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      Sensitive infant care tunes a frontotemporal interbrain network in adolescence

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          Abstract

          Caregiving plays a critical role in children’s cognitive, emotional, and psychological well-being. In the current longitudinal study, we investigated the enduring effects of early maternal behavior on processes of interbrain synchrony in adolescence. Mother-infant naturalistic interactions were filmed when infants were 3–4 months old and interactions were coded for maternal sensitivity and intrusiveness with the Coding Interactive Behavior Manual. In early adolescence (Mean = 12.30, SD = 1.25), mother-adolescent interbrain synchrony was measured using hyperscanning EEG during a naturalistic interaction of positive valence. Guided by previous hyperscanning studies, we focused on interbrain connections within the right frontotemporal interbrain network. Results indicate that maternal sensitivity in early infancy was longitudinally associated with neural synchrony in the right interbrain frontotemporal network. Post-hoc comparisons highlighted enhancement of mother-adolescent frontal-frontal connectivity, a connection that has been implicated in parent-child social communication. In contrast, maternal intrusiveness in infancy was linked with attenuation of interbrain synchrony in the right interbrain frontotemporal network. Sensitivity and intrusiveness are key maternal social orientations that have shown to be individually stable in the mother-child relationship from infancy to adulthood and foreshadow children’s positive and negative social-emotional outcomes, respectively. Our findings are the first to demonstrate that these two maternal orientations play a role in enhancing or attenuating the child’s interbrain frontotemporal network, which sustains social communication and affiliation. Results suggest that the reported long-term impact of maternal sensitivity and intrusiveness may relate, in part, to its effects on tuning the child’s brain to sociality.

          Supplementary Information

          The online version contains supplementary material available at 10.1038/s41598-024-73630-2.

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          Nonparametric statistical testing of EEG- and MEG-data.

          In this paper, we show how ElectroEncephaloGraphic (EEG) and MagnetoEncephaloGraphic (MEG) data can be analyzed statistically using nonparametric techniques. Nonparametric statistical tests offer complete freedom to the user with respect to the test statistic by means of which the experimental conditions are compared. This freedom provides a straightforward way to solve the multiple comparisons problem (MCP) and it allows to incorporate biophysically motivated constraints in the test statistic, which may drastically increase the sensitivity of the statistical test. The paper is written for two audiences: (1) empirical neuroscientists looking for the most appropriate data analysis method, and (2) methodologists interested in the theoretical concepts behind nonparametric statistical tests. For the empirical neuroscientist, a large part of the paper is written in a tutorial-like fashion, enabling neuroscientists to construct their own statistical test, maximizing the sensitivity to the expected effect. And for the methodologist, it is explained why the nonparametric test is formally correct. This means that we formulate a null hypothesis (identical probability distribution in the different experimental conditions) and show that the nonparametric test controls the false alarm rate under this null hypothesis.
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            Meeting of minds: the medial frontal cortex and social cognition.

            Social interaction is a cornerstone of human life, yet the neural mechanisms underlying social cognition are poorly understood. Recently, research that integrates approaches from neuroscience and social psychology has begun to shed light on these processes, and converging evidence from neuroimaging studies suggests a unique role for the medial frontal cortex. We review the emerging literature that relates social cognition to the medial frontal cortex and, on the basis of anatomical and functional characteristics of this brain region, propose a theoretical model of medial frontal cortical function relevant to different aspects of social cognitive processing.
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              Brain-to-brain coupling: a mechanism for creating and sharing a social world.

              Cognition materializes in an interpersonal space. The emergence of complex behaviors requires the coordination of actions among individuals according to a shared set of rules. Despite the central role of other individuals in shaping one's mind, most cognitive studies focus on processes that occur within a single individual. We call for a shift from a single-brain to a multi-brain frame of reference. We argue that in many cases the neural processes in one brain are coupled to the neural processes in another brain via the transmission of a signal through the environment. Brain-to-brain coupling constrains and shapes the actions of each individual in a social network, leading to complex joint behaviors that could not have emerged in isolation. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Feldman.ruth@gmail.com
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                30 September 2024
                30 September 2024
                2024
                : 14
                : 22602
                Affiliations
                [1 ]Center for Developmental Social Neuroscience, Reichman University, ( https://ror.org/01px5cv07) Herzliya, 0460101 Israel
                [2 ]Department of Criminology and Gonda Brain Research Center, Bar-Ilan University, ( https://ror.org/03kgsv495) Ramat-Gan, Israel
                [3 ]Department of Psychology and Gonda Brain Research Center, Bar-Ilan University, ( https://ror.org/03kgsv495) Ramat-Gan, Israel
                [4 ]Child Study Center, Yale University, ( https://ror.org/03v76x132) New Haven, USA
                Article
                73630
                10.1038/s41598-024-73630-2
                11442694
                39349700
                bb5f9c02-e907-466d-97b1-f40f3db0dbe8
                © The Author(s) 2024

                Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

                History
                : 10 July 2024
                : 19 September 2024
                Funding
                Funded by: Bezos Family Foundation
                Award ID: 001
                Categories
                Article
                Custom metadata
                © Springer Nature Limited 2024

                Uncategorized
                social neuroscience,hyperscanning,eeg,synchrony,social development,mother-child relationships,maternal sensitivity,human behaviour,neuroscience,social behaviour

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