A failure to grasp the affective meaning of actions in autism spectrum disorder subjects

Laboratoire de Neurosciences Cognitives, INSERM U960 & DEC, Ecole Normale Supérieure, Paris, France.
Neuropsychologia (Impact Factor: 3.3). 08/2009; 47(8-9):1816-25. DOI: 10.1016/j.neuropsychologia.2009.02.021
Source: PubMed


The ability to grasp emotional messages in everyday gestures and respond to them is at the core of successful social communication. The hypothesis that abnormalities in socio-emotional behavior in people with autism are linked to a failure to grasp emotional significance conveyed by gestures was explored. We measured brain activity using fMRI during perception of fearful or neutral actions and showed that whereas similar activation of brain regions known to play a role in action perception was revealed in both autistics and controls, autistics failed to activate amygdala, inferior frontal gyrus and premotor cortex when viewing gestures expressing fear. Our results support the notion that dysfunctions in this network may contribute significantly to the characteristic communicative impairments documented in autism.

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Available from: Julie Grèzes
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    • "In an fMRI study we conducted, atypical processing of emotional expressions in adults with ASD was found to be subtended by a weaker functional connectivity between the AMG and PM (Grèzes et al., 2009). Similarly, Gotts et al. (2012) showed, using a whole-brain functional connectivity approach in fMRI, a decoupling between brain regions in the evaluation of socially relevant signals from motor-related circuits in ASDs. "
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    ABSTRACT: Emotional signals influence others' behavior. They trigger a host of responses in the observer. Perception of emotional signals incorporates not only the appraisal of the emotional content of the signal but also the preparation of an adaptive reaction to it. This interplay between two processes is reflected in the limbic–motor interactions in the human brain. Data showing impaired connectivity between the limbic and motor brain regions in pathologies associated with diminished social skills also support this claim.
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    • "Particularly critical brain regions for meaningful sentence comprehension include, broadly, middle and inferior temporal cortex; pars orbitalis; bilateral superior temporal sulci; Heschl's gyrus, in dorsal temporal lobe and containing primary auditory cortex; and inferior parietal lobule, which contains the angular gyrus (Dichter, 2012; Price, 2010). Studies of language processing in ASD have shown atypical activations during language processing, including impaired functional connectivity (Catarino et al., 2011; Kleinhans et al., 2008; Verly et al., 2014), abnormal lateralization (Boddaert et al., 2003; Eigsti et al., 2012; Grezes et al., 2009; Groen et al., 2010; Hesling et al., 2010), and some recruitment of brain regions not typically involved in language (e.g., Catarino et al., 2011; Knaus et al., 2010; Mizuno et al., 2011; Redcay and Courchesne, 2008). Thus, fMRI studies of language in ASD show both atypical regions of activation during language processing, as well as atypical activation of typical language-implicated brain regions. "
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    ABSTRACT: Although Autism Spectrum Disorder (ASD) is generally a lifelong disability, a minority of individuals with ASD overcome their symptoms to such a degree that they are generally indistinguishable from their typically-developing peers. That is, they have achieved an optimal outcome (OO). The question addressed by the current study is whether this normalized behavior reflects normalized brain functioning, or alternatively, the action of compensatory systems. Either possibility is plausible, as most participants with OO received years of intensive therapy that could alter brain networks to align with typical function or work around ASD-related neural dysfunction. Individuals ages 8 to 21years with high-functioning ASD (n=23), OO (n=16), or typical development (TD; n=20) completed a functional MRI scan while performing a sentence comprehension task. Results indicated similar activations in frontal and temporal regions (left middle frontal, left supramarginal, and right superior temporal gyri) and posterior cingulate in OO and ASD groups, where both differed from the TD group. Furthermore, the OO group showed heightened “compensatory” activation in numerous left- and right-lateralized regions (left precentral/postcentral gyri, right precentral gyrus, left inferior parietal lobule, right supramarginal gyrus, left superior temporal/parahippocampal gyrus, left middle occipital gyrus) and cerebellum, relative to both ASD and TD groups. Behaviorally normalized language abilities in OO individuals appear to utilize atypical brain networks, with increased recruitment of language-specific as well as right homologue and other systems. Early intensive learning and experience may normalize behavioral language performance in OO, but some brain regions involved in language processing may continue to display characteristics that are more similar to ASD than typical development, while others show characteristics not like ASD or typical development.
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    • "In contrast, DCM assesses the effective connectivity among the brain regions and yields biophysically interpretable models that can be linked to the individual symptoms of each patient [Stephan and Mathys, 2014]. Researchers have therefore revealed alterations of the effective connectivity in patients diagnosed with autism[Grèzes et al., 2009;Radulescu et al., 2013], raising hope that computational approaches will be of benefit to psychiatry in the future. In this regard, our results demonstrate that the paradigm presented here may offer an innovative and reliable approach in computational psychiatry (in particular when refining the present approach to adopt more realistic, dynamic tasks, and a more extended network), enabling the investigation of intra-and interhemispheric integration in the face perception network and thus providing deeper insight into the pathophysiology of autism and other psychiatric disorders. "
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    ABSTRACT: Computational approaches have great potential for moving neuroscience toward mechanistic models of the functional integration among brain regions. Dynamic causal modeling (DCM) offers a promising framework for inferring the effective connectivity among brain regions and thus unraveling the neural mechanisms of both normal cognitive function and psychiatric disorders. While the benefit of such approaches depends heavily on their reliability, systematic analyses of the within-subject stability are rare. Here, we present a thorough investigation of the test-retest reliability of an fMRI paradigm for DCM analysis dedicated to unraveling intra- and interhemispheric integration among the core regions of the face perception network. First, we examined the reliability of face-specific BOLD activity in 25 healthy volunteers, who performed a face perception paradigm in two separate sessions. We found good to excellent reliability of BOLD activity within the DCM-relevant regions. Second, we assessed the stability of effective connectivity among these regions by analyzing the reliability of Bayesian model selection and model parameter estimation in DCM. Reliability was excellent for the negative free energy and good for model parameter estimation, when restricting the analysis to parameters with substantial effect sizes. Third, even when the experiment was shortened, reliability of BOLD activity and DCM results dropped only slightly as a function of the length of the experiment. This suggests that the face perception paradigm presented here provides reliable estimates for both conventional activation and effective connectivity measures. We conclude this paper with an outlook on potential clinical applications of the paradigm for studying psychiatric disorders. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc.
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