Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing
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...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/71890 |
| _version_ | 1797998626448867328 |
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| author | Thomas Pfeffer Christian Keitel Daniel S Kluger Anne Keitel Alena Russmann Gregor Thut Tobias H Donner Joachim Gross |
| author_facet | Thomas Pfeffer Christian Keitel Daniel S Kluger Anne Keitel Alena Russmann Gregor Thut Tobias H Donner Joachim Gross |
| author_sort | Thomas Pfeffer |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T10:51:40Z |
| format | Article |
| id | doaj.art-10c9e48b34a041a1a79a2bd9797df8b3 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:51:40Z |
| publishDate | 2022-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-10c9e48b34a041a1a79a2bd9797df8b32022-12-22T04:28:53ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.71890Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processingThomas Pfeffer0https://orcid.org/0000-0001-9561-3085Christian Keitel1https://orcid.org/0000-0003-2597-5499Daniel S Kluger2https://orcid.org/0000-0002-0691-794XAnne Keitel3https://orcid.org/0000-0003-4498-0146Alena Russmann4Gregor Thut5Tobias H Donner6https://orcid.org/0000-0002-7559-6019Joachim Gross7https://orcid.org/0000-0002-3994-1006Universitat Pompeu Fabra, Center for Brain and Cognition, Computational Neuroscience Group, Barcelona, Spain; University Medical Center Hamburg-Eppendorf, Department of Neurophysiology and Pathophysiology, Hamburg, GermanyUniversity of Stirling, Psychology, Stirling, United Kingdom; Centre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United KingdomInstitute for Biomagnetism and Biosignal Analysis, University of Münster, Malmedyweg, Muenster, Germany; Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Münster, Muenster, GermanyUniversity of Dundee, Psychology, Dundee, United KingdomUniversity Medical Center Hamburg-Eppendorf, Department of Neurophysiology and Pathophysiology, Hamburg, GermanyCentre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United KingdomUniversity Medical Center Hamburg-Eppendorf, Department of Neurophysiology and Pathophysiology, Hamburg, GermanyCentre for Cognitive Neuroimaging, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, United Kingdom; Institute for Biomagnetism and Biosignal Analysis, University of Münster, Malmedyweg, Muenster, Germany; Otto Creutzfeldt Center for Cognitive and Behavioral Neuroscience, University of Münster, Muenster, GermanyFluctuations 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.https://elifesciences.org/articles/71890arousallocus coeruleusnoradrenalineacetylcholinecortical statepupil |
| spellingShingle | Thomas Pfeffer Christian Keitel Daniel S Kluger Anne Keitel Alena Russmann Gregor Thut Tobias H Donner Joachim Gross Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing eLife arousal locus coeruleus noradrenaline acetylcholine cortical state pupil |
| title | Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing |
| title_full | Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing |
| title_fullStr | Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing |
| title_full_unstemmed | Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing |
| title_short | Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing |
| title_sort | coupling of pupil and neuronal population dynamics reveals diverse influences of arousal on cortical processing |
| topic | arousal locus coeruleus noradrenaline acetylcholine cortical state pupil |
| url | https://elifesciences.org/articles/71890 |
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