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      Empathic brain responses in insula are modulated by levels of alexithymia but not autism

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          Abstract

          Difficulties in social cognition are well recognized in individuals with autism spectrum conditions (henceforth ‘autism’). Here we focus on one crucial aspect of social cognition: the ability to empathize with the feelings of another. In contrast to theory of mind, a capacity that has often been observed to be impaired in individuals with autism, much less is known about the capacity of individuals with autism for affect sharing. Based on previous data suggesting that empathy deficits in autism are a function of interoceptive deficits related to alexithymia, we aimed to investigate empathic brain responses in autistic and control participants with high and low degrees of alexithymia. Using functional magnetic resonance imaging, we measured empathic brain responses with an ‘empathy for pain’ paradigm assessing empathic brain responses in a real-life social setting that does not rely on attention to, or recognition of, facial affect cues. Confirming previous findings, empathic brain responses to the suffering of others were associated with increased activation in left anterior insula and the strength of this signal was predictive of the degree of alexithymia in both autistic and control groups but did not vary as a function of group. Importantly, there was no difference in the degree of empathy between autistic and control groups after accounting for alexithymia. These findings suggest that empathy deficits observed in autism may be due to the large comorbidity between alexithymic traits and autism, rather than representing a necessary feature of the social impairments in autism.

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          Most cited references72

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          Diagnostic and statistical manual of mental disorders.

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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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              Interoception: the sense of the physiological condition of the body.

              Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.
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                Author and article information

                Journal
                Brain
                brainj
                brain
                Brain
                Oxford University Press
                0006-8950
                1460-2156
                May 2010
                5 April 2010
                5 April 2010
                : 133
                : 5
                : 1515-1525
                Affiliations
                1 Department of Psychological Sciences, Birkbeck College, London WC1E 7HX, United Kingdom
                2 Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, United Kingdom
                3 Laboratory for Social and Neural Systems Research, Institute for Empirical Research in Economics, University of Zurich, Zurich CH-8006, Switzerland
                Author notes
                Correspondence to: Giorgia Silani, Laboratory for Social and Neural Systems Research, Institute for Empirical Research in Economics, University of Zurich, Blümlisalpstrasse 10, CH-8006 Zurich, Switzerland E-mail: silani@ 123456iew.uzh.ch

                *These authors contributed equally to this work.

                Article
                awq060
                10.1093/brain/awq060
                2859151
                20371509
                ae9715ca-4a5a-4da5-8c6d-94a13274f355
                © The Author(s) 2010. Published by Oxford University Press on behalf of Brain.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 November 2009
                : 2 February 2010
                : 21 February 2010
                Categories
                Original Articles

                Neurosciences
                autism,empathy,theory of mind,mentalizing,interoception,anterior insula,alexithymia
                Neurosciences
                autism, empathy, theory of mind, mentalizing, interoception, anterior insula, alexithymia

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