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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

Mentalizing network. Panel A depicts the activation map of a mixed-effects ANOVA showing brain regions with a significant effect of Opponent's Response in the Human-Opponent runs (Show > No-Show) and Opponent Type in all participants (n = 27, qFDR < 0.05). These regions included the temporoparietal junction (TPJ), temporal pole (TP), medial prefrontal cortex (MPFC), posterior cingulate cortex (PCC), ventrolateral prefrontal cortex (VLPFC), fusiform gyrus (FG) and putamen. Panel B shows the map of brain areas exhibiting an interaction between Human Show vs. No-Show events and Group, masked with the mentalizing network as presented in panel A. Bilateral MTGexhibited a significant effect such that controls showed a greater response to Show vs. No-Show compared to individuals with ASDs (left MTG Pcluster = 0.03 FWE, right MTG Pcluster = 0.04 FWE; for presentation purposes, clusters are shown at a threshold of P < 0.05 uncorrected, k = 20). Percent signal change of the different events in these regions are shown in Panels C & D. **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.
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f0015: Mentalizing network. Panel A depicts the activation map of a mixed-effects ANOVA showing brain regions with a significant effect of Opponent's Response in the Human-Opponent runs (Show > No-Show) and Opponent Type in all participants (n = 27, qFDR < 0.05). These regions included the temporoparietal junction (TPJ), temporal pole (TP), medial prefrontal cortex (MPFC), posterior cingulate cortex (PCC), ventrolateral prefrontal cortex (VLPFC), fusiform gyrus (FG) and putamen. Panel B shows the map of brain areas exhibiting an interaction between Human Show vs. No-Show events and Group, masked with the mentalizing network as presented in panel A. Bilateral MTGexhibited a significant effect such that controls showed a greater response to Show vs. No-Show compared to individuals with ASDs (left MTG Pcluster = 0.03 FWE, right MTG Pcluster = 0.04 FWE; for presentation purposes, clusters are shown at a threshold of P < 0.05 uncorrected, k = 20). Percent signal change of the different events in these regions are shown in Panels C & D. **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.

Mentions: As described above and previously (Assaf et al., 2009), to examine the brain areas involved in mentalizing processes regardless of outcome (i.e. motivation) we used the Group by Opponent Type by Opponent Response mixed-effects ANOVA and determined which regions were activated more during Human Show than No-Show events and also more during all human-opponent than computer-opponent events (i.e. main effect of Opponent Type), across all subjects (qFDR < 0.05, k = 50), while controlling for age and IQ. The resulting network is depicted in Fig. 3A and Table 3 and is composed of bilateral temporal poles (TP), temporoparietal junctions (TPJ), including superior temporal sulcus, middle and inferior temporal gyri (STS, MTG and ITG), medial prefrontal cortex (MPFC), posterior cingulate cortex (PCC) and putamen, plus right ventrolateral prefrontal cortex (VLPFC) and fusiform gyrus (FG).


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)

Mentalizing network. Panel A depicts the activation map of a mixed-effects ANOVA showing brain regions with a significant effect of Opponent's Response in the Human-Opponent runs (Show > No-Show) and Opponent Type in all participants (n = 27, qFDR < 0.05). These regions included the temporoparietal junction (TPJ), temporal pole (TP), medial prefrontal cortex (MPFC), posterior cingulate cortex (PCC), ventrolateral prefrontal cortex (VLPFC), fusiform gyrus (FG) and putamen. Panel B shows the map of brain areas exhibiting an interaction between Human Show vs. No-Show events and Group, masked with the mentalizing network as presented in panel A. Bilateral MTGexhibited a significant effect such that controls showed a greater response to Show vs. No-Show compared to individuals with ASDs (left MTG Pcluster = 0.03 FWE, right MTG Pcluster = 0.04 FWE; for presentation purposes, clusters are shown at a threshold of P < 0.05 uncorrected, k = 20). Percent signal change of the different events in these regions are shown in Panels C & D. **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f0015: Mentalizing network. Panel A depicts the activation map of a mixed-effects ANOVA showing brain regions with a significant effect of Opponent's Response in the Human-Opponent runs (Show > No-Show) and Opponent Type in all participants (n = 27, qFDR < 0.05). These regions included the temporoparietal junction (TPJ), temporal pole (TP), medial prefrontal cortex (MPFC), posterior cingulate cortex (PCC), ventrolateral prefrontal cortex (VLPFC), fusiform gyrus (FG) and putamen. Panel B shows the map of brain areas exhibiting an interaction between Human Show vs. No-Show events and Group, masked with the mentalizing network as presented in panel A. Bilateral MTGexhibited a significant effect such that controls showed a greater response to Show vs. No-Show compared to individuals with ASDs (left MTG Pcluster = 0.03 FWE, right MTG Pcluster = 0.04 FWE; for presentation purposes, clusters are shown at a threshold of P < 0.05 uncorrected, k = 20). Percent signal change of the different events in these regions are shown in Panels C & D. **p < 0.001; *p < 0.05; ^p = 0.06; L = left; R = right hemisphere.
Mentions: As described above and previously (Assaf et al., 2009), to examine the brain areas involved in mentalizing processes regardless of outcome (i.e. motivation) we used the Group by Opponent Type by Opponent Response mixed-effects ANOVA and determined which regions were activated more during Human Show than No-Show events and also more during all human-opponent than computer-opponent events (i.e. main effect of Opponent Type), across all subjects (qFDR < 0.05, k = 50), while controlling for age and IQ. The resulting network is depicted in Fig. 3A and Table 3 and is composed of bilateral temporal poles (TP), temporoparietal junctions (TPJ), including superior temporal sulcus, middle and inferior temporal gyri (STS, MTG and ITG), medial prefrontal cortex (MPFC), posterior cingulate cortex (PCC) and putamen, plus right ventrolateral prefrontal cortex (VLPFC) and fusiform gyrus (FG).

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