Abnormal activation of the social brain during face perception in autism

Abstract

ASD involves a fundamental impairment in processing social-communicative information from faces. Several recent studies have challenged earlier findings that individuals with autism spectrum disorder (ASD) have no activation of the fusiform gyrus (fusiform face area, FFA) when viewing faces. In this study, we examined activation to faces in the broader network of face-processing modules that comprise what is known as the social brain. Using 3T functional resonance imaging, we measured BOLD signal changes in 10 ASD subjects and 7 healthy controls passively viewing nonemotional faces. We replicated our original findings of significant activation of face identity-processing areas (FFA and inferior occipital gyrus, IOG) in ASD. However, in addition, we identified hypoactivation in a more widely distributed network of brain areas involved in face processing [including the right amygdala, inferior frontal cortex (IFC), superior temporal sulcus (STS), and face-related somatosensory and premotor cortex]. In ASD, we found functional correlations between a subgroup of areas in the social brain that belong to the mirror neuron system (IFC, STS) and other face-processing areas. The severity of the social symptoms measured by the Autism Diagnostic Observation Schedule was correlated with the right IFC cortical thickness and with functional activation in that area. When viewing faces, adults with ASD show atypical patterns of activation in regions forming the broader face-processing network and social brain, outside the core FFA and IOG regions. These patterns suggest that areas belonging to the mirror neuron system are involved in the face-processing disturbances in ASD.

Figure 1

Ventral view of a 3D reconstruction of a brain. A shows the location of the IOG (orange), the FG (red), and the ITG (blue). B and C show activation for faces in a random‐effect average for ASD subjects in the present study (B) and in our previous study (C). FG: Fusiform Gyrus; ITG: Inferior Temporal Gyrus.

Figure 2

Location of random‐effect average activation for faces in the right hemisphere in normal controls (A and B) and in ASD (C and D). In A and C, the hemispheres have been inflated in order to show the sulci (darker shade of gray) and the gyri (lighter shade of gray). In the right hemisphere of the NC group, activation can be seen in the lateral superior and inferior occipital cortex. In addition, activation is seen in the STS, as well as in S1 and PM, at the level of face representation, and in IFC. These areas were weakly or not activated in the left hemisphere in NC group, and in either hemisphere in the ASD group. The areas of “missing” (S1, PM) or diminished (IFC, STS) activation in the ASD group correspond to areas where we previously described a thinning of the cortex in another group of subjects, shown in E [Hadjikhani et al., 2006].

Figure 3

BOLD signal change in areas of the face‐processing network in subjects with ASD and healthy controls. A shows activation in the FFA and IOG, and B in the S1, PM, STS, IRF, and amygdala. Note the difference in scale between panels. FFA and IOG are significantly activated in both groups (P < 0.0001). There is no significant difference between ASD and NC in FFA (rh: t = 1.5, df = 11, P = 0.16; lh: t = 0.9, df = 10, P = 0.41) or in IOG (rh: t = 0.4, df = 8, P = 0.72; lh: t = 0.4, df = 10, P = 0.74). There is a significant activation for faces in the NC group in right S1 (t = 3.5, df = 782, P < 0.001), right PM (t = 6.9, df = 782, P < 0.0001), right STS (t = 3.8, df = 782, P < 0.001), right IFC (t = 6.2, df = 782, P < 0.0001), right amygdala (t = 2.1, df = 782, P < 0.05), and left amygdala (t = 5.4, df = 782, P < 0.0001). In the ASD group, significant activation is only found in IFC (t = 3.1; df = 782; P < 0.01) and in the left amygdala (t = 3.1; df = 782; P < 0.01). A one‐tailed Mann‐Whitney test between groups showed close to significant difference between groups in S1 (P = 0.082) and significant difference in PM (P = 0.036), STS (P = 0.009), IFC (P = 0.036), and right amygdala (P = 0.049).

Figure 4

Correlation between the severity of the social symptoms as measured by the ADOS and the cortical thickness in the IFC (r² = 0.72; P = 0.02).