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Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing

The dynamic integration of sensory and bodily signals is central to adaptive behaviour. Although the anterior cingulate cortex (ACC) and the anterior insular cortex (AIC) play key roles in this process, their context-dependent dynamic interactions remain unclear. Here, we studied the spectral featur...

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Autores principales: Sonkusare, Saurabh, Wegner, Katharina, Chang, Catie, Dionisio, Sasha, Breakspear, Michael, Cocchi, Luca
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312263/
https://www.ncbi.nlm.nih.gov/pubmed/37397892
http://dx.doi.org/10.1162/netn_a_00295
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author Sonkusare, Saurabh
Wegner, Katharina
Chang, Catie
Dionisio, Sasha
Breakspear, Michael
Cocchi, Luca
author_facet Sonkusare, Saurabh
Wegner, Katharina
Chang, Catie
Dionisio, Sasha
Breakspear, Michael
Cocchi, Luca
author_sort Sonkusare, Saurabh
collection PubMed
description The dynamic integration of sensory and bodily signals is central to adaptive behaviour. Although the anterior cingulate cortex (ACC) and the anterior insular cortex (AIC) play key roles in this process, their context-dependent dynamic interactions remain unclear. Here, we studied the spectral features and interplay of these two brain regions using high-fidelity intracranial-EEG recordings from five patients (ACC: 13 contacts, AIC: 14 contacts) acquired during movie viewing with validation analyses performed on an independent resting intracranial-EEG dataset. ACC and AIC both showed a power peak and positive functional connectivity in the gamma (30–35 Hz) frequency while this power peak was absent in the resting data. We then used a neurobiologically informed computational model investigating dynamic effective connectivity asking how it linked to the movie’s perceptual (visual, audio) features and the viewer’s heart rate variability (HRV). Exteroceptive features related to effective connectivity of ACC highlighting its crucial role in processing ongoing sensory information. AIC connectivity was related to HRV and audio emphasising its core role in dynamically linking sensory and bodily signals. Our findings provide new evidence for complementary, yet dissociable, roles of neural dynamics between the ACC and the AIC in supporting brain-body interactions during an emotional experience.
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spelling pubmed-103122632023-07-01 Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing Sonkusare, Saurabh Wegner, Katharina Chang, Catie Dionisio, Sasha Breakspear, Michael Cocchi, Luca Netw Neurosci Research Article The dynamic integration of sensory and bodily signals is central to adaptive behaviour. Although the anterior cingulate cortex (ACC) and the anterior insular cortex (AIC) play key roles in this process, their context-dependent dynamic interactions remain unclear. Here, we studied the spectral features and interplay of these two brain regions using high-fidelity intracranial-EEG recordings from five patients (ACC: 13 contacts, AIC: 14 contacts) acquired during movie viewing with validation analyses performed on an independent resting intracranial-EEG dataset. ACC and AIC both showed a power peak and positive functional connectivity in the gamma (30–35 Hz) frequency while this power peak was absent in the resting data. We then used a neurobiologically informed computational model investigating dynamic effective connectivity asking how it linked to the movie’s perceptual (visual, audio) features and the viewer’s heart rate variability (HRV). Exteroceptive features related to effective connectivity of ACC highlighting its crucial role in processing ongoing sensory information. AIC connectivity was related to HRV and audio emphasising its core role in dynamically linking sensory and bodily signals. Our findings provide new evidence for complementary, yet dissociable, roles of neural dynamics between the ACC and the AIC in supporting brain-body interactions during an emotional experience. MIT Press 2023-06-30 /pmc/articles/PMC10312263/ /pubmed/37397892 http://dx.doi.org/10.1162/netn_a_00295 Text en © 2023 Massachusetts Institute of Technology https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. For a full description of the license, please visit https://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Sonkusare, Saurabh
Wegner, Katharina
Chang, Catie
Dionisio, Sasha
Breakspear, Michael
Cocchi, Luca
Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
title Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
title_full Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
title_fullStr Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
title_full_unstemmed Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
title_short Dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
title_sort dynamic interactions between anterior insula and anterior cingulate cortex link perceptual features and heart rate variability during movie viewing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312263/
https://www.ncbi.nlm.nih.gov/pubmed/37397892
http://dx.doi.org/10.1162/netn_a_00295
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