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      Closing the Gap between the Inside and the Outside: Interoceptive Sensitivity and Social Distances

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          Abstract

          Humans’ ability to represent their body state from within through interoception has been proposed to predict different aspects of human cognition and behaviour. We focused on the possible contribution of interoceptive sensitivity to social behaviour as mediated by adaptive modulation of autonomic response. We, thus, investigated whether interoceptive sensitivity to one's heartbeat predicts participants' autonomic response at different social distances. We measured respiratory sinus arrhythmia (RSA) during either a Social or a Non-social task. In the Social task each participant viewed an experimenter performing a caress-like movement at different distances from their hand. In the Non-social task a metal stick was moved at the same distances from the participant's hand. We found a positive association between interoceptive sensitivity and autonomic response only for the social setting. Moreover, only good heartbeat perceivers showed higher autonomic response 1) in the social compared to the non-social setting, 2) specifically, when the experimenter's hand was moving at boundary of their peripersonal space (20 cm from the participant's hand). Our findings suggest that interoceptive sensitivity might contribute to interindividual differences concerning social attitudes and interpersonal space representation via recruitment of different adaptive autonomic response strategies.

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          The polyvagal theory: phylogenetic substrates of a social nervous system.

          The evolution of the autonomic nervous system provides an organizing principle to interpret the adaptive significance of physiological responses in promoting social behavior. According to the polyvagal theory, the well-documented phylogenetic shift in neural regulation of the autonomic nervous system passes through three global stages, each with an associated behavioral strategy. The first stage is characterized by a primitive unmyelinated visceral vagus that fosters digestion and responds to threat by depressing metabolic activity. Behaviorally, the first stage is associated with immobilization behaviors. The second stage is characterized by the sympathetic nervous system that is capable of increasing metabolic output and inhibiting the visceral vagus to foster mobilization behaviors necessary for 'fight or flight'. The third stage, unique to mammals, is characterized by a myelinated vagus that can rapidly regulate cardiac output to foster engagement and disengagement with the environment. The mammalian vagus is neuroanatomically linked to the cranial nerves that regulate social engagement via facial expression and vocalization. As the autonomic nervous system changed through the process of evolution, so did the interplay between the autonomic nervous system and the other physiological systems that respond to stress, including the cortex, the hypothalamic-pituitary-adrenal axis, the neuropeptides of oxytocin and vasopressin, and the immune system. From this phylogenetic orientation, the polyvagal theory proposes a biological basis for social behavior and an intervention strategy to enhance positive social behavior.
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            The polyvagal theory: new insights into adaptive reactions of the autonomic nervous system.

            The polyvagal theory describes an autonomic nervous system that is influenced by the central nervous system, sensitive to afferent influences, characterized by an adaptive reactivity dependent on the phylogeny of the neural circuits, and interactive with source nuclei in the brainstem regulating the striated muscles of the face and head. The theory is dependent on accumulated knowledge describing the phylogenetic transitions in the vertebrate autonomic nervous system. Its specific focus is on the phylogenetic shift between reptiles and mammals that resulted in specific changes to the vagal pathways regulating the heart. As the source nuclei of the primary vagal efferent pathways regulating the heart shifted from the dorsal motor nucleus of the vagus in reptiles to the nucleus ambiguus in mammals, a face-heart connection evolved with emergent properties of a social engagement system that would enable social interactions to regulate visceral state.
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              Overlapping activity in anterior insula during interoception and emotional experience.

              Classic theories of emotion posit that awareness of one's internal bodily states (interoception) is a key component of emotional experience. This view has been indirectly supported by data demonstrating similar patterns of brain activity - most importantly, in the anterior insula - during both interoception and emotion elicitation. However, no study has directly compared these two phenomena within participants, leaving it unclear whether interoception and emotional experience truly share the same functional neural architecture. The current study addressed this gap in knowledge by examining the neural convergence of these two phenomena within the same population. In one task, participants monitored their own heartbeat; in another task they watched emotional video clips and rated their own emotional responses to the videos. Consistent with prior research, heartbeat monitoring engaged a circumscribed area spanning insular cortex and adjacent inferior frontal operculum. Critically, this interoception-related cluster also was engaged when participants rated their own emotion, and activity here correlated with the trial-by-trial intensity of participants' emotional experience. These findings held across both group-level and individual participant-level approaches to localizing interoceptive cortex. Together, these data further clarify the functional role of the anterior insula and provide novel insights about the connection between bodily awareness and emotion. Copyright © 2012 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                1 October 2013
                : 8
                : 10
                : e75758
                Affiliations
                [1 ]Department of Neuroscience, University of Parma, Parma, Italy
                [2 ]Brain Center for Social and Motor Cognition, Italian Institute of Technology (IIT), Parma, Italy
                Royal Holloway, University of London, United Kingdom
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: FF M. Ardizzi VG. Performed the experiments: M. Ardizzi M. Ambrosecchia. Analyzed the data: M. Ardizzi. Contributed reagents/materials/analysis tools: VG. Wrote the paper: FF M. Ardizzi VG.

                Article
                PONE-D-13-13134
                10.1371/journal.pone.0075758
                3787958
                24098397
                59b896b2-206a-4dea-a95d-91ee1a3f7e59
                Copyright @ 2013

                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
                : 28 March 2013
                : 19 August 2013
                Page count
                Pages: 11
                Funding
                This work was supported by the EU grant TESIS to VG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article

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