The present study examined the functioning of the default network during self and other-person reflection and at rest in autism. There were four primary findings. First, the autism group had reduced functional activity in the vMPFC/vACC at rest. Second, when collapsed across all person judgment conditions, reduced activity was again found in the vMPFC/vACC in autism, but there were no group differences in the dMPFC, RSC/PCC or lANG. Third, although overall levels of activity were similar between groups in the dMPFC and RSC/PCC, there were group by condition interactions across INTERNAL/EXTERNAL judgments in these regions. Finally, there were no group by condition interactions across SELF/OTHER judgments for any ROI. Together, these findings give a more detailed view of default network functionality and abnormality in autism. Below, we discuss the implications of these findings.
Findings of abnormal vMPFC/vACC activity at rest are consistent with a growing body of literature demonstrating resting functional abnormalities of the default network in autism (Kennedy et al
; Cherkassky et al
; Kennedy and Courchesne, 2008
). As activity in default network regions correlates to ones’ propensity to daydream (Mason et al
) and to the amount of task-unrelated thoughts (McKiernan et al
) and self-referential thoughts (D’Argembeau et al
), one interpretation is that these group differences in functional activity reflect group differences in resting cognitive processes (Kennedy et al
). Preliminary support for this possibility comes from an interesting behavioral study that attempted to assess the self-reported inner experience of adults with Asperger's syndrome (Hurlburt et al
). Remarkably, two of the three individuals tested had difficulty simply understanding what it meant to describe their inner experience and thoughts (though, importantly, their verbal IQ was in the normal range and both could describe observable features of their immediate environment). Thus, the reduced propensity or reduced ability to introspect may underlie the reduced vMPFC/vACC activity at rest.
However, an alternative explanation of reduced levels of resting activity in autism is that there might be a pervasive dysfunction of these regions—in other words, the abnormality might be task- or cognition-independent. Previous task-based studies have provided preliminary support for this possibility, but the implicit nature of the socioemotional tasks used previously (Castelli et al
; Pierce et al
; Kennedy et al
) leaves open the possibility that the autism subjects simply did not engage the socioemotional processes of interest. In the present study, we ensured that subjects engaged in introspective and socially oriented processing, by requiring true/false responses to self- and other-relevant statements. Even with these explicit tasks, we observed abnormality in the vMPFC/vACC region of the default network, supporting the idea that such functional abnormality of this region might be task-independent and pervasive. Importantly, such pervasive dysfunction of the vMPFC/vACC could also explain the introspective difficulties described earlier.
Group differences were also observed in the dMPFC and RSC/PCC, although the nature of these abnormalities was quite different from the vMPFC/vACC abnormality described earlier. In these regions, group differences were found in the relative pattern of activity between INTERNAL and EXTERNAL conditions, rather than group differences in overall levels of activity when collapsed across these tasks (as found in the vMPFC/vACC). In other words, group differences in the dMPFC and RSC/PCC were task-specific (i.e. group by condition interactions), rather than reflecting a more general, non-specific and pervasive dysfunction (i.e. main effects of group). For both regions, this interaction seems to have been driven primarily by reduced activity during the INTERNAL condition in the autism group, while exhibiting similar or slightly increased activity during the EXTERNAL condition. Such functional differences between groups cannot be accounted for simply by differences in reliability of judgments, because using this performance measure as a covariate did not change the results. However, a number of other plausible cognitive and behavioral explanations may account for these abnormalities. One possibility is that individuals with autism may have a specific deficit in making judgments that rely on inference (e.g. INTERNAL judgments), but an intact ability in making judgments that rely on observation (e.g. EXTERNAL judgments). This suggestion is consistent with previous behavioral findings of autism. When asked to describe a scene composed of geometric shapes moving in such a way to imply intentionality, subjects with autism can accurately describe the physical, observable features of the stimuli, but are impaired in describing the non-observable, but readily inferable, intentions of the stimuli (Klin, 2000
; Castelli et al
). Second, and potentially relating to a bias toward the observable over the inferable, individuals with autism may have less experience and expertise in making inferential personality judgments, but more experience and expertise in making judgments of externally observable characteristics of people. Lastly, there may be group differences in the depth of processing (e.g. the richness, detail and completeness of person representations) across INTERNAL and EXTERNAL judgments. For instance, the autism group may have had less elaborate representations of themselves and others during INTERNAL judgments but more elaborate representations during EXTERNAL judgments. Regardless of the explanation, however, since overall levels of activity were similar between groups, these findings point toward task-specific dysfunction of the dMPFC and the RSC/PCC, rather than a more pervasive task-independent dysfunction.
Although the above described abnormalities of default regions were found, perhaps equally interesting are the functional similarities between groups. With the exception of the vMPFC/vACC, the responses of the dMPFC, RSC/PCC and lANG were indistinguishable between groups during SELF and OTHER judgments. In the dMPFC, both groups had similar levels of activity in the SELF and OTHER conditions, a finding consistent with several previous studies of self and close other person reflection in control subjects (Schmitz et al
; Ochsner et al
; however, also see Heatherton et al
). Furthermore, in the RSC/PCC and lANG, both groups had greater activity in OTHER relative to the SELF condition. This typical pattern of RSC/PCC activity in autism, given the abnormal pattern of RSC/PCC activity across INTERNAL/EXTERNAL judgments, further underscores the task-specific, as opposed to task-independent, dysfunction of this region. These findings suggest that, at a neural level, high functioning individuals with autism and Asperger's syndrome are able to differentiate between judgments of themselves and others, and, with the exception of the vMPFC/vACC, recruit the same default network regions to do so.
While the importance of using explicitly defined and well-controlled experimental conditions is clear, we should emphasize the importance of also measuring brain activity during unconstrained or underspecified tasks, since each approach provides a unique perspective on brain functioning.1
On the one hand, using a non-task resting state or an underspecified experimental task can reveal what the autistic brain does naturally (i.e. what it defaults to) when unconstrained by often artificial, rigidly defined and externally imposed task demands. On the other hand, studies using experimentally constrained tasks with explicit instructions and explicit requirements can reveal what the autistic brain is capable of doing when challenged with a particular task or situation. Although it is possible that brain activity (and underlying mental processes) can be similar during both unconstrained and constrained contexts, this relationship cannot be assumed, especially in patient populations. For instance, in the present study, the control group had significant positive correlations between resting activity and task-evoked (MENTAL) activity in each ROI, while such correlations were absent in the autism group. A recent study by Wang and colleagues (2007
) also explored the relationship between implicit and explicit task demands on brain activity in high-functioning individuals with autism. After viewing and listening to short cartoon vignettes, subjects were asked to determine whether or not a story character's utterance was sincere or sarcastic. When given vague instructions (i.e. ‘pay attention’), the autism group did not activate several brain regions that were active in control subjects (including the dMPFC). Remarkably, however, when given explicit directions to attend to faces or prosody of voices, the autism group had more normal levels of activity in the dMPFC, further underscoring the task-dependent nature of dMPFC abnormality. Furthermore, early reports on hypoactivation of the fusiform face area in autism (Schultz et al
; Pierce et al
) might be explained by differences in unconstrained processes [e.g. task engagement (Pierce et al
); eye gaze patterns (Hadjikhani et al
; Dalton et al
)], as opposed to pervasive regional dysfunction.
Several limitations of the current study should also be addressed. First, the full extent of regional dysfunction during rest in autism is likely not entirely captured in the present study. Given the inherently unconstrained (and thus, varied) nature of rest, the sample size might be too small to detect less robust regional differences in resting activity. Furthermore, REST blocks were randomly interspersed between the various person judgment conditions, which may have led to carry-over processing of self- and other-reflection, thus reducing the power to detect group differences. Second, as default regions are responsive to the evaluation of emotionally salient stimuli (Maddock, 1999
; Maddock et al
; Moran et al
), possible group differences in incidental affective processing associated with self- and other-reflection may have contributed in part to the group differences reported here. Additional studies will be necessary to further explore this possibility.
In sum, the present experiment gives further insight into the nature of default network functionality and abnormality in autism. We provide evidence for task-specific deficits within particular default network regions (dMPFC and RSC/PCC) as well as evidence for more pervasive task-independent abnormalities (vMPFC/vACC). Such distinctions between the type of functional abnormality in these and other brain regions involved in social, emotional and introspective processes will likely be important for understanding the nature of such difficulties in autism.