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Evidence from pupillometry and fMRI indicates reduced neural response during vicarious social pain but not physical pain in autism.

ABSTRACT: Autism spectrum disorder (ASD) is characterized by substantial social deficits. The notion that dysfunctions in neural circuits involved in sharing another's affect explain these deficits is appealing, but has received only modest experimental support. Here we evaluated a complex paradigm on the vicarious social pain of embarrassment to probe social deficits in ASD as to whether it is more potent than paradigms currently in use. To do so we acquired pupillometry and fMRI in young adults with ASD and matched healthy controls. During a simple vicarious physical pain task no differences emerged between groups in behavior, pupillometry, and neural activation of the anterior insula (AIC) and anterior cingulate cortex (ACC). In contrast, processing complex vicarious social pain yielded reduced responses in ASD on all physiological measures of sharing another's affect. The reduced activity within the AIC was thereby explained by the severity of autistic symptoms in the social and affective domain. Additionally, behavioral responses lacked correspondence with the anterior cingulate and anterior insula cortex activity found in controls. Instead, behavioral responses in ASD were associated with hippocampal activity. The observed dissociation echoes the clinical observations that deficits in ASD are most pronounced in complex social situations and simple tasks may not probe the dysfunctions in neural pathways involved in sharing affect. Our results are highly relevant because individuals with ASD may have preserved abilities to share another's physical pain but still have problems with the vicarious representation of more complex emotions that matter in life.

SUBMITTER: Krach S

PROVIDER: S-EPMC6869621 | biostudies-literature | 2015 Nov

REPOSITORIES: biostudies-literature

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Evidence from pupillometry and fMRI indicates reduced neural response during vicarious social pain but not physical pain in autism.

Krach Sören S Kamp-Becker Inge I Einhäuser Wolfgang W Sommer Jens J Frässle Stefan S Jansen Andreas A Rademacher Lena L Müller-Pinzler Laura L Gazzola Valeria V Paulus Frieder M FM

Human brain mapping 20150914 11

Autism spectrum disorder (ASD) is characterized by substantial social deficits. The notion that dysfunctions in neural circuits involved in sharing another's affect explain these deficits is appealing, but has received only modest experimental support. Here we evaluated a complex paradigm on the vicarious social pain of embarrassment to probe social deficits in ASD as to whether it is more potent than paradigms currently in use. To do so we acquired pupillometry and fMRI in young adults with ASD ...[more]

PMID: 26367817

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Project description:Persistent pain is measured by means of self-report, the sole reliance on which hampers diagnosis and treatment. Functional magnetic resonance imaging (fMRI) holds promise for identifying objective measures of pain, but brain measures that are sensitive and specific to physical pain have not yet been identified.In four studies involving a total of 114 participants, we developed an fMRI-based measure that predicts pain intensity at the level of the individual person. In study 1, we used machine-learning analyses to identify a pattern of fMRI activity across brain regions--a neurologic signature--that was associated with heat-induced pain. The pattern included the thalamus, the posterior and anterior insulae, the secondary somatosensory cortex, the anterior cingulate cortex, the periaqueductal gray matter, and other regions. In study 2, we tested the sensitivity and specificity of the signature to pain versus warmth in a new sample. In study 3, we assessed specificity relative to social pain, which activates many of the same brain regions as physical pain. In study 4, we assessed the responsiveness of the measure to the analgesic agent remifentanil.In study 1, the neurologic signature showed sensitivity and specificity of 94% or more (95% confidence interval [CI], 89 to 98) in discriminating painful heat from nonpainful warmth, pain anticipation, and pain recall. In study 2, the signature discriminated between painful heat and nonpainful warmth with 93% sensitivity and specificity (95% CI, 84 to 100). In study 3, it discriminated between physical pain and social pain with 85% sensitivity (95% CI, 76 to 94) and 73% specificity (95% CI, 61 to 84) and with 95% sensitivity and specificity in a forced-choice test of which of two conditions was more painful. In study 4, the strength of the signature response was substantially reduced when remifentanil was administered.It is possible to use fMRI to assess pain elicited by noxious heat in healthy persons. Future studies are needed to assess whether the signature predicts clinical pain. (Funded by the National Institute on Drug Abuse and others.).

Project description:BackgroundPeople with autism have abnormal preferences, ranging from an apparent lack of preference for social stimuli to unusually strong preferences for restricted sets of highly idiosyncratic stimuli. Yet the profile of preferences across social and nonsocial domains has not been mapped out in detail, and the processes responsible remain poorly understood.MethodsTo assess preferences across a range of stimuli, we measured real monetary donations to 50 charities spanning categories pertaining to people, mental health, animals, or the environment. We compared the donations made by 16 high-functioning adults with autism to those made by neurotypical controls matched on age, gender and education. We additionally collected ratings of how people evaluated the different charities.ResultsCompared with controls, high-functioning adults with autism donated less overall and also showed a significantly disproportionate reduction in donations to people charities compared with donations to the other charities. Furthermore, whereas controls discriminated strongly between different people charities, choosing to donate a lot of money to some and very little to others, much less discrimination was seen in the autism group. Ratings that probed how participants constructed their preferences did not differ between groups, except for a difference in the perceived impact of pictures and text information about people charities. Strikingly, there were some charities related to mental health, and autism in particular, to which the autism group donated considerably more than did the controls.ConclusionsPeople with autism were found to have reduced preference and sensitivity towards charities benefiting other people. The findings provide evidence for a domain-specific impairment in social cognition in autism spectrum disorder, and in particular in linking otherwise intact social knowledge to the construction of value signals on which preferences regarding other people are based.

Dataset Information

Evidence from pupillometry and fMRI indicates reduced neural response during vicarious social pain but not physical pain in autism.

Publications

Evidence from pupillometry and fMRI indicates reduced neural response during vicarious social pain but not physical pain in autism.

Similar Datasets

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