Development and Psychopathology

Transcription

1 Development and Psychopathology Atypical development of configural face recognition in children with Autism Spectrum Disorders, Down syndrome and Williams syndrome Journal: Development and Psychopathology Manuscript ID: Draft Manuscript Type: Original Article Keyword: Autism Spectrum Disorders, Down syndrome, Williams syndrome, face recognition, configural processing Abstract: Background: Configural processing in face recognition is a sensitivity to the spacing between facial features. It has been argued both that it represents a high level of expertise in face recognition, and also that it is a developmentally vulnerable process. We report a cross-syndrome investigation of the development of configural face recognition in schoolaged children with Autism Spectrum Disoders, Down syndrome, Williams syndrome compared to a typically developing control group. Method: Cross-sectional trajectories analyses were used to compare configural and featural face recognition utilising the Jane Faces task (Mondloch et al., 000). Trajectories were constructed linking configural and featural performance either to chronological age or to different measures of mental age (receptive vocabulary, visuospatial construction, and the Benton face recognition task). Results: An emergent inversion effect across age for detecting configural but not featural changes in faces was established as the marker of typical development. All three disorder groups displayed an atypical profile which differed across groups. Conclusion: We discuss the implications for the nature of face processing within the respective developmental disorders, and how the cross-syndrome comparison informs the constraints that shape the typical development of face recognition. Abstract.docx

2 Page of Development and Psychopathology Atypical development of configural face recognition in children with Autism Spectrum Disorders, Down syndrome and Williams syndrome Abstract Background: Configural processing in face recognition is a sensitivity to the spacing between facial features. It has been argued both that it represents a high level of expertise in face recognition, and also that it is a developmentally vulnerable process. We report a crosssyndrome investigation of the development of configural face recognition in school-aged children with Autism Spectrum Disoders, Down syndrome, Williams syndrome compared to a typically developing control group. Method: Cross-sectional trajectories analyses were used to compare configural and featural face recognition utilising the Jane Faces task (Mondloch et al., 000). Trajectories were constructed linking configural and featural performance either to chronological age or to different measures of mental age (receptive vocabulary, visuospatial construction, and the Benton face recognition task). Results: An emergent inversion effect across age for detecting configural but not featural changes in faces was established as the marker of typical development. All three disorder groups displayed an atypical profile which differed across groups. Conclusion: We discuss the implications for the nature of face processing within the respective developmental disorders, and how the crosssyndrome comparison informs the constraints that shape the typical development of face recognition. Keywords: Autism Spectrum Disorders, Down syndrome, Williams syndrome, face recognition, configural processing

3 Development and Psychopathology Page of Introduction Faces have a special status as visual stimuli, both in terms of their social relevance and the expertise that adults demonstrate in their recognition. In this paper, we focus on two processes implicated in face recognition, featural and configural processing, and examine their developmental trajectories in children with Autism Spectrum Disorders (ASD), Down syndrome(ds), and Williams syndrome (WS) in comparison to typically developing children (TD). Several studies have suggested that featural, configural and holistic aspects of face recognition are dissociable cognitive processes. These processes can be broadly described as follows: () in featural processing, also known as local or analytical processing, recognition is driven by individual features such as eyes, nose, and mouth; () in configural processing, recognition is driven by the arrangement of the features in the face. This may be in terms of the relative positioning of the features, termed first-order configural information (e.g., nose above mouth), or in terms of the exact distances between features, termed second-order configural or relational information (e.g., distances of eye separation); () in holistic processing, sometimes referred to as global or gestalt processing, the face is recognised as a whole. Holistic processing is sometimes conceived of in terms of a fast template-matching procedure (see Diamond & Carey, ; Tanaka & Farah,, and Tanaka & Sengco, ). In TD, the contribution of these three processes to face recognition changes gradually with chronological age, with configural processing being the last to appear (Maurer et al., 00; Mondloch, Le Grand, & Maurer, 00). Configural processing emerges by 0 years of age (Carey & Diamond, ; Diamond & Carey, ; Mondloch, Geldart, Maurer, & Le Grand, 00), while holistic processing has been identified as early as (Brace et al., 00) and even years of age (Annaz et al., 00; Freire & Lee, 00; Pellicano & Rhodes, 00).

4 Page of Development and Psychopathology The qualitative and quantitative differences between featural and configural encoding have important implications in real world context, and have been hotly debated even in some very early studies of visual perception. Indeed, while some research has suggested a qualitative shift in face processing during childhood (e.g., Diamond & Carey, ; Mondloch et al., 00; Leonard, Karmiloff-Smith & Johnson, 00), others have argued that any changes in face processing abilities are due to the maturation of general cognitive processes, such as attention and memory (see Crookes & McKone, 00, for a review). It is also possible that any change from featural to configural processing that is found during development is not the result of changing sensitivity to these types of facial information; rather, young children may be just as sensitive to configural information but do not spontaneously use it in face processing tasks until they are older, or until have greater expertise with face stimuli in the environment (Leonard et al., 00; Schwarzer, 000, 00). Notably, configural face processing has been found to have greater developmental vulnerability, with deficits reported in typically developing (TD) individuals with early visual deprivation (LeGrand, Mondloch, Maurer & Brent, 00), and in developmental disorders such as autism and Williams syndrome (Karmiloff-Smith et al., 00; Rutherford et al., 00). In the current study, we examine featural processing and second-order configural processing (perceiving distances between the internal face-features) in three developmental disorders: ASD, DS and WS. One of the main hallmarks of expertise in face recognition is the inversion effect, in which faces presented upside-down are more difficult to recognise than upright faces. The inversion effect disrupts configural processing whilst leaving featural processing relatively unimpaired (see Rakover, 00, for review). We adopted a crosssectional, developmental trajectories approach to trace the emergence of configural processing in TD children, and compared similar trajectories in the three disorders (see Thomas et al.,

5 Development and Psychopathology Page of , for methods). Our key questions were whether deficits existed in all three disorders, whether deficits were similar or differed across disorders, and whether configural processing abilities were in line with face recognition skills, as assessed by a standardised test. We begin with a brief review of the relevant literature from the three disorders. Autism Spectrum Disorders (ASDs) ASDs form a common neurodevelopmental syndrome with a strong genetic basis (Abrahams & Geschwind, 00). They are characterised by three core impairments in social interaction, communication and stereotypic behaviours. However, there are marked differences in the extent and quality of the symptoms amongst individuals with ASDs. One of the most common features of ASDs is their striking difficulty with social skills, in particular face recognition. Atypical face recognition in ASDs has been found using both behavioural and functional brain imaging tasks. A number of studies have reported that children with ASDs show greater attention to the mouth rather than to the eyes region (e.g., Annaz, Karmiloff- Smith, Johnson, & Thomas, 00; Klin, Jones, Schultz, Volkmar, & Cohen, 00; Riby, Doherty-Sneddon, & Bruce, 00), and rely on different spatial frequencies for face recognition compared to controls (Deruelle, Rondan, Salle-Collemiche, Bastard-Rosset, & Da Fonséca, 00; Deruelle, Rondan, Gepner, & Tardif, 00; Leonard, Annaz, Karmiloff-Smith, & Johnson, in press). Several functional imaging studies report atypical or weak activation of the fusiform gyrus in ASDs, an area that is activated during face recognition in typical adults (Critchley et al., 000; Dalton et al., 00; Schultz et al., 000), perhaps related to atypical scanning pathways or reduced looking to the eyes (Dalton et al., 00; Perlman et al., 00). Findings from electrophysiological studies have indicated that individuals with ASDs exhibit atypical event-related brain potentials to faces, characterised by an absent or reduced N0 waveform component and more bilateral than right lateralized voltage distribution (Dawson,

6 Page of Development and Psychopathology et al., 00; McPartland, Dawson, Webbs, Panagiotides, & Carver, 00). Furthermore, individuals with ASDs show reduced looking times to people, and to faces in particular, in both static and dynamic social scenes (e.g., Annaz, et al., 00; Klin et al., 00; Riby & Hancock, 00). Investigations of configural processing in adults with ASDs have yielded mixed results (Faja et al., 00; Nishimura et al., 00; Rutherford et al., 00; Wallace et al., 00). Specifically, using paradigms in which stimuli were presented simultaneously and for unlimited time, Nishimura et al. (00) did not find performance differences between their adult ASD participants and TD participants. Rutherford et al. (00) reported a deficit for adult ASD participants in perceiving differences in eye-to-eye spacing, but not mouth-to-nose spacing. Poorer performance of ASDs was evident in processing configural information on a sequential same different paradigm (Faja et al., 00; Wallace et al., 00). To date, no studies have explored the actual development of configural processing in ASDs. In addition, most of the preceding findings are based on studies of high-functioning individuals with autism or with Asperger syndrome. In the current study, we also included low-functioning children with autism to explore individual variation in face recognition characteristics across the ASDs. Williams syndrome (WS) Williams syndrome is a rare genetic disorder caused by a hemizygous microdeletion of some genes on chromosome q. (Tasabehji, 00). The incidence of WS is approximately in 0,000 live births (Morris, Demsey, Leonard, Dilts & Blackburn, ). The main cognitive characteristics of WS include overall IQ between and (Mervis et al., 000; Searcy et al., 00), and a hyper-social personality profile. Compared to overall mental age,

7 Development and Psychopathology Page of face recognition and language skills are relatively proficient whereas visuo-spatial skills are relatively poor (Donnai & Karmiloff-Smith, 000; Mervis & Bertrand, ). Several studies have suggested that relatively good face recognition abilities in WS are achieved by atypical underlying processes, and in particular the preferential use of featural encoding, leading to a reduced inversion effect (Annaz at al., 00; Deruelle, Mancini, Livet, Cassé-Perrot & de Schonen, ; Karmiloff-Smith et al., 00; Mills et al., 000). For instance, in their holistic face recognition study, Annaz and collegues (00) found that children in the WS group showed no inversion effect on the whole face trials but an emerging inversion effect on features. Furthermore, Leonard, Annaz, Karmiloff-Smith and Johnson (0) found typical spatial frequency biases for face recognition in older children with WS, but different developmental pathways led to this outcome between WS and control groups. These atypical patterns may be due to unusual attention towards faces and scanning patterns of facial information (e.g., Riby, Doherty-Sneddon & Bruce, 00; Riby, Doherty-Sneddon & Bruce, 00; Riby et al., 0). This atypical behavioural evidence is in line with a small number of imaging and ERP studies indicating anomalous brain activation during face recognition (Grice et al., 00; Mobbs et al., 00). In an imaging study that contrasted WS with autism, Grice et al. (00) observed differences in electroencephalographic gamma band oscillations between a WS group and both the autism and TD control groups. These authors argued that both WS and autism rely more on featural processing in face recognition but achieve a featural style of processing in different ways. These imaging results are suggestive, but require more detailed complementary behavioural studies that directly compare the development of featural processing in the two disorders. Down syndrome (DS)

8 Page of Development and Psychopathology Down syndrome is the most common sporadic genetic disorder (/00 live births) usually associated with the presence of three copies of chromosome (trisomy ). Children with DS have an average IQ falling between and 0, which significantly declines with increasing age to between 0 and 0 (Roizen & Patterson, 00). Only a handful of studies have examined face processing in DS, and have mostly focused on emotion recognition. Annaz and colleagues (00) investigated the development of holistic face recognition in school-age children with DS and reported atypical face recognition based on a part whole task. Unlike the other groups tested (ASD, WS and TD control groups), children with DS discriminated features better when presented in whole faces than when presented in isolation. The authors suggested that individuals with DS are poor at processing features and need the context of a whole face to support the recognition of individual features. Wishart and Pitcairn (000) carried out two experiments to investigate face recognition skills in children with DS. In their first experiment, children were tested on two tasks: identity matching and expression matching. Their performance was compared to TD children matched on overall mental age (MA). Although children with DS were slower than the MA-matched group at identity-matching tasks and their accuracy was not significantly different from the controls. However, their performance was significantly poorer on the expression-matching task. Children with DS had particular difficulties in decoding emotions such as surprise and fear. In a second study, faces were now additionally shown in either upright or inverted positions. Children were presented with familiar and unfamiliar faces, and asked to choose the face that they had seen before. Again, the results indicated that children with DS were less accurate and slower in response than MA-matched controls. Furthermore, unlike the TD group, the accuracy of the children in the DS group was not sensitive to the orientation of the faces, which would imply weaker or absence of configural

9 Development and Psychopathology Page of processing (see also, Williams, Wishart, Pitcairn, & Willis, 00; Wishart, Cebula, Willis & Pitcairn, 00). Method Participants Thirty-three children with ASDs ( male, female; mean age = :), children with DS (0 male, female; mean age = :0), children with WS ( male, 0 female; mean age = :) and TD children ( male, female; mean age = :) participated in our study (see Table for group details). The TD sample had a greater age range in order to permit comparisons between disorder and TD trajectories either on the basis of Chronological Age (CA) or on the basis of Mental Age (MA), where disorder groups may have lower mental ages. Children in the ASD group met established criteria for autism, as specified in DSM-IV (American Psychiatric Association, 000) and ADOS (Lord, Rutter, DiLavore, & Risi, ), and all scored above cut-off for ASD on the Childhood Autism Rating Scale (CARS) (Schopler et al., ). The gender bias for the autistic group was characteristic of the disorder (Baird et al., 00). All children in the DS group had previously been tested positively for trisomy of chromosome. Children with WS had been diagnosed clinically as well as by means of the fluorescence in situ hybridisation (FISH) test for microdeletion of specific gene markers. Participants were recruited from the North London schools and, for WS, via the Williams Syndrome Foundation, UK. All individuals had normal or corrected-to-normal vision. The experimental protocol was approved by the Birkbeck, University of London Ethics Committee prior to recruitment of participants. Both parental informed consent and the child s assent were obtained before participation.

10 Page of Development and Psychopathology Face recognition skills were assessed using the Benton Facial Recognition Test (henceforth Benton) (Benton et al., ). In addition, all children completed the British Picture Vocabulary Scale (BPVS), (Dunn et al., ) and the Pattern Construction (PC) test from the BAS-II (Elliot et al., ), to give measures of verbal and visuospatial mental age, respectively. Children in the ASD group were assessed on the CARS (Schopler et al., ), and were divided into a low-functioning group (defined as CARS range 0 points: male, female; mean age = :; henceforth referred to as the LFA group); and a highfunctioning group (CARS range 0 points: male, female; mean age = :; henceforth referred to as the HFA group). ================== Insert Table about here ================== Stimuli The stimuli were developed by Mondloch and colleagues (Mondloch et al., 00). They were derived from a black and white photo of a woman (called Jane in this study) to create varied versions of the same face. The featural version was created by replacing the eyes or the mouth features of Jane s face with features of other people. In the configural version (referred to as the spacing set by Mondloch et al., 00), features such as the eyes were moved in either direction (horizontally or vertically) of the inner face, for example, the eyes were moved closer together by mm relative to the original. All stimuli were 0. cm wide and. cm high (Figure ). More detailed information about the stimuli can be found in Mondloch et al., (00).

11 Development and Psychopathology Page 0 of =================== Insert Figure about here =================== Procedure The procedure employed a well-established paradigm for differentiating between featural and configuring processing of real faces. Trials were blocked into featurally- or configurallyaltered sets and were shown in upright and inverted orientations. Trials were blocked to encourage the participants to adopt specific face-processing strategies (Mondloch et al., 00). Participants were presented with two faces simultaneously () on a -inch computer monitor using SuperLab Pro.0 software and were asked to determine whether the two faces were the same or different. In half the trials, the faces were identical, while in the other half, one of the faces had been altered either featurally or configurally. The testing session began with a game and practice trials to ensure that all participants understood the instructions and the meaning of the words same and different. The experimenter played a short game with each child, which involved placing objects that were the same on one side and different separately. Once the experimenter was satisfied that the child understood the rules of the game, the practice trials began. A small number of practice trials ( upright and inverted for each condition) proceeded the proper test. Each participant was presented with 0 trials from the featural and configural sets respectively. Mondloch et al. (00) presented the stimuli sequentially. However, as impairments in verbal and visuospatial short-term and/or long-term memory have been reported in all three disorders under study (e.g., Jarrold, Baddeley, & Phillips, 00; Minshew & Goldstein, 00; Sampaio, Sousa, Fernandez, Henriques, & Goncalves, 00), the memory component was removed. 0

12 Page of Development and Psychopathology Following Mondloch et al. s (00) procedure, the upright block was always presented before the inverted block and the order of configural and featural blocks within these was counterbalanced. Each block consisted of same (identity trials) and different (transformed trials) in randomised order. The experimenter initiated the task by saying: Now we are going to play another game, like the game you have just played. Look. This is Jane and these are her sisters (original model with other modified versions of Jane were presented on the screen). Some sisters look the same because they are twins. Do you know any twins?... Some sisters look different and they are not twins. Now we are going to play a game where sometimes you will see twin sisters, sometimes not. When you see two faces that you think look the same, press this button (experimenter shows the relevant button) and when you think that the faces look different, press this button (experimenter shows the relevant button). Are you ready?... Try to answer as fast as possible. During each trial, two target faces were presented simultaneously, to which the participant had to respond with the same or different keys on the keyboard. The stimulus was displayed until the response button was pressed. Only two keys on the keyboard were visible, so the child was not able to press the wrong key. Two cards were placed under the relevant key, one had two dots of the same colour (representing same response - S key) and the other card had two different colours (representing different response - L key). Children were monitored for tiredness and provided with stickers as rewards during the breaks. The dependent variable was accuracy of correct choices for the upright and inverted trials in the featural and configural conditions.

13 Development and Psychopathology Page of Results The task comprised two components: difference detection (where the difference was due either to a configural or featural transformation) and identity recognition (for all trials where no change had been made between model and target). We analysed the difference detection and identity recognition trials for featural and configural blocks separately, since configural/featural transformation only applied to difference detection, whereas upright/inverted orientation applied to all trial types (see Karmiloff-Smith et al., 00 for a similar approach). Initially, developmental trajectories were constructed linking accuracy to chronological age for each group. A fully factorial ANCOVA was used, with age as the covariate and orientation (upright, inverted) and, for difference detection, face transformation (configural, featural) as within-participants factors (see Thomas et al., 00, for more detail of methods). Each disorder group was then compared individually to the TD group, by adding a between-participant factor of group to the design. In addition, we performed two planned comparisons. These were: (i) to assess the effect of the severity of autistic symptoms (measured according to CARS test) on face recognition by comparison of the HFA and LFA groups; and (ii) to examine whether the WS and HFA groups responded in a similar way on the Jane faces task, since both disorders have previously been characterised as having a featural approach to face recognition. Finally, we repeated this design, but instead constructed developmental trajectories linking task accuracy with performance on the three standardised tests: face recognition (Benton), receptive vocabulary (BPVS), and visuospatial construction (Pattern Construction). The first of these was the most relevant since it addressed the key question: for each disorder group, was the normal pattern of face configural processing observed given their level of accuracy on a standardised face recognition task?

14 Page of Development and Psychopathology Identity Recognition We first deal briefly with performance on trials where the two faces were identical, and the participant should have responded same. Group means per condition are shown in Table. No group revealed a main effect of orientation: identity match was equally accurate for pairs of inverted faces. Whether identity recognition trials were presented in configural or featural blocks had no effect on performance in any of the groups. There was no significant interaction of block type on orientation or any other variables, suggesting that trial-blocking of the featural versus configural condition did not trigger specific face-recognition strategies sufficient to affect identify recognition. A comparison of accuracy levels in identity recognition revealed no significant difference between TD group and HFA group (main effect of group: F(,) =., p =., η p =.), nor between TD and DS group (main effect of group: F(,) =.0, p =., η p =.). Children with WS performed reliably better than the TD group on identity recognition (main effect of group: F(,) =., p =.00, η p =.), while the LFA group performed reliably poorer (main effect of group: F(,) =., p =.00, η p =.). ======================= Insert Tables and about here Difference Detection ======================= The mean accuracy levels for each group are provided in Table. Figure depicts developmental trajectories for each group in terms of correct percentage accuracy scores plotted against chronological age (CA). Due to a large number of main effects and interactions, only comparisons directly relevant to current study will be reported. =================== Insert Figure about here

15 Development and Psychopathology Page of =================== TD control group For this stimulus set, participants found it harder to detect configural changes to faces than featural changes (F(,) =., p <.00, η p =.). Developmentally, a different pattern was observed for responses to featurally altered trials than configurally altered trials. Performance on featural trials increased with age (F(,) =., p <.00, η p =.) while orientation of the stimuli had no influence on the accuracy level (F(,) =.0, p =., η p =.0). By contrast, on configural trials, a steady increase in accuracy with age was evident for upright faces (F(,) =., p <.00, η p =.) but a decline in accuracy with age was observed for inverted trials (F(,) =., p =.00, η p =.; interaction of age x orientation: F(,) =.00, p <.00, η p =.). This produced a reliable -way interaction of orientation x transformation type x age (F(,) = 0., p <.00, η p =.). For configural trials, the upright and inverted trajectories diverged at :0 (the point at which the confidence intervals around the regression lines ceased to overlap). For this task, then, the inversion effect for configural trials therefore emerged shortly before years of age. This pattern replicates previous findings demonstrating that configural face processing, measured by sensitivity to spacing changes between the features in a face, is later developing that featural processing (e.g., Mondloch et al., 00). Configural processing is disrupted by inversion while featural processing is not, explaining the increasing inversion effect observed for configurally altered faces across development. Disorder group analyses HFA group As with the TD group, the HFA group performed more poorly on configurally altered faces than featurally altered faces (F(,) = 0., p <.00, η p =.). Performance on featural

16 Page of Development and Psychopathology trials increased with age (F(,) =., p =.0, η p =.) and again, orientation of the stimuli had no influence on the accuracy level (F(,) =.0, p =., η p =.0). Notably, for the HFA group, configural trials exhibited the same pattern, with a reliable increase across age (F(,) =., p =.00, η p =.) but no effect of orientation (F(,) =., p =., η p =.0). The marker for the emergence of configural processing an increasing inversion effect with age was noticeably absent. Comparison to TD trajectory The HFA group was overall less accurate in comparison to the TD group (F(,) =., p =.0, η p =.), indicating a delayed onset in development. The HFA and TD groups had a similar rate of improvement with age (effect of age x group: F(,) =., p =.00, η p =.0), but note that it was at the marginal level. Inversion effects emerged differently in the two groups across age (interaction of orientation x age x group: F(,) =., p =.0, η p =. ), and a reliable -way interaction including trial type confirms that this was due to the lack of an emerging inversion effect for configural trials (F(,) =., p =.00, η p =.). Children in the HFA group failed to exhibit the hallmark of the typical development of face recognition skills. As a more sensitive comparison of the rate of development, we focused on group differences on upright trials. This is because group overlap could result either from delayed improvement on upright trials in the disorder group or from the normal decline in performance on inverted configural trials in the TD group. Focusing on configural upright faces, the HFA group was marginally less accurate in comparison to the TD group (F(,) =., p =.0, η p =.), indicating a delayed onset in development, but had similar rate of improvement with age (effect of age x group: F(,) =., p =., η p =.0). By contrast, there were no differences on the featural upright faces between the groups (all p>.0).

17 Development and Psychopathology Page of LFA group The LFA group displayed the most variability in the performance of all the disorder groups. In line with the other groups, the LFA children exhibited a greater difficulty in the recognition of configurally transformed faces than featurally transformed faces (F(,) =.0, p =.0, η p =.). Overall performance did not improve with age (F(, ) =.0, p =.00, η p =.) but this masks one surprising interaction. Strikingly, for featural trials, performance was initially better on inverted than upright trials. Inverted performance then declined with age, while that on upright trials improved, with the two trajectories crossing over around years of age (interaction of age x orientation: F(,) =., p =.00, η p =.; negative gradient for inverted trials with age: F(,) =., p =.00, η p =.). That is, for featural trials, until the age of, young children in the LFA group performed better on inverted trials than upright ones; and indeed, Table shows that the overall accuracy on the inverted trials was higher (%) than on the upright ones (0%). For configural trials, neither effects of age nor orientation nor their interaction were reliable (all p >.). Comparison to TD trajectory An inspection of Figure suggests that the LFA group had lower overall performance compared to the TD group. However, there were neither reliable differences in the onset of development nor rate of improvement across age (all p>.0) The two groups showed a different relationship in the way inversion altered performance across age (-way interaction of orientation x age x group: F(,) =., p <.00, η p =.), an interaction that was observed separately for featural and configural trials (F(,) =., p =.00, η p =.; F(,) =., p <.00, η p =.). As with the HFA group, the LFA group did not exhibit the hallmark of the development of configural processing the emerging inversion effect on

18 Page of Development and Psychopathology configural trials which was confirmed by a reliable -way interaction of task x orientation x age x group (F(,) =., p <.00, η p =.). A focus on upright trials revealed that for the configural condition, the LFA group were no less accurate compared to the TD group, indicating a similar onset in development (F(,) =.0, p =., η p =.0), but had a slower rate of improvement with age (effect of age x group: F(,) =., p =.0, η p =.). There were no group differences on the featural upright faces (all p>.). DS group As depicted in Figure, the DS trajectories exhibited the familiar pattern of better accuracy on featural over configural trials (F(,) =., p =.00, η p =.). Overall, presentation of the faces in different orientations had no influence on accuracy levels (F(,) =.0, p =., η p =.0) and performance did not improve reliably with increasing age, although there is a very weak trend in that direction (F(, ) =.00, p =.0, η p =.). This pattern held when featural and configural trials were analysed separately. Comparison to TD trajectory Direct comparison against the TD group indicated that the rate of development of the DS group improved significantly more slowly with age (interaction of group x age: F(,) =., p <.00, η p =.), but not reliable statistical group difference emerged in the onset (p<.0). The DS group was less affected by stimulus orientation compared to the TD group (interaction of orientation x group: F(,) = 0., p =.00, η p =.). This overall effect stemmed from the lack of an emerging inversion effect for configural trials, once more resulting in a reliable -way interaction of task x orientation x age x group (F(,) =., p <.00, η p =.). Focusing on the upright faces, the DS group was no less accurate at onset

19 Development and Psychopathology Page of in comparison to the TD group (p>.), but a slower rate of development in the DS group approached significance (effect of age x group: F(,) =., p =.0, η p =.0). No group differences were apparent on upright featural trials (p>.). WS group As with the other groups, children in the WS group found it easier to detect featural alterations between faces than configural changes (F(,) =., p =.0, η p =.). Accuracy performance increased reliably with age (F(, ) =.0, p =.0, η p =.0), but was not influenced by orientation (F(,) =., p =., η p =.0). Neither did these two factors interact. This pattern was also found when featural and configural trials were analysed individually, with the exception that performance on configural trials was poor and did not improve with increased age (F(,) =., p =., η p =.0). Comparison to TD trajectory An inspection of Figure suggests that the WS group had lower overall performance compared to the TD group. However, there were neither reliable differences in the onset of development nor rate of improvement across age (all p<.0) Once more, inversion affected the disorder group and the TD group differently. The emerging inversion effect for configural faces was absent in WS, leading to a reliable -way interaction of task x orientation x age x group: (F(,) =.0, p <.00, η p =.). The WS group did not yield poorer accuracy on the upright faces in comparison to the TD group (p>.), indicating a similar onset in development, but rate of improvement with age on the configural trials was slower (effect of age x group: F(,) =., p =.00, η p =.). No group differences were apparent on upright featural trials (p>.).

20 Page of Development and Psychopathology Intra- and inter-disorder comparisons Autism groups The two autism groups were compared to investigate the influence of the severity of the disorder on configural processing. Overall, there was no main effect of group (F(,) =., p =.0, η p =.0). However, children in the HFA group exhibited a faster rate of improvement over development than the LFA group (age x group: F(,) =., p =.0, η p =.). For featurally transformed faces, a differential effect of inversion was apparent. As we noted previously, for the LFA group, inverted faces are initially processed more accurately but this declines with age, whereas the HFA group did not show this pattern (group x orientation x age: F(,) =., p =.0, η p =.). ASDs and WS Autism and WS have both been characterised as exhibiting featural face recognition. A comparison of HFA and WS groups indicated no overall group difference (F(,) =., p =., η p =.0), although the WS group showed a slower rate of improvement with age (effect of age x group: F(,) =., p =.0, η p =.). Separate analysis of conditions revealed a similar pattern of development on featural sets (F(,) =.0, p =., η p =.0), but the HFA group showed faster rate of development on configural trials (age x group: F(,) =., p =.0, η p =.). The deficit in configural processing therefore appeared to be more severe in the WS group than the high-functioning autism group. In contrast, LFA group showed similar performance with age on configural (age x group: F(,) =., p =., η p =.) but the WS group was significantly faster on featural trials (F(,) =., p =.0, η p =.).. Mental age as a predictor Although none of the disorder groups exhibited an inversion effect - the behavioural hallmark of the emergence of configural processing. This might have represented the pattern of

21 Development and Psychopathology Page 0 of performance one would expect for their level of face recognition. Configural processing, after all, is argued to be related to expertise in face recognition, and each disorder group has been reported to have deficits in this ability. In other words, for the developmental stage that the face recognition system had reached in each disorder, perhaps configural processing would not yet have been expected. We tested this by constructing developmental trajectories linking task accuracy with performance on a standardised test of face recognition, the Benton. We used the Benton raw score, which for the TD group exhibited a linear increase with CA, with age accounting for % of the variance (F(, ) = 0., p <.00). In addition, we constructed the trajectories according to test age on the BPVS and on Pattern Construction. If the differences in configural processing between a given disorder group and the TD group were caused by generally delayed development in the disorder group, then plotting trajectories according to the appropriate measure of Mental Age would serve to normalise the disorder trajectories that is, they should now match the pattern observed in the appropriate CA band of the TD trajectories. Figure displays the developmental trajectories plotted against Benton raw score, for all groups. In no case was the pattern in a disorder group normalised by plotting according to performance on a face recognition test. A similar picture emerged when BPVS and PC Mental Age were used to predict performance. Moreover, neither served as a better predictor of performance than CA. Crucially, then, even when the groups were matched on how well they recognised faces, differences were very apparent between the trajectories of the TD group and each disorder group. =================== Insert Figure about here =================== 0

22 Page of Development and Psychopathology Discussion Configural processing in face recognition is a sensitivity to the spacing of features within the face, and it has been argued both that represents a higher level of expertise in face recognition, and also that it is a developmentally vulnerable process. Moreover, processing of configural information is more easily disrupted by inversion than the processing of featural information, and this was the manipulation that we used to test the emergence of configural processing in typical and atypical development. In a cross-sectional sample of typically developing children between the ages of and, we observed an emerging inversion effect to detect configural changes but not featural changes between faces, against a background of improving face recognition performance. This pattern is consistent with previous findings (e.g., Brace et al., 00; Freire et al., 000; Freire & Lee, 00; Leder & Bruce, 000; Mondloch et al., 00). In our study, cross-sectional developmental trajectories for detecting configural changes in upright versus inverted faces reliably diverged by around years of age. We investigated whether the developmental disorders of autism spectrums, Down syndrome, and Williams syndrome also displayed this pattern, with the first group split into high- and low-functioning children. With respect to the two principal experimental manipulations (transformation type, orientation), all groups showed the same qualitative pattern for transformation type for all participants it was easier to detect featural changes than configural changes of faces. This gives us confidence that all groups were engaged in the task and that task performance was sensitive to the experimental manipulations. The effect of inversion, and its interaction with transformation, differed across disorder groups. The high-functioning children with autism exhibited no inversion effect for either featurally or configurally altered faces, while task performance improved robustly across the - year range examined. Assessed over a similar age range, the low-functioning group performed at a lower level and developed more slowly. Once more, no inversion effect was

23 Development and Psychopathology Page of observed for configurally altered faces. However, for featurally altered faces, the youngest children found it easiest to make the discrimination for inverted rather than upright faces, a unique pattern among all the groups. A similar pattern was reported for this group of children in a different task involving holistic processing (Annaz et al., 00), and also in a study by Hobson and colleagues (), suggesting this unusual effect is a real one. Its likely interpretation is an aversion to upright faces (or the eye region of upright faces) in young lowfunctioning children with autism and thus more focused attention on inverted faces A recent review of face recognition in ASDs by Weigelt, Koldewyn and Kanwisher (0) concluded that face processing in ASDs was not qualitatively different from typical development but was quantitatively poorer. We did not find that result here: the absence of configural inversion effects in both ASD groups and the presence of a featural inversion effect in the low-functioning group appear qualitatively atypical, even when cross-sectional trajectories were constructed in relation to performance on a standardised test of face recognition (we return to this point below). Weigelt, Koldewyn and Kanwisher s conclusion was based on reviewing the literature on markers of typical face processing, including the following effects: inversion, part-whole, composite, inner vs. outer features, face space, Thatcher illusion, and left-side bias. It is notable that of these, the face-space marker which is a clear index of configural processing showed the strongest evidence of qualitative differences (see Weigelt, Koldewyn & Kanwisher, 0, Figure ). The current data, then, are in keeping with the view that configural processing may be the most (or only) qualitatively atypical characteristic of face recognition in autism, and may point to a greater reliance on featural processing. Face recognition in WS has also sometimes been referred to as featural (Deruelle et al., ; Karmiloff-Smith, ; Karmiloff-Smith et al., 00). Here, the data were suggestive of an effect of inversion, but it was far from reliable, nor did it emerge across

24 Page of Development and Psychopathology development in the configural condition. Configural processing was slow to develop in this group, more so than in the HFA group. The interpretation then, is that configural processing represents a particular deficit in the WS group (Karmiloff-Smith et al., 00). For the DS group, performance on the task was poor, revealing only slight improvement across age and no reliable inversion effect (though the data here were noisy). As with the WS group, the trajectories were indicative of an inversion effect but far from reliable. Again, there was no evidence of the emerging inversion effect in the configural condition, contrary what is observed in typical development. This result, along with previous reports (Kaiser et al., 00; Wishart & Pitcairn, 000), points overall to poor face recognition abilities in DS group. When developmental trajectories were constructed linking task performance against performance on a standardised task of face recognition (Benton et al., ) instead of chronological age, the main results still held. This supports the view that the differences between groups were not due to different levels of face recognition ability. Some caution is required here, since the Benton test can be performed using a pixel-matching strategy instead of a face-identity matching strategy (Duchaine & Nakayama, 00). Nevertheless, for the lack of an inversion effect in the configural condition to have been explained by delay alone, no disorder group would need to have face recognition abilities beyond those of a -year-old, something we deem unlikely for the children tested here. Overall, our findings are consistent with the view that configural processing is developmentally vulnerable, since we did not find markers of its presence in any of our disorder groups. The data nevertheless suggest that there are alternative developmental pathways to achieve relatively good performance levels in face recognition. However, these differ between disorder groups. In the HFA group, the level of performance appeared to be driven by reliance on strong featural processing. In the WS group, it is likely to be driven by

25 Development and Psychopathology Page of the brute force of massive of practice effects (given the unusual interest in faces shown from infancy onwards by individuals with WS), sufficient to reduce some deficits in configural processing (see Annaz et al., 00, for discussion). Compensation, however, is not always possible: performance in the LFA and DS groups was much poorer. Yet again, the pattern in these two groups differed. There was an apparent aversion to upright faces observed in the younger children with in the LFA group, a behaviour not observed in the DS group. In sum, our study highlights the importance of cross-syndrome approacj which revealed the constraints that shape the typical development of face recognition. The relative balance of featural and configural processing as strategies to drive recognition, the protracted developmental trajectory of configural processing as a pathway to drive expert levels of recognition, and the influence of motivation factors in perceiving faces and providing the input to driving improving recognition.

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30 Page of Development and Psychopathology Lord C, Rutter M, DiLavore P, Risi S. Autism Diagnostic Observation Schedule (ADOS). Los Angeles: Western Psychological Services,. Maurer, D., Le Grand, R., & Mondloch, C. J. (00). The many faces of configural processing. Trends in Cognitive Sciences, (), -0. McPartland, J., Dawson, G., Webbs, S. J., Panagiotides, H., & Carver, L. J. (00). Eventrelated brain potentials reveal anomalies in temporal processing of faces in autism spectrum disorder. Journal of Child Psychology and Psychiatry, (), -. Mervis, C. B., & Bertrand, J. (). Developmental relations between cognition and language: Evidence from Williams syndrome. In L. B. Adamson & M. A. Romski (Eds.), Research on communication and language disorders: Contributions to theories of language development (p. -0). New York: Brookes. Mervis, C.B., Robinson B.F., Bertrand, J., Morris, C.A., Klein-Tasman, B.P., & Armstrong, S.C. (000). The Williams syndrome cognitive profile. Brain and Cognition,, 0-. Mills, D., Alvarez, T., St. George, M., & Appelbaum, L. Bellugi, U. & Neville, H. (000). Electrophysiological studies of face processing in Williams syndrome. Journal of Cognitive neuroscience, : Supplement, -. Mobbs, D., Garrett, A. S., Menon, V., Rose, F. E., Bellugi, U. & Reiss, A.L. (00). Anomalous brain activation during face and gaze processing in Williams syndrome. Neurology, (/), Mondloch, C. J., Le Grand, R., & Maurer, D. (00). Configural face processing develops more slowly than featural face processing. Perception, (), -. Morris, C. A., Demsey, S. A., Leonard, C. O., Dilts, C. & Blackburn, B. L. (). The natural history of Williams syndrome: physical characteristics. Journal of Paediatrics,, -.

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32 Page of Development and Psychopathology individuals with autism and Asperger syndrome. Archives of General Psychiatry,, -0. Schopler, E., Reichler, R., & Rochen, B. (). The Childhood Autism Rating Scale. Western Psychological Services, Los Angeles. Searcy et al., (00). The relationship between age and IQ in adults with Williams syndrome. American Journal on Mental Retardation, 0(), -. Tassabehji, M. (00). Williams-Beuren syndrome: a challenge for genotype-phenotype correlations. Human Molecular Genetics, (), -. Thomas, M. S. C., Annaz, D., Ansari, D., Scerif, G., Jarrold, C., & Karmiloff-Smith, A. (00). The use of developmental trajectories in studying genetic developmental disorders. Journal of Speech, Language, and Hearing Research,, -. Wallace, S., Coleman, M., & Bailey, A. (00). Face and object processing in autism spectrum disorders. Autism Research,,. Williams, K.R., Wishart, J. G., Pitcairn, T. K., & Willis, D. S. (00). Emotion recognition by children with Down syndrome: investigation of specific impairments and error profiles. American Journal on Mental Retardation, 0, -. Wishart, J. G., & Pitcairn, T. K. (000) The recognition of identity and expression in faces by children with Down syndrome. American Journal on Mental Retardation, 0, -. Wishart, J. G., Cebula, K. R., Willis, D. S. & Pitcairn, T.K. (00). Understanding of facial expressions of emotion by children with intellectual disabilities of differing aetiology. Journal of Intellectual Disability Research,, -.

33 Development and Psychopathology Page of Figure captions Figure. Example of the Jane faces stimuli (Mondloch et al., 00). Panel A illustrates a sample of featurally altered faces and configurally altered faces, panel B shows upright and inverted orientations. Reproduced with permission. Figure. Developmental trajectories for accuracy scores on the Jane faces task plotted against chronological age (in months), for each disorder group. Figure. Developmental trajectories for accuracy scores on the Jane faces task plotted against raw score on the Benton face recognition test (Benton, ), for each disorder group.

34 Page of Development and Psychopathology Figure A B