Social perception in autism spectrum disorders: impaired category selectivity for dynamic but not static images in ventral temporal cortex

Abstract

Studies of autism spectrum disorders (ASDs) reveal dysfunction in the neural systems mediating object processing (particularly faces) and social cognition, but few investigations have systematically assessed the specificity of the dysfunction. We compared cortical responses in typically developing adolescents and those with ASD to stimuli from distinct conceptual domains known to elicit category-related activity in separate neural systems. In Experiment 1, subjects made category decisions to photographs, videos, and point-light displays of people and tools. In Experiment 2, subjects interpreted displays of simple, geometric shapes in motion depicting social or mechanical interactions. In both experiments, we found a selective deficit in the ASD subjects for dynamic social stimuli (videos and point-light displays of people, moving geometric shapes), but not static images, in the functionally localized lateral region of the right fusiform gyrus, including the fusiform face area. In contrast, no group differences were found in response to either static images or dynamic stimuli in other brain regions associated with face and social processing (e.g. posterior superior temporal sulcus, amygdala), suggesting disordered connectivity between these regions and the fusiform gyrus in ASD. This possibility was confirmed by functional connectivity analysis.

Keywords: Asperger's syndrome; MRI/fMRI; autism; fusiform gyrus; social cognition.

Figure 1.

Sample stimuli from Experiments 1 and 2. (A) Sample frames of dynamic full color video clips and point-light depictions of humans and tools in Experiment 1. During scanning, participants indicated if each stimulus was a human or a tool. (B) Selected frames from a social vignette that elicited the concept of sharing (see Martin and Weisberg, 2003 for details). (C) Photographs of faces, tools, and their scrambled counterparts from the localizer task in Experiment 2.

Figure 2.

Peak coordinates for individual subjects in the right lateral fusiform region that showed a heightened response to images of people (Experiment 1) or faces (Experiment 2), relative to tools. The location of each individual's cluster maximum is plotted on a drawing of the ventral surface of the right hemisphere.

Figure 3.

Experiment 1: Responses to video and point-light stimuli in the independently localized lateral region of the right fusiform gyrus. (A) The activation map for the main effect of Category from the Group × Category ANOVA on static photographs only (people vs. tools, q < 0.05) is superimposed on a template coronal brain slice. Regions in red were more active for viewing static images of people than static tools and regions in blue showed the opposite preference. The histogram below the coronal slice shows the average hemodynamic response to static images of people and tools for each group across all voxels within the right lateral fusiform ROI identified by the static image localizer (circled region). (B) Histogram shows group-averaged hemodynamic responses to dynamic depictions of people and tools within the independently localized right fusiform region. Asterisks indicate a Category effect (P < 0.001) for the dynamic stimuli. Error bars in all figures indicate the standard error of the mean.

Figure 4.

Experiment 1: Responses to static, video, and point-light stimuli in the right pSTS. (A) As in Figure 3, the activation map for the main effect of Category (people vs. tools, thresholded at q < 10⁻⁴ for display purposes) from the Group × Category ANOVA on static stimuli shows activation in the pSTS (red circle). Increased activation in the right lateral fusiform gyrus for people and in the left medial fusiform region for tools is also visible. Below, the histogram shows the average hemodynamic response to images of static people and tools for each group across voxels within the pSTS region (circled) identified by the static images localizer. (B) Histogram shows group-averaged hemodynamic responses for each dynamic stimulus format extracted from the right pSTS cluster identified by the static localizer. Asterisks indicate a Category effect for dynamic stimuli (P < 0.001).

Figure 5.

Experiment 2: Responses to the localizer and vignette tasks in the right amygdala and right pSTS. (A) Activation maps show the main effect of Category (faces vs. tools, q < 0.05) from the face localizer Group × Category ANOVA, in the right amygdala (circled, top) and right pSTS (circled, bottom). Regions in red were more active for viewing photographs of faces than tools and regions in blue showed the opposite preference. Histograms in (A) show group-averaged hemodynamic responses to faces and tools within the circled amygdala (top) and pSTS (bottom) regions. (B) Histograms of group-averaged hemodynamic responses to the vignette task within the right amygdala (top) and pSTS (bottom) regions identified by the localizer task. Asterisks indicate a significant effect of Vignette Type (P < 0.001 in pSTS; P < 0.05 in amygdala). Crosshatch indicates a trend in the same direction (social > mechanical, P = 0.066) for the ASD group.

Figure 6.

Experiment 2: Responses to the face localizer and vignette tasks in the right lateral fusiform gyrus. (A) As in Figure 5, activations show the main effect of Category (faces vs. tools, q < 0.05) for the localizer Group × Category ANOVA. Circle indicates the FFA ROI in the right lateral fusiform gyrus, shown on a coronal slice. The histogram below shows the group-averaged hemodynamic responses to faces and tools during the localizer task within the circled region. (B) Group-averaged hemodynamic responses during the vignette task extracted from the FFA region identified by the localizer task. Asterisk indicates a significant effect of Vignette Type (P < 0.05).