Abstract
McPartland, J. C., Wu, J., Bailey, C. A., Mayes, L. C., Schultz, R. T., & Klin, A. (2011). Atypical neural specialization for social percepts in autism spectrum disorder. Social Neuroscience, 6, 436–451.
The ability to efficiently perceive the human face is a crucial and early-emerging social ability. Specialized processing for faces emerges in the first days of life and is enhanced by developmental experience. We develop specific processes to differentiate between faces that rely as much on the configuration (the structural relationship between individual features on the face) as the details of individual face features, such as the eyes, nose, and mouth. Most people can still recognize an image of a face that has been rotated upside down, and they still do even when altered in rather major ways. Look at these two photos, then turn the page upside down.
You were probably surprised to discover that the eyes and mouth were inverted in the upside-down photo. The face in which the eyes and the mouth were rotated 180 degrees looks grotesque—but only if we see them the right side up. Upside down, the differences between a normal face and altered face are hardly recognizable. Most persons fail to notice alterations in upside-down faces. Only when we view the face right side up do the upside-down facial features strike us. This does not bother us all that much when the faces are upside down. In fact, we often do not even notice it, and the expression looks pretty close to the normal face. The illusion is often called the Thatcher illusion because it was first demonstrated with a photo of Margaret Thatcher. Because face perception is a well-studied social behavior, it has been employed as an avenue to understand social development in autism spectrum disorder (ASD). In ASD, decreased attention to human faces is evident by 6 to 12 months, and abnormalities in face perception and recognition have been observed throughout the life span (Hobson, Ouston, & Lee, 1988; Klin et al., 1999; Wolf et al., 2008). Individuals with ASD often exhibit abnormal viewing patterns to faces.
Studies of electrophysiological markers of face perception suggest decreased sensitivity to face inversion in individuals with ASD, as well as first-degree relatives (Dawson, Webb, Wijsman, et al., 2005; McCleery, Akshoomoff, Dobkins, & Carver, 2009), although some studies suggest at least partially preserved face perception in some subgroups of individuals with ASD (Webb et al., 2010). The social motivation hypothesis (Dawson, Webb, & McPartland, 2005) posits that, due to abnormalities in social drive very early in childhood, children with ASD do not attend to faces during sensitive developmental periods. Consequently, people with ASD fail to develop typical proficiency in face processing and associated patterns of behavioral and brain specialization. Because the social motivation hypothesis implicates reduced social drive as the basis for face perception difficulties (rather than specific dysfunction of brain regions subserving face perception), it presumes that individuals with ASD, given appropriate exposure to and interest in a stimulus class, should develop both behavioral and brain specialization (Sasson, 2006).
The Study
In this study, electrophysiological and behavioral methods were applied to compare neural specialization for faces and letters in individuals with ASD. Experiments contrasted neural response to faces versus houses, faces versus inverted faces, and letters versus pseudoletters, and compared these parameters to behavioral measures assessing proficiency in face recognition, and letter and word perception.
This study hypothesized that individuals with ASD would exhibit impaired face recognition and delayed brain response to faces in the right hemisphere, as well as decreased sensitivity to face inversion. In keeping with the notion that these atypicalities reflect developmental sequelae of social deficits, it was predicted that similar anomalies would not be observed for nonsocial stimuli; individuals with ASD would show typical skills in terms of letter and word perception, and comparably enhanced response to letter stimuli with respect to unfamiliar pseudoletters.
Participants
Two groups participated in the study: individuals with ASD and healthy individuals with typical development. All had IQs of 80 or higher. All individuals with ASD had a preexisting diagnosis confirmed with standard diagnostic assessments for research and clinical diagnosis based on the Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev. [DSM-IV-TR]; American Psychiatric Association, 2000) criteria by an expert clinician.
Stimuli
Participants watched stimuli on a computer. The first set consisted of grayscale, digitized images of neutral faces, houses, and inverted faces, all displayed from a direct frontal perspective. The second set included letters and pseudoletters. To maximally engage attention to individual stimuli, participants were asked to press a button whenever a stimulus repeated. Because this behavioral task was confounded with face recognition, attention to task was monitored in real time through closed circuit video, enabling pausing of data collection and redirection of attention-to-stimulus presentation if needed. Event-related potentials (ERP) were recorded continuously throughout each stimulus-presentation trial. Data were averaged for each subject by stimulus type across trials.
Behavioral Procedures
Face perception
Face recognition was measured with the Benton Facial Recognition Test (Bentin, Deouell, & Soroker, 1999). Participants viewed a grayscale image of a face and specified one or three matches from an array of six faces, varying in shadowing and orientation.
Letter perception
The Letter-Word Identification and Word Attack subtests of the Woodcock-Johnson Tests of Achievement–Third Edition (Woodcock, McGrew, & Mather, 2001) required the participant to read words aloud, with the former using genuine English words and the latter using novel words.
Results
Individuals with autism displayed slowed face processing and decreased sensitivity to face inversion; however, they showed comparable brain responses to houses and letters, which were associated with behavioral performance in both groups. This suggests that individuals with autism display atypical neural specialization for social information but intact specialization for nonsocial information.
Individuals with ASD showed reduced hemispheric specialization compared with typical counterparts, who showed a marked right lateralization effect for faces.
On a behavioral measure of face recognition, individuals with ASD performed significantly worse than typically developing counterparts.
Face-recognition performance was associated with processing efficiency for faces; in both groups, individuals with better face-recognition abilities displayed faster ERPs.
Among individuals with ASD, increased inversion effects, as reflected by a stronger response to inverted faces, were associated with better face-recognition performance.
These findings support the hypothesis of specific dysfunction in social brain systems. This decreased efficiency of processing, insensitivity to inversion, and impaired face recognition are hypothesized to reflect underdeveloped specialization for faces, a downstream effect of decreased attention to faces during childhood secondary to reduced social drive from infancy (Dawson, Webb, Wijsman, et al., 2005). The researchers interpret the observed correlation between neural response to face inversion and recognition performance as indicating that development of expertise and processing proficiency are related. This interpretation of the study results has clinical implications for the detection and treatment of ASD. The authors note that when children are appropriately engaged and attuned to information, for example, letters, typical patterns of neural specialization develop. They hypothesize that given the right input—attention to social information—the brain of the person with ASD could begin to function like that of typical peers. This provides a rationale for interventions such as Floortime (Greenspan & Wieder, 1998) and Relationship Development Intervention.