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Mentalizing and motivation neural function during social interactions in autism spectrum disorders.

Assaf M, Hyatt CJ, Wong CG, Johnson MR, Schultz RT, Hendler T, Pearlson GD - Neuroimage Clin (2013)

Bottom Line: Two theories have been suggested to explain these deficits: mind-blindness theory posits impaired mentalizing processes (i.e. decreased ability for establishing a representation of others' state of mind), while social motivation theory proposes that diminished reward value for social information leads to reduced social attention, social interactions, and social learning.These results demonstrate that while MTG and NAcc, which are critical structures in the mentalizing and motivation networks, respectively, activate normally in a non-social context, they fail to respond in an otherwise identical social context in ASD compared to controls.We discuss implications to both the mind-blindness and social motivation theories of ASD and the importance of social context in research and treatment protocols.

View Article: PubMed Central - PubMed

Affiliation: Olin Neuropsychiatry Research Center, Institute of Living, Hartford, CT, USA ; Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA.

ABSTRACT
Autism Spectrum Disorders (ASDs) are characterized by core deficits in social functions. Two theories have been suggested to explain these deficits: mind-blindness theory posits impaired mentalizing processes (i.e. decreased ability for establishing a representation of others' state of mind), while social motivation theory proposes that diminished reward value for social information leads to reduced social attention, social interactions, and social learning. Mentalizing and motivation are integral to typical social interactions, and neuroimaging evidence points to independent brain networks that support these processes in healthy individuals. However, the simultaneous function of these networks has not been explored in individuals with ASDs. We used a social, interactive fMRI task, the Domino game, to explore mentalizing- and motivation-related brain activation during a well-defined interval where participants respond to rewards or punishments (i.e. motivation) and concurrently process information about their opponent's potential next actions (i.e. mentalizing). Thirteen individuals with high-functioning ASDs, ages 12-24, and 14 healthy controls played fMRI Domino games against a computer-opponent and separately, what they were led to believe was a human-opponent. Results showed that while individuals with ASDs understood the game rules and played similarly to controls, they showed diminished neural activity during the human-opponent runs only (i.e. in a social context) in bilateral middle temporal gyrus (MTG) during mentalizing and right Nucleus Accumbens (NAcc) during reward-related motivation (Pcluster < 0.05 FWE). Importantly, deficits were not observed in these areas when playing against a computer-opponent or in areas related to motor and visual processes. These results demonstrate that while MTG and NAcc, which are critical structures in the mentalizing and motivation networks, respectively, activate normally in a non-social context, they fail to respond in an otherwise identical social context in ASD compared to controls. We discuss implications to both the mind-blindness and social motivation theories of ASD and the importance of social context in research and treatment protocols.

No MeSH data available.


Related in: MedlinePlus

Reward-related Motivation network. Panel (A) shows the activation map of a mixed-effects ANOVA showing brain regions with a significant main effect of Outcome during both human- and computer-opponent runs in all participants (n = 27, qFDR < 0.05). This network includes bilateral NAcc, MFG and SPL. Panel (B) depicts brain regions showing a significant interaction between Outcome and Group masked with regions showing a significant main effect of Outcome as shown in panel A. The right NAcc was the only region showing a significant interaction (Pcluster = 0.05 FWE; for presentation purposes cluster is shown at a threshold of P < 0.05 uncorrected, k = 20), such that TD individuals showed significantly more activations for Gains than Losses for both opponents in this region, while individuals with ASDs showed such an effect during the Computer-Opponent games only (panel C). **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.
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f0020: Reward-related Motivation network. Panel (A) shows the activation map of a mixed-effects ANOVA showing brain regions with a significant main effect of Outcome during both human- and computer-opponent runs in all participants (n = 27, qFDR < 0.05). This network includes bilateral NAcc, MFG and SPL. Panel (B) depicts brain regions showing a significant interaction between Outcome and Group masked with regions showing a significant main effect of Outcome as shown in panel A. The right NAcc was the only region showing a significant interaction (Pcluster = 0.05 FWE; for presentation purposes cluster is shown at a threshold of P < 0.05 uncorrected, k = 20), such that TD individuals showed significantly more activations for Gains than Losses for both opponents in this region, while individuals with ASDs showed such an effect during the Computer-Opponent games only (panel C). **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.

Mentions: To assess activation related to motivation we used the Group by Opponent Type by Outcome mixed-effects ANOVA and examined the main effect of Outcome (gains vs. losses) across Opponent Type and Group (qFDR < 0.05, k = 50), while controlling for age and IQ. This network included bilateral NAcc, middle frontal gyri (MFG) and superior parietal lobules (SPL), as depicted in Fig. 4A.


Mentalizing and motivation neural function during social interactions in autism spectrum disorders.

Assaf M, Hyatt CJ, Wong CG, Johnson MR, Schultz RT, Hendler T, Pearlson GD - Neuroimage Clin (2013)

Reward-related Motivation network. Panel (A) shows the activation map of a mixed-effects ANOVA showing brain regions with a significant main effect of Outcome during both human- and computer-opponent runs in all participants (n = 27, qFDR < 0.05). This network includes bilateral NAcc, MFG and SPL. Panel (B) depicts brain regions showing a significant interaction between Outcome and Group masked with regions showing a significant main effect of Outcome as shown in panel A. The right NAcc was the only region showing a significant interaction (Pcluster = 0.05 FWE; for presentation purposes cluster is shown at a threshold of P < 0.05 uncorrected, k = 20), such that TD individuals showed significantly more activations for Gains than Losses for both opponents in this region, while individuals with ASDs showed such an effect during the Computer-Opponent games only (panel C). **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3815022&req=5

f0020: Reward-related Motivation network. Panel (A) shows the activation map of a mixed-effects ANOVA showing brain regions with a significant main effect of Outcome during both human- and computer-opponent runs in all participants (n = 27, qFDR < 0.05). This network includes bilateral NAcc, MFG and SPL. Panel (B) depicts brain regions showing a significant interaction between Outcome and Group masked with regions showing a significant main effect of Outcome as shown in panel A. The right NAcc was the only region showing a significant interaction (Pcluster = 0.05 FWE; for presentation purposes cluster is shown at a threshold of P < 0.05 uncorrected, k = 20), such that TD individuals showed significantly more activations for Gains than Losses for both opponents in this region, while individuals with ASDs showed such an effect during the Computer-Opponent games only (panel C). **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.
Mentions: To assess activation related to motivation we used the Group by Opponent Type by Outcome mixed-effects ANOVA and examined the main effect of Outcome (gains vs. losses) across Opponent Type and Group (qFDR < 0.05, k = 50), while controlling for age and IQ. This network included bilateral NAcc, middle frontal gyri (MFG) and superior parietal lobules (SPL), as depicted in Fig. 4A.

Bottom Line: Two theories have been suggested to explain these deficits: mind-blindness theory posits impaired mentalizing processes (i.e. decreased ability for establishing a representation of others' state of mind), while social motivation theory proposes that diminished reward value for social information leads to reduced social attention, social interactions, and social learning.These results demonstrate that while MTG and NAcc, which are critical structures in the mentalizing and motivation networks, respectively, activate normally in a non-social context, they fail to respond in an otherwise identical social context in ASD compared to controls.We discuss implications to both the mind-blindness and social motivation theories of ASD and the importance of social context in research and treatment protocols.

View Article: PubMed Central - PubMed

Affiliation: Olin Neuropsychiatry Research Center, Institute of Living, Hartford, CT, USA ; Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA.

ABSTRACT
Autism Spectrum Disorders (ASDs) are characterized by core deficits in social functions. Two theories have been suggested to explain these deficits: mind-blindness theory posits impaired mentalizing processes (i.e. decreased ability for establishing a representation of others' state of mind), while social motivation theory proposes that diminished reward value for social information leads to reduced social attention, social interactions, and social learning. Mentalizing and motivation are integral to typical social interactions, and neuroimaging evidence points to independent brain networks that support these processes in healthy individuals. However, the simultaneous function of these networks has not been explored in individuals with ASDs. We used a social, interactive fMRI task, the Domino game, to explore mentalizing- and motivation-related brain activation during a well-defined interval where participants respond to rewards or punishments (i.e. motivation) and concurrently process information about their opponent's potential next actions (i.e. mentalizing). Thirteen individuals with high-functioning ASDs, ages 12-24, and 14 healthy controls played fMRI Domino games against a computer-opponent and separately, what they were led to believe was a human-opponent. Results showed that while individuals with ASDs understood the game rules and played similarly to controls, they showed diminished neural activity during the human-opponent runs only (i.e. in a social context) in bilateral middle temporal gyrus (MTG) during mentalizing and right Nucleus Accumbens (NAcc) during reward-related motivation (Pcluster < 0.05 FWE). Importantly, deficits were not observed in these areas when playing against a computer-opponent or in areas related to motor and visual processes. These results demonstrate that while MTG and NAcc, which are critical structures in the mentalizing and motivation networks, respectively, activate normally in a non-social context, they fail to respond in an otherwise identical social context in ASD compared to controls. We discuss implications to both the mind-blindness and social motivation theories of ASD and the importance of social context in research and treatment protocols.

No MeSH data available.


Related in: MedlinePlus