Distinct face-processing strategies in parents of autistic children

Abstract

In his original description of autism, Kanner [1] noted that the parents of autistic children often exhibited unusual social behavior themselves, consistent with what we now know about the high heritability of autism [2]. We investigated this so-called Broad Autism Phenotype in the parents of children with autism, who themselves did not receive a diagnosis of any psychiatric illness. Building on recent quantifications of social cognition in autism [3], we investigated face processing by using the "bubbles" method [4] to measure how viewers make use of information from specific facial features in order to judge emotions. Parents of autistic children who were assessed as socially aloof (N = 15), a key component of the phenotype [5], showed a remarkable reduction in processing the eye region in faces, together with enhanced processing of the mouth, compared to a control group of parents of neurotypical children (N = 20), as well as to nonaloof parents of autistic children (N = 27, whose pattern of face processing was intermediate). The pattern of face processing seen in the Broad Autism Phenotype showed striking similarities to that previously reported to occur in autism [3] and for the first time provides a window into the endophenotype that may result from a subset of the genes that contribute to social cognition.

Figure 1

Construction of the stimuli. On the far left is one of the base images we began with (an expression of happiness or of fear from the Pictures of Facial Affect [24]). The base face was decomposed and randomly filtered so as to reveal only small parts of it. The amount of the face revealed was adjusted interactively so as to keep performance accuracy relatively stable throughout the experiment, except for the first few trials. A sample stimulus image is shown on the far lower right.

Figure 2

Classification images showing the use of facial information. A: Controls (parents of a child without autism). B: Difference between Controls and BAP+ (the image shows the region of the face used more by controls). C: Difference between Controls and BAP−. All classification images are based on the accuracy with which subjects performed the task, and are statistically thresholded at P<0.001 (corrected). The regions of the face that are visible in the images thus correlate with performance accuracy at P<0.001.

Figure 3

Classification difference image between BAP groups and between BAP and autism. A: Information used more by BAP+ than by BAP−. B: Information used more by BAP− than by BAP+. For comparison purposes, panels C and D reproduce prior published findings by us, using the identical task and analysis, in people with autism. C: Information used more by autism subjects than by controls. D: Information used more by controls than by autism subjects. Panels C and D from [3]. E: Information used more by BAP+ than autism subjects. F: Information used more by BAP− than autism subjects. The converse classification images of autism-BAP revealed no regions where autism subjects used more information than BAP subjects, for either of the two BAP groups.

Figure 4

Numerical quantification of the use of facial information. The three bar graph categories plot the use of information from the right eye, left eye, and mouth region of the face. The y-axis plots the structural similarity metric (SSIM; see Methods), a measure of the degree to which information was used from a specific region of interest on the face. White bars: Controls. Light gray bars: BAP−. Dark Gray bars: BAP+. Means and SEM are shown for each subject group.