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      The integration of social and neural synchrony: a case for ecologically valid research using MEG neuroimaging

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          Abstract

          The recent decade has seen a shift from artificial and environmentally deprived experiments in neuroscience to real-life studies on multiple brains in interaction, coordination and synchrony. In these new interpersonal synchrony experiments, there has been a growing trend to employ naturalistic social interactions to evaluate mechanisms underlying synchronous neuronal communication. Here, we emphasize the importance of integrating the assessment of neural synchrony with measurement of nonverbal behavioral synchrony as expressed in various social contexts: relaxed social interactions, planning a joint pleasurable activity, conflict discussion, invocation of trauma, or support giving and assess the integration of neural and behavioral synchrony across developmental stages and psychopathological conditions. We also showcase the advantages of magnetoencephalography neuroimaging as a promising tool for studying interactive neural synchrony and consider the challenge of ecological validity at the expense of experimental rigor. We review recent evidence of rhythmic information flow between brains in interaction and conclude with addressing state-of-the-art developments that may contribute to advance research on brain-to-brain coordination to the next level.

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          Most cited references121

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          Empathy for pain involves the affective but not sensory components of pain.

          Our ability to have an experience of another's pain is characteristic of empathy. Using functional imaging, we assessed brain activity while volunteers experienced a painful stimulus and compared it to that elicited when they observed a signal indicating that their loved one--present in the same room--was receiving a similar pain stimulus. Bilateral anterior insula (AI), rostral anterior cingulate cortex (ACC), brainstem, and cerebellum were activated when subjects received pain and also by a signal that a loved one experienced pain. AI and ACC activation correlated with individual empathy scores. Activity in the posterior insula/secondary somatosensory cortex, the sensorimotor cortex (SI/MI), and the caudal ACC was specific to receiving pain. Thus, a neural response in AI and rostral ACC, activated in common for "self" and "other" conditions, suggests that the neural substrate for empathic experience does not involve the entire "pain matrix." We conclude that only that part of the pain network associated with its affective qualities, but not its sensory qualities, mediates empathy.
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            A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.

            At any one moment, many neuronal groups in our brain are active. Microelectrode recordings have characterized the activation of single neurons and fMRI has unveiled brain-wide activation patterns. Now it is time to understand how the many active neuronal groups interact with each other and how their communication is flexibly modulated to bring about our cognitive dynamics. I hypothesize that neuronal communication is mechanistically subserved by neuronal coherence. Activated neuronal groups oscillate and thereby undergo rhythmic excitability fluctuations that produce temporal windows for communication. Only coherently oscillating neuronal groups can interact effectively, because their communication windows for input and for output are open at the same times. Thus, a flexible pattern of coherence defines a flexible communication structure, which subserves our cognitive flexibility.
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              Measuring phase synchrony in brain signals

              This article presents, for the first time, a practical method for the direct quantification of frequency‐specific synchronization (i.e., transient phase‐locking) between two neuroelectric signals. The motivation for its development is to be able to examine the role of neural synchronies as a putative mechanism for long‐range neural integration during cognitive tasks. The method, called phase‐locking statistics (PLS), measures the significance of the phase covariance between two signals with a reasonable time‐resolution (<100 ms). Unlike the more traditional method of spectral coherence, PLS separates the phase and amplitude components and can be directly interpreted in the framework of neural integration. To validate synchrony values against background fluctuations, PLS uses surrogate data and thus makes no a priori assumptions on the nature of the experimental data. We also apply PLS to investigate intracortical recordings from an epileptic patient performing a visual discrimination task. We find large‐scale synchronies in the gamma band (45 Hz), e.g., between hippocampus and frontal gyrus, and local synchronies, within a limbic region, a few cm apart. We argue that whereas long‐scale effects do reflect cognitive processing, short‐scale synchronies are likely to be due to volume conduction. We discuss ways to separate such conduction effects from true signal synchrony. Hum Brain Mapping 8:194–208, 1999. © 1999 Wiley‐Liss, Inc.
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                Author and article information

                Contributors
                Journal
                Soc Cogn Affect Neurosci
                Soc Cogn Affect Neurosci
                scan
                Social Cognitive and Affective Neuroscience
                Oxford University Press (UK )
                1749-5016
                1749-5024
                Jan-Feb 2021
                07 May 2020
                07 May 2020
                : 16
                : 1-2 , Interpersonal Synchrony Special Issue
                : 143-152
                Affiliations
                Department of Neuroscience and Biomedical Engineering , Aalto University, 02150 Espoo, Finland
                Interdisciplinary Center , Baruch Ivcher School of Psychology, Herzliya 46150, Israel
                Department of Radiology , Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA, USA
                Department of Radiology , Harvard Medical School, Boston, MA, USA
                Department of Neuroscience and Biomedical Engineering , Aalto University, 02150 Espoo, Finland
                Faculty of Sport and Health Sciences , University of Jyväskylä, Jyväskylä, Finland
                Interdisciplinary Center , Baruch Ivcher School of Psychology, Herzliya 46150, Israel
                Yale University , Child Study Center, New Haven, CT 06520, USA
                Author notes
                Correspondence should be addressed to Ruth Feldman and Jonathan Levy, Baruch Ivcher School of Psychology, Interdisciplinary Center, Herzlia 461010, Israel. E-mail: feldman.ruth@ 123456gmail.com and yoniilevy@ 123456gmail.com
                Article
                nsaa061
                10.1093/scan/nsaa061
                7812634
                32382751
                23fc9926-8f73-46fe-9b14-877828a04a29
                © The Author(s) 2020. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 02 January 2020
                : 06 April 2020
                : 27 April 2020
                Page count
                Pages: 10
                Funding
                Funded by: National Alliance for Research on Schizophrenia and Depression, DOI 10.13039/100009670;
                Categories
                Original Manuscript
                AcademicSubjects/SCI01880

                Neurosciences
                neural synchrony,social interaction,meg,ecological validity,social neuroscience
                Neurosciences
                neural synchrony, social interaction, meg, ecological validity, social neuroscience

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