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      Personal Space Regulation by the Human Amygdala

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          Abstract

          The amygdala plays key roles in emotion and social cognition, but how this translates to face-to-face interactions involving real people remains unknown. Here we found that a patient with complete amygdala lesions lacks any sense of personal space. Furthermore, healthy individuals showed amygdala activation to close personal proximity. The amygdala may be required to trigger the strong emotional reactions normally following personal space violations, thus regulating interpersonal distance in humans.

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          Most cited references11

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          The human amygdala in social judgment.

          Studies in animals have implicated the amygdala in emotional and social behaviours, especially those related to fear and aggression. Although lesion and functional imaging studies in humans have demonstrated the amygdala's participation in recognizing emotional facial expressions, its role in human social behaviour has remained unclear. We report here our investigation into the hypothesis that the human amygdala is required for accurate social judgments of other individuals on the basis of their facial appearance. We asked three subjects with complete bilateral amygdala damage to judge faces of unfamiliar people with respect to two attributes important in real-life social encounters: approachability and trustworthiness. All three subjects judged unfamiliar individuals to be more approachable and more trustworthy than did control subjects. The impairment was most striking for faces to which normal subjects assign the most negative ratings: unapproachable and untrustworthy looking individuals. Additional investigations revealed that the impairment does not extend to judging verbal descriptions of people. The amygdala appears to be an important component of the neural systems that help retrieve socially relevant knowledge on the basis of facial appearance.
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            Collective memory and spatial sorting in animal groups.

            We present a self-organizing model of group formation in three-dimensional space, and use it to investigate the spatial dynamics of animal groups such as fish schools and bird flocks. We reveal the existence of major group-level behavioural transitions related to minor changes in individual-level interactions. Further, we present the first evidence for collective memory in such animal groups (where the previous history of group structure influences the collective behaviour exhibited as individual interactions change) during the transition of a group from one type of collective behaviour to another. The model is then used to show how differences among individuals influence group structure, and how individuals employing simple, local rules of thumb, can accurately change their spatial position within a group (e.g. to move to the centre, the front, or the periphery) in the absence of information on their current position within the group as a whole. These results are considered in the context of the evolution and ecological importance of animal groups.
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              The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta).

              The role of the amygdala in dyadic social interactions of adult rhesus monkeys (Macaca mulatta) was assessed after bilateral ibotenic acid lesions. Social, nonsocial, and spatial behaviors of amygdalectomized and control monkeys were assessed in 3 dyadic experiments: constrained, unconstrained, and round robin. Lesions produced extensive bilateral damage to the amygdala. Across all experiments, the amygdalectomized monkeys demonstrated increased social affiliation, decreased anxiety, and increased confidence compared with control monkeys, particularly during early encounters. Normal subjects also demonstrated increased social affiliation toward the amygdalectomized subjects. These results indicate that amygdala lesions in adult monkeys lead to a decrease in the species-normal reluctance to immediately engage a novel conspecific in social behavior. The altered behavior of the amygdalectomized monkeys may have induced the increased social interactions from their normal companions. This is contrary to the idea that amygdalectomy produces a decrease in social interaction and increased aggression from conspecifics.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                15 July 2009
                30 August 2009
                October 2009
                1 April 2010
                : 12
                : 10
                : 1226-1227
                Affiliations
                [1 ] Division of Humanities and Social Sciences California Institute of Technology
                [2 ]Division of Biology California Institute of Technology
                Author notes

                Author Contributions D.P.K. and R.A. designed the experiment and wrote the paper; D.P.K. executed the studies; D.P.K., J.G., and J.M.T. analyzed the data.

                Article
                nihpa131528
                10.1038/nn.2381
                2753689
                19718035
                65a599fb-b29d-4dc0-bb2c-eb172afc4a75

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                History
                Funding
                Funded by: National Institute of Mental Health : NIMH
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: R01 MH080721-01A1 ||MH
                Funded by: National Institute of Mental Health : NIMH
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: P01 NS019632-230003 ||NS
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                Neurosciences
                Neurosciences

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