Revealing the neurobiology underlying interpersonal neural synchronization with multimodal data fusion

Leon D Lotter; Simon H Kohl; Christian Gerloff; Laura Bell; Alexandra Niephaus; Jana A Kruppa; Juergen Dukart; Martin Schulte-Rüther; Vanessa Reindl; Kerstin Konrad

doi:10.1016/j.neubiorev.2023.105042

Revealing the neurobiology underlying interpersonal neural synchronization with multimodal data fusion

Neurosci Biobehav Rev. 2023 Mar:146:105042. doi: 10.1016/j.neubiorev.2023.105042. Epub 2023 Jan 11.

Authors

Affiliations

¹ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany; Institute of Neuroscience and Medicine - Brain & Behaviour (INM-7), Jülich Research Centre, Jülich, Germany; Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany; Max Planck School of Cognition, Stephanstrasse 1A, 04103 Leipzig, Germany. Electronic address: l.lotter@fz-juelich.de.
² Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany; JARA Brain Institute II, Molecular Neuroscience and Neuroimaging (INM-11), Jülich Research Centre, Jülich, Germany.
³ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany; JARA Brain Institute II, Molecular Neuroscience and Neuroimaging (INM-11), Jülich Research Centre, Jülich, Germany; Chair II of Mathematics, Faculty of Mathematics, Computer Science and Natural Sciences, RWTH Aachen University, Aachen, Germany.
⁴ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany; Audiovisual Media Center, Medical Faculty, RWTH Aachen University, Aachen, Germany.
⁵ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany.
⁶ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany; JARA Brain Institute II, Molecular Neuroscience and Neuroimaging (INM-11), Jülich Research Centre, Jülich, Germany; Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Center Göttingen, Göttingen, Germany.
⁷ Institute of Neuroscience and Medicine - Brain & Behaviour (INM-7), Jülich Research Centre, Jülich, Germany; Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany.
⁸ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany; JARA Brain Institute II, Molecular Neuroscience and Neuroimaging (INM-11), Jülich Research Centre, Jülich, Germany; Psychology, School of Social Sciences, Nanyang Technological University, S639818, Singapore.

PMID: 36641012
DOI: 10.1016/j.neubiorev.2023.105042

Abstract

Humans synchronize with one another to foster successful interactions. Here, we use a multimodal data fusion approach with the aim of elucidating the neurobiological mechanisms by which interpersonal neural synchronization (INS) occurs. Our meta-analysis of 22 functional magnetic resonance imaging and 69 near-infrared spectroscopy hyperscanning experiments (740 and 3721 subjects) revealed robust brain regional correlates of INS in the right temporoparietal junction and left ventral prefrontal cortex. Integrating this meta-analytic information with public databases, biobehavioral and brain-functional association analyses suggested that INS involves sensory-integrative hubs with functional connections to mentalizing and attention networks. On the molecular and genetic levels, we found INS to be associated with GABAergic neurotransmission and layer IV/V neuronal circuits, protracted developmental gene expression patterns, and disorders of neurodevelopment. Although limited by the indirect nature of phenotypic-molecular association analyses, our findings generate new testable hypotheses on the neurobiological basis of INS.

Keywords: Activation likelihood estimation; Excitation/inhibition; FMRI; FNIRS; GABA; Hyperscanning; Interpersonal neural synchronization; Multimodal data fusion.

Publication types

Meta-Analysis
Review
Research Support, Non-U.S. Gov't

MeSH terms

Brain
Brain Mapping* / methods
Humans
Interpersonal Relations
Neurobiology*
Prefrontal Cortex / physiology