Abstract
Impairments in using eye gaze to establish joint attention and to comprehend the mental states and intentions of other people are striking features of autism. Here, using event-related functional MRI (fMRI), we show that in autism, brain regions involved in gaze processing, including the superior temporal sulcus (STS) region, are not sensitive to intentions conveyed by observed gaze shifts. On congruent trials, subjects watched as a virtual actor looked towards a checkerboard that appeared in her visual field, confirming the subject's expectation regarding what the actor 'ought to do' in this context. On incongruent trials, she looked towards empty space, violating the subject's expectation. Consistent with a prior report from our laboratory that used this task in neurologically normal subjects, 'errors' (incongruent trials) evoked more activity in the STS and other brain regions linked to social cognition, indicating a strong effect of intention in typically developing subjects (n = 9). The same brain regions were activated during observation of gaze shifts in subjects with autism (n = 10), but did not differentiate congruent and incongruent trials, indicating that activity in these regions was not modulated by the context of the perceived gaze shift. These results demonstrate a difference in the response of brain regions underlying eye gaze processing in autism. We conclude that lack of modulation of the STS region by gaze shifts that convey different intentions contributes to the eye gaze processing deficits associated with autism.
Highlights
Autism is an aetiologically complex, severe and pervasive neurodevelopmental disorder characterized by deficits in social interactions, language and communication abnormalities, as well as the presence of restricted, repetitive behaviours, and a characteristic developmental course (American Psychiatric Association, 1994)
In the present research, using event-related functional MRI (fMRI) at 1.5 T, we evaluated the hypothesis that, in autism, brain regions normally involved in eye gaze processing are not sensitive to intentions conveyed by gaze shifts
The anatomical location of this eye gaze-evoked superior temporal sulcus (STS) activity is consistent with the area of the STS region identified in several prior reports of activity in neurologically normal adult subjects evoked by observation of eye movements (Puce et al, 1998; Wicker et al, 1998; Hoffman and Haxby, 2000; Pelphrey et al, 2003, 2004a)
Summary
Autism is an aetiologically complex, severe and pervasive neurodevelopmental disorder characterized by deficits in social interactions, language and communication abnormalities, as well as the presence of restricted, repetitive behaviours, and a characteristic developmental course (American Psychiatric Association, 1994). Among the most striking features of the social impairments in autism are deficits in coordinating visual attention with others (i.e. initiating and responding to joint attention) and understanding the mental states and social intentions of other people on the basis of information gathered from the eyes (Loveland and Landry, 1986; Mundy et al, 1986; BaronCohen, 1995; Dawson et al, 1998; Leekam et al, 1998, 2000; Baron-Cohen et al, 1999a; Frith and Frith, 1999). Gaze processing deficits in autism do not appear to be based in eye gaze discrimination per se, but result from impairment in using gaze to understand the intentions and mental states of other people (Baron-Cohen, 1995, BaronCohen et al, 1999a, 2001; Leekam et al, 1998, 2000). Baron-Cohen (1995) carried out an experiment in which he showed pictures of a cartoon face (named ‘Charlie’)
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