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Recognition of biologicalmotion in children withautistic spectrum disorders

C . P A R R O N CNRS, Marseille, France

D. D A F O N S E C A Ste Marguerite Hospital, Marseille, France

A . S A N T O S CNRS, Marseille, France

D. G . M O O R E University of East London, UK

E . M O N F A R D I N I CNRS, Marseille, France

C . D E R U E L L E CNRS, Marseille, France

A B S T R A C T It is widely accepted that autistic children experiencedifficulties in processing and recognizing emotions. Most relevantstudies have explored the perception of faces. However, context andbodily gestures are also sources from which we derive emotionalmeanings. We tested 23 autistic children and 23 typically developingcontrol children on their ability to recognize point-light displays of aperson’s actions, subjective states and emotions. In a control task,children had to recognize point-light displays of everyday objects. Thechildren with autism only differed from the control children in theirability to name the emotional point-light displays. This suggests thatchildren with autism can extract complex meanings from bodily move-ments but may be less sensitive to higher-order emotional informationconveyed by human movement. The results are discussed in the contextof a specific deficit in emotion perception in children with autism.

A D D R E S S Correspondence should be addressed to: C H R I S T I N E D E RU E L L E ,CNRS-INCM, 31 Chemin Joseph Aiguier, 13402 Marseille Cedex 20, France. e-mail: deruelle@incm.cnrs-mrs.fr

Introduction

Humans are an intensely social species. As a consequence, the human visualsystem may have evolved to rapidly and effortlessly detect and extractsocially relevant information, even from perceptually degraded stimuli.One classic example of this process is demonstrated in people’s responsesto human point-light displays (PLDs). Human PLDs are made by attachinga set of point lights to the joints of a human who is then filmed moving

autism © 2008SAGE Publicationsand The National

Autistic SocietyVol 12(3) 291–304; 089520

1362-3613(200805)12:3

www.sagepublications.comDOI: 10.1177/1362361307089520

K E Y W O R D S

autisticchildren;

biologicalmotion;

configuralprocessing;

emotion

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in a dark room (e.g. Maas and Johansson, 1971). Studies have demonstratedthat these displays provide sufficient information for typical adults andchildren to derive very subtle meanings about the person filmed, such asthe kind of action they are executing (e.g. Dittrich, 1993), their gender,their identity (Cutting, 1978; Troje, 2002), their deceptive intentions andeven the their emotional state (Dittrich et al., 1996; Pollick et al., 2003).

People with autistic spectrum disorders (ASDs) are reported to haveperceptual difficulties (e.g. Deruelle et al., 2006), and their perception ofmotion may be particularly impaired (e.g. Milne et al., 2002). Consequentlyone might suspect that people with autism would have difficulties in perceiv-ing the meaning of human PLDs. Furthermore, while deficits in emotionprocessing in faces are well documented in people with autism (e.g. Begeeret al., 2006), less is known about their abilities to perceive emotions ingesture. If emotion perception is a general problem then one might expectchildren with autism to be poor at picking up the emotional gesturesdepicted in human PLDs.

To date there have only been a few studies of autistic children’s responsesto human point-light displays. The first was conducted by Moore andcolleagues (1997) who tested the ability of typically developing children,children and adolescents with mental retardation, and children and adol-escents with ASD to recognize a moving person’s action and emotion-related attitudes when presented in point-light form.

Surprisingly, given the problems that people with ASD are reported tohave in motion perception (e.g. Milne et al., 2002), Moore et al. (experi-ment 1) found that the adolescents and children with and without autismwere similarly able to rapidly identify what a point-light display represented,i.e. whether it was a person or a moving object – suggesting, for this sampleof children at least, that their basic ability to recognize the underlying formof human point-light displays was relatively intact. However, differenceswere found in the abilities of the children with autism to name the person’semotional and subjective states (experiments 2 and 3).

Moore et al. compared mentally retarded children and adolescentsmatched for chronological and mental age with children and adolescentswith autism. They found that the participants with autism were specificallyimpaired in naming subjective states compared to children with intellec-tual difficulties of similar IQ but had few problems in naming humanactions. The study also showed no differences between the performance ofthe children with learning difficulties and typically developing childrenmatched on mental age. However, as the children with autism had low IQsit was possible that the difficulties these children had with emotion recog-nition might have been related to other intellectual difficulties specific toautism.

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A more recent study by Blake et al. (2003) explored the abilities ofyounger children with autism aged 8 to 10 years to discriminate andperceive point-light displays. Blake et al. presented participants with 1second clips of point-light displays which represented a person engaged inactions such as throwing, jumping and kicking, or out-of-phase, scrambledand thereby meaningless versions of these original actions. Children wereasked to decide whether the display represented a person or not and thiswas repeated over 50 trials. The performance of children with autism wascompared to that of typically developing children matched on mental age.The findings indicated that, compared to typically developing controls,children with autism were impaired in discriminating human from scram-bled motion in these brief point-light displays, while being similar in theirperformance on another visual discrimination task.

The discrepancy between these data and those of Moore et al. may orig-inate from differences in the methods. Whereas Moore et al. (1997) inexperiment 1 used a task that required participants to identify from briefvideo clips an object or a person only once, Blake et al. (2003) employeda task in which participants had to discriminate over many trials. As Hubertand collaborators (2007) commented, it may be that the identification taskused by Moore et al. made fewer sustained attentional demands on childrenwith autism than the prolonged discrimination task used by Blake andcolleagues. Repeated discrimination tasks with short clips may makedemands on working memory that are IQ related. As Blake et al.’s controlgroup was not IQ comparable, it is not possible to discount the effects thatIQ-related information and motion processing abilities might have had onthe PLD task performance of the autistic children.

While Blake et al. did administer a control task on which the childrendid not show any differences, and this was contrasted with the performancedifferences on the target task, this control task was very different from thetarget task. It consisted of a stepwise signal detection task where partici-pants had to detect a static global circular form amongst changing degreesof visual noise. Given that the target biological motion task was examin-ing ability to discriminate between moving displays, whereas the control taskwas examining abilities to detect static forms amongst noise, it is not clearthat the control task was appropriate for determining a specific problemwith biological motion per se – in that it did not actually control for generalmotion perception abilities, which are known to be poorer in childrenwith autism. Differences in performance between the target and controltask in the autistic children may have been a product of general motionperception problems and poorer thresholds of general motion detection inchildren with autism rather than a product of any specific problem withbiological motion. These would be expected to have an additional constraint

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leading to more errors specifically on the target task, which may be morelikely to be apparent over a large number of trials with trials of short dura-tion. In Blake et al.’s biological motion discrimination task there were 50trials with exposure to the moving stimulus lasting only 1 second, whereasin the control task with static stimuli the children had as long as theyneeded to point out the location of the shape. In contrast, in Moore et al.’sexperiment 3, the clips of biological motion of actions lasted for 5 seconds.Here no difficulties were found for the children with autism, compared toIQ-comparable children with IDs, in labelling the actions of the humanPLDs. Thus, while there may be problems in motion detection in childrenwith autism, it is not yet clear from Blake’s findings alone that there areadditional specific problems with the detection of biological motion.

Another source of differences between the findings could rest in thedifferent age range, with the autistic participants being younger in theBlake et al. (2003) study than in the Moore et al. (1997) study. It may bethat the ability to recognize and discriminate between human and non-human point-light displays improves with age. To partly reconcile theseissues, Hubert et al. (2007) replicated experiment 3 of Moore et al. (1997)’sstudy. However, to exclude the possible impact of IQ-related effects theyexplored the responses of high-functioning adults with ASD who did nothave mental retardation. Consistent with Moore et al.’s (1997) data, theirfindings indicated that the adults with ASD performed as well as the controlgroup in describing (5 second) point-light movies depicting simple actionsand in identifying manipulated objects. In contrast, the high-functioningASD adults performed significantly poorer than controls in the emotionand state labelling condition.

The finding that the adults with ASD had few problems in identifyingactions, but had a specific problem with recognizing subjective states andactions, suggests that the recognition of higher-level subjective meaning maybe a core deficit for adults and older children with autism. However, aremaining question is whether younger children with ASD show a generaldeficit in perceiving PLDs or also show a selective deficit in perceiving theemotional meaning they convey.

The purpose of this study was first to assess the performance of high-functioning children with autism and compare this with IQ-comparabletypically developing children to see if the problems identified in low-IQchildren with autism (Moore et al., 1997) and in high-functioning adultswith autism (Hubert et al., 2007) were also found in high-functioningchildren with autism. The second objective was to compare the perform-ance of the high-functioning children with autism to the data reported byHubert et al. (2007) to see whether there were any developmental trendsin the perception of these displays as from childhood to adulthood.

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The children and adolescents tested here were similar in age to thosetested by Moore et al. (1997) and also were closer in age to those testedby Blake et al. (2003), although of higher ability. As with the Hubert et al.study, we used the stimuli developed by Moore et al. (1997) and partlyreplicated experiment 3 of this study, showing children human point-lightdisplays depicting actions, subjective states and emotions, and also controldisplays that showed point-light displays of moving objects. Our mainquestions were: (1) whether high-functioning children with autismshowed the same specific problem with perceiving emotional material inthese displays; and (2) to what extent performance is comparable or notto that reported for high-functioning adults with autism.

Method

ParticipantsTwo experimental groups participated in this study. The first groupincluded 23 children with ASD (20 boys and three girls) aged 7 to 18 years(mean = 11 years 7 months; SD = 3 years 2 months). They were diag-nosed according to the DSM-IV (American Psychiatric Association, 1994)and/or the ADI–R (Lord et al., 1994). In addition, parents of all subjectswere asked to answer the Autism Spectrum Screening Questionnaire (ASSQ:Ehlers et al., 1999) during a semi-directive interview. All participantsscored positively on the ASSQ. Full-scale IQ scores were measured usingthe WAIS–III or WISC–III (Wechsler, 1997 and 1996 respectively), accord-ing to the subject’s age. IQs ranged from 85 to 120 (mean = 93.7; SD=15). Note that no significant difference was observed between verbal andperformance IQ scores (mean verbal = 93, SD = 19.4; mean performance= 89, SD = 13; t(1, 22) = 0.91, p = 0.36).

As the mean scores of IQ were in the normal range, the ASD partici-pants were matched to a control group of 23 typically developing children(20 boys and three girls) on the basis of gender and CA (mean age = 12years, SD = 2 years 5 months). These children were recruited via localschools and daycare centres and they all attended normal classes corre-sponding to their age level. Their teachers were asked to select children onthe average level of the class, thus avoiding including children eitherparticularly advanced or delayed relative to their age.

Children with ASD were recruited via the Department of Child Psychi-atry at the local hospital (Sainte-Marguerite Hospital, Marseille). They allattended normal classes at local schools. At the time of testing, none of theparticipants had known associated medical disorders or overt physicalhandicap. All participants were native French speakers and had normal or

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corrected-to-normal vision and audition. Informed consent was obtainedfor all subjects and the experimental procedure was approved by the localethics committee

Tasks and stimuliTasks and stimuli were similar to those used in Moore et al. (1997, exper-iments 2 and 3). There were a total of 20 video clips each of around 5seconds duration displaying dynamic PLDs. Ten video clips were of a maleactor performing actions (see Table 1 for a detailed description). The humanpoint-light displays were the same as those used in Moore et al. (1997).There were also five clips of the actor displaying subjective states – actionsthat reflect an underlying state such as itchiness or tiredness – and five clipsof the actor depicting emotional actions – happy, angry etc. (again seeTable 1 for detailed descriptions). There were also a further five controlstimuli of manipulated PLDs of everyday objects: a ball rotating, a pair ofkitchen balance scales moving as a weight was added, an ironing board beingopened and closed, a dustpan and brush sweeping, and a saw in action. Ineach case 10 reflective point lights were distributed across the object in amanner that meant the object was not recognizable from a still image.

ProcedureParticipants were individually tested in a quiet room at the National Centrefor Scientific Research. They were seated in front of a computer screen ata viewing distance of 60 cm. Participants were told that they were goingto be presented with short movies and that they were going to be asked todescribe orally what they had seen. Verbal responses were noted by theexperimenter. Responses were scored as correct when participants accu-rately captured the object, the action, the state or the emotion portrayed bythe PLDs. It is important to note that responses were also considered ascorrect when participants provided a synonymous word that indicated theobject, the action, the state or the emotion captured by the PLDs. Eachsubject underwent a total of 25 trials: 10 in action condition (Act), five inthe subjective states condition (Subj), five in the emotional states condition(Em), and five in the object condition (Obj). The order of trials presentationwas randomized across subjects.

Results

Accuracy rates1 obtained by the two groups in the four conditions wereanalysed using a two-way ANOVA with group (ASD versus control) as thebetween-subjects factor and condition (actions versus subjective statesversus emotions versus objects) as the within-subjects factor. The main

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imes

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gets

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son

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e fr

ont

and

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left

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e 1

Des

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05 PARRON 089520 27/2/08 2:51 am Page 297

effects of both group (F(1, 44) = 14.3, p < 0.001) and condition (F(3,132) = 46.4, p < 0.001) were found to be significant.

Most importantly, the group by condition interaction was also signifi-cant (F(3, 132) = 6.5, p < 0.001) (see Figure 1). To further explore thesource of the interaction effect, post hoc analyses were conducted using TukeyHSD tests. The results of these analyses revealed that the performance ofASD children differed from that of TD children in the emotion condition(p < 0.001) but not in the other three conditions (all p > 0.05). In addition,the results of Tukey HSD tests showed that control children were moreaccurate on the emotion than on the object condition (p < 0.001). Bycontrast, no such difference between emotion and object recognition wasfound for ASD children (p > 0.05).

In order to assess the possible effect of IQ on the performance of theASD group, analyses of covariance (ANCOVA) were conducted on accuracyrates using condition (action, subjective state, emotion and object) as awithin-subjects factor and with IQ as a covariate. These analyses revealed

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Figure 1 Illustration of the mean modified accuracy rates and correspondingstandard errors in the four conditions of point-light displays (actions, subjectivestates, emotions, objects) for the ASD and the typically developing control groups

setarycar

uccadeifi

do

mnae

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Conditions

0

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ASD

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that the IQ did not modulate differences found across conditions (F(1, 87)= 3.01, p > 0.05).

Additional analyses of regression were also conducted to further trackresults. In particular, these analyses aimed at determining whether theability to perceive the emotional meaning of PLDs might change with age.To this aim, we pooled together data from 46 children (current study) and38 adults with ASD (Hubert et al., 2007; see note 2 for a detailed descrip-tion of adult participants). Note that data from the adults with ASD werecollected using the same experimental paradigm as that used in the presentstudy. Analyses of regression were thus conducted on 84 individuals withASD. The basic regression model used in this analysis comprised a groupcontrast (control = –1,ASD = +1) and chronological age (months). Analyseson performance in the emotion condition yielded an overall effect for thebasic model (F(2, 81) = 19.78, p < 0.0001 (R2 = 0.32)). The groupcontrast was a significant negative predictor of emotion recognition (F(1,81) = –5.99, p < 0.001 (� = –0.54)), suggesting that the ASD group wasless accurate than the control group in the emotion condition. In contrast,chronological age was not a significant predictor of emotion recognition(� = 0.15), indicating that the performance in emotion condition was un-related to age. Interestingly, multiple regression analyses on the other threeconditions showed a significant age effect on actions (F(1, 81) = 2.69,p < 0.01 (� = 0.27)), subjective states (F(1, 81) = 3.07, p < 0.01 (� =0.30)), and object conditions (F (1, 81) = 4.52, p < 0.001 (� = 0.45)).

Note that the factor gender was not included because preliminaryanalyses showed no significant effect on performance.

Discussion

This study compared the perception of emotional and non-emotional bio-logical motion in children with autism and typically developing children.Several important conclusions can be drawn from this experiment.

The main finding of the current study is that children with ASD do havethe ability to extract meaning from PLDs. Yet this ability was found to bedependent on the nature of stimuli displayed. In fact, children with ASDwere impaired in interpreting PLDs with emotional value, but performedas accurately as controls on point-light movies depicting simple personalactions, subjective states and objects. These results clearly indicate thatchildren with autism understood the task demands and were able tocorrectly label PLDs. The interpretation of point-light biological motionanimations undoubtedly requires the ability to integrate information toextract the form of the animate figure (e.g. Johansson, 1973). In that respect,our findings are at odds with Blake’s results showing that children with

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autism were impaired in point-light display processing. Furthermore, ourfindings are consistent with both Moore et al.’s (1997) and Hubert et al.’s(2007) results which also showed selective impairments in the interpret-ation of PLDs with emotional value.

The findings of the present study take us further in our understandingof how ASD children without mental retardation recognize biologicalmotion. Interestingly, IQ (in this range) was not found to influence ASDchildren’s overall ability to perceive PLDs. In particular, the low accuracyrates on the emotion condition were unrelated to ASD children’s IQ, suggest-ing that deficits in emotion interpretation in autism are independent of theoverall level of functioning, at least with ASD children in the normal IQrange. The relationships between emotional discrimination and mentalretardation have been widely questioned. Although some studies havedemonstrated that subjects with mental retardation do not perform as wellon emotion recognition tasks as control subjects (e.g. McAlpine et al., 1991;Rojahn et al., 1995), the nature of these deficits is unclear (see Moore, 2001and Santos et al., 2007 for reviews on this topic). The results of the presentstudy support the idea that basic emotion-perception capacities are un-related to IQ. In this case, one may hypothesize that difficulties in decodingemotional meaning in autism are due to a specific deficit in emotionalprocessing rather than the result of overall lower intellectual functioning.

The second main finding of this article concerns the absence of adevelopmental trend in emotional processing in autism. Children with ASDexhibited similar difficulties with labelling emotional PLDs as found inadults with ASD (Hubert et al., 2007). In contrast, the regression analysesdemonstrated that for children and adults with ASD the performance onobject, action and subjective state conditions did increase with age. Thissuggests that difficulties in processing emotional information are a constantthroughout development in individuals with ASD. Although in line withprevious studies showing emotional deficit in both ASD adults (e.g. Hefteret al., 2005) and children (e.g. Robel et al., 2004), this supposition mayappear at odds with previous reports demonstrating a developmental trendin several cognitive competences that are supposed to be directly involvedin emotion processing such as configural processing. For instance, visualconfigural processing abilities have been shown to increase with age in ASDindividuals with either meaningless (spatial and motion integration withuse of Gabor patches, Del Viva et al., 2006; geometrical stimuli, Rondanand Deruelle, 2005) or meaningful (facial identity, Rondan and Deruelle,2004) tasks. However, the discrepancy between our results and thoseshowing age-related differences in performance may come from the use ofemotional versus non-emotional material. Indeed, none of the studiesshowing increased abilities with age used emotional materials. Thus, the

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results of the present study seem to suggest that improvements with agedo not apply to the processing of emotional materials but perhaps do forother meaningful objects.

Taken together, current findings are in line with previous studies high-lighting specific emotional face-processing deficits in the autistic population(e.g. Celani et al., 1999; Hobson et al., 1988). This conclusion is strength-ened by the finding that whereas control children recognize emotional statesbetter than moving objects, no such difference between emotion and objectrecognition was found for children with ASD. In other words, emotionsseem to have no special status relative to objects for autistic children. Thislack of difference between emotional stimuli and objects is reminiscent ofseveral previous reports on ASD pathology. In Hubert et al. (in press), electro-dermal activity was significantly increased for emotional faces comparedto objects in typically developing adults but not in adults with autism. Inanother study, brain event-related potentials (ERPs) were recorded inchildren with and without ASD presented with photos of the face of thechild’s mother versus an unfamiliar female face and photos of a favouriteversus an unfamiliar toy (Dawson et al., 2002). Data clearly showed thatERP amplitudes were different between familiar and unfamiliar faces andbetween familiar and unfamiliar objects in typically developing children.Children with ASD failed to show any differences in ERPs for a familiarversus an unfamiliar face, but they did show amplitude differences for afamiliar versus an unfamiliar object. Furthermore, neuroimaging studieshave shown that, during face recognition tasks, individuals with autismactivate areas that are thought to underlie object recognition when activatedin typically developing individuals (e.g. Schultz et al., 2000). Together withour findings, this suggests that individuals with autism fail to attributespecial status both to emotional faces and to bodies.

Notes1 In order to normalize the distribution of the percentage of correct answers,

modified accuracy rates were calculated [2 � (ASIN (RACINE (%correct answers/100)))] for each subject in each condition (action/expression/subjective state/object). Before normalization, the average percentages of correct responses were:action = 82.7% (SD = 2.8), emotion = 61.3% (SD = 4.7), subjective states =58.6% (SD = 4.2), objects = 38% (SD = 4.5) for the ASD group; and action =77.2% (SD = 2.9), emotion = 34.4% (SD = 4.9), subjective states = 45.1% (SD = 4.4), objects = 34.8% (SD = 4.8) for the control group.

2 Nineteen high-functioning adolescents and adults with autism or with Aspergersyndrome (mean age = 21 years 6 months, SD = 6 years 1 month; 17 men andtwo women) were included in Hubert et al.’s (in press) study. They were alldiagnosed according to the DSM-IV (American Psychiatric Association, 1994) andthe ADI–R (Lord et al., 1994) criteria for autism. The ASSQ scale (Ehlers et al.,1999) defined 15 participants with Asperger syndrome and four as

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high-functioning autistic individuals. IQ scores were measured with the WAIS–R(Wechsler, 1981) and ranged from 60 to 112 (mean = 83.3, SD = 15.9). None ofthem had known associated mental or physical disorders at the time of testing andvisual examination was found to be normal.

AcknowledgementsThe authors are especially indebted to the autistic and control childrenwho participated in this study. This research was funded by a grant SEDSU(FP6–2003-NEST-PATH).

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