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      The role of touch in regulating inter-partner physiological coupling during empathy for pain

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          Abstract

          The human ability to synchronize with other individuals is critical for the development of social behavior. Recent research has shown that physiological inter-personal synchronization may underlie behavioral synchrony. Nevertheless, the factors that modulate physiological coupling are still largely unknown. Here we suggest that social touch and empathy for pain may enhance interpersonal physiological coupling. Twenty-two romantic couples were assigned the roles of target (pain receiver) and observer (pain observer) under pain/no-pain and touch/no-touch conditions, and their ECG and respiration rates were recorded. The results indicate that the partner touch increased interpersonal respiration coupling under both pain and no-pain conditions and increased heart rate coupling under pain conditions. In addition, physiological coupling was diminished by pain in the absence of the partner’s touch. Critically, we found that high partner’s empathy and high levels of analgesia enhanced coupling during the partner’s touch. Collectively, the evidence indicates that social touch increases interpersonal physiological coupling during pain. Furthermore, the effects of touch on cardio-respiratory inter-partner coupling may contribute to the analgesic effects of touch via the autonomic nervous system.

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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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            Contributions of anterior cingulate cortex to behaviour

            Assessments of anterior cingulate cortex in experimental animals and humans have led to unifying theories of its structural organization and contributions to mammalian behaviour. The anterior cingulate cortex forms a large region around the rostrum of the corpus callosum that is termed the anterior executive region. This region has numerous projections into motor systems, however, since these projections originate from different parts of anterior cingulate cortex and because functional studies have shown that it does not have a uniform contribution to brain functions, the anterior executive region is further subdivided into 'affect' and 'cognition' components. The affect division includes areas 25, 33 and rostral area 24, and has extensive connections with the amygdala and periaqueductal grey, and parts of it project to autonomic brainstem motor nuclei. In addition to regulating autonomic and endocrine functions, it is involved in conditioned emotional learning, vocalizations associated with expressing internal states, assessments of motivational content and assigning emotional valence to internal and external stimuli, and maternal-infant interactions. The cognition division includes caudal areas 24' and 32', the cingulate motor areas in the cingulate sulcus and nociceptive cortex. The cingulate motor areas project to the spinal cord and red nucleus and have premotor functions, while the nociceptive area is engaged in both response selection and cognitively demanding information processing. The cingulate epilepsy syndrome provides important support of experimental animal and human functional imaging studies for the role of anterior cingulate cortex in movement, affect and social behaviours. Excessive cingulate activity in cases with seizures confirmed in anterior cingulate cortex with subdural electrode recordings, can impair consciousness, alter affective state and expression, and influence skeletomotor and autonomic activity. Interictally, patients with anterior cingulate cortex epilepsy often display psychopathic or sociopathic behaviours. In other clinical examples of elevated anterior cingulate cortex activity it may contribute to tics, obsessive-compulsive behaviours, and aberrent social behaviour. Conversely, reduced cingulate activity following infarcts or surgery can contribute to behavioural disorders including akinetic mutism, diminished self-awareness and depression, motor neglect and impaired motor initiation, reduced responses to pain, and aberrent social behaviour. The role of anterior cingulate cortex in pain responsiveness is suggested by cingulumotomy results and functional imaging studies during noxious somatic stimulation. The affect division of anterior cingulate cortex modulates autonomic activity and internal emotional responses, while the cognition division is engaged in response selection associated with skeletomotor activity and responses to noxious stimuli. Overall, anterior cingulate cortex appears to play a crucial role in initiation, motivation, and goal-directed behaviours.(ABSTRACT TRUNCATED AT 400 WORDS)
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              Lending a hand: social regulation of the neural response to threat.

              Social contact promotes enhanced health and well-being, likely as a function of the social regulation of emotional responding in the face of various life stressors. For this functional magnetic resonance imaging (fMRI) study, 16 married women were subjected to the threat of electric shock while holding their husband's hand, the hand of an anonymous male experimenter, or no hand at all. Results indicated a pervasive attenuation of activation in the neural systems supporting emotional and behavioral threat responses when the women held their husband's hand. A more limited attenuation of activation in these systems occurred when they held the hand of a stranger. Most strikingly, the effects of spousal hand-holding on neural threat responses varied as a function of marital quality, with higher marital quality predicting less threat-related neural activation in the right anterior insula, superior frontal gyrus, and hypothalamus during spousal, but not stranger, hand-holding.
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                Author and article information

                Contributors
                goldsteinpav@gmail.com
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                12 June 2017
                12 June 2017
                2017
                : 7
                : 3252
                Affiliations
                [1 ]ISNI 0000 0004 1937 0562, GRID grid.18098.38, Department of Psychology, , University of Haifa, ; Haifa, Israel
                [2 ]ISNI 0000 0004 1937 0562, GRID grid.18098.38, Department of Statistics, , University of Haifa, ; Haifa, Israel
                [3 ]ISNI 0000 0004 1937 0562, GRID grid.18098.38, The Emili Sagol Creative Arts Therapies Research Center, , University of Haifa, ; Haifa, Israel
                [4 ]ISNI 0000 0004 1937 0562, GRID grid.18098.38, Physical Therapy Department, , Faculty of Social Welfare and Health Sciences, University of Haifa, ; Haifa, Israel
                Article
                3627
                10.1038/s41598-017-03627-7
                5468314
                28607375
                9540511b-a3fb-41da-946b-ab5c6104de63
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 January 2017
                : 2 May 2017
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