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Abstract

Autism spectrum disorder (ASD) is characterized by a core difference in theory-of-mind (ToM) ability, which extends to alterations in moral judgment and decision-making. Although the function of the right temporoparietal junction (rTPJ), a key neural marker of ToM and morality, is known to be atypical in autistic individuals, the neurocomputational mechanisms underlying its specific changes in moral decision-making remain unclear. Here, we addressed this question by using a novel fMRI task together with computational modeling and representational similarity analysis (RSA). ASD participants and healthy control subjects (HCs) decided in public or private whether to incur a personal cost for funding a morally good cause (Good Context) or receive a personal gain for benefiting a morally bad cause (Bad Context). Compared with HC, individuals with ASD were much more likely to reject the opportunity to earn ill gotten money by supporting a bad cause than were HCs. Computational modeling revealed that this resulted from heavily weighing benefits for themselves and the bad cause, suggesting that ASD participants apply a rule of refusing to serve a bad cause because they evaluate the negative consequences of their actions more severely. Moreover, RSA revealed a reduced rTPJ representation of the information specific to moral contexts in ASD participants. Together, these findings indicate the contribution of rTPJ in representing information concerning moral rules and provide new insights for the neurobiological basis underpinning moral behaviors illustrated by a specific difference of rTPJ in ASD participants.SIGNIFICANCE STATEMENT Previous investigations have found an altered pattern of moral behaviors in individuals with autism spectrum disorder (ASD), which is closely associated with functional changes in the right temporoparietal junction (rTPJ). However, the specific neurocomputational mechanisms at play that drive the altered function of the rTPJ in moral decision-making remain unclear. Here, we show that ASD individuals are more inflexible when following a moral rule although an immoral action can benefit themselves, and experience an increased concern about their ill-gotten gains and the moral cost. Moreover, a selectively reduced rTPJ representation of information concerning moral rules was observed in ASD participants. These findings deepen our understanding of the neurobiological roots that underlie atypical moral behaviors in ASD individuals.

Keywords: autism; decision-making; fMRI; moral.

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Figures

Figure 1.

Figure 1.

Illustration of experimental design and…

Figure 1.

Illustration of experimental design and trial procedure. A , We used a 2…

Figure 1. Illustration of experimental design and trial procedure. A, We used a 2 × 2 within-subject design by independently manipulating Audience (Private or Public) and Moral Context (Good or Bad), which yielded four experimental conditions (i.e., PublicGood, PublicBad, PrivateGood, and PrivateBad). The Public condition was indicated by the picture of “eyes,” and the Private condition was indicated by the picture of a “lock.” The Good Context involved a tradeoff between personal losses and benefits for a charity, whereas in the Bad Context participants traded personal benefits against benefits for a morally bad cause. B, Monetary payoffs (in Brazilian Real) for participants (8 levels: from 1 to 8, in steps of 1) and the association (8 levels: from 4 to 32, in steps of 4) were orthogonally varied, yielding 64 unique offers for each condition. In the example trial (one for the PublicGood and the other for the PrivateBad condition), participants were presented with an offer and decided whether to accept or reject the offer with no time limit. If they accepted the offer, both parties involved (i.e., the participant and the association) might undergo the financial consequences as proposed. If they rejected the offer, neither party would profit. In the Private condition, once a response was made, the screen was unchanged for 0.5 s to keep the chosen option private. In the Public condition, the chosen option was highlighted with a larger font and the nonchosen option disappeared, this lasted slightly longer (1.5 s) to further emphasize the presence of a witness. Each trial was ended with an intertrial interval (ITI) showing a jittered fixation (2.5 ∼ 6.5 s).
Figure 2.

Figure 2.

Results of choice behavior. A…

Figure 2.

Results of choice behavior. A , Rate of choosing the moral option as…

Figure 2. Results of choice behavior. A, Rate of choosing the moral option as a function of group (ASD or HC), reputation (Private or Public), and context (Good or Bad). B, Heat map of the mean proportion (percentage) of moral choices as a function of payoffs (monetary units) for participants and for associations in each experimental condition for each group. Each dot represents the data of a single participant. Error bars represent the SEM.
Figure 3.

Figure 3.

Model comparison and validation. A…

Figure 3.

Model comparison and validation. A , Bayesian model evidence. Model evidence (relative to…

Figure 3. Model comparison and validation. A, Bayesian model evidence. Model evidence (relative to the model with the worst accuracy of out-of-sample prediction; i.e., model 5) clearly favors model 4 (m4). Lower (i.e., more negative) LOOIC scores indicate a better model. B, Posterior predictive check of the winning model. Each dot represents the data of a single participant. For each participant, we calculated the mean of the predicted proportion of moral choice (%; y-axis) by averaging moral choices generated using the whole posterior distribution of estimated parameters specific to that participant based on the winning model. Regardless of experimental conditions, these dots almost fell on the diagonal, indicating that the winning model captured the actual behaviors of all participants in this task.
Figure 4.

Figure 4.

Results of parameter estimates. A…

Figure 4.

Results of parameter estimates. A , Group-level mean of individual-level posterior mean of…

Figure 4. Results of parameter estimates. A, Group-level mean of individual-level posterior mean of α and β across moral contexts (good or bad) derived from the winning model. B, Scatter plot of individual-level posterior mean of α and β across moral contexts (Good or Bad) in each group. Each dot represents the data of a single participant. Error bars represent the SEM; significance: **p < 0.01, after controlling for the age difference between groups.
Figure 5.

Figure 5.

Results of decision time (in…

Figure 5.

Results of decision time (in milliseconds). A , Bar plot of the mean…

Figure 5. Results of decision time (in milliseconds). A, Bar plot of the mean decision time as a function of group (ASD or HC), reputation (Private or Public), and context (Good or Bad). B, Heat map of the mean decision time regardless of specific choices as a function of payoffs (monetary units) for participants and for associations in each experimental condition of each group.
Figure 6.

Figure 6.

Illustration of within-subject RSAs. For…

Figure 6.

Illustration of within-subject RSAs. For each individual, we first constructed a neural RDM…

Figure 6. Illustration of within-subject RSAs. For each individual, we first constructed a neural RDM measuring the correlational distances of multivoxel patterns of the decision-relevant neural activities within either left or right TPJ between each pair of valid trials, respectively. Next, we constructed four cognitive RDMs by calculating the Euclidean distances between each pair of valid trials with respect to the following information: (1) Audience (i.e., social reputation; Private or Public); (2) Moral Context (i.e., Good or Bad); (3) payoffs for the participant; and (4) payoffs for associations. Notably, we sorted all trials according to the order of Audience, Moral Context, payoff for the participant, and payoff for associations to guarantee the information contained by both the neural and cognitive RDMs was matched with each other. Then we performed the Spearman rank-ordered correlation between the neural and the cognitive RDMs. Finally, an independent two-sample permutation-based t test was conducted to compare the between-group difference on the z-transformed Spearman's ρ.
Figure 7.

Figure 7.

A , B , Within-subject…

Figure 7.

A , B , Within-subject RSA results using the parcellation-based ROI ( A…
Figure 7. A, B, Within-subject RSA results using the parcellation-based ROI (A) and the coordinate-based ROI (B) of TPJ. For each participant, we only adopted valid trials (see Materials and Methods for details) in these analyses. Each dot represents the data of a single participant. Error bars represent the SEM; significance: *ppermutation < 0.05, **ppermutation < 0.01, after controlling for the age difference.
Figure 8.

Figure 8.

A , B , Robustness…

Figure 8.

A , B , Robustness check of within-subject RSA results using the parcellation-based…
Figure 8. A, B, Robustness check of within-subject RSA results using the parcellation-based ROI (A) and the coordinate-based ROI (B) of TPJ. For each participant, we adopted all 256 trials in these analyses. Each dot represents the data of a single participant. Error bars represent the SEM; significance: *ppermutation < 0.05, ***ppermutation < 0.001, after controlling for the age difference.
Figure 9.

Figure 9.

Univariate results of TPJ in…

Figure 9.

Univariate results of TPJ in healthy control subjects. A , Bar plot of…

Figure 9. Univariate results of TPJ in healthy control subjects. A, Bar plot of TPJ signals. For visualization, we extracted the mean activity (contrast value) of lTPJ and rTPJ from the parcellation-based or coordinate-based mask as a function of reputation (Private or Public) and context (Good or Bad). Each dot represents the data of a single participant. Error bars represent the SEM. B, Relationship between neural audience effect in TPJ and behavioral audience effect across individuals. Each dot represents the data of a single participant. Each line represents the linear fit. Shaded areas represent the 95% confidence interval.
Figure 10.

Figure 10.

A , B , Univariate…

Figure 10.

A , B , Univariate results of TPJ in the HC and ASD…
Figure 10. A, B, Univariate results of TPJ in the HC and ASD groups using the parcellation-based mask (A) and the coordinate-based mask (B). For visualization, we extracted the mean activity (contrast value) of lTPJ and rTPJ from the corresponding masks as a function of group (ASD or HC), reputation (Private or Public), and context (Good or Bad). Each dot represents the data of a single participant. Error bars represent the SEM.
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References

    1. Ahn W-Y, Krawitz A, Kim W, Busmeyer JR, Brown JW (2011) A model-based fMRI analysis with hierarchical Bayesian parameter estimation. J Neurosci Psychol Econ 4:95–110. 10.1037/a0020684 - DOI - PMC - PubMed
    1. Ahn W-Y, Haines N, Zhang L (2017) Revealing neuro-computational mechanisms of reinforcement learning and decision-making with the hBayesDM package. Comput Psychiatr 1:24–57. 10.1162/CPSY_a_00002 - DOI - PMC - PubMed
    1. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders: DSM-5, Ed 5. Arlington, VA: American Psychiatric Association.
    1. Baron-Cohen S (2001) Theory of mind and autism: a review. Int Rev Res Ment Retard 23:169–184.
    1. Baron-Cohen S, Leslie AM, Frith U (1985) Does the autistic child have a “theory of mind”? Cognition 21:37–46. 10.1016/0010-0277(85)90022-8 - DOI - PubMed
Show all 73 references

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