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      The amygdala and the relevance detection theory of autism: an evolutionary perspective

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          Abstract

          In the last few decades there has been increasing interest in the role of the amygdala in psychiatric disorders and, in particular, in its contribution to the socio-emotional impairments in autism spectrum disorders (ASDs). Given that the amygdala is a component structure of the “social brain,” several theoretical explanations compatible with amygdala dysfunction have been proposed to account for socio-emotional impairments in ASDs, including abnormal eye contact, gaze monitoring, face processing, mental state understanding, and empathy. Nevertheless, many theoretical accounts, based on the Amygdala Theory of Autism, fail to elucidate the complex pattern of impairments observed in this population, which extends beyond the social domain. As posited by the Relevance Detector theory ( Sander et al., 2003), the human amygdala is a critical component of a brain circuit involved in the appraisal of self-relevant events that include, but are not restricted to, social stimuli. Here, we propose that the behavioral and social–emotional features of ASDs may be better understood in terms of a disruption in a “Relevance Detector Network” affecting the processing of stimuli that are relevant for the organism’s self-regulating functions. In the present review, we will first summarize the main literature supporting the involvement of the amygdala in socio-emotional disturbances in ASDs. Next, we will present a revised version of the Amygdala Relevance Detector hypothesis and we will show that this theoretical framework can provide a better understanding of the heterogeneity of the impairments and symptomatology of ASDs. Finally, we will discuss some predictions of our model, and suggest new directions in the investigation of the role of the amygdala within the more generally disrupted cortical connectivity framework as a model of neural organization of the autistic brain.

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          The neural bases of emotion regulation: reappraisal and suppression of negative emotion.

          Emotion regulation strategies are thought to differ in when and how they influence the emotion-generative process. However, no study to date has directly probed the neural bases of two contrasting (e.g., cognitive versus behavioral) emotion regulation strategies. This study used functional magnetic resonance imaging (fMRI) to examine cognitive reappraisal (a cognitive strategy thought to have its impact early in the emotion-generative process) and expressive suppression (a behavioral strategy thought to have its impact later in the emotion-generative process). Seventeen women viewed 15 sec neutral and negative emotion-eliciting films under four conditions--watch-neutral, watch-negative, reappraise-negative, and suppress-negative--while providing emotion experience ratings and having their facial expressions videotaped. Reappraisal resulted in early (0-4.5 sec) prefrontal cortex (PFC) responses, decreased negative emotion experience, and decreased amygdala and insular responses. Suppression produced late (10.5-15 sec) PFC responses, decreased negative emotion behavior and experience, but increased amygdala and insular responses. These findings demonstrate the differential efficacy of reappraisal and suppression on emotional experience, facial behavior, and neural response and highlight intriguing differences in the temporal dynamics of these two emotion regulation strategies.
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            Autism spectrum disorders: developmental disconnection syndromes.

            Autism is a common and heterogeneous childhood neurodevelopmental disorder. Analogous to broad syndromes such as mental retardation, autism has many etiologies and should be considered not as a single disorder but, rather, as 'the autisms'. However, recent genetic findings, coupled with emerging anatomical and functional imaging studies, suggest a potential unifying model in which higher-order association areas of the brain that normally connect to the frontal lobe are partially disconnected during development. This concept of developmental disconnection can accommodate the specific neurobehavioral features that are observed in autism, their emergence during development, and the heterogeneity of autism etiology, behaviors and cognition.
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              Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity.

              The brain activation of a group of high-functioning autistic participants was measured using functional MRI during sentence comprehension and the results compared with those of a Verbal IQ-matched control group. The groups differed in the distribution of activation in two of the key language areas. The autism group produced reliably more activation than the control group in Wernicke's (left laterosuperior temporal) area and reliably less activation than the control group in Broca's (left inferior frontal gyrus) area. Furthermore, the functional connectivity, i.e. the degree of synchronization or correlation of the time series of the activation, between the various participating cortical areas was consistently lower for the autistic than the control participants. These findings suggest that the neural basis of disordered language in autism entails a lower degree of information integration and synchronization across the large-scale cortical network for language processing. The article presents a theoretical account of the findings, related to neurobiological foundations of underconnectivity in autism.
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                Author and article information

                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                30 December 2013
                2013
                : 7
                : 894
                Affiliations
                [1] 1Institut Jean Nicod, Centre National de la Recherche Scientifique, Ecole Normale Supérieure Paris, France
                [2] 2Laboratoire Mémoire et Cognition, Institut de Psychologie, Université Paris Descartes Boulogne-Billancourt, France
                [3] 3Inserm U894, Centre de Psychiatrie et Neurosciences, Université Paris Descartes Paris, France
                Author notes

                Edited by: Corrado Corradi-Dell’Acqua, University of Geneva, Switzerland

                Reviewed by: Sebastian B. Gaigg, City University London, UK; Bhismadev Chakrabarti, University of Reading, UK; Danilo Bzdok, Research Center Jülich, Germany

                *Correspondence: Tiziana Zalla, Institut Jean Nicod, Centre National de la Recherche Scientifique, Ecole Normale Supérieure, 29 rue d’Ulm, 75005 Paris, France e-mail: tiziana.zalla@ 123456ens.fr

                This article was submitted to the journal Frontiers in Human Neuroscience.

                Article
                10.3389/fnhum.2013.00894
                3874476
                23355817
                3f936f32-8182-4c17-a64e-93492e973da9
                Copyright © 2013 Zalla and Sperduti.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 May 2013
                : 08 December 2013
                Page count
                Figures: 0, Tables: 1, Equations: 0, References: 212, Pages: 15, Words: 0
                Categories
                Neuroscience
                Review Article

                Neurosciences
                amygdala,self-relevance,social brain,autism spectrum disorders,ventromedial prefrontal cortex

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