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Influence of emotional complexity on the neural substrates of affective theory of mind.

ABSTRACT: Affective theory of mind (ToM) depends on both the decoding of emotional expressions and the reasoning on emotional mental states from social situations. While previous studies characterized the neural substrates underlying these processes, it remains unclear whether the nature of the emotional state inferred from others can influence the brain activation associated with affective ToM. In the present study, we focused on two types of emotions: basic emotions (BEs) (e.g., anger and surprise), which are innate and universal and self-conscious emotions (e.g., pride and embarrassment), which correspond to a special class of emotions involving the self and including a representation of one's relative reactions to internal and external standards. Specifically, we used an ecological functional MRI paradigm, on 21 healthy young subjects, to compare brain activations during the decoding of and the reasoning on others' self-conscious, basic and neutral mental states. Our results showed that compared to neutral states, the inference of self-conscious and basic emotional states from others elicited more activation in several core regions of affective ToM. Direct comparisons between emotional conditions revealed more activation for self-conscious than BEs in the right temporoparietal junction during the reasoning process and in left middle occipital regions during the decoding process. Further analyses using a localizer task showed that the extrastriate body area was more recruited for decoding others' self-conscious versus BEs, which emphasize the importance of body clues to properly infer these emotions. Using an original task allowing for an ecological assessment of the affective ToM, these results demonstrate that the complexity of the emotion inferred to others can influence the recruitment of ToM network. This study also validates the use of our task as an ecological tool to assess the affective ToM, constituting an avenue for the characterization of ToM impairments in neurological conditions.

SUBMITTER: Caillaud M

PROVIDER: S-EPMC7267895 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Influence of emotional complexity on the neural substrates of affective theory of mind.

Caillaud Marie M Bejanin Alexandre A Laisney Mickael M Gagnepain Pierre P Gaubert Malo M Viard Armelle A Clochon Patrice P de La Sayette Vincent V Allain Philippe P Eustache Francis F Desgranges Béatrice B

Human brain mapping 20190930 1

Affective theory of mind (ToM) depends on both the decoding of emotional expressions and the reasoning on emotional mental states from social situations. While previous studies characterized the neural substrates underlying these processes, it remains unclear whether the nature of the emotional state inferred from others can influence the brain activation associated with affective ToM. In the present study, we focused on two types of emotions: basic emotions (BEs) (e.g., anger and surprise), whi ...[more]

PMID: 31566290

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Project description:Background: Several meta-analyses highlight pronounced problems in general Theory of Mind (ToM), the ability to infer other persons' mental states, in patients with psychosis in comparison to non-clinical controls. In addition, first studies suggest associations between Hyper-ToM, an exaggerated inference of mental states to others, and delusions. Research on different ToM subtypes (Cognitive ToM, Affective ToM, and Hyper-ToM) and symptom clusters of psychosis (positive, negative, and disorganized symptoms) have gathered conflicting findings. Thus, the present study examined group differences between patients with psychosis and non-clinical controls concerning Cognitive ToM/Affective ToM and Hyper-ToM. Further, the association between ToM subtypes and symptom clusters (positive, negative, and disorganized symptoms) were examined. Methods: Patients with psychotic disorders (n = 64, 1/3 with present delusions indicated by a minimum score of four in the PANSS P1 item) and non-clinical controls (n = 21) were examined with assessments of Cognitive ToM and Affective ToM abilities and Hyper-ToM errors using the Frith-Happé animations. Psychopathology was assessed using the Positive and Negative Syndrome Scale. Results: Patients with psychosis presented more pronounced problems in Cognitive and Affective ToM in comparison to non-clinical controls, whereas there were no group differences with regard to Hyper-ToM errors. Furthermore, deficits in Cognitive ToM were associated with general delusions, whereas problems in Affective ToM were associated with negative and disorganized symptoms. In addition, there was no association between Hyper-ToM errors and any symptoms when controlling for years of education. Conclusions: Our findings suggest that deficits in ToM subtypes might not be directly related to delusions and positive symptoms and are in line with more recently developed cognitive models of delusions. In addition, our results support the well-established finding of associations between ToM alterations and negative or disorganized symptoms. Our results shed light on the role of different dimensions of ToM in specific symptoms of psychosis.

Project description:Deficits in theory of mind (ToM) are common after neurological insult acquired in the first and second decade of life, however the contribution of large-scale neural networks to ToM deficits in children with brain injury is unclear. Using paediatric traumatic brain injury (TBI) as a model, this study investigated the sub-acute effect of paediatric traumatic brain injury on grey-matter volume of three large-scale, domain-general brain networks (the Default Mode Network, DMN; the Central Executive Network, CEN; and the Salience Network, SN), as well as two domain-specific neural networks implicated in social-affective processes (the Cerebro-Cerebellar Mentalizing Network, CCMN and the Mirror Neuron/Empathy Network, MNEN). We also evaluated prospective structure-function relationships between these large-scale neural networks and cognitive, affective and conative ToM. 3D T1- weighted magnetic resonance imaging sequences were acquired sub-acutely in 137 children [TBI: n = 103; typically developing (TD) children: n = 34]. All children were assessed on measures of ToM at 24-months post-injury. Children with severe TBI showed sub-acute volumetric reductions in the CCMN, SN, MNEN, CEN and DMN, as well as reduced grey-matter volumes of several hub regions of these neural networks. Volumetric reductions in the CCMN and several of its hub regions, including the cerebellum, predicted poorer cognitive ToM. In contrast, poorer affective and conative ToM were predicted by volumetric reductions in the SN and MNEN, respectively. Overall, results suggest that cognitive, affective and conative ToM may be prospectively predicted by individual differences in structure of different neural systems-the CCMN, SN and MNEN, respectively. The prospective relationship between cerebellar volume and cognitive ToM outcomes is a novel finding in our paediatric brain injury sample and suggests that the cerebellum may play a role in the neural networks important for ToM. These findings are discussed in relation to neurocognitive models of ToM. We conclude that detection of sub-acute volumetric abnormalities of large-scale neural networks and their hub regions may aid in the early identification of children at risk for chronic social-cognitive impairment.

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Influence of emotional complexity on the neural substrates of affective theory of mind.

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Influence of emotional complexity on the neural substrates of affective theory of mind.

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