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      The Neural Bases of Social Intention Understanding: The Role of Interaction Goals

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          Abstract

          Decoding others' intentions is a crucial aspect of social cognition. Neuroimaging studies suggest that inferring immediate goals engages the neural system for action understanding (i.e. mirror system), while the decoding of long-term intentions requires the system subserving the attribution of mental states (i.e. mentalizing). A controversial issue, stimulated by recent inconsistent results, concerns whether the two systems are concurrently vs. exclusively involved in intention understanding. This issue is particularly relevant in the case of social interactions, whose processing has been mostly, but not uncontroversially, associated with the mentalizing system. We tested the alternative hypothesis that the relative contribution of the two systems in intention understanding may also depend on the shared goal of interacting agents. To this purpose, 27 participants observed social interactions differing in their cooperative vs. affective shared goal during functional-Magnetic-Resonance-Imaging. The processing of both types of interactions activated the right temporo-parietal junction involved in mentalizing on action goals. Additionally, whole-brain and regions-of-interest analyses showed that the action understanding system (inferior prefrontal-parietal cortex) was more strongly activated by cooperative interactions, while the mentalizing-proper system (medial prefrontal cortex) was more strongly engaged by affective interactions. These differences were modulated by individual differences in empathizing. Both systems can thus be involved in understanding social intentions, with a relative weighting depending on the specific shared goal of the interaction.

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          Most cited references34

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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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            Empathic neural responses are modulated by the perceived fairness of others.

            The neural processes underlying empathy are a subject of intense interest within the social neurosciences. However, very little is known about how brain empathic responses are modulated by the affective link between individuals. We show here that empathic responses are modulated by learned preferences, a result consistent with economic models of social preferences. We engaged male and female volunteers in an economic game, in which two confederates played fairly or unfairly, and then measured brain activity with functional magnetic resonance imaging while these same volunteers observed the confederates receiving pain. Both sexes exhibited empathy-related activation in pain-related brain areas (fronto-insular and anterior cingulate cortices) towards fair players. However, these empathy-related responses were significantly reduced in males when observing an unfair person receiving pain. This effect was accompanied by increased activation in reward-related areas, correlated with an expressed desire for revenge. We conclude that in men (at least) empathic responses are shaped by valuation of other people's social behaviour, such that they empathize with fair opponents while favouring the physical punishment of unfair opponents, a finding that echoes recent evidence for altruistic punishment.
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              People thinking about thinking people. The role of the temporo-parietal junction in "theory of mind".

              Humans powerfully and flexibly interpret the behaviour of other people based on an understanding of their minds: that is, we use a "theory of mind." In this study we distinguish theory of mind, which represents another person's mental states, from a representation of the simple presence of another person per se. The studies reported here establish for the first time that a region in the human temporo-parietal junction (here called the TPJ-M) is involved specifically in reasoning about the contents of another person's mind. First, the TPJ-M was doubly dissociated from the nearby extrastriate body area (EBA; Downing et al., 2001). Second, the TPJ-M does not respond to false representations in non-social control stories. Third, the BOLD response in the TPJ-M bilaterally was higher when subjects read stories about a character's mental states, compared with stories that described people in physical detail, which did not differ from stories about nonhuman objects. Thus, the role of the TPJ-M in understanding other people appears to be specific to reasoning about the content of mental states.
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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
                2012
                27 July 2012
                : 7
                : 7
                : e42347
                Affiliations
                [1 ]Center for Cognitive Neuroscience, Vita-Salute San Raffaele University, Milan, Italy
                [2 ]CERMAC, Vita-Salute San Raffaele University, Milan, Italy
                [3 ]Division of Neuroscience, San Raffaele Scientific Institute, Milan, Italy
                [4 ]Department of Psychology, University of Milano-Bicocca, Milan, Italy
                [5 ]Institute of Molecular Bioimaging and Physiology, Consiglio Nazionale delle Ricerche, Milan-Segrate, Italy
                [6 ]Nuclear Medicine Unit, San Raffaele Scientific Institute, Milan, Italy
                Katholieke Universiteit Leuven, Belgium
                Author notes

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

                Conceived and designed the experiments: NC AZ AMP DP SFC. Performed the experiments: NC FA FR NM. Analyzed the data: NC FA. Contributed reagents/materials/analysis tools: AMP AZ DP SFC. Wrote the paper: NC SFC. Contributed to study design and data discussion: NC FA AZ AMP DP SFC.

                Article
                PONE-D-11-08927
                10.1371/journal.pone.0042347
                3407127
                22848759
                4938c7c4-27fd-4165-8ca4-bc7c28c869bb
                Copyright @ 2012

                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
                : 23 February 2012
                : 4 July 2012
                Page count
                Pages: 11
                Funding
                This project was partially supported by a Cariplo Foundation “Formazione universitaria d′eccellenza” grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Neurological System
                Neural Pathways
                Biochemistry
                Neurochemistry
                Neuromodulation
                Neuroscience
                Cognitive Neuroscience
                Cognition
                Neuroimaging
                Fmri
                Neuropsychology
                Social and Behavioral Sciences
                Psychology
                Behavior
                Emotions
                Social Psychology

                Uncategorized
                Uncategorized

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