This is the first study to investigate the neural correlates of social orienting in autism using a spatial cueing paradigm. One of the most striking results was that TD and ASD children and adolescents demonstrated similar social orienting behavior in the laboratory task, yet the brain activity underlying that behavior showed clear group differences. The TD group exhibited greater activity for social cues than for nonsocial cues in many regions, while the ASD group showed less distinction that also differed anatomically. These results are consistent with the hypothesis that social cues are not assigned the same privileged status in the autistic brain as in the typically developing brain.
Behaviorally, both TD and ASD children and adolescents demonstrated facilitation effects for gaze and arrow cues with no differences between groups. This is consistent with previous studies conducted in laboratory settings (Chawarska et al., 2003
; Kylliainen and Hietanen, 2004
; Senju et al., 2004
; Swettenham et al., 2003
), displaying “normal” orienting responses by social and nonsocial cues in ASD. Additionally, both groups were faster for gaze-cued trials than for arrow-cued trials, suggesting a comparable distinction between social and nonsocial cues between groups. However, the similar orienting behavior did not translate into similar brain activity in the two groups. Rather, the TD group showed extensive differences in neural activity for social and nonsocial cues, while the ASD group only showed differences in one parietal region and lower-level visual regions.
The TD group demonstrated greater brain activity in several regions for social cues than for nonsocial cues, supporting the idea that social cues have a special status in the neurotypical brain. Given the behavioral result that participants were faster for gaze-cued trials than for arrow-cued trials, one might argue that differences in brain activity simply reflect differences in reaction time. However, brain activity typically increases for conditions with slower reaction times, whereas our participants showed increased activity when reaction times were faster (gaze cue condition). Specifically, gaze cues elicited more activity in frontoparietal regions, including the IFG, premotor cortex, SPL, and SMG, which have been identified as part of a network for orienting attention. The posterior parietal cortex (PPC), which encompasses the SPL and SMG, and ventral prefrontal regions are consistently implicated in disorders of spatial attention (Bisiach et al., 1981
; Heilman et al., 2003
; Mesulam, 1999
) and are reliably activated in neuroimaging studies of spatial orienting (for a review, see Corbetta and Shulman, 2002
). Additional frontoparietal activity was found in the cingulate cortex and postcentral gyrus. The anterior cingulate cortex is reliably activated in studies of executive attention (Bush et al., 2000
), and both precentral and postcentral gyri have been shown to activate during target response in spatial orienting tasks like the one used here (Hopfinger et al., 2000
). Thus, our data show that TD children and adolescents engage several frontoparietal attention regions to a greater extent when their attention is cued by a social stimulus compared to a nonsocial stimulus.
While previous fMRI studies in adults also found greater activity for social cues than for nonsocial cues, such activity was not reported in the PPC, and only Engell et al. (2010)
reported a cluster in the IFG. Further, Hietanen et al. (2006)
, whose paradigm was most similar to ours, reported greater frontoparietal activity for arrow cues than for gaze cues. They concluded that gaze cues are more automatic than arrow cues based on previous neuroimaging data showing larger extents of activation for controlled (endogenous, top-down) than for automatic (exogenous, bottom-up) orienting (Kim et al., 1999
; Rosen et al., 1999
). Not only did we find greater frontoparietal activity for gaze cues than for arrow cues, but we also did not find any regions that were more active for arrow cues than for gaze cues. Thus, the different patterns of results in our study and in previous studies of adults may suggest that children are still developing automaticity for orienting attention in response to social stimuli. Post-hoc regression analyses with age in the TD group lend some support to this notion, as we found that activity for gaze cueing within the right SMG decreased as age increased (r
= −.46, p
The TD group also showed greater activity in visual processing areas for gaze cues, notably in the right fusiform gyrus and in the lateral occipital cortex (LOC). It is not surprising that regions involved in visual processing of social stimuli showed more activity for gaze cues than for arrows cues. However, our results did not show stronger activation in these regions for all gaze cues compared to all arrow cues. Rather, directional gaze cues elicited more activity than all other conditions, including neutral gaze cues. Previous neuroimaging data have shown that the fusiform gyrus is not only reliably activated by face perception, but is also modulated by selective attention (Hoffman and Haxby, 2000
; Hooker et al., 2003
). Thus, it is possible that even though our participants knew that the cues did not predict the location of the target and were instructed to ignore the direction of the cues, they paid more attention to the directional gaze cues, resulting in increased fusiform activity. Likewise, the LOC showed increased activity for directional gaze cues compared to all other condition. This is consistent with previous neuroimaging studies of social orienting in adults that reported greater LOC activity for social cues than for nonsocial cues (Engell et al., 2010
; Greene et al., 2009
; Tipper et al., 2008
). Our data extend these findings to developing populations, and confirm that LOC activity was not simply driven by visual processing of social stimuli.
The putamen also showed robust bilateral activation for directional gaze cues compared to the other cue conditions. This finding was unexpected, but suggests a role for the striatum in social orienting during typical development. It is well known that the putamen lies at the center of motor circuitry, with anatomical connections to cortical motor and somatosensory regions (for a review, see Alexander et al., 1986
). Interestingly, it has been shown that cells in the putamen may respond when a stimulus is important to behavior, but not when the behavioral significance is removed (Evarts et al., 1984
). Thus, it is possible that directional gaze cues were interpreted as more behaviorally significant than the other cue conditions. The clusters of activity in the putamen also extended into the insula, consistent with previous studies that found activation in the putamen/insula region for spatial cueing tasks (Gitelman et al., 1999
; Hopfinger et al., 2000
). Further research is necessary to understand the link between the striatum/insula regions and social orienting and whether this relationship is only observed during development.
The ASD group showed much less difference in brain activity between gaze cues and arrow cues than the TD group, with differential responses for social and nonsocial cues only observed in the SPL and visual association cortices. One explanation for this result is that the ASD group paid less attention to the task than the TD group or did not look at the cues as much. However, we found no differences in the behavioral effects between groups, and we were able to verify that both groups looked at the center of the screen (where the cue appeared) throughout the task. Another possibility is that individuals with ASD relied upon visual analysis of gaze direction rather than automatically making use of eye gaze due to its inherent social significance. Further, the observed SPL activity may reflect recruitment of top-down attentional resources, as this region is considered part of the dorsal frontoparietal attention network that supports controlled, endogenous shifts in attention (Corbetta and Shulman, 2002
Direct comparison of brain activity between groups verified differences in activity in several regions when attention was directed by gaze cues vs. arrow cues in TD as compared to ASD. Interestingly, these interactions revealed an opposite pattern of responses in the STS between groups, such that TD children showed decreased activity for arrow cues whereas children with ASD showed decreased activity for gaze cues. The STS is reliably involved in perception of biological stimuli, particularly eye gaze (Puce and Perrett, 2003
). Moreover, Pelphrey and Carter (2008)
have suggested that the STS may also be involved in utilizing eye gaze to understand the intentions of others. Here we demonstrate that the STS may also play a role in utilizing social cues to orient attention during typical development. In ASD, however, the STS may not be sensitive to the social meaning conveyed by eye-gaze (e.g., Pelphrey et al., 2005
), consistent with our results showing that the ASD group treated social cues similarly to the way in which the TD group treated nonsocial cues.
Taken together, our findings indicate that the ASD brain does not distinguish between social and nonsocial cues in the same way as the TD brain, relying upon different strategies to arrive at similar behavior. While this study did not examine the developmental trajectory of gaze processing, it is possible that high-functioning children and adolescents with ASD may have learned that gaze direction conveys meaning about the surrounding environment. Hence, typical behavior may be achieved through more ‘effortful’ orienting responses based on this acquired knowledge. To this end, our results could help explain why most prior laboratory experiments reported intact social orienting behavior in ASD. While individuals with ASD may be able to utilize lower-level physical properties of eye gaze and thus direct their attention in a controlled setting, they do not assign special social significance to such stimuli. As suggested by Nation and Penny (2008)
, individuals with ASD engage nonsocial mechanisms to process social cues. In more complex naturalistic paradigms as well as in daily life, these nonsocial mechanisms may not be otherwise engaged or may not function as efficiently, resulting in altered social orienting. Face and gaze processing impairments in ASD could originate from dysfunction in the basic neural system for face processing, or from abnormal development of that system due to lack of experience with faces (for a review, see Dawson et al., 2002
). Either way, early social orienting deficits can directly impact the ability to establish joint attention, which is notably impaired in autism, leading to a cascade of negative consequences for subsequent development (Dawson et al., 2002
; Mundy et al., 1990
; Mundy et al., 1986
; Sheinkopf, 2005