Perception of dynamic changes in facial affect and identity in autism

Abstract

Despite elegant behavioral descriptions of abnormalities for processing emotional facial expressions and biological motion in autism, identification of the neural mechanisms underlying these abnormalities remains a critical and largely unmet challenge. We compared brain activity with dynamic and static facial expressions in participants with and without high-functioning autism using event-related functional magnetic resonance imaging (fMRI) and three classes of face stimuli-emotion morphs (fearful and angry), identity morphs and static images (fearful, angry and neutral). We observed reduced activity in the amygdala (AMY) and fusiform gyrus (FFG) to dynamic emotional expressions in people with autism. There was also a lack of modulation by dynamic compared with static emotional expressions of social brain regions including the AMY, posterior superior temporal sulcus (STS) region and FFG. We observed equivalent emotion and identity morph-evoked activity in participants with and without autism in a region corresponding to the expected location of the more generally motion-sensitive area MT or V5. We conclude that dysfunctions in key components of the human face processing system including the AMY, FFG and posterior STS region are present in individuals with high-functioning autism, and this dysfunction might contribute to the deficits in processing emotional facial expressions.

Keywords: amygdala; autism; emotion; fMRI; face processing.

Fig. 1

Depiction of experimental paradigm. Examples of static angry and neutral expressions and four frames of a fear morph are depicted. ISI, interstimulus interval.

Fig. 2

Results from a random-effects analysis comparing participants with autism with participants without autism. (A) Red-to-yellow colormap indicates regions of significant neurotypical > autism activity evoked during observation of emotional morphs. The map is thresholded at a voxelwise uncorrected P < 0.05 (two-tailed) and a spatial extent of four contiguous voxels. (B) Time courses of the average BOLD signal change from the right hemisphere AMY region of neurotypical > autism activation. Bars indicate s.e.m.

Fig. 3

Results from a random-effects analysis contrasting dynamic and static emotional expressions. (A, B), The red-to-yellow activation maps indicate regions where the average response at expected peak amplitude to emotion morphs was greater than the average response to static emotions in participants without autism (A) and participants with autism (B) Maps are thresholded at a voxelwise uncorrected P < 0.05 (two-tailed) and a spatial extent of four contiguous voxels.

Fig. 4

Bar graphs reflect average percent signal change and standard error by condition and group at expected peak (6–9 s post-stimulus onset) for the right hemisphere (A) amygdala, (B) fusiform gyrus, (C) superior temporal sulcus and (D) MT/V5. The error bars indicate s.e.ms.