Cortico-Cerebellar neurodynamics during social interaction in Autism Spectrum Disorders.

Autism Cerebellum Digital Psychiatry Human-machine interaction (HMI) Neurodevelopment Social Cognition Theta Oscillations

Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2023
Historique:
received: 02 12 2022
revised: 24 06 2023
accepted: 27 06 2023
medline: 18 9 2023
pubmed: 17 7 2023
entrez: 16 7 2023
Statut: ppublish

Résumé

Exploring neural network dynamics during social interaction could help to identify biomarkers of Autism Spectrum Disorders (ASD). A cerebellar involvement in autism has long been suspected and recent methodological advances now enable studying cerebellar functioning in a naturalistic setting. Here, we investigated the electrophysiological activity of the cerebro-cerebellar network during real-time social interaction in ASD. We focused our analysis on theta oscillations (3-8 Hz), which have been associated with large-scale coordination of distant brain areas and might contribute to interoception, motor control, and social event anticipation, all skills known to be altered in ASD. We combined the Human Dynamic Clamp, a paradigm for studying realistic social interactions using a virtual avatar, with high-density electroencephalography (HD-EEG). Using source reconstruction, we investigated power in the cortex and the cerebellum, along with coherence between the cerebellum and three cerebral-cortical areas, and compared our findings in a sample of participants with ASD (n = 107) and with typical development (TD) (n = 33). We developed an open-source pipeline to analyse neural dynamics at the source level from HD-EEG data. Individuals with ASD showed a significant increase in theta band power over the cerebellum and the frontal and temporal cortices during social interaction compared to resting state, along with significant coherence increases between the cerebellum and the sensorimotor, frontal and parietal cortices. However, a phase-based connectivity measure did not support a strict activity increase in the cortico-cerebellar functional network. We did not find any significant differences between the ASD and the TD group. This exploratory study uncovered increases in the theta band activity of participants with ASD during social interaction, pointing at the presence of neural interactions between the cerebellum and cerebral networks associated with social cognition. It also emphasizes the need for complementary functional connectivity measures to capture network-level alterations. Future work will focus on optimizing artifact correction to include more participants with TD and increase the statistical power of group-level contrasts.

Sections du résumé

BACKGROUND
Exploring neural network dynamics during social interaction could help to identify biomarkers of Autism Spectrum Disorders (ASD). A cerebellar involvement in autism has long been suspected and recent methodological advances now enable studying cerebellar functioning in a naturalistic setting. Here, we investigated the electrophysiological activity of the cerebro-cerebellar network during real-time social interaction in ASD. We focused our analysis on theta oscillations (3-8 Hz), which have been associated with large-scale coordination of distant brain areas and might contribute to interoception, motor control, and social event anticipation, all skills known to be altered in ASD.
METHODS
We combined the Human Dynamic Clamp, a paradigm for studying realistic social interactions using a virtual avatar, with high-density electroencephalography (HD-EEG). Using source reconstruction, we investigated power in the cortex and the cerebellum, along with coherence between the cerebellum and three cerebral-cortical areas, and compared our findings in a sample of participants with ASD (n = 107) and with typical development (TD) (n = 33). We developed an open-source pipeline to analyse neural dynamics at the source level from HD-EEG data.
RESULTS
Individuals with ASD showed a significant increase in theta band power over the cerebellum and the frontal and temporal cortices during social interaction compared to resting state, along with significant coherence increases between the cerebellum and the sensorimotor, frontal and parietal cortices. However, a phase-based connectivity measure did not support a strict activity increase in the cortico-cerebellar functional network. We did not find any significant differences between the ASD and the TD group.
CONCLUSIONS
This exploratory study uncovered increases in the theta band activity of participants with ASD during social interaction, pointing at the presence of neural interactions between the cerebellum and cerebral networks associated with social cognition. It also emphasizes the need for complementary functional connectivity measures to capture network-level alterations. Future work will focus on optimizing artifact correction to include more participants with TD and increase the statistical power of group-level contrasts.

Identifiants

pubmed: 37454469
pii: S2213-1582(23)00154-7
doi: 10.1016/j.nicl.2023.103465
pmc: PMC10368923
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

103465

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: D.E. is a full-time employee of F. Hoffmann-La Roche Ltd. All other authors report no biomedical financial interests or potential conflicts of interest.

Auteurs

Fleur Gaudfernau (F)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR 3571 CNRS, University Paris Diderot, Paris, France; Inria, HeKA, PariSantéCampus, Paris, France; Inserm, Centre de Recherche des Cordeliers, Sorbonne Université, Université de Paris Cité, Paris, France.

Aline Lefebvre (A)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR 3571 CNRS, University Paris Diderot, Paris, France; Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Denis-Alexander Engemann (DA)

Roche Pharma Research and Early Development, Neuroscience and Rare Diseases, Roche Innovation Center Basel, F. Hoffmann-La Roche Ltd., Basel, Switzerland; Université Paris-Saclay, Inria, CEA, Palaiseau, France.

Amandine Pedoux (A)

Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Anna Bánki (A)

Research Unit Developmental Psychology, Department of Developmental and Educational Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria.

Florence Baillin (F)

Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Benjamin Landman (B)

Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Anna Maruani (A)

Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Frederique Amsellem (F)

Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Thomas Bourgeron (T)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR 3571 CNRS, University Paris Diderot, Paris, France.

Richard Delorme (R)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR 3571 CNRS, University Paris Diderot, Paris, France; Department of Child and Adolescent Psychiatry, Robert Debré Hospital, APHP, Paris University, Paris, France.

Guillaume Dumas (G)

Human Genetics and Cognitive Functions, Institut Pasteur, UMR 3571 CNRS, University Paris Diderot, Paris, France; Department of Psychiatry, Faculty of Medicine, Université de Montréal, Montréal, QC, Canada; Precision Psychiatry and Social Physiology laboratory, CHU Sainte-Justine Research Centre, Université de Montréal, Montréal, QC, Canada. Electronic address: guillaume.dumas@centraliens.net.

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