Frontal contributions to face processing differences in autism: evidence from fMRI of inverted face processing

Abstract

Functional neuroimaging studies of face processing deficits in autism have typically focused on visual processing regions, such as the fusiform face area (FFA), which have shown reduced activity in autism spectrum disorders (ASD), though inconsistently. We recently reported reduced activity in the inferior frontal region in ASD, implicating impaired mirror-neuron systems during face processing. In the present study, we used fMRI during a face processing task in which subjects had to match faces presented in the upright versus inverted position. Typically developing (TD) children showed a classic behavioral inversion effect, increased reaction time for inverted faces, while this effect was significantly reduced in ASD subjects. The fMRI data showed similar responses in the fusiform face area for ASD and TD children, with both groups demonstrating increased activation for inverted faces. However, the groups did differ in several brain regions implicated in social cognition, particularly prefrontal cortex and amygdala. These data suggest that the behavioral differences in processing upright versus inverted faces for TD children are related not to visual information processing but to the social significance of the stimuli. Our results are consistent with other recent studies implicating frontal and limbic dysfunction during face processing in autism.

Fig. 1

Examples of stimuli used in the upright condition (A), the inverted condition (B), and the forms condition (C). Participants were asked to choose one of the two bottom faces or forms to match the target at the top.

Fig. 2

Statistical Parametric Mapping (SPM) in the ventral cortex during upright face processing (vs. forms matching control). Left, control subjects, right, ASD. Both groups of subjects show bilateral activation in Fusiform gyrus, while only controls show activity in the amygdala. Left side of the image = left hemisphere. Foci of activations are found in Table 3.

Fig. 3

Statistical Parametric Mapping (SPM) within-groups results, inverted face task. A: (top) shows ASD subjects with unique activation in the precuneus and reduced activation in right prefrontal cortex. B: (bottom) shows TD children with prominent activation in prefrontal cortex (left) for inverted faces.

Fig. 4

Fusiform gyrus ROI values. There was a main effect of task with more fMRI activation for inverted compared with upright faces, but no differences between control and ASD children.

Fig. 5

Prefrontal cortex ROIs demonstrate a main effect for task, with more activation for inverted compared with upright faces and a group × hemisphere interaction, with greater PFC activation for control compared with ASD children in the left hemisphere; right hemisphere differences showed a nonsignificant trend in the same direction.