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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

Domino game paradigm. The upper panel describes the 4 intervals that comprise each round of the game: Decision Making, Ready, Anticipation to Outcome and Response to Outcome. The latter is the main focus of this study, thus it is highlighted in gray. The duration of each interval and the command (i.e. event) that starts it are described in the bolded arrows below. The lower panel depicts the Domino Game sequence and corresponding consequences. At the beginning of each game the player (participant scanned) receives 12 playing chips and his/her goal is to dispose of them within 4 min. A constant opponent's chip (in this example 6:5, shown enlarged in the yellow ellipsoid) to which the player matches one chip in each round of the game, is displayed in the upper left corner of the screen throughout the game. Each round starts with the player instructed to decide what chip he/she will play next by the command ‘Choose’ (Decision-making interval). Then the player is instructed to move the cursor to this chip (Ready interval). The chip can either match the opponent's (i.e. have one of the numbers match those on the opponent's chip, upper row, 5:1 in this example) or not (lower row:3:3). After placing the selected chip face down next to the opponent's, he/she awaits the opponent's response (Anticipation of Outcome interval). The opponent can either challenge the player's choice (‘Show’) or not (‘No-Show’). Based on the player's choice and the opponent's response there are four possible consequences for each round (Response to Outcome interval): Show Match (overt gain); No-Show Match (relative loss, as the player could have been rewarded if challenged); Show Non-Match (overt loss) and No-Show Non-Match (relative gain, as the player could have been punished if challenged).
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f0005: Domino game paradigm. The upper panel describes the 4 intervals that comprise each round of the game: Decision Making, Ready, Anticipation to Outcome and Response to Outcome. The latter is the main focus of this study, thus it is highlighted in gray. The duration of each interval and the command (i.e. event) that starts it are described in the bolded arrows below. The lower panel depicts the Domino Game sequence and corresponding consequences. At the beginning of each game the player (participant scanned) receives 12 playing chips and his/her goal is to dispose of them within 4 min. A constant opponent's chip (in this example 6:5, shown enlarged in the yellow ellipsoid) to which the player matches one chip in each round of the game, is displayed in the upper left corner of the screen throughout the game. Each round starts with the player instructed to decide what chip he/she will play next by the command ‘Choose’ (Decision-making interval). Then the player is instructed to move the cursor to this chip (Ready interval). The chip can either match the opponent's (i.e. have one of the numbers match those on the opponent's chip, upper row, 5:1 in this example) or not (lower row:3:3). After placing the selected chip face down next to the opponent's, he/she awaits the opponent's response (Anticipation of Outcome interval). The opponent can either challenge the player's choice (‘Show’) or not (‘No-Show’). Based on the player's choice and the opponent's response there are four possible consequences for each round (Response to Outcome interval): Show Match (overt gain); No-Show Match (relative loss, as the player could have been rewarded if challenged); Show Non-Match (overt loss) and No-Show Non-Match (relative gain, as the player could have been punished if challenged).

Mentions: During each round of the game, the player first mentally decides which chip to play next, following the command ‘Choose’; then moves the cursor to it following the command ‘Ready’; next places it face down adjacent to the opponent's chip, following the command ‘Go’; and finally awaits the opponent's response (either 3.4, 5.4 or 7.4 s later) of either ‘Show’ or ‘No-Show’ (see Fig. 1). The ‘Show’ command exposes the player's selected chip, while ‘No-Show’ leaves it unexposed. Following a 5.4 ± 2 second pause after the opponent's response (Response to Outcome interval; see below), the next round begins with the presentation of the ‘Choose’ command.


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)

Domino game paradigm. The upper panel describes the 4 intervals that comprise each round of the game: Decision Making, Ready, Anticipation to Outcome and Response to Outcome. The latter is the main focus of this study, thus it is highlighted in gray. The duration of each interval and the command (i.e. event) that starts it are described in the bolded arrows below. The lower panel depicts the Domino Game sequence and corresponding consequences. At the beginning of each game the player (participant scanned) receives 12 playing chips and his/her goal is to dispose of them within 4 min. A constant opponent's chip (in this example 6:5, shown enlarged in the yellow ellipsoid) to which the player matches one chip in each round of the game, is displayed in the upper left corner of the screen throughout the game. Each round starts with the player instructed to decide what chip he/she will play next by the command ‘Choose’ (Decision-making interval). Then the player is instructed to move the cursor to this chip (Ready interval). The chip can either match the opponent's (i.e. have one of the numbers match those on the opponent's chip, upper row, 5:1 in this example) or not (lower row:3:3). After placing the selected chip face down next to the opponent's, he/she awaits the opponent's response (Anticipation of Outcome interval). The opponent can either challenge the player's choice (‘Show’) or not (‘No-Show’). Based on the player's choice and the opponent's response there are four possible consequences for each round (Response to Outcome interval): Show Match (overt gain); No-Show Match (relative loss, as the player could have been rewarded if challenged); Show Non-Match (overt loss) and No-Show Non-Match (relative gain, as the player could have been punished if challenged).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f0005: Domino game paradigm. The upper panel describes the 4 intervals that comprise each round of the game: Decision Making, Ready, Anticipation to Outcome and Response to Outcome. The latter is the main focus of this study, thus it is highlighted in gray. The duration of each interval and the command (i.e. event) that starts it are described in the bolded arrows below. The lower panel depicts the Domino Game sequence and corresponding consequences. At the beginning of each game the player (participant scanned) receives 12 playing chips and his/her goal is to dispose of them within 4 min. A constant opponent's chip (in this example 6:5, shown enlarged in the yellow ellipsoid) to which the player matches one chip in each round of the game, is displayed in the upper left corner of the screen throughout the game. Each round starts with the player instructed to decide what chip he/she will play next by the command ‘Choose’ (Decision-making interval). Then the player is instructed to move the cursor to this chip (Ready interval). The chip can either match the opponent's (i.e. have one of the numbers match those on the opponent's chip, upper row, 5:1 in this example) or not (lower row:3:3). After placing the selected chip face down next to the opponent's, he/she awaits the opponent's response (Anticipation of Outcome interval). The opponent can either challenge the player's choice (‘Show’) or not (‘No-Show’). Based on the player's choice and the opponent's response there are four possible consequences for each round (Response to Outcome interval): Show Match (overt gain); No-Show Match (relative loss, as the player could have been rewarded if challenged); Show Non-Match (overt loss) and No-Show Non-Match (relative gain, as the player could have been punished if challenged).
Mentions: During each round of the game, the player first mentally decides which chip to play next, following the command ‘Choose’; then moves the cursor to it following the command ‘Ready’; next places it face down adjacent to the opponent's chip, following the command ‘Go’; and finally awaits the opponent's response (either 3.4, 5.4 or 7.4 s later) of either ‘Show’ or ‘No-Show’ (see Fig. 1). The ‘Show’ command exposes the player's selected chip, while ‘No-Show’ leaves it unexposed. Following a 5.4 ± 2 second pause after the opponent's response (Response to Outcome interval; see below), the next round begins with the presentation of the ‘Choose’ command.

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