Using a simple charitable donation task, we tested the hypothesis that people with ASD would show reduced social preferences. We found a significant reduction in the frequency and magnitude of donations made to charities benefitting other people compared with those benefitting mental health, animals or the environment. In addition, the group with ASD was less sensitive to specific information that discriminated amongst people charities, donating the same (abnormally low) amount to all of them. Control participants rated the impact of pictures and text descriptions on their donation amount particularly highly for people charities, whereas those with ASD gave significantly lower ratings to their impacts. This suggests that higher donations to people charities may normally be driven by the high social salience that they have, a component that is lacking in people with ASD. Taken together, this pattern of findings supports the hypothesis of abnormal social preferences in ASD and suggests specific reasons for it. The abnormally low ratings of the impact of visual and descriptive information provided for each charity given by the group with ASD argues that socially relevant empathy evoking information was not incorporated into normal valuation for the charity. Consequently, there was little discrimination among the people charities, and the entire category of charities benefitting people was devalued in terms of the actual donations made. While ratings given by people with ASD for the impact of pictures on donations was low for people charities, we did find the group with ASD rated the impact of pictures as high as the control group for animal charities. This is interesting to note because studies have reported people with autism having an easier time connecting with animals than with people.
Several other recent studies have investigated reward processing in people with autism, and have suggested disproportionate impairments in social reward processing, as well as more general impairments in processing rewards across multiple stimulus types. For instance, it was reported that children with autism showed generally impaired implicit reward learning to both money and social stimuli, although the neural response to such stimuli measured with functional magnetic resonance imaging also showed a disproportionate abnormality for the social stimuli in particular [
20]. Another study [
21] found that the neural response to monetary reward learning was abnormal in people with ASD, but that this abnormality disappeared during processing of interesting objects, possibly corresponding to the restricted interests aspects of the autism phenotype. These studies are broadly consistent with three aspects of our present study: people with ASD donated less overall (a domain-general impairment in reward processing); donated disproportionately less to people charities (a domain-specific impairment in social reward processing); and donated a lot to a few idiosyncratic nonsocial charities (intact or even exaggerated reward processing for a few unusual stimuli). These patterns show that high-functioning people with ASD are not altogether incapable of evaluating stimuli and making reward-based decisions about them - but how they evaluate particular categories of stimuli is abnormal.
Across studies, the specific processes and neural structures that have been found abnormal in reward processing in autism are always a subset of those now well-documented to process the value of stimuli, actions and outcomes in healthy participants. These include regions such as the ventral striatum as well as ventral and medial parts of the prefrontal cortex [
22-
24], and there is now good evidence that these regions process reward value from all different types of stimuli (such as money, juice or social stimuli), conveyed to these regions through convergent inputs from various sensory association cortices [
6-
8,
15,
25-
28]. In particular, there is evidence that additional processing is required in order to interpret the value of socially relevant stimuli, originating in part from regions known to process social information, such as cortices in the superior temporal gyrus [
12].
Impairments in such additional processing of socially relevant stimuli have been reported in high-functioning people with autism. One study found a remarkably selective impairment in combining outcomes with intentions to evaluate moral actions as good or bad in high-functioning people with autism [
29], suggesting that the ability to incorporate multiple sources of social information is particularly compromised. Izuma
et al. recently reported that people with autism do not show the normal modulation of prosocial behavior (donations to a charity) when they are observed by another person, suggesting that they are insensitive to social reputation effects [
30]. In addition, they found that people with autism were insensitive to social reputation effects on charitable donations, and they also observed that overall donations were considerably less than in the control group.
In our present study, we found a similar effect: people with ASD donated less on average, across all stimuli, but in addition they also showed a disproportionate reduction in donations specifically to charities benefitting other people.
One caveat worth mentioning here is while there was no explicit monitoring in our study, as in the Izuma study [
30], we concede that participants could have been thinking about the analysis at the end of the experiment and how in principle we could trace who gave to what and how much. This could have created an observer effect that would partly explain the lower average donation amount in people with autism compared with controls.
One special category also worth highlighting is mental health. While we found abnormally low donations in ASD for people charities, we found the highest amount of donations were to the mental health category. When we collapsed the people and mental health categories, the significant difference between participants with ASD and controls disappeared in a one-tailed t-test. An ANOVA comparing non-people (collapsing animal and environment charities) versus people (collapsing people and mental health charities) also showed no significant interaction effects and only a main effect of non-people versus people. This suggests that people with autism treat charities in the mental health category (specifically those benefiting autism) in a special manner, different from their usual donation pattern for other people charities. Indeed the group with ASD gave these charities higher ratings for ‘benefit to self’ and ‘benefit to friends’ than did the control group, as shown in Figure . One interpretation of this pattern in the results could be that thinking about charities benefiting people in general requires some empathy. For the control group, this may be one factor driving their donations to the people charities; for the group with ASD, it may be one lacking factor accounting for their low donations to people charities. In the mental health category, however, empathy may not have been required for the participants with ASD to recognize the value since several of these charities were closely related to their own condition.
The phenotype of ASD shows a complex pattern of impairments, typically diagnosed as falling into three classes that together constitute the criteria for clinical diagnosis: language development, reciprocal social interactions, and repetitive behaviors and restricted interests. Arguably, the present findings may contribute to both of the last two, in that they suggest that people with autism have reduced interests in, or preferences for, charities benefitting people as compared to charities benefitting other categories. Moreover, we found a few charities that elicited unusually high donations from the group with ASD, a finding that should be followed up in future studies to better understand what it is about these particular charities that makes them preferable to people with autism. It is also interesting that we found a negative correlation between the amounts that participants with ASD donated to the people charities and the ADOS-B subscale. This subscale comprises items assessing unusual eye contact, facial expression directed to others, empathy and comments on others’ emotions, responsibility, quality of social overtures, quality of social response and amount of reciprocal social communication. While exploratory, this finding provides preliminary evidence that the abnormal social preferences revealed in our task may relate to abnormal social interactions in people with autism.
Returning to the social motivation hypothesis of autism [
3,
9,
10], it remains an intriguing question how precisely the pattern of impairments we report here emerges during development. One possibility is that early domain-general impairments in reward processing, in a developmental context, give rise to impairments disproportionate for social stimuli [
31]. Similarly, early domain-general impairments in integrating complex contextual information may result in impairments particularly acute for social stimuli, simply because these draw more upon integrating multiple sources of information. An important future task will be to map out the abilities, and the concomitant brain responses, of people with ASD to process and evaluate a broad range of stimuli. Finally, a full understanding of motivated behavior in ASD will also need to examine the flip-side of reward processing: aversive behavior elicited by actively disliked stimuli.