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      Parental neural responsivity to infants’ visual attention: How mature brains influence immature brains during social interaction

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          Abstract

          Almost all attention and learning—in particular, most early learning—take place in social settings. But little is known of how our brains support dynamic social interactions. We recorded dual electroencephalography (EEG) from 12-month-old infants and parents during solo play and joint play. During solo play, fluctuations in infants’ theta power significantly forward-predicted their subsequent attentional behaviours. However, this forward-predictiveness was lower during joint play than solo play, suggesting that infants’ endogenous neural control over attention is greater during solo play. Overall, however, infants were more attentive to the objects during joint play. To understand why, we examined how adult brain activity related to infant attention. We found that parents’ theta power closely tracked and responded to changes in their infants’ attention. Further, instances in which parents showed greater neural responsivity were associated with longer sustained attention by infants. Our results offer new insights into how one partner influences another during social interaction.

          Author summary

          We are a social species. Most infants and young children spend the majority of their early waking hours in the company of others. However, almost everything that we know about how the brain subserves early attention and learning comes from studies that examined brain function in one individual at a time just because it is easier to do experiments that way. Here, we examine the neural correlates of how attention is shared between two people engaged in social interaction. We recorded brain activity from infants and parents using scalp electroencephalogram during parallel solo play with toys and during joint play. We examined the associations between attention and brain activity in each member of the dyad independently (infant attention–infant brain, parent attention–parent brain), and we also examined cross-dyad associations (infant attention–parent brain). Our findings suggested that infants’ attention is more endogenously controlled during solo play than joint play. They also suggested that parents are neurally responsive to their infants during social play, and that, when the parent is more neurally responsive, the infant is more attentive.

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          Most cited references48

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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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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              Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention

              P. Fries (2001)
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Project administrationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Project administration
                Role: InvestigationRole: Methodology
                Role: InvestigationRole: MethodologyRole: Project administration
                Role: InvestigationRole: MethodologyRole: Project administration
                Role: Formal analysisRole: Investigation
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                13 December 2018
                December 2018
                13 December 2018
                : 16
                : 12
                : e2006328
                Affiliations
                [1 ] University of East London, London, United Kingdom
                [2 ] Cambridge University, Cambridge, United Kingdom
                [3 ] Nanyang Technological University, Singapore
                Stanford University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-7421-3493
                Article
                pbio.2006328
                10.1371/journal.pbio.2006328
                6292577
                30543622
                793d4d9f-a7b0-4215-ae74-fb4d32e295f9
                © 2018 Wass et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 11 April 2018
                : 9 November 2018
                Page count
                Figures: 6, Tables: 0, Pages: 18
                Funding
                Economic and Social Research Council (grant number ES/N017560/1). to VL and SW. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Economic and Social Research Council (grant number ES/N006461/1). to SW. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Nanyang Technological University (grant number Grant M4081585.SS0). to VL. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Custom metadata
                Data are publicly accessible at the UK Data Reshare service by following this link: http://reshare.ukdataservice.ac.uk/853123/. Data underlying the main and supplementary figures can be found in S1 and S2 Data.

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