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Atypical Face Gaze in Autism
CHERYL TREPAGNIER, Ph.D., MARC M. SEBRECHTS, Ph.D., and REBECCA PETERSON, M.A.
ABSTRACT An eye-tracking study of face and object recognition was conducted to clarify the character of face gaze in autistic spectrum disorders. Experimental participants were a group of individuals diagnosed with Asperger’s disorder or high-functioning autistic disorder according to their medical records and confirmed by the Autism Diagnostic Interview–Revised (ADI-R). Controls were selected on the basis of age, gender, and educational level to be comparable to the experimental group. In order to maintain attentional focus, stereoscopic images were presented in a virtual reality (VR) headset in which the eye-tracking system was installed. Preliminary analyses show impairment in face recognition, in contrast with equivalent and even superior performance in object recognition among participants with autism-related diagnoses, relative to controls. Experimental participants displayed less fixation on the central face than did control-group participants. The findings, within the limitations of the small number of subjects and technical difficulties encountered in utilizing the helmet-mounted display, suggest an impairment in face processing on the part of the individuals in the experimental group. This is consistent with the hypothesis of disruption in the first months of life, a period that may be critical to typical social and cognitive development, and has important implications for selection of appropriate targets of intervention. INTRODUCTION pacity for social connection,2 impaired ability to shift attention,3 inability to represent and manipulate complex information,4 inability to conceive of others’ mental states,5 an impairment of central coherence, the ability to extract organizing principles,6 and more multifaceted cognitive deficits.7 Research has increasingly pointed to reductions in the connectivity among brain regions that typically work as integrated systems.8–10 It is important to note, however, that functional and structural brain differences can reflect as well as cause atypical behavior.11 Gaze-disruption hypothesis A hypothesis proposed by the first author12 suggests that disruption of social attention dur-
is a behaviorally defined condition, diagnosed by severe impairments in social and communicative domains, and the presence of repetitive behaviors and/or restrictive, narrow interests.1 Asperger’s disorder, considered a less severe variant of autistic disorder, is similar to high-functioning autistic disorder, such that there remain unresolved questions about whether they should be treated as distinct diagnostic categories. For convenience, autistic disorder and Asperger’s disorder will be referred to here as autistic spectrum disorder, or simply, autism. Accounts of the core psychobiological deficit in autism have included impairment in the caUTISTIC DISORDER
Department of Psychology, The Catholic University of America, Washington, D.C.
214 TREPAGNIER ET AL. Each image was presented for 4 sec. at .15–17 Children with autistic disorder did not look at faces to discern intention. however. and modify their own actions and responses accordingly. Face attention and interpretation By 1 year of age. with width determined by the outer corners of the eyes). ing the early months of life due to underlying neuropsychiatric disorder may be sufficient to bring about autistic development.16 and adults with Asperger’s were more likely to look at someone’s face when they themselves were talking to that person. Recognition stimuli remained present until the participant responded. The acquisition images of the third and fourth blocks included inverted as well as upright images.20 In a pilot study using eye-tracking during a face recognition task. a high-functioning young adult with autism spent much less time than controls looking at eyes and the central face. Participants were asked to indicate by saying “yes” or “no” whether or not they had seen the image before. participants were shown four faces and four objects. relative to controls. Participants were asked to look at and remember a series of images of faces and objects presented stereoscopically in a virtual reality (VR) head-mounted display equipped with an ISCAN eye-tracking system.14 In the presence of intact vision. In each acquisition set. 21 This study of face and object recognition extends those preliminary findings and makes two predictions: that individuals with autistic spectrum disorders would be impaired in face recognition. children and many adolescents and adults with autism do not. Four blocks of trials were presented sequentially. experience that is critical to normal social. MATERIALS AND METHODS Participants were individuals with autism spectrum diagnoses according to their medical records and confirmed by the Autism Diagnostic Interview–Revised (ADI-R). Point of regard (POR) was sampled at 60 Hz. cognitive. including one individual with a graduate degree and a successful professional career. and a group of controls of similar age. all experimental participants were very high-functioning. rather than looking at someone who was speaking to them. and emotional development.18 A recent study of children with autism seen at the Yale Child Study Center over a period of several years found that all were impaired in face recognition relative to controls. and a videotaped recording was acquired. Each recognition set included eight previously presented images and eight foils. each with eight acquisition trials (images to learn) followed by 16 recognition trials (images to evaluate as already seen or not). Verbal intelligence and nonverbal intelligence were not controlled for. There is increasing evidence of elevated incidence of neuropsychiatric disorder of the anxiety disorders/depressive disorders type among individuals with autism and their first-degree relatives (prior to the birth of the disabled individual). Very early onset or precursor symptoms may disrupt infant social interaction by impairing the infant’s ability to tolerate the overwhelming excitement of social stimuli.22 carried out by the first author. this was not the case for individuals with autism carrying out the same tasks.19 In functional imaging studies. and successful students and college-bound adolescents. whose vision is restored by surgery even as early as age 2 months.13 Individuals born blind because of cataracts. the fusiform gyrus of controls was activated during performance of face-recognition tasks. with a 4-sec interstimulus interval. and then to view subsequently a longer series of images and indicate which they had already seen. but not in object recognition or recognition of inverted faces (in which configurational information is not preserved). have a persistent impairment in configurational face processing. impaired configurational face processing may be the marker for a failure to engage in very early social interaction. typically developing infants routinely monitor their adults’ facial expressions. and that persons with autistic spectrum disorder would spend less of their time than controls fixating on the central face region (from the eyebrows down to and including the mouth. In contrast.
not significant. Where differences reached significance.05.s. Data are reported here from five individuals with autism spectrum disorder (one female.s. au- . These were individuals who responded to a call for subjects disturbed via the Autism Society of America chapter newsletters and local physicians treating individuals with autism. Since difficulty in shifting attention is expected to the autism population.s. points to a face-recognition impairment. recognition accuracy predictions were confirmed (Table 1). were not helpful). resulting from technical difficulties in managing the buffer size of the Onyx workstation.4 years). technical problems in the data-acquisition program (some of the data from two participants). straight blonde hair (i. and six controls (two females. Fixation locations were examined with respect to predefined regions of the face stimuli. Other candidates and some subsets of the data from the participants were excluded for the following reasons: failure to meet criterion for autism on the social subscale of the ADI-R (one participant). The superior performance of the autism participants with objects.1. The same comparison for the initial second out of the four did not reach significance. n.05. C > Aa C > Aa n.5 years).s. one-tailed).. autistic group. RESULTS Participants’ initial fixations occurred in the general area at which they had been looking as the image appeared. Results for allocation of gaze to the central face region for 4 sec of exposure (Table 2) are consistent with predictions. and skin color.3 data visualizations for all files (up to 96 per participant) were reviewed to determine start time of the first fixation after shift.s. Objects n.ATYPICAL FACE GAZE IN AUTISM 215 TABLE 1.e. C > Ab n. Examination revealed cases of artifact appended to the beginning of several files. Foils for objects such as a stapler or a chair were another stapler and another chair. they were in the expected direction. DISCUSSION When between-group differences in recognition accuracy reached significance. showing a cursor representing the PORs superimposed on a two-dimensional image of the stimulus. A. mean age 18. < 0. along with their reduced success with faces. C. tism participants were slower overall than controls to make the shift from their starting point to active examination of the image (p < 0. Verifiable artifacts were removed. their relatively superior performance in recognizing objects does not support an underlying visual perceptual deficit or short-term visual memory impairment. RECOGNITION ACCURACY Faces Block 1 Block 2 Block 3 Block 4 All upright All inverted ap bp approximately 30 frames/sec. attesting to the experimental group’s impairment in face recognition.. for a target female with light skin and long. possibly an impairment in processing configurational information. Temporal and spatial thresholds were set to define fixation as a gaze of at least 100 msec in length. A > Ca A > Ca n. mean age 19. Individuals with severe disorder self-excluded when they or their parents were informed that the study involved wearing a headset that covered much of the front of the face. within approximately 1 degree of visual angle of the mean location of the points. the most salient features. A > Cb n.s. < 0. with the difference residing in features of color or detail. there was a foil who was also a light-complexioned female with long. n. control group. At the same time. familiarity with one or more of the people whose images were used (exclusion of three individuals. error (some of the data from one participant). exclusion of half the data from one participant). and age (one participant). Further constraints were introduced into the fixationdetection algorithm to reduce the effects of spurious points and dropped tracking. such as hair length and color. Foils for faces were selected to resemble the corresponding target images. straight blonde hair.s. for example. and as expected. one-tailed.
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