Journal of Experimental Child Psychology 109 (2011) 430–444

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Journal of Experimental ChildPsychology

journal homepage: www.elsevier .com/locate/ jecp

Early processing of emotional faces in childrenwith autism: An event-related potential study

Magali Batty a,⇑, Emilie Meaux a, Kerstin Wittemeyer b, Bernadette Rogé c,Margot J. Taylor d

a UMRS Inserm U930, CNRS ERL 3106, Université François Rabelais de Tours, CHRU de Tours, 37044 Tours, Franceb School of Education, University of Birmingham, Birmingham B15 2TT, UKc Unité de Recherche Interdisciplinaire Octogone (EA 4156), Centre d’Etudes et de Recherche en Psychopathologie,Université Toulouse II Le Mirail, 31058 Toulouse, Franced Diagnostic Imaging and Research Institute, Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada M5G 1X8

a r t i c l e i n f o

Article history:Received 2 September 2010Revised 3 February 2011Available online 1 April 2011

Keywords:Emotional facesAutismDevelopmentEvent-related potentials (ERPs)Visual processingAutism spectrum disorders (ASDs)

0022-0965/$ - see front matter � 2011 Elsevier Indoi:10.1016/j.jecp.2011.02.001

⇑ Corresponding author. Fax: +33 2 47 47 38 46.E-mail address: m.batty@chu-tours.fr (M. Batty

a b s t r a c t

Social deficits are one of the most striking manifestations of autismspectrum disorders (ASDs). Among these social deficits, the recog-nition and understanding of emotional facial expressions has beenwidely reported to be affected in ASDs. We investigated emotionalface processing in children with and without autism using event-related potentials (ERPs). High-functioning children with autism(n = 15, mean age = 10.5 ± 3.3 years) completed an implicit emo-tional task while visual ERPs were recorded. Two groups of typi-cally developing children (chronological age-matched and verbalequivalent age-matched [both ns = 15, mean age = 7.7 ± 3.8 years])also participated in this study. The early ERP responses to faces (P1and N170) were delayed, and the P1 was smaller in children withautism than in typically developing children of the same chrono-logical age, revealing that the first stages of emotional face process-ing are affected in autism. However, when matched by verbalequivalent age, only P1 amplitude remained affected in autism.Our results suggest that the emotional and facial processing diffi-culties in autism could start from atypicalities in visual perceptualprocesses involving rapid feedback to primary visual areas andsubsequent holistic processing.

� 2011 Elsevier Inc. All rights reserved.

c. All rights reserved.

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Introduction

The popular image of autism is still one of a person who is not interested in others, communicatespoorly, engages in stereotypical behaviors, and does not express emotions. However, people with aut-ism can demonstrate enthusiasm, motivation, and excitement or strong dissatisfaction. The problem isthat often these emotions are not understood by people they encounter because they are not adaptedto the social norms. The abnormal modulation of emotion and expression seems to be more charac-teristic of autism than does the absence of emotion.

The classic work of Kanner (1943) described emotional abnormalities in autism, and since thenresearchers have published numerous studies confirming the emotional deficits in this population(Adolphs, Sears, & Piven, 2001; Baron-Cohen, Tager-Flusberg, & Cohen, 1993; Celani, Battacchi, &Arcidiacono, 1999; Dawson, Meltzoff, Osterling, Rinaldi, & Brown, 1998; Deruelle, Monin, Gepner,Tardif, & Rondan, 2001; Gepner, Deruelle, & Grynfeltt, 2001; Hobson, Ouston, & Lee, 1988; Teunisse& De Gelder, 1994; Weeks & Hobson, 1987). Understanding the affective state of others is crucialfor the appropriate adaptation to social situations and the development of relationships with others.People with autism often fail to understand the mental state of others, and this can cause them to besocially inappropriate and constitute a real impairment in their everyday lives. This deficit issignificant enough to be part of the diagnostic criteria defined by the DSM-IV (Diagnostic and StatisticalManual of Mental Disorders–fourth edition) (American Psychological Association [APA], 1994).

Although most reports have focused on difficulties in understanding facial expressions, individualswith autism have also been found to display fewer expressions than matched controls (Snow, Hertzig,& Shapiro, 1987), and they also seem to be relatively unaffected by other people’s expressions of feel-ings (Sigman, Kasari, Kwon, & Yirmiya, 1992). Furthermore, a deficit in matching visual and/or audi-tory stimuli was found in autism only when the stimuli were emotional (Baron-Cohen, Wheelwright,Hill, Raste & Plumb, 2001; Celani et al., 1999; Hobson, 1986). Baron-Cohen and colleagues showed thatparticipants with autism had poor discrimination of emotions expressed by the eyes, a more subtlebut important aspect of facial emotions (for a review, see Itier & Batty, 2009). Baron-Cohen (1995)used the word ‘‘mindblindness’’ for explaining difficulties in making sense and predicting others’ feel-ings, thoughts, and behaviors. However, even low-functioning children with autism show expectan-cies concerning the social behaviors of close family members or caregivers. A study using anadaptation of the still face paradigm revealed that children with autism were positively expressivewhen expected contacts appeared and negatively expressive when the contacts did not occur(Escalona, Field, Nadel, & Lundy, 2002). Thus, despite a deficit in emotional processing, the data donot reveal a total insensitivity to social and emotional cues in autism (see also Lacroix, Guidetti,Rogé, & Reilly, 2009).

The perception of emotional facial expressions involves an extensive neural network that includesposterior and temporal cortical areas, such as the fusiform gyri and superior temporal sulci (STS), aswell as the amygdalae and orbital frontal cortices. Nonhuman primate models report that lesions inthese areas produce difficulties in evaluating potentially threatening situations and reduction in socialinteractions, which are core symptoms defining autism (Amaral, Bauman, & Schumann, 2003;Bachevalier, 1991; Machado & Bachevalier, 2003). Structural and functional imaging studies havefound abnormalities or dysfunction in these regions in autism spectrum disorder (ASD) participants(Baron-Cohen et al., 2000), particularly in the temporal lobes (Carper, Moses, Tigue, & Courchesne,2002; Zilbovicius et al., 2006). Hypoperfusion in children with autism has been reported in the STS(Zilbovicius et al., 2000) as well as hypoactivation of the fusiform gyri (Dalton et al., 2005; Daprettoet al., 2006; Schultz et al., 2000), areas well known to be involved in processing social stimuli (Allison,Puce, & McCarthy, 2000). In a working memory task involving faces with high-functioning adults withASDs, Koshino and colleagues (2008) reported lower functional connectivity between the fusiform andthe frontal areas as well as lower activation of prefrontal areas. Activation abnormalities were alsofound in the amygdalae (Amaral et al., 2003; Kemper & Bauman, 1993; Kleinhans et al., 2009;Lombardo, Chakrabarti, & Baron-Cohen, 2009; Pierce, Muller, Ambrose, Allen, & Courchesne, 2001),regions implicated in assigning affective significance to events, particularly those involved in fear pro-cessing (Adolphs, Damasio, Tranel, Cooper, & Damasio, 2000; Breiter et al., 1996; Morris et al., 1996;Phillips et al., 1997; Young, Hellawell, Van De Wal, & Johnson, 1996).

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Basic to processing emotions is the processing of faces themselves, and the behavioral literaturehas also reported face processing disorders in autism (Boucher, Lewis, & Collis, 1998; Dawson et al.,2002; Jambaque, Mottron, Ponsot, & Chiron, 1998; Klin et al., 1999). Faces are key to social commu-nication, and face recognition is crucial for successful interpersonal relationships. Clinical reportsand behavioral studies have shown that individuals with autism avoid eye contact (Hobson & Lee,1998) and consequently show abnormal patterns of looking at faces. The first studies of face process-ing and autism that investigated looking behavior reported atypical visual exploration of faces; youngchildren with autism focused more on the lower part of the face, whereas controls spent more timelooking at the upper part of the face (Langdell, 1978). More recently, using eye tracking techniques,Spezio and colleagues confirmed that high-functioning adults with autism do not use informationfrom the eye region during facial emotional judgments (Boraston & Blakemore, 2007; Spezio, Adolphs,Hurley, & Piven, 2007). For children with autism, experience with faces is impoverished due to thisavoidance of the eye region, and the development of face processing is unlikely to be normal. In thecontext of this reduced experience with faces, some researchers have shown a lack of the face inver-sion effect in autism (Hobson et al., 1988; Tantam, Monaghan, Nicholson, & Stirling, 1989). When facesare presented upside-down, typically developing participants are impaired in face recognition,whereas individuals with autism are not. One explanation is that individuals with autism process fa-cial stimuli through a selective analysis of features rather than configurally, with the assumption thatit is the configural processing that shows the most marked development, with experience, over child-hood. This abnormal face processing strategy was confirmed by Deruelle and colleagues, who foundthat children with autism, unlike matched control children, relied more on local cues (using high spa-tial frequency) than on configural cues (using low spatial frequencies) when processing faces(Deruelle, Rondan, Gepner, & Tardif, 2004). This preference for processing details to the detrimentof a more global processing was also shown in studies of general visual processing (Frith, 1989; Happeet al., 1996).

Brain regions involved in face detection are well established in functional neuroimaging studies(e.g., Haxby et al., 1996; Puce, Allison, Asgari, Gore, & McCarthy, 1996; Sergent, Ohta, & MacDonald,1992). Faces preferentially activate regions of the fusiform gyri, whereas adjacent areas in the infe-rior and occipito-temporal cortices were activated by nonface stimuli. Functional magnetic reso-nance imaging (fMRI) data also confirmed the feature-based strategies in autism, showing apattern of brain activity during face processing that was similar to the pattern of control partici-pants during object processing: activation in the inferior temporal gyri rather than the fusiform gyri(Schultz et al., 2000).

Event-related potentials (ERPs) are a powerful means of assessing the timing of cognitive functionsthat are readily used in paediatric populations. The fMRI and positron emission tomography (PET)studies of face processing in autism cannot fully address the question of the timing of brain activity,and a major change with development is the increased speed or efficiency in cognitive and face pro-cessing (e.g., Taylor, Batty, & Itier, 2004). ERPs index face-sensitive activity over temporo-occipitalsites; the N170 component is now an established measure of early stages of face processing in adultsas well as children (Bentin, Allison, Puce, Perez, & McCarthy, 1996; George, Evans, Fiori, Davidoff, &Renault, 1996; Itier & Taylor, 2004; Rossion et al., 2000; Taylor et al., 2004; Taylor, Edmonds,McCarthy, & Allison, 2001). The earlier P1 component, measured at occipital and posterior temporalsites, has also been found to be sensitive to faces (Itier & Taylor, 2002; Linkenkaer-Hansen et al.,1998; Taylor, Edmonds et al., 2001). These two early ERP components are modulated by emotionalexpression, demonstrating that facial expressions are discriminated during the early stages of visualprocessing (Batty & Taylor, 2003; Caharel et al., 2007; Eger, Jedynak, Iwaki, & Skrandies, 2003;Pourtois, Grandjean, Sander, & Vuilleumier, 2004; Williams et al., 2004).

McPartland and colleagues found that the N170 was delayed in adults with autism comparedwith controls, with no inversion effect, suggesting not only a slower processing of faces but alsoa qualitatively different processing strategy (McPartland, Dawson, Webb, Panagiotides, & Carver,2004). This latency delay was also reported in other studies using faces (Grice et al., 2001;O’Connor, Hamm, & Kirk, 2005) or isolated eyes and mouth (O’Connor, Hamm, & Kirk, 2007).However, a recent study in children with autism during both implicit and explicit processing ofemotional faces reported normal ERP components (P1 and N170), although source analyses

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revealed abnormalities in the strength and dipole orientation of these components (Wong, Fung,Chua, & McAlonan, 2008).

Thus, over the past several decades, numerous studies have investigated emotional and face pro-cessing in ASDs to better understand the clinical features, particularly the impaired social interactionsthat are one of the criteria of the disorders. However, recent reviews have suggested that face process-ing impairments in ASDs might not be as important as previously thought (see Jemel, Mottron, &Dawson, 2006) and could be attributable to visual atypicalities (Behrmann, Thomas, & Humphreys,2006). The current study investigated the neural responses related to face processing in children withautism, exploring both the early visual component (P1) and the more ‘‘visuo-social’’ component(N170). In light of the recent reports and the clinical observation that people with ASDs perceiveand express emotions, we expected to find subtle abnormalities in the face-sensitive components,with perhaps more marked effects in the early visual processes.

Method

Participants

A total of 18 children on the autism spectrum participated in this study. Despite the care given tothe preparation (see below), 1 child ended up refusing to wear the electroencephalogram (EEG) cap.Thus, 17 children with autism completed the protocol, but 2 further children were rejected for toomany artifacts in the EEG recordings. Our clinical sample (N = 15, 13 boys and 2 girls, mean chrono-logical age = 10.55 years, SD = 3.31) is reflective of the much higher prevalence rate of autism in malesthan in females (APA, 1994). Diagnosis of autism was made according to the DSM-IV (APA, 1994) by ateam of experienced clinicians (child psychiatrists and psychologists) who referred the children on theautism spectrum to us for this study. Children with epilepsy were not included. The Childhood AutismRating Scale (CARS) (Schopler, Rechler, & Rochen Renner, 1988) was also completed by a child psychol-ogist, and scores ranged between 29.5 and 36.0 across the sample (M = 32.5), with 30 being the cutofffor a diagnosis of autism. The verbal and nonverbal mental ages of the children with autism were as-sessed by the Test de vocabulaire en Images (Légé & Dague, 1974), a standardized measure of verbalintelligence designed for use with pediatric populations that assesses language comprehension (theFrench version of the Peabody Picture Vocabulary Test), and the Raven’s Progressive Matrices (Raven,Court, & Raven, 1990), respectively. These two assessments are frequently used as matching measuresand provide quick and easy assessments across a wide age range. The verbal equivalent age of the chil-dren with autism was 7.65 ± 4.75 years, whereas the nonverbal equivalent age was 10.19 ± 3.9 years.The chronological age of children with autism was not significantly different from their nonverbalequivalent age (t = 0.73, p = .48), whereas it was significantly different from their verbal equivalentage (t = –3.77, p < .002).

Because it has previously been argued that the selection of the control group in studies of emo-tional processing can significantly affect the results (Hobson, 1991), we matched our sample of chil-dren on the autism spectrum with two groups of typically developing children by chronological ageand verbal developmental age, with the latter being used as a proxy for cognitive development. Eachparticipant with autism was individually matched to 2 typically developing children: 1 child of com-parable chronological age and 1 child of comparable verbal equivalent age. A total of 30 control chil-dren were selected from our previous developmental study, which used the same paradigm and ERPrecording protocol (see Batty & Taylor, 2006). All control children successfully completed two subtestsof the Wechsler Intelligence Scales for Children–third edition (WISC-III), block design and vocabulary,to ensure that all were in the normal cognitive range for their age. Table 1 summarizes the matchingbetween children with autism and the two different control groups. We acknowledge that the wideage range could make comparisons difficult, but it also provides us with a means of assessing changeswith age. Recruitment of a large number of children with autism in a narrow range, and who can alsodo the task, is very difficult. We were very careful to match control children by both age and verbal ageto allow as clear comparisons as possible. Parents of all participating children gave written informedconsent, and the children provided informed verbal assent.

Table 1Description of ASD group and two control groups (chronological age matching and verbal equivalent age matching).

ASD group (n = 15, 13 boys and 2 girls) Chronological age (years) Verbal equivalent age (years)

Mean 10.55 7.65Standard deviation 3.31 4.75Minimum–maximum 5.25–16.5 2.06–19.47

Control groups Chronological age matching (n = 15) Verbal age matching (n = 15)Mean 10.51 7.70Standard deviation 3.20 3.82Minimum–maximum 5.33–15.92 4.08–15.92Sex ratio 9 boys and 6 girls 9 boys and 6 girlst 0.32 –0.18p .75 .86

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Task and stimuli

First, pictures of experimenters, the room, and the EEG cap were sent to the families with childrenon the autism spectrum together with a little timetable explaining the different stages of the protocol.If the parents thought that their children could participate successfully in the study, the children wereexposed briefly to experimental conditions identical to the real ones. These preparations were veryefficient at avoiding too much stress for these children encountering the unknown laboratory environ-ment. Children were tested individually, completing the ERP study and the behavioral tests on thesame visit.

The stimuli and task were those used in previous studies in adults (Batty & Taylor, 2003) and inchildren with typical development (Batty & Taylor, 2006). We took 210 different black and white pho-tographs of faces expressing emotions; all of the faces included were correctly categorized at P80%accuracy by emotion (Fig. 1; see also Batty & Taylor, 2003). These faces were divided into three equalblocks, each containing 70 emotional faces (10 of each of the six basic emotions [anger, disgust, hap-piness, sadness, surprise, and fear] plus neutral faces, with each emotion being expressed by 5 menand 5 women) and 15 nonface objects (cars, butterflies, and planes, depending on the block) in randomorder. The three blocks were presented twice. The stimulus duration was 500 ms, with an interstim-ulus interval (ISI) randomized between 1200 and 1600 ms. Children pressed a button when they saw anonface object; thus, it was an implicit face processing task given that attention was not directed to-ward the faces or the emotions they expressed. The task was introduced to maintain the children’sattention toward the stimuli presented on the screen. Preliminary interviews with parents allowed

Fig. 1. Examples of the emotional faces used in this study (fear, disgust, anger, sadness, neutral, surprise, and happy).

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us to avoid the presentation of targets that corresponded either to special interests of the children(e.g., cars) or to phobias (e.g., butterflies). In these particular cases (n = 2), the blocks were specificallytransformed to nonface targets with no specific interest. The task was simple enough for all of thesechildren to be able to complete it. No difference in the accuracy for the target detection was found,confirming that the groups did not differ on this index of attention. Children with autism detected67.8% (±15.1) of the targets; children in the typically developing group with a comparable chronolog-ical age detected 78.9% (±27.0) (t = –1.02, p = .33), and those with a comparable verbal equivalent agedetected 67.8% (±21.0) (t = 0, p = 1.00) of the targets.

ERPs

ERPs were recorded from 30 active electrodes (FP1, FP2, F3, F4, F7, F8, Fz, FT9, FT10, FP5, FP6, T7, T8,C3, C4, CP5, CP6, TP9, TP10, P3, P4, P7, P8, Pz, Poz, PO9, PO10, O1, O2, and Oz) inserted into an Easycapelectrode cap (FMS Falk Minow, http://www.easycap.de). Cz served as reference during the recording;an average reference was calculated off-line. Electrode impedances were below 5 kX. EEG was sam-pled by Synamps for 1100 ms, with a 100-ms prestimulus at 500 Hz and a bandpass of 0.1–30 Hz. Ver-tical and horizontal electrooculograms (EOGs) were recorded simultaneously from electrodes at theouter canthus and left supraorbital ridge, and trials contaminated with activity greater than±120 lV were rejected before averaging. Trials were averaged separately for the seven emotions. Onlythe nontarget face stimuli were analyzed. The target trials were potentially interesting but were asso-ciated with movement during behavioral response, and the majority of those trials were rejected, inparticipants with autism particularly, because of muscle artifact.

Data analysis and statistics

Analyses were completed on two ERP components that are reported to be sensitive to faces (P1 andN170). The peak latencies and amplitudes of these two early components were measured at the elec-trodes where they were largest. The P1 was measured at O1 and O2 (between 90 and 140 ms), and theN170 was measured at P7 and P8 (between 140 and 240 ms). Because there were no significant dif-ferences between left and right hemisphere responses (verified with Student’s t tests), the amplitudeand latency data were collapsed across hemisphere for further analyses. A repeated two-way analysisof variance (ANOVA) was performed using two levels by group (children with autism and control chil-dren) and seven levels in the emotion expressed by the face presented (angry, disgusted, happy, sur-prised, sad, fearful, and neutral) and with age as a covariate. This analysis was completed for the twotypes of matching (chronological age and verbal age).

Results

The two early ERP components were clearly identifiable in the three groups of children. Fig. 2shows the grand averaged ERPs for the children with autism and the two control groups. The compo-nents measured (P1 and N170) are indicated by arrows.

Chronological age matching

Children with autism showed a significantly delayed P1, F(1, 27) = 4.88, p < .04, compared with age-matched controls. The P1 peaked at 103 ms (±7) in typically developing children, whereas it peaked at110 ms (±12) in children with autism (Figs. 3 and 4). P1 amplitude was smaller in children with autism(17.2 lV ± 7) than in control children (22 lV ± 7.5), F(1, 27) = 6.79, p < .02 (Figs. 2 and 4).

A main effect of age was found on P1 latency, F(1, 27) = 16.64, p < .0004, and amplitude,F(1, 17) = 18.34, p < .0001; both decreased with increasing age. There were no interactions betweenage and group.

No main effect of emotion was seen on P1 amplitude, F(6, 162) = 1.87, p = .09; however, a trend wasnoticed for P1 latency, F(6, 162) = 2.07, p = .06. Because our previous normative studies found emotion

Fig. 2. Grand averaged waveforms for all emotions at four posterior electrodes (O1, O2, P7, and P8). Black lines: children withASDs; gray solid lines: typically developing (TD) children matched by chronological age; gray dotted lines: TD children matchedby verbal equivalent age. The P1 and N170 are indicated by arrows.

Fig. 3. Mean P1 and N170 latencies for the three groups of children. TD, typically developing. ⁄p 6 0.05

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effects on the P1, we completed planned post hoc tests (Newman–Keuls with Bonferroni corrections)that revealed that the control group had a longer latency P1 to disgust than to happy (p < .005), sur-prised (p < .005), and sad (p < .05) expressions.

Children with autism also showed a delayed N170, F(1, 27) = 6.67, p < .02. The N170 peaked at 175ms (±35) in typically developing children, whereas it peaked 20 ms later in children with autism (195ms ± 31) (Figs. 2 and 3). No significant group effect was seen on N170 amplitude.

A main effect of age was noticed on N170 latency, F(1, 27) = 38.37, p < .0001, and amplitude,F(1, 27) = 7.00, p < .02; both decreased with increasing age.

Neither facial emotional effects nor interactions of age with group were found on the N170.

Verbal equivalent age matching

The group effect on P1 latency, seen when children with autism were matched by chronological agewith control children, did not remain significant using verbal matching. The main age effect persisted

Fig. 4. P1 latencies (A) and amplitudes (B) in children with autism (ASDs) and typically developing (TD) children matched forchronological age.

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on P1 latency, although it was less strong with verbal matching, F(1, 27) = 7.69, p < .01, than with chro-nological matching, p < .0004.

P1 amplitude showed a significant group effect as well as an age effect regardless of the matching(Figs. 2 and 4). P1 amplitude was smaller in children with autism (17.2 lV ± 7) than in verbal ageequivalent control children (27.5 lV ± 11.5), F(1, 27) = 16.48, p < .0004. The age main effect also re-mained on P1 amplitude, F(1, 27) = 17.71, p < .0004.

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The main age effect was also present on N170 latency, F(1, 27) = 30.79, p < .0001, whereas N170amplitude did not show any effect of group, age, or emotion using this matching. Table 2 summarizesthe main effects found.

Discussion

ERP differences between children with autism and controls

The classic face ERPs (P1 and N170) were clearly identifiable for children with and without autism,and visual inspection of the ERPs did not show obvious abnormalities. However, the analyses revealedsignificant differences; a clinical versus control group effect was found for most of the ERP measures(P1 amplitude and latency and N170 latency) when using chronological age matching. These effectsrevealed that the processes involved in implicit emotional face perception are affected in autism.When matched by verbal age, only the group effect on P1 amplitude remained, suggesting a robustabnormality of the P1 component in autism. In this study, the low amplitude of this early visual com-ponent does not appear to be due to developmental delay; rather, it appears to be due to autism diag-nosis per se. On the N170, the group effect did not persist when children on the autism spectrum werematched with younger control children (verbal age matching). Thus, we did not demonstrate anunequivocally abnormal N170 in autism; the development of this component may only be delayedin children with autism.

The results in the literature are inconsistent. Some authors report abnormalities in early ERP re-sponses to faces in ASDs (McPartland et al., 2004; O’Connor et al., 2005; Webb, Dawson, Bernier, &Panagiotides, 2006), whereas others do not (Grice et al., 2005; Webb et al., 2009; Webb et al.,2010). Wong and colleagues (2008) did not find reliable group differences on ERPs or a main effectof facial emotion, but they found that the activity of the underlying sources (occipital and temporal)contributing to these early ERP responses differed between autism and control groups.

The considerable behavioral and neuropsychological heterogeneity in ASDs may account for the var-iability in findings across studies. Although most of the neuroimaging studies selected high-functioningor Asperger syndrome participants (who could cope with the task demands, accept the constraints ofthe electrodes/caps, and stay still during the recordings), the range of participants who participatedin the above studies was still quite large. The IQs varied from 80 to 135, and the severity of the autisticdisorders was also heterogeneous (as specified by the CARS scores from 33.0 to 47.5, e.g., in Grice et al.,2005). Another explanation for the discrepancies could be the type of control group used. Three differ-ent kinds of matching are possible; the individuals on the autism spectrum could be matched withtypically developing peers by chronological age, by age equivalent verbal ability, or by age equivalentnonverbal ability. The type of matching used can significantly alter findings (Jarrold & Brock, 2004;Wright et al., 2008). For studies focusing on high-functioning autism, chronological age and IQ matchingis the most used. However, although children with Asperger syndrome do not have language difficulties,high-functioning children with autism often present with language delays.

The variability of the task could also explain the discrepancy of the findings in the literature. Somestudies focused on the face versus object processing (McPartland et al., 2004; Webb et al., 2006),

Table 2Main significant effects on P1 and N170 between children with autism and two typically developing child groups.

ERP component Chronological age matching Equivalent verbal age matching

P1 Amplitude Age effect (p < .001) Age effect (p < .001)Group effect (p < .02) Group effect (p < .001)

Latency Age effect (p < .001) Age effect (p < .02)Group effect (p < .04)Emotional effect (p = .06)

N170 Amplitude Age effect (p < .02)Latency Age effect (p < .001) Age effect (p < .001)

Group effect (p < .02)

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whereas others were interested in the inversion effect (Webb et al., 2009), familiarity (Webb et al.,2010), gaze direction (Grice et al., 2005), and emotions (O’Connor et al., 2005; Wong et al., 2008);some of the tasks were implicit, whereas others were explicit.

However, those studies that did not report significant group effects between individuals with aut-ism and controls have nevertheless always found interactions by group (e.g., group by gaze directioninteraction in Grice et al., 2005), suggesting differences in the processes involved.

Our study is more comparable to the studies of O’Connor and colleagues (2005) and Wong and col-leagues (2008) because they focused on emotional processes. Both of those studies reported a slowerspeed of face processing in ASDs. When using chronological age matching, our data are in agreementwith this delay, as is evident by a slower P1 and N170. However, we found that the effects on the earlyERP latencies do not remain when using verbal age equivalent matching, suggesting that the slowerspeed of face processing is not an effect of autism per se. The differences with the results of O’Connorand colleagues (2005) may be explained by the fact that they used a verbal response as their behavioralmeasure but did not control or match for verbal age in their groups. Although demonstrating differencesprobably linked to a delay in the maturation of face processing, our data did not reveal a reliable orstrong abnormality of face processing in children with autism. These data are in agreement with a recentreview suggesting that face processing impairments in autism may be less significant than has been re-ported in the past (see Jemel et al., 2006), and some researchers have proposed that the emotional deficitcould also be less marked than has been shown previously (Lacroix et al., 2009; Wright et al., 2008).

The consistent group effect on the P1 to faces instead suggests abnormal early visual processing.Although sensory difficulties were central in autism research 20 years ago, they have been largelyabandoned for high-level social and cognitive explanations. Recently, however, there has been a re-newed interest in sensory processing in ASDs. Numerous studies have presented evidence of atypicalsensory processing (Ashwin, Ashwin, Rhydderch, Howells, & Baron-Cohen, 2009; Bertone, Mottron,Jelenic, & Faubert, 2005; Frith, 1989; Mottron & Burack, 2001; Scherf, Luna, Kimchi, Minshew, &Behrmann, 2008) and suggested that these fundamental impairments could help to explain the socialand cognitive difficulties. Although auditory processes have been investigated using ERPs (Bruneau,Bonnet-Brilhault, Gomot, Adrien, & Barthelemy, 2003; Bruneau, Roux, Adrien, & Barthelemy, 1999),the literature on visual evoked potentials in autism is quite poor. In a recent review by Jeste andNelson (2009), there was no reference to any investigation on the P1 as an early index of visualprocessing in autism (except as related to investigating face processing). However, structural abnor-malities have been reported in occipital cortices in individuals with ASDs. Hyde and colleagues foundincreased gray matter in visual primary and associative areas (Hyde, Samson, Evans, & Mottron, 2010),and reduced occipital white matter in ASDs has also been reported (Bonilha et al., 2008). Moreover,Vandenbroucke and colleagues noted a specific impairment in object boundary detection in ASDs thatwas evident as early as 120 ms, and they attributed this deficit to a dysfunction of horizontal connec-tions within early visual areas (Vandenbroucke, Scholte, van Engeland, Lamme, & Kemner, 2008).

Even though the P1 is known to reflect visual processing and occipital activity, this component hasbeen shown to be sensitive to attention (Taylor, 2002; Taylor, Itier, Allison, & Edmonds, 2001), facialinformation (eyes: Taylor, Edmonds, et al., 2001; gaze direction: Senju, Tojo, Yaguchi, & Hasegawa,2005), and emotions (Batty & Taylor, 2003; Utama, Takemoto, Koike, & Nakamura, 2009). Moreover,a recent study found that P1 amplitude correlated with the skill of emotion regulation in healthydevelopment; the authors suggested that early ERPs could be used to detect early risk of psychopa-thology (Dennis, Malone, & Chen, 2009). Thus, the P1 is more than simply an index of early low-levelvisual processing; it is also sensitive to top-down influences and early rapid feedback. Sutherland andCrewther (2010) reported that cortical responses to magnocellular afferents were weaker in a groupwith a higher tendency toward autism (as measured by the autism quotient) and that the magnocel-lular activity was delayed. They suggested that this could decrease the ability of autistic individuals tobenefit from perceptual feedback associated with the magnocellular system.

Development of ERPs

We found age effects on the P1 and N170 regardless of the matching used (except for N170 ampli-tude, for which the age effect was nonsignificant using verbal age equivalent matching), confirming

440 M. Batty et al. / Journal of Experimental Child Psychology 109 (2011) 430–444

the maturation of emotional processes throughout childhood (Batty & Taylor, 2006). A possible expla-nation for the exception of N170 amplitude could be the developmental pattern of the N170. Althoughthe P1 shows the more typical pattern of a decrease in amplitude with increasing age, N170 amplitudedecreases from 4 to 11 years of age and then increases until adulthood (Taylor et al., 2004). This non-linear pattern, associated with the change in the morphology of the N170 at around 11 years of age,could yield a less consistent age effect with our limited sample.

The absence of an age by group interaction demonstrated that both amplitude and latency of theearly visual components changed with age in the group of children with autism similarly to the typ-ically developing children, suggesting a normal pattern of maturation. The fact that most of the differ-ences between clinical and control groups found when using chronological age matching do notremain when using verbal equivalent age matching is, however, in favor of a delay in the maturationof the neural substrates involved in emotional face processing. We suggest that although the matura-tion is slightly delayed in children with autism, the development follows a similar pattern in the twogroups. Nevertheless, the difference between groups seems to be larger at the younger ages and de-creases with increasing age (Fig. 4). This could help to explain why most of the studies investigatingface processing in adults with autism did not report abnormal ERPs.

Face expertise and the N170 have been linked in numerous studies. Avoidance of eye contact fromearly in life would impact the acquisition of face expertise and face processing skills, and this could bereflected in the N170. However, it is important to note that the ASD groups studied are typically highfunctioning and, thus, are likely to have undergone remedial interventions and to have developedcompensatory strategies.

Emotional effects

None of the components measured in the current study was found to be significantly affected bythe emotions expressed by the face stimuli. The modulation of early visual ERPs by emotional facialexpressions is controversial in the literature. Older studies reported only late effects of emotionalexpressions (Balconi & Pozzoli, 2003; Munte et al., 1998), in agreement with the classical model of faceprocessing (Bruce & Young, 1986). But recently, many adult studies have shown evidence of N170 sen-sitivity to the processing of the emotional aspect of faces (Batty & Taylor, 2003; Caharel, Courtay,Bernard, Lalonde, & Rebai, 2005; Campanella, Quinet, Bruyer, Crommelinck, & Guerit, 2002;Sprengelmeyer & Jentzsch, 2006; Utama et al., 2009). Investigations have also reported emotionaleffects around 100 ms affecting P1 amplitude in adults (Batty & Taylor, 2003; Pizzagalli, Regard, &Lehmann, 1999; Pourtois, Thut, Grave de Peralta, Michel, & Vuilleumier, 2005; Utama et al., 2009).

In our previous developmental study (Batty & Taylor, 2006), we showed that the N170 is not ma-ture until late adolescence and its sensitivity to emotions appeared only late during typical develop-ment (at 14–15 years). Thus, the absence of emotional effects on the N170 in our current study is notsurprising given that the children were younger. In the previous study, we found that the P1 latencyemotional effect was due to the younger children (4- to 7-year-olds). Dawson and colleagues also re-ported an emotional effect on the latency of the early visual component in 3- and 4-year-olds(Dawson, Webb, Carver, Panagiotides, & McPartland, 2004), and Dennis and colleagues (2009)reported an emotional effect on P1 latency in 5- to 9-year-olds. Although we found no significantemotional effect on P1 latency, a trend was seen and post hoc analyses showed a longer latency P1to disgust than to happy, surprised, and sad expressions in control children only.

In Batty and Taylor (2006), we suggested that the P1 could index rapid, likely superficial, and notvery sophisticated processing of facial emotions in young children. The longer latency to disgust couldsuggest less familiarity with this emotion and is consistent with the later development of recognitionof negative emotions (Gao & Maurer, 2010). This early global emotional processing would be replacedgradually by more configural processing, with the extraction of second-order spatial relations in facesallowing subtle emotional discrimination indexed by the N170. Although we could not determinewhether emotional processing would be seen on the ERPs in teenagers with autism because our groupwas a younger cohort, the P1 latency effect, seen only in the control group, further suggests an earlyanomaly in visual processing in children with autism—early in terms of processing (�100 ms) andearly in childhood. Thus, a contributing factor to the face processing difficulties in children with

M. Batty et al. / Journal of Experimental Child Psychology 109 (2011) 430–444 441

autism could start from atypicalities in visual perceptual processes, rapid feedback to primary visualareas, and subsequent holistic processing. People with autism may process visual information differ-ently from those without autism; this could cause ripple effects in the perceptual stream and contrib-ute to difficulties in higher level/cognitive domains.

Acknowledgments

We thank Chantal Brousse for her wonderful collaboration and her precious help in child recruit-ment. Our greatest thanks go to the parents and children who participated in this study for their timeand exceptional efforts. This work was supported by the Fondation Orange.

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