Hyperscanning of Interpersonal Trust in Autism

P. Read Montague, Ph.D.

Baylor College of Medicine

Funded in December, 2005: $10000 for 3 years
LAY SUMMARY . ABSTRACT . HYPOTHESIS . SELECTED PUBLICATIONS .

LAY SUMMARY

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Imaging Interpersonal Trust in Autism

Baylor researchers will use a new imaging technology they have developed to  image simultaneously the brains of highly functioning individuals with autism engaged in social interactions.  This is the first study of its kind and may provide insight into why people with autism are unable to form trust relationships associated with normal social bonds.  Autism Speaks will contribute $90,000 for this project.

People with autism lack the capacity to understand and respond to social signals, making it difficult for them to engage and communicate effectively.  The researchers hypothesize that people with autism are not able to engage in effective social interactions because they lack the ability to interpret social signals and predict the expected actions of others.  Their hypothesis is based on initial findings from a new imaging technology they developed, called “hyperscan fMRI” (h-fMRI). This technique allows simultaneous functional imaging of brain activity in interacting individuals.

The Baylor group first tested h-fMRI in healthy volunteers who participated in a two-person “trust” game.  Using h-fMRI, the Baylor researchers visualized brain activity as participants developed trust and as they built models of one another through repeated interactions.  Results showed that a response pattern develops in a specific area of the brain when individuals decide to invest trust. A response also develops in a separate area of the brain when participants view their partners’ decisions to trust them.

In contrast, in a pilot study of seven males with a highly functional form of autism, researchers found that their brains associated their actions and their game partners' actions as though both were the actions of someone else.  Now, the Baylor researchers will study people with autism paired with healthy partners and pairs in which both partners are healthy.  The Baylor group will determine whether people with autism lack the ability to develop trust in another, whether this “trust” response is present but weak, or whether this response is affected by something that was not captured in the pilot data.  The researchers also will determine whether people with autism lack the ability to model their partner’s responses.  They hypothesize that people with autism lack this modeling capacity and that this absence is the immediate cause of their incapacity to engage in effective social interactions. 

Significance: This approach holds the potential for fundamentally advancing the study of autism by identifying impairment in a brain function required for social interaction.

ABSTRACT

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Hyperscanning of Interpersonal Trust in Autism

Our laboratory has recently developed a technology, called hyperscan-fMRI, that permits the simultaneous functional magnetic resonance imaging (fMRI) of interacting human subjects while they carry out simple forms of interactive social exchanges. Using this technology, we have generated a large database of normal human brain responses related to social signaling. The first new brain response appears in the caudate nucleus and correlates with the formation of each subject's model of their partner's likely next move. The second appears as a series of mapped responses across the anterior-posterior axis of the cingulated cortex. These responses are best described as a social agency map, a systematic spatial variation in fMRI signals that indicate the social agent ("self" or "other") responsible for the data currently being presented to both brains.

Inspired by these results with healthy participants, we have now carried out pilot h-fMRI trust games with high-functioning males with autism (n=7) and found that their cingulated cortex expresses only "other" responses with the "self" responses completely absent. This remarkable deficit in brain response in this special group may represent an important phenotype with which other features of autism spectrum disorders may correlate. This is the first time that brain responses of individuals with autism have been measured during an active social exchange. Using hyperscan-fMRI, this project seeks to substantiate (or not) the pilot findings and evaluate the hypothesis that the absent "self" response in autistic subject may be on proximate cause of their insensitivity to social signals from other humans.

HYPOTHESIS

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Hypothesis:
Two hypotheses will be tested using the iterated trust game and hyperscan-fMRI in individuals with autism:
1. Individuals with autism will exhibit anomalous cingulate responses that reflect difficulty in inferring social agency;
2. Anomalies in social learning, as assessed by temporal shifts in cross-brain caudate response, are a proximate cause of the incapacity to engage in effective social interactions in autism.

Goals:
The aim of this project is to characterize, for the first time, the neural substrates of abnormal social interactions seen in individuals with autistic spectrum disorders (ASDs).  Despite the distinct clinical picture of autism as a disorder with vast social sequelae, technical limitations of standard functional imaging have, until now, precluded the ability to image the brains of multiple interacting individuals engaged in a dynamic social exchange.  The advent of a novel imaging technique, hyperscan functional magnetic imaging (h-fMRI), allows exactly this—the simultaneous measurement of brain activity of two socially interacting people—and may be applied to characterize the neural dynamics contributing to the anomalous social behavior seen in autism.  We thus use a well-documented social exchange task and h-fMRI in individuals with autism to a) explore behavioral and neural correlates of social learning in individuals with autism, and b) investigate whether individuals with autism exhibit anomalous cingulate activation in regions associated with inferring social agency.

Methods:
Our laboratory has recently developed a technology, called hyperscan-fMRI, that permits the simultaneous functional magnetic resonance imaging of interacting human subjects while they carry out simple yet dynamic social exchanges.  The development of h-fMRI allows us to synchronize functional image acquisition across multiple scanners and, thus, permits us to measure interacting brains in the act of interacting.  We previously used hyperscanning to implement a multi-round trust game wherein two individuals interact to repeatedly express and repay trust between one another (King-Casas et al., 2005).  Using hyperscanning and cross-brain correlation analyses in this iterated trust game, we identified robust neural responses in 96 healthy individuals that distinguish one's own social action from that of a social partner and correlate with both the development of a reputation of one player in the brain of the partner and the intention to trust in the near future.  Using hyperscanning and building upon the initial fMRI database of trust interactions that we have developed in a healthy population, we extend our work to investigate the neural substrates of the anomalous social behavior seen in autism.

SELECTED PUBLICATIONS

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King-Casas B., Tomlin D., Anen C., Camerer C.F., Quartz S.R., and Montague P.R.   Getting to know you: Reputation and trust in a two-person economic exchange. Science. 2005 Apr 1;308(5718):78-83Commentary 

Montague P.R., Berns G.S., Cohen J.D., McClure S.M., Pagnoni G., Dhamala M., Wiest M.C., Karpov I., King R.D., Apple N., and Fisher R.E.   Hyperscanning: simultaneous fMRI during linked social interactions. Neuroimage. 2002 Aug;16(4):1159-64PDF