Deviant gaze processing in children with autism: an ERP study
Introduction
Autism is characterized by deficits in social interaction and communication, and by stereotyped, restrictive, and repetitive behavior and interests (DSM-IV, American Psychiatric Association, 1994). Among the characteristics of autism, a qualitative impairment in eye contact behavior is commonly reported in clinical and observational studies (Buitelaar, 1995; Volkmar & Mayes, 1990). Moreover, such atypical eye contact behavior can be observed from very early stage of their development (Baranek, 1999, Charman et al., 1997). Atypical fixation patterns during viewing facial stimuli in high-functioning individuals with autism were also revealed through recent studies with eye-tracking devices; their fixation time on facial features, especially the eye region, is significantly shorter than that of individuals without autism (Klin, Jones, Schultz, Volkmar, & Cohen, 2002; Pelphrey et al., 2002). These atypical patterns of eye gaze processing are assumed to be relevant to the characteristic social and communicative developmental deficits of this disorder in the current ‘theory of mind’ or ‘social brain’ hypothesis (Baron-Cohen, 1995). However, while several studies have found atypical neural activation while perceiving faces (Carver & Dawson, 2002; Pierce, Miller, Ambrose, Allen, & Courchesne, 2001; Schultz et al., 2000, but see also Hadjikhani et al., 2004), identifying faces (Dawson et al., 2002), and processing facial emotion (Critchley et al., 2000), to date very little is known about the neural bases of eye gaze processing in individuals with autism.
Several previous ERP or MEG studies have investigated the effect of gaze direction of perceived facial stimuli in typically developed population, but results were inconsistent. Some have found that laterally averted gaze elicited larger occipito-temporal negativity (N170; Bentin, Allison, Puce, Perez, & McCarthy, 1996; Eimer, 2000; Sagiv & Bentin, 1999) than did direct gaze (Puce, Smith, & Allison, 2000; Watanabe, Kakigi, & Puce, 2001; Watanabe, Miki, & Kakigi, 2002) in adult participants. Farroni, Csibra, Simion, and Johnson (2002), in contrast, recorded ERPs from infants and found larger occipital negativity (infant N170) for direct gaze than for averted gaze. Others, however, failed to find differences between ERPs or event-related electro-magnetic fields (ERFs) in response to direct gaze or laterally averted gaze (Taylor, George, & Ducorps, 2001; Taylor, Itier, Allison, & Edmonds, 2001), although both direct and averted gaze elicited larger N170 than upward gaze and closed eyes.
To the best of authors’ knowledge, there is only one previous study, which investigated the neural correlates of gaze perception in individuals with autism with ERP measurement (Grice et al., in press). Grice et al. (in press) recorded high-density ERPs from young children (3.5–7 years old) with autism while they are passively viewing faces with varying eye gaze directions, and found that perceived direct gaze elicited larger occipito-parietal negativity than averted gaze, just like 4-month-old infants (Ferroni, Csibra, Simion, & Johnson, 2002) but ERPs of age-matched control children or those of non-autistic adults were not sensitive to the perceived gaze direction. Their findings, which may indicate the delayed development of gaze processing in autism, are intriguing. But it is surprising they did not find any gaze-direction effect in non-autistic participants, considering the sensitivity to the perceived eye gaze direction often found in other behavioral studies (e.g., Senju & Hasegawa, in press; von Grünau & Anston, 1995). It might be due to the use of passive viewing paradigm, rather than active detection or discrimination tasks usually used in behavioral studies. Thus, neural correlates of active, rather than passive, processing of gaze direction need to be investigated in individuals with and without autism.
This study explored the electrophysiological or neurocognitive basis of active gaze processing, especially the active detection of direct gaze, by concurrent measurement of ERPs in individuals with and without autism. Because atypical orienting to social stimuli in individuals with autism has been reported (Ceponiene et al., 2003; Dawson, Meltzoff, Osterling, Rinaldi, & Brown, 1998), it was predicted that ERPs corresponding to active detection of change in gaze direction are deviant in individuals with autism.
During the ERP recording, stimuli with various eye gaze directions were presented according to the visual oddball paradigm, which involves presenting a series of frequent stimuli into which rare stimuli are inserted. This study used two kinds of rare stimuli: one in a direct gaze condition and the other in an averted gaze condition. The participants were instructed to respond to one of the two rare stimuli, while ignoring the other. Thus, participants in this study were required to actively detect gaze direction, rather than passively as in previous studies (Farroni et al., 2002, Puce et al., 2000; Taylor, George, et al., 2001; Taylor, Itier, et al., 2001; Watanabe et al., 2001, Watanabe et al., 2002). Although gaze discrimination has never been examined in an oddball paradigm, it seems a promising way to explore the electrophysiological activities corresponding to the detection of changeable aspects of face such as gaze direction and facial expression. For example, the visual oddball paradigm was used in a previous study to record the ERPs while participants were discriminating facial expressions and found that the occipital negative component (N2) in the difference wave, accompanied by a frontal positive component (P3a), reflects the behavioral performance of the discrimination of facial expressions (Campanella et al., 2002).
Section snippets
Participants
Thirteen children with autism (all males; mean age 12:1 years, range 9:10–14:11 years) and 15 age-matched typically developing children (13 males and 2 females; mean age 12:1 years, range 9:5–14:10 years) participated in this study. All of the children were students or graduates of a primary school that is attended by both autistic and typically developing children. Informed consent was obtained from each child, his or her parents, and the school director, and the study was first approved by
Behavioral performance
Behavioral performance has been presented elsewhere (Senju, Yaguchi, Tojo, & Hasegawa, 2003). Results with typically developing children replicated previous reports, in that stimuli with direct gaze were more accurately detected than those with averted gaze (d′ = 2.62 for direct gaze and 1.47 for averted gaze, F (1, 26) = 13.91, p < .01). Results with children with autism, however, found no effect of gaze direction on their performance (d′ = 1.10 for direct gaze and 0.93 for averted gaze, F < 1, p > .1).
Discussion
This study is the first to investigate the ERP correlates of active detection of gaze direction in children with and without autism, and the second to report the ERP correlates of gaze processing in children with autism. The effect of a change in eye direction was most prominent in the enhancement of the occipito-temporal negativity (N2). In typically developed children, N2 was lateralized to the right hemisphere, and N2 amplitude was greater when detecting a direct gaze as compared to an
Acknowledgements
We appreciate the support and cooperation of all of the participants and their parents, and the teachers and staff at The National Institute of Special Education. AS was supported by a Grant-in-Aid for JSPS Fellows No. 14-08419 by the Ministry of Education, Science, Sports, and Culture, Japan.
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