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

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Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing. / Pfeffer, Thomas; Keitel, Christian; Kluger, Daniel S; Keitel, Anne; Russmann, Alena; Thut, Gregor; Donner, Tobias H; Gross, Joachim.

in: ELIFE, Jahrgang 11, e71890, 08.02.2022.

Publikationen: SCORING: Beitrag in Fachzeitschrift/Zeitung › SCORING: Zeitschriftenaufsatz › Forschung › Begutachtung

Harvard

Pfeffer, T, Keitel, C, Kluger, DS, Keitel, A, Russmann, A, Thut, G, Donner, TH & Gross, J 2022, 'Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing', ELIFE, Jg. 11, e71890. https://doi.org/10.7554/eLife.71890

APA

Pfeffer, T., Keitel, C., Kluger, D. S., Keitel, A., Russmann, A., Thut, G., Donner, T. H., & Gross, J. (2022). 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

Vancouver

Pfeffer T, Keitel C, Kluger DS, Keitel A, Russmann A, Thut G et al. Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing. ELIFE. 2022 Feb 8;11. e71890. https://doi.org/10.7554/eLife.71890

Bibtex

@article{4a07543dc026415c8fbbe99f4b4900b6,
title = "Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing",
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.",
keywords = "Adult, Arousal/physiology, Brain/diagnostic imaging, Cerebral Cortex/diagnostic imaging, Cognition, Female, Humans, Magnetoencephalography/methods, Male, Neurons/physiology, Pupil/physiology",
author = "Thomas Pfeffer and Christian Keitel and Kluger, {Daniel S} and Anne Keitel and Alena Russmann and Gregor Thut and Donner, {Tobias H} and Joachim Gross",
note = "{\textcopyright} 2022, Pfeffer et al.",
year = "2022",
month = feb,
day = "8",
doi = "10.7554/eLife.71890",
language = "English",
volume = "11",
journal = "ELIFE",
issn = "2050-084X",
publisher = "eLife Sciences Publications",

}

RIS

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 - © 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 - Adult

KW - Arousal/physiology

KW - Brain/diagnostic imaging

KW - Cerebral Cortex/diagnostic imaging

KW - Cognition

KW - Female

KW - Humans

KW - Magnetoencephalography/methods

KW - Male

KW - Neurons/physiology

KW - Pupil/physiology

U2 - 10.7554/eLife.71890

DO - 10.7554/eLife.71890

M3 - SCORING: Journal article

C2 - 35133276

VL - 11

JO - ELIFE

JF - ELIFE

SN - 2050-084X

M1 - e71890

ER -