In this study, we found that children with ASD show both a behavioral impairment in implicit learning, as well as a reduced neural response to SR and socially rewarded learning in canonical reward-processing brain regions. First we examined whether TD and ASD children were able to implicitly learn the stimulus–outcome associations. TD children demonstrated significant learning over the course of the paradigm for both neutral and rewarded trials within both the social and monetary tasks. However, classification accuracy within the ASD group remained near chance for rewarded and neutral trials for the duration of both social and monetary tasks. These findings indicate impaired implicit learning in ASD, independent from reward processing. Next, we examined the neural response to rewards, independent of learning, by examining responses to both random and deterministic rewards. Although significant VS activity for both monetary and SR was observed in TD, but not ASD, children, significant between-group differences were found only for SR, indicating reduced neural responses to SR in children with ASD. We then investigated whether there were differences in the networks associated with rewarded learning between ASD and TD children. Again, we found that children with ASD showed significantly reduced activation of frontostriatal networks relative to TD children during socially rewarded learning. Finally, we examined the degree to which the neural response to reward was related to measures of social functioning and found a positive correlation in the VS in TD children only, such that better social functioning was related to greater activity in the VS in response to positive social feedback.
Our goal was to test the social motivation hypothesis by examining rewarded learning within monetary and social contexts in children with ASD. Using traditional behavioral measures, such as looking preferences, the reward response to social stimuli in autism is difficult to assess. With fMRI we were able to investigate both the behavioral and neural correlates of rewarded learning in autism. Our findings are consistent with the prediction that children with ASD do not find social stimuli rewarding, as evidenced by reduced neural responses to SR in regions associated with reward processing. When we examined the general neural response to monetary and social reward events, we discovered that only TD children showed VS activity for both reward types, whereas ASD children did not demonstrate a significant response to either monetary or SR. However, significant between-group differences were shown only for SR, suggesting that children with ASD may be specifically impaired on processing SR. These findings are consistent with the behavioral evidence that children with autism do not find social stimuli rewarding. Furthermore, comparisons between positive reward feedback and positive neutral feedback indicate a strong valuation signal in pregenual cingulate cortex in TD children specifically in response to SR. This suggests that during typical development, positive social feedback may be particularly salient and have a high intrinsic reward value [
de Araujo, Kringelbach, Rolls, & McGlone, 2003;
Hare, O’Doherty, Camerer, Schultz, & Rangel, 2008;
Plassmann, O’Doherty, Shiv, & Rangel, 2008]. This signal was not seen for either reward type in ASD children, nor for MR in TD children, thus further supporting the hypothesis of abnormal social reward processing in children with ASD.
As there is a demonstrated relationship between learning and reward, we also examined the neural correlates of instructive feedback processing (i.e., feedback which can guide learning of stimulus–outcome associations) via correct deterministic reward trials (i.e. trials in which the stimulus–outcome association are constant). At the behavioral level, TD children were able to learn the stimulus–outcome associations for both reward types, whereas the children with ASD were unable to learn the associations during the task and overall accuracy remained near chance. Post-test data confirmed that neither group explicitly memorized the stimulus–outcome associations. These behavioral results indicate impaired implicit learning in children with ASD, though this is largely an unexplored area in the field. To control for this difference in learning between the ASD and TD children, an estimate of each child’s learning rate was included as a covariate in all between-group analyses. At the neural level, TD children demonstrated activity in networks involved in reward processing and implicit learning, including dorsal and VS, frontal cortices, and hippocampus for both monetary and social tasks. Children with ASD demonstrated activity in these regions during the monetary-rewarded learning task but not during the social condition. Between-group comparisons revealed greater frontostriatal activity for TD than ASD children for social reward learning trials. Together, the between-group differences in basic reward processing and rewarded learning specifically within the social context supports impaired socially rewarded learning in children with ASD. Thus, this finding provides empirical support for the social motivation hypothesis of autism [
Dawson, Meltzoff, Osterling, Rinaldi, & Brown, 1998a;
Dawson et al., 2004,
2005;
Schultz, 2005] which posits that decreased reward value of social stimuli in children with ASD can negatively impact the development of social behaviors.
Finally, we investigated whether activity in the reward system, particularly the response to SR, related to the children’s level of social functioning. We found a relationship between a previously validated measure of reciprocal social behaviors [SRS;
Constantino et al., 2003] and the amount of VS activity for SR that guide learning in TD children only. This correlation was not seen in children with ASD, supporting the hypothesis that appropriate response to SR, especially those that inform learning, are related to the development of social skills in children. The lack of a correlation in the ASD group may also reflect decreased variance in the percent signal change due to the overall small amount of activity observed in the VS. Notably, however, our findings are not likely due to a failure on the part of the children with ASD to attend to the task, as there was activation of similar neural networks for all events (as compared to rest) across groups, as well as comparable RT data. Furthermore, equivalent amounts of activity in fusiform cortices during trials involving the presentation of facial expressions suggest that differences between groups during processing of social feedback are not likely due to a failure of ASD children to attend to or process the faces.
One previous fMRI study examined reward responsiveness in adults with ASD using MR and did not find between-group differences in reward-related areas such as VS or OFC [
Schmitz et al., 2008]. By also examining responses to SR, we were able to reveal significant reduction in reward circuitry activity during processing of SR in children with ASD. Our findings are also consistent with previous structural [
Haznedar et al., 2006;
Hollander et al., 2005;
Kates et al., 1998;
Langen, Durston, Staal, Palmen, & van Engeland, 2007;
Sears et al., 1999] and functional [
Haznedar et al., 2006;
Takarae, Minshew, Luna, & Sweeney, 2007] MRI studies demonstrating abnormalities in the striatum in individuals with autism. However, it is unclear to what extent these functional and structural differences are primary or secondary to social abnormalities. While the current study is limited in the ability to draw conclusions about causality, the evidence supporting early differences in social motivation and response to rewarding social stimuli in children with autism are suggestive of abnormal function and structure early in life contributing to the development of abnormal social behaviors. This hypothesis will need to be addressed in younger cohorts in future studies. An additional limitation of our study is the potential confound due to the medication status of nine of our participants with ASD. However, when we examined activity in our primary region of interest, the VS, we did not find evidence for an association between medication status and activity in this region. In fact, unmedicated children demonstrated some of the lowest VS responses. The children in this study were primarily taking psychostimulants, which have demonstrated no effects on the hemodynamic response [
Rao et al., 2000] and antipsychotics, which have been shown to normalize BOLD responses [
Lencz et al., 2000;
Schlosser et al., 2003;
Snitz et al., 2005]. Thus, the use of medication in several ASD participants may have actually decreased group differences between ASD and TD children. However, both stimulants and antipsychotics act on the dopamine system, albeit in opposite directions, which is one of the neurotransmitters involved in reward signaling. As such, the presence of these medications may alter the neural response to reward. Future studies on reward processing controlling for the effects of medication should be pursued.
By placing rewards within an implicit learning paradigm, we were able to examine the relationship between reward processing and implicit learning, functions which have been shown to rely on neighboring frontostriatal networks [
Shohamy, Myers, Kalanithi, & Gluck, 2008]. As suggested by computational models, impaired implicit learning may have repercussions for the development of social behaviors such as joint attention [
Triesch et al., 2006]. A previous investigation by
Mostofsky et al. [2000] found impaired procedural learning—a type of implicit learning—in individuals with ASD which the authors interpreted as reflective of cerebellar dysfunction. Our behavioral findings show an implicit learning deficit in children with ASD, providing additional evidence of impaired implicit learning in this population. However, future studies should be pursued to better characterize the nature of this impairment. Behaviors that arise from rewarded learning trials are often conceptualized in terms of classical conditioning [
Pavlov, 1927] and modeled as a function of a prediction error, that is, the difference between expected rewards and actual reward receipt. For instance, the Rescorla–Wagner learning model [
Rescorla & Wagner, 1972] presumes that prediction error estimates will converge towards 0 irrespective of accuracy in a deterministic context, effectively assuming that subject accuracy is not dependent on the prediction error. Currently, there are no data that investigate the applicability of this model for learning impaired subjects, and for this reason we did not employ that prediction error model. Future studies should further examine implicit learning and prediction error in individuals with ASD.
Our investigation into the neural correlates of rewarded learning in ASD is a direct test of the social motivation hypothesis of autism. In at least some animals, it appears that social stimuli serve as important primary rewards that influence behaviors important for survival. For example, the same neural networks involved in other forms of reward processing (e.g., food, drugs, etc.), underlie social processes such as pair-bonding [
Young, Murphy Young, & Hammock, 2005;
Young & Wang, 2004] and mother–offspring bonding [
Levy, Kendrick, Goode, Guevara-Guzman, & Keverne, 1995] in small rodents [
Febo, Numan, & Ferris, 2005] and voles [
Young et al., 2005]. Impaired reward processing and learning may be the underlying factor for the abnormal development of some social behaviors in children with ASD, and targeting brain regions involved in social rewarded learning for possible therapeutic intervention in this population may prove to be a valuable early treatment approach. For example, oxytocin, a neurohypophyseal hormone linked to pro-social behaviors, has a high density of receptors within the nucleus accumbens. Administration of this neurohormone to individuals with ASD has been shown to decrease repetitive behaviors [
Hollander et al., 2003] and increase affective speech comprehension [
Hollander et al., 2007]. Furthermore, oxytocin administration has been shown to modulate BOLD activity in regions associated with social cognition and reward in human [
Kirsch et al., 2005] and rodent [
Febo et al., 2005]. Conversely, our results may reflect differences in the structural integrity of a distributed reward processing and learning network, in which case future studies should examine the developmental trajectory of these structures and their connectivity. Our data would suggest that increasing reward responsiveness in ASD, perhaps through pharmacotherapy, might augment social learning. Future studies may investigate the degree to which manipulating VS activity affects social responsiveness, and ultimately autistic symptomatology, in children with autism spectrum disorders.
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