We asked high-functioning subjects with autism to identify emotional facial expressions, a task people with autism often perform normally. In line with previous findings, we also observed normal accuracy and normal face gaze, provided that whole upright faces were used as the stimuli. When the difficulty of the task was increased and only sparse regions of a face were revealed using the bubbles technique, we still observed normal performance levels in the autism group. However, their gaze onto these sparse facial features became dramatically abnormal. People with autism looked much more often and longer (autism, 27.3%; control, 8.7% of all saccades; autism, 216
ms; control, 48
ms) at the mouth.
When they fixated the mouth, we did not observe any abnormality in how viewing time is influenced by contrast changes. Despite their overall bias, higher contrast in the mouth region and lower contrast in the eye region increases the viewing time as it did for normals. The autism group rarely looked at the eyes in the bubbles condition, and they did not look at them more frequently when the mouth was not revealed, or shown with low contrast.
We then studied to what extent the eye movements to those target regions are influenced by bottom-up saliency information and compared the fixations made by the subjects with the predictions from a computational model. For the mouth region we found a strong reduction in predictability for the autism group, while the use of saliency information in the eyes, despite differences in the gaze behavior, are remarkably similar in both groups.
Returning to our initial hypotheses, it is unlikely that the autism group is attracted by the mouth because of its salient features. The normal influence of contrast changes on mouth viewing, as well as the absence of the bias in the full contrast condition, speaks against this possibility. The low correlation between the low-level visual information for saccades made to the mouth instead suggests an impaired top-down modulation of attention in the autism group.
Our results are consistent with earlier findings that autism subjects are impaired when judging complex social information from the eyes, but not from the mouth (Baron-Cohen, 1995
), and that they rely more on information from the mouth for emotional judgments (Spezio et al
). The differences in attentional processing suggest a possible general mechanism for the neurodevelopmental progression of impaired face gaze in autism (Dawson et al
). We failed to observe a deficit in using low-level visual saliency cues, or bottom-up attention, while we found differences in top-down modulation for saccades made to the mouth. We propose that this evidence is consistent with a neurodevelopmental progression that begins in infancy with a failure in directing attention to the faces and more specifically to the eyes in a face, along with preservation of bottom-up attentional processing. This is consistent with the major deficits in social engagement rather than in nonsocial areas when autism is evident in early infancy (Kanner, 1943
). Reported signs of lower social engagement in infants with autism include less interest in people (Volkmar et al
) and less looking at faces (Osterling et al
). The abnormal top-down attentional processing of faces may be due to abnormal reward circuitry (Dawson et al
) or to abnormal circuitry for emotional salience (Schultz, 2005
). Over the course of development, via learning, top-down attention may cause the propensity for mouth gaze in autism. This hypothesized mechanism adds to previous hypotheses about the causes of deficits in top-down attention to the face, and draws on our findings that bottom-up attention to the face is normal in high-functioning people with autism.
Another possibility is that the bubbles stimuli reveal an impairment in how attention is directed to local vs
global features. In contrast to earlier reports, we observed a normal eye gaze to whole faces. This could also be due to a social training program most of our autism subjects participated in. Despite their overall normal gaze to whole faces, the sparse bubbles stimuli might reveal an underlying impairment in deploying attention to local (vs
global) features (Dakin and Frith, 2005
The similar influence of contrast and other visual saliency information on eye movements in both groups suggests that the subcortical and cortical brain networks for bottom-up attention might be unimpaired in the autism group. Subcortically, the superior colliculus and the pulvinar are involved in the deployment of overt and covert spatial attention. The computation of the conspicuity maps is attributed to areas in the visual cortex (Lee et al
; Treue, 2003
). In contrast to bottom-up tasks, top-down attentional tasks activate parietal and frontal areas. The frontal areas, such as the frontal eye fields and in the parietal eye field (lateral intraparietal area in macaques), encode attention, but not the actual eye movements (Bisley and Goldberg, 2003
). Studies of patients with lesions to the temporoparietal junction and ventral frontal cortices suggest an involvement in the detection of visually salient events. Unilateral lesions in these brain areas result in a contralateral spatial neglect, and activity in the temporoparietal junction correlates with the recovery from spatial neglect after damage to the ventral frontal cortex (Corbetta, 2005
). In autism subjects, the cerebral cortex has been reported to be thinner in areas involved in attention and social cognition (inferior frontal cortex, inferior parietal lobe, the superior temporal gyrus; Hadjikani et al
). When looking at faces, activity in the superior temporal gyrus fails to be enhanced for eye gaze that is directed towards a target vs
gaze into the void (Pelphrey et al
Our results are consistent with an impairment in top-down modulation of attention for faces, along with preservation of bottom-up attentional processing. Future development of behavioral interventions in autism may benefit from using low-level visual cues, in addition to top-down instructions, to train eye gaze.