience

KW - noradrenaline

KW - pupil

UR - https://www.scopus.com/pages/publications/85124809504

UR - https://www.webofscience.com/wos/woscc/full-record/WOS:000760315100001?SID=EUW1ED0ABDhAtLvbrHO5lc4OGpAvx

U2 - 10.7554/eLife.71890

DO - 10.7554/eLife.71890

M3 - Article

C2 - 35133276

SN - 2050-084X

VL - 11

JO - eLife

JF - eLife

M1 - e71890

ER -