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Emotion recognition by children with Down syndrome: A longitudinal study a

a

Régis Pochon & Christelle Declercq a

Cognition, Health and Socialisation Laboratory, University of Reims Champagne-Ardenne, Reims, France Published online: 23 Aug 2013.

To cite this article: Régis Pochon & Christelle Declercq (2013) Emotion recognition by children with Down syndrome: A longitudinal study, Journal of Intellectual and Developmental Disability, 38:4, 332-343, DOI: 10.3109/13668250.2013.826346 To link to this article: http://dx.doi.org/10.3109/13668250.2013.826346

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Journal of Intellectual & Developmental Disability, 2013 Vol. 38, No. 4, 332–343, http://dx.doi.org/10.3109/13668250.2013.826346

ORIGINAL ARTICLE

Emotion recognition by children with Down syndrome: A longitudinal study

RÉGIS POCHON & CHRISTELLE DECLERCQ

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Cognition, Health and Socialisation Laboratory, University of Reims Champagne-Ardenne, Reims, France

Abstract Background According to the literature, children with Down syndrome (DS) have difficulties recognising facial expressions. Yet abilities to recognise emotional expressions are often assessed in tasks that imply comprehension of words for emotions. We investigated the development of these abilities in children with DS in a longitudinal study that did not involve lexical knowledge of emotions. Method Children with DS and nonspecific intellectual disability and typically developing children matched for developmental age (DA) were assessed once a year over 3 years. They were asked to recognise the facial expression of an emotion after hearing a vocalisation. Results In each annual session, children with DS were not significantly different from others at recognising emotions. Their abilities to discriminate basic emotions improved significantly and to a similar extent to those of other children. Conclusion The findings indicate that children with DS develop emotion recognition abilities similarly to other children of the same DA.

Keywords: Down syndrome, intellectual disability, emotion recognition, emotional development, emotion regulation

Introduction The ability to decode the facial expression of others is considered crucial for the development of socioemotional communication and interpersonal relations (Denham & Weissberg, 2004; Izard et al., 2001). The identification of specific emotional deficits is therefore essential to orient educational and psychological support. As Fidler, Most, and Philofsky (2009) emphasised, current research attempts to increase the understanding of specific outcomes caused by genetic disorders in order to describe the behavioural phenotype linked to a given disorder. Among these, Down syndrome (DS) is the most common genetic intellectual disability; in fact, contrary to widespread expectations, the population with DS is growing rather than decreasing (Wishart, 2007). Yet although DS has received growing attention from researchers in the two last decades (Fidler, 2005, 2006), emotional development has remained underexplored, particularly from a

longitudinal perspective (Cebula, Moore, & Wishart, 2010; Wishart, 2007). The current study, which has a longitudinal design, aims to expand our knowledge of emotional development in DS. This field has long attracted only limited interest among researchers, notably because of the stereotype of high sociability in persons with DS (Pitcairn & Wishart, 1994). This positive stereotype has often led researchers to recruit children with DS as a control group. For instance, in studies of impaired social interaction and communication in autism spectrum disorder, children with DS were chosen because of their presumed “protected” social-emotional functioning (Celani, Battacchi, & Arcidiacono, 1999; Dawson, Meltzoff, Osterling, Rinaldi, & Brown, 1998; Loveland et al., 1994). Some studies have found little or no emotion recognition deficit in children with DS. For example, Turk and Cornish (1998) reported no difference

Correspondence: Régis Pochon, Laboratoire C2S (Cognition, Santé, Socialisation), EA 6291, Université de Reims Champagne-Ardenne, 57 rue Pierre Taittinger, 51096 Reims Cedex, France. E-mail: [email protected] © 2013 Australasian Society for Intellectual Disability, Inc.

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Emotion recognition by children with DS between children with fragile X syndrome (mental age of 3–7 years), children with DS, or typically developing (TD) children, matched for mental age, in recognition of facial expressions (happiness, sadness, anger, and fear) or emotional vocalisations. Nevertheless, in this experiment children with DS performed worse than TD children in matching a context with the appropriate facial expression. Still, as Moore (2001) pointed out, this kind of task makes a greater cognitive demand and seems unsuitable for children with intellectual disability. Celani et al. (1999) compared the performance of children with autism spectrum disorder (ASD), children with DS, and TD children at a delayed emotionmatching task, in groups that were matched for verbal mental age (around 7 years). The children with DS presented similar abilities to the TD children when asked to recognise expressions of happiness and sadness, and when required to rate the valence of emotional expressions or emotional situations. On the basis of their previous work (Kasari, Freeman, Mundy, & Sigman, 1995; Kasari, Mundy, Yirmiya, & Sigman, 1990), Kasari, Freeman, and Hughes (2001) initially assumed that the interest of children with DS in other people’s faces could be an advantage in developing socioemotional abilities. Contrary to this positive expectation, the researchers’ results showed a tendency toward stabilisation of emotional knowledge in children with DS with a mental age of 4 years and older and difficulties in identifying anger. Similarly, several later studies dedicated to DS noted weaknesses in emotion recognition (Williams, Wishart, Pitcairn, & Willis, 2005; Wishart, Cebula, Willis, & Pitcairn, 2007; Wishart & Pitcairn, 2000). In the Wishart and Pitcairn (2000) study, children with DS aged 8–14 years old were matched using the face recognition task from the Kaufman Assessment Battery for Children (K-ABC; Kaufman & Kaufman, 1983) with younger TD children (3–5 years). Another control group consisted of children with nonspecific intellectual disability (NSID) of similar chronological age (CA). Compared to the TD group, children with DS performed significantly worse on a facial expression matching task involving six primary emotions (happiness, sadness, surprise, fear, anger, and disgust); they had particular difficulty recognising fear and surprise. The results of the children with NSID were no different from those of the TD children. Given the poor performance of children with DS noted in Wishart and Pitcairn’s (2000) experiment, as in Kasari et al.’s (2001) study, Williams et al. (2005) hypothesised that there might be a specific impairment of emotion recognition in DS. DS, TD,

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and NSID groups were matched for mental age and Benton Facial Recognition Test scores. The visualemotional stimuli were black-and-white slides expressing the six basic emotions. When matching an emotion label with a facial expression, the score obtained by children with DS was lower than that of TD children of the same mental age (3–6 years) but similar to that of their peers with NSID. An analysis of the results per expression showed that their performance was lower essentially when recognising fear. This difficulty recognising the expression of fear, in comparison with TD children, was also found by Wishart et al. (2007) in a cross-syndromic study that aimed to compare emotion recognition capacities in children with DS, fragile X syndrome, and NSID. Other deficits in emotion recognition are mentioned in the literature about DS. For instance, Porter, Coltheart, and Langdon (2007) presented emotional stimuli (faces, voices, and postures) to children and adults with Williams syndrome (WS) and DS and TD participants individually matched for mental age (4–6 years) and CA (5–44 years). The results showed that the DS group had more difficulties recognising negative emotions, particularly sadness, than the WS and TD groups. Another aspect of difficulties in children with DS is the hedonic processing of emotion expressed by faces. Kasari et al. (2001) noticed that children with DS more often chose a positive expression instead of a negative expression and vice versa. Such hedonic tone misidentification was also found in Porter et al.’s (2007) study. Finally, atypical errors are highlighted by Williams et al. (2005) and Wishart et al. (2007): children with DS tended to confuse fear with sadness, whereas the other children tended instead to confuse fear with surprise. In conclusion, the review of the literature revealed that children with DS (a) have more difficulties recognising negative basic emotions, especially fear; (b) they often fail in the processing of emotional valence; and (c) they produce more atypical error patterns. The convergent nature of the problems shown by different studies supplies growing evidence of an impairment of emotion recognition specific to children with DS. Yet this conclusion may be premature for several reasons. First, it should be stressed that the problems previously mentioned were found in comparisons with TD children. No studies showed significant differences when comparing recognition scores between children with DS and children with NSID. This fact reduces the strength of the conclusion that there may be a specific deficit: consequently, how should we interpret the results

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of the children with NSID? Should they be considered as typical or as the possible consequence of a subtle deficit? Second, although the methods used minimised the use of language and/or controlled for linguistic level, they often involved the understanding of emotional labels. Given that Lindquist, Barrett, Bliss-Moreau, and Russell (2006) showed that emotional language influences the perception of emotion, the use of emotional lexicon in the assessment of children with language impairment, as is often the case for children with DS (Yoder & Warren, 2004), seems inappropriate. Moreover, Williams et al. (2005) and Wishart et al. (2007) emphasised the need for longitudinal data to confirm their findings. Indeed, as emphasised by Thomas et al. (2009), longitudinal studies are better suited than cross-sectional designs for validating developmental trajectories and identifying atypical development. Furthermore, Williams et al. (2005) suggested diversifying the nature of the stimuli in future studies, including vocal information. Thus our purpose was to assess, in a longitudinal study, the ability of children with DS to recognise expressions of emotion, and to observe age-related changes in the development of emotional understanding. This is an important issue because a deficit affecting emotion recognition could impede emotional regulation and adjustment in interpersonal relationships. We wondered whether the developmental sequence of basic emotion recognition in these children followed the typical pattern. The comparison with typical development was based on taskspecific data collected in a longitudinal study in 3- to 8-year-old children (Pochon & Mellier, 2012). These data showed that, at the ages studied, sadness and happiness were the first expressions to be well recognised, followed by anger and disgust, a little later by surprise, and finally by fear. Given the high frequency of language impairment in DS (Yoder & Warren, 2004), we chose to investigate the children’s abilities by means of a multimodal task like those used by Walker-Andrews (1986) with TD children, and Hobson, Ouston, and Lee (1988) with children with ASD and children with NSID. Children were asked to pair an emotional auditory stimulus (vocalisation) with an emotional visual stimulus (facial expression). One of our major goals was to adopt a developmental perspective given the lack of longitudinal studies of emotion recognition in children with intellectual disability. This perspective requires an annual reassessment of participants’ cognitive level, which allows one to compare and control the developmental rate of different experimental groups. Given previous findings (Kasari et al., 2001; Williams et al., 2005;

Wishart et al., 2007), we expected our longitudinal data to reveal evidence of a specific disorder affecting the recognition of emotion in children with DS. We anticipated that we would observe (a) a significant impairment in the recognition of emotional facial expressions in children with DS in comparison with children with NSID of the same CA and the same developmental age (DA); (b) a significant impairment in the recognition of emotional facial expressions in children with DS in comparison with TD children of the same DA; and (c) a slower rate of increase in emotion recognition capacities 24 months later in comparison with NSID and TD children. The originality of our study resided in its longitudinal dimension, with the children being tested three times at 1-year intervals, and the use of nonverbal material to avoid a disadvantage due to impaired language processing capacities in children with DS. The composition of the groups, using strict individual matching for both chronological and mental age, as well as a control task, satisfied the methodological requirements recommended by Moore (2001) for the study of emotion recognition in persons with intellectual disability.

Method Participants Seventy-two children took part in the whole longitudinal study: 24 children with DS (15 males and nine females, 6.0–14.8 years old, M age = 11.0 years at entry), 24 children with NSID (11 males and 13 females, 6.3–14.6 years old, M age = 10.7 years at entry), and 24 TD children (10 males and 14 females, 3–6.8 years old, M age = 4.0 years at entry). Furthermore, to maintain the individual pairing on DA across the study, which included three sessions, two additional TD groups were created. Twenty-four additional children participated in Session 2 (14 males and 10 females, 3–7 years old) and 22 others in Session 3 (15 males and nine females, 3.1–7 years old). The characteristics of each group are presented in Tables 1 and 2. The children with intellectual disability were drawn from mainstream schools (inclusion) or from specialised institutions, and the TD children were recruited from kindergarten and primary schools. The children with NSID presented disabilities of unknown aetiology; children with disability of genetic origin were excluded from this group. Similarly, children with sensory disorders and with ASD were not included in the study. The TD groups (longitudinal and cross-sectional) were drawn from

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Table 1. Chronological age of developmental age-matched groups with longitudinal and cross-sectional TD groups Group

Session S1 S2 S2 S3 S3

Longitudinal TD

Cross-sectional TD

Down syndrome

Nonspecific ID

M

SD

M

SD

M

SD

M

SD

ANOVA value F(2, 69)

132.67 144.39 144.39 156.57 156.57

30.72 30.74 30.74 30.94 30.94

128.50 140.84 140.84 153.00 153.00

29.09 29.89 29.89 29.85 29.85

47.83 59.76 – 71.03 –

10.65 10.78 – 11.35 –

– – 50.35 – 57.74

– – 12.03 – 13.96

86.51∗∗ 84.41∗∗ 103.16∗∗ 85.23∗∗ 110.76∗∗

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Note. n = 24 for each group. Ages are reported in months. ID = intellectual disability; TD = typically developing. ∗∗ p < .01.

Table 2. Developmental agea of developmental age-matched groups with longitudinal and cross-sectional TD groups Group

Session S1 S2 S2 S3 S3

Longitudinal TD

Cross-sectional TD

Down syndrome

Nonspecific ID

M

SD

M

SD

M

SD

M

SD

ANOVA value F(2, 69)

45.63 50.25 50.25 57.50 57.50

13.33 12.12 12.12 13.38 13.38

44.96 50.58 50.58 53.79 53.79

9.43 11.26 11.26 12.06 12.06

47.83 59.76 – 71.03 –

10.65 10.78 – 11.35 –

– – 50.35 – 57.74

– – 12.03 – 13.96

0.43 5.38∗∗ 0.00 13.01∗∗ 0.68

Note. n = 24 for each group. Ages are reported in months. ID = intellectual disability; TD = typically developing. a Not measured for TD children who are matched by chronological age with developmental age of children with DS. ∗∗ p < .01.

a developmental study (N = 103, 3–8 years old) carried out by one of the authors (Pochon & Mellier, 2012), in which the same experimental tasks were administered to TD children. The children met with the experimenters in a quiet and pleasant room at their usual school or institution. The level of cognitive development of the children with intellectual disability was assessed using the French version of the nonverbal scale of the Kaufman Assessment Battery for Children (KABC, Kaufman & Kaufman, 1993), in the form provided for 4- to 5-year-old children. The nonverbal KABC scale we used consists of a battery of 3 subtests1 (Face Recognition, Hand Movements, and Triangles) that correspond to the three nonverbal subtests of the K-ABC designed for children aged under 5 years. The K-ABC allows out-of-level testing, so that subtests initially meant for young children may be administered to older children with developmental delay. This instrument allows a short and reliable assessment of nonverbal capacities, thus preventing attention decline and fatigue in young children. This point is important because of the frequency of persistence task deficits in children

with DS (Kasari et al., 2001; Pitcairn & Wishart, 1994). The raw scores collected were used to determine an initial average DA for each child with intellectual disability according to the instruction manual. A retest was planned 1 year later (Session 2) and another 2 years later (Session 3), at the same time as the experimental tasks were presented. Thus, from a developmental perspective, three repeated measures with a reduced instrument were preferred over a single prior measure. As recommended by Moore (2001), the experimental and control groups were created using an individual matching method. Each child with DS was matched to a child with NSID of the same CA and the same DA. Typically developing children were selected individually, matching their CA with the DA of the children with DS. They were randomly chosen from among the participants in our developmental study (Pochon & Mellier, 2012), which we conducted in parallel to obtain typical data from the experimental tasks. Children who participated were in a regular class at the expected grade level, and had no psychological, learning, or behavioural disorders.

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As the rate of development is by definition slower in children with intellectual disability, it was not surprising that the group of TD children developed faster over the two years of the study. The cognitive level of the children with intellectual disability no longer coincided with that of the TD children at the time of the second and third sessions (see Table 2). So, as previously mentioned, it was necessary to create cross-sectional TD groups to make developmental age-based comparisons possible in Sessions 2 and 3. As a result, we had a “longitudinal” TD group that we observed in all three sessions and two “cross-sectional” TD groups with a CA matching the DA of the children with intellectual disability in the second and third sessions. To ensure the validity of the cognitive assessments, the developmental sensitivity of the nonverbal KABC measures was estimated across the three sessions (spaced at 1-year intervals). The data reported in Table 2 show a constant improvement in the mean scores obtained by the two groups of children with intellectual disability. These data were analysed by performing a 2 (group) × 3 (session) repeated measures ANOVA, with K-ABC scores expressed in DA as the dependent variable. This showed a significant main effect of session, F(2, 92) = 57.99, p = .01, ηp = .56. Post hoc analyses showed significant progress from Session 1 to Session 3 in both groups (Scheffe test, p < .01), which confirms the developmental sensitivity of the psychometric instrument used. No significant main effect of group and no significant interaction between group and session was found. Ethics approval This study was conducted with the approval of the academic authorities (Seine-Maritime School Inspectorate, France). Each participant was tested by a person with the title of psychologist, as protected by French law, in compliance with the Code of Ethics for Psychologists, published by the National Consultative Commission of Ethics for Psychologists. All the children took part in the study following written consent from their parents. All data were anonymised and kept confidential. Experimental tasks The experimental protocol included two tasks in which the children were required to point to an image or a photograph after hearing an animal cry or a human vocalisation. Expressive language was not required for the answer, which was given by simply pointing to visual stimuli presented on the screen of a laptop computer. The monitor had a 17-inch

diagonal measurement (resolution of 1024 by 768 pixels), and the internal speakers were replaced by a pair of high-quality external speakers. The stimuli were displayed on screen in two rows, each with three images or photographs. The protocol included 12 series (six series containing six images of animals and six series containing six photographs of faces). For the control task, six monochromatic images depicting animals were selected. Each of the images was used at least once as the target image; the spatial layout was modified with each presentation to ensure that each target animal was in a different place. The child was asked to listen closely to the sound, and then one of the six series was displayed on the computer. After hearing the sound, the child was required to point to the corresponding image, in response to the instruction “show me the animal that made this noise.” Six animal sounds were presented in the following order: dog, duck, bird, cow, cat, and horse. Each correct answer received 1 point; all answers were noted in order to analyse the errors that were made. The use of such a familiar and easy task promoted the children’s confidence and task understanding. The emotional recognition task used a similar method, presenting photographs and vocalisations related to the six basic emotions. The emotionalvisual support material was composed of six photographs of a young woman displaying different facial expressions (happiness, sadness, anger, fear, surprise, disgust). These photographs of faces were coded by an expert using Ekman and Friesen’s (1978) FACS criteria. The photographs that were selected for the study were those for which the expression had been successfully identified by 10 independent judges (four men and six women aged between 20 and 40 years). These greyscale pictures, with a white background, were presented in exactly the same way as the animal images. The recorded vocalisations were produced by the same young woman while she was posing for the emotional photographs. The selected vocalisations were those that were successfully associated by adults with the corresponding emotional photographs from a set of six comprising five distractors. As soon as a human vocalisation was played, a series of photographs was displayed on screen and the child was asked to point to the corresponding face, in response to the instruction “show me the person who made this noise.” The six emotional vocalisations occurred in the following order: happy, scared, disgusted, surprised, sad, and angry. The control and emotional tasks were presented alternately during the experiment, with each control item being followed by an emotional item. Such a

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Emotion recognition by children with DS presentation forced the refreshing of working memory between emotional items, which minimised the possibility of reasoning by elimination or by deduction. Each task yielded a score with a minimum value of 0 and a maximum of 6. In the developmental phase, the experimental tasks were administered to children from 2.6 to 11 years old. The emotional task was well understood by most 3-year-old children but was less accessible under this age. The final version was used for our longitudinal study (Pochon & Mellier, 2012) of TD children (N = 103, initial age of 3–6 years, three annual sessions) in order to obtain developmental data. Based on these results, we know that the recognition of basic emotions in this multimodal task improves very rapidly between the ages of 3 and 6 years, CAs which correspond to the DAs of the children with intellectual disability observed in the present study. However, we observed that the full recognition of the basic emotional repertory has yet to be mastered at 6 years of age. Happiness and sadness were identified by more than half the 3-year-old children; this proportion grew to nine out of 10 for 6year-old children. At 4 years old, half of the children could recognise anger and disgust, and over twothirds of children could 2 years later. The recognition of surprise developed a little more slowly but was acquired by over two-thirds of 6-year-old children. Finally, the ability to recognise the expression of fear improved steadily but very slowly: only four out of 10 children succeeded at 6 years of age.

Results Five sets of analyses were conducted: (a) a series of Student’s t-tests was used to compare mean scores

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in emotional and control tasks with chance; (b) an ANOVA was used to compare the recognition of emotions between children with DS, children with NSID, and TD children in the longitudinal design; (c) a logistic regression was computed to analyse recognition of each emotion; (d) a descriptive analysis of error patterns was done to determine whether children with DS had specific patterns compared to TD children and children with NSID; and (e) our final analyses investigated the relationships between assessment measures and experimental task scores for each group. Comparison of scores with random results As indicated in Table 3, the observed means ranged from 2.42 (DS, emotional task, Session 1) to 6 (TD, control task, Session 3). Given that the data came from tasks in which the possibility of choice was limited, with binary scoring, scores were compared to the probability expected by chance using Student’s t-test. Because multiple t-tests were performed, we used the Bonferroni correction and considered significant only those results for which p < .002. For all means, comparisons with chance (1/6, M = 1) were significant (refer to Table 3), therefore all results were retained for the analysis. Overall results: Do children with DS recognise basic emotions less well than TD children and children with NSID? As a precaution, the effect of gender was examined on the cumulative results of the three sessions and the three groups. A single factor ANOVA showed that scores did not differ significantly between the girls and the boys for the control task, F(1, 70) =

Table 3. Control and emotional scores in developmental age-matched groups Group

Task/Session Control task Session 1 Session 2 Session 3 Total Emotional task Session 1 Session 2 Session 3 Total

Down syndrome

Nonspecific ID

Typically developing

Cross-sectional TD

M

SD

M

SD

M

SD

M

SD

5.25∗∗∗ 5.63∗∗∗ 5.79∗∗∗ 16.67

1.22 0.77 0.51 1.90

5.50∗∗∗ 5.63∗∗∗ 5.71∗∗∗ 16.83

1.06 0.77 0.55 2.06

5.29∗∗∗ 5.96∗∗∗ 6.00 17.25

0.95 0.20 0.00 0.94

– 5.25∗∗∗ 5.62∗∗∗ –

– 1.11 0.97 –

2.42∗∗∗ 3.17∗∗∗ 3.83∗∗∗ 9.42

1.41 1.13 1.27 2.72

2.71∗∗∗ 2.88∗∗∗ 3.88∗∗∗ 9.46

1.37 1.42 0.99 2.75

2.54∗∗∗ 3.71∗∗∗ 4.46∗∗∗ 10.71

1.25 1.52 0.78 2.51

– 3.08∗∗∗ 3.96∗∗∗ –

– 1.25 1.60 –

Note. Maximum possible score = 6 for each session and 18 for total score. Comparison with chance: ∗∗∗ p < .001. ID = intellectual disability; TD = typically developing.

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0.019, NS, or the emotional task, F(1, 70) = 0.19, NS. Consequently, the data were combined in the subsequent analyses. For all groups, the control task produced better results than the emotional task (see Table 3). With scores between 5 and 6, the control task proved easier than expected for the children. Descriptively, we observed a steady improvement in scores from Session 1 to Session 3 in each group, but in the absence of homogeneous variance at the last sessions, it was not possible to conduct an ANOVA. However, this ceiling effect did not prevent subsequent analysis because our hypothesis did not concern the control task. This task was essentially designed to ensure that the children understood the task and to refresh their working memory between emotional items. The mean scores on the emotional task (Table 3) improved steadily from session to session in the three groups. As expected, the annual gain was greater in TD children because of delayed development in the other groups. On average, the TD children recognised almost two more expressions from Session 1 to Session 3. Over the same period, children with DS and children with NSID recognised on average at least one additional expression. A repeated-measures ANOVA was performed on the results of the emotional task (Table 3), with group as a between-participants factor (DS, NSID, TD) and session as a within-participants factor (3 sessions). There was no significant main effect of group, F(2, 69) = 1.83, NS, but a significant main effect of session, F(2, 138) = 34, p < .001, ηp = .33. No interaction effect was observed, F(4, 138) = 1.71, NS. Post hoc comparisons using Scheffe’s test showed a significant improvement in scores from Session 1 to Session 3, except for the NSID group (+1.17, NS). The effect size is large in the TD group (+1.92, p < .001, d = 1.49, 95% CI [0.65, 3.17]) and medium in the DS group (+1.42, p = .014, d = 0.77, 95% CI [0.15, 2.68]). Betweengroup comparisons revealed no significant difference regardless of session. In sum, the main result is that emotion recognition develops in both DS and TD children, but the change is faster in TD children. Comparison with the TD cross-sectional groups at Session 2 and Session 3 As originally planned, comparisons were also carried out with cross-sectional TD groups made up of individuals matched for DA at Sessions 2 and 3, in order to obtain comparison groups of a similar cognitive level. Only the emotional task results were analysed (refer to Table 3), and only DS and TD cross-sectional groups were compared. The observed means

were very close in value for each session. Singlefactor ANOVAs showed no significant effect of group in Session 2, F(2, 69) = 0.39, NS, or Session 3, F(2, 69) = 0.06, NS, as no significant group differences were observed in post hoc analyses (Scheffe test). Thus, additional cross-sectional analyses, restoring the equivalence in DA between the groups, revealed that children with DS did not progress more slowly than TD children in the recognition of basic emotions.

Analysis for each individual emotion Table 4 presents the combined scores for the three sessions for individual emotions. As the dependent variable was the sum of within-subjects measures (except for cross-sectional TD groups), the use of variance analysis was not appropriate. In order to examine group differences in recognition of each emotion, we constructed a logistic regression model with emotion recognition performance as a predictor of group differences. In this model, the group factor was reduced to two terms and became a dichotomous dependent variable, and the emotion recognition scores were treated as independent variables. In a first analysis, the DS group was opposed to the NSID group. The results showed that no emotion recognition score could predict group differences. In the second analysis, which compared the DS group with the TD longitudinal group, the recognition of disgust predicted a group difference (OR = 3.01, p = .05), to the advantage of the TD group, as in the last comparison (NSID vs. TD, OR = 2.30, p = .05). In order to exclude effects due to differences in cognitive capacities, the analysis was performed again with the cross-sectional group’s combined scores for each emotion (see Table 4). These results showed that no emotion recognition score distinguished the children with DS or the children with NSID from the TD children when the equivalence of DAs was respected.

Descriptive analysis of error patterns Table 5 shows each group’s answers, with the data combined for the three sessions. Typical data came from the cross-sectional groups in order to maintain the equivalence of DA, despite the fact that these children came from three different groups. Overall, regardless of group, all children tended to confuse the same emotions. Although the children with DS more often chose sadness when the target was anger or fear, these findings do not constitute a specific error pattern in this group.

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Table 4. Combined scores by expression at the emotional task in developmental age-matched groups Group Down syndrome Emotion Sadness Happiness Anger Disgust Surprise Fear

Nonspecific ID

Longitudinal TD

Cross-sectional TDa

M

SD

M

SD

M

SD

M

SD

2.54 2.21 1.29 1.21 1.25 0.92

0.78 0.72 1.00 0.83 0.99 0.83

2.38 2.13 1.42 1.29 1.13 1.13

0.88 0.85 1.10 1.00 0.80 1.08

2.50 2.38 1.58 1.92 1.29 1.04

0.72 0.65 0.93 0.83 0.91 0.75

2.33 2.13 1.46 1.54 1.17 1.04

0.92 0.54 0.78 1.06 0.92 0.69

Note. Maximum possible score = 3. ID = intellectual disability; TD = typically developing. a Combined scores of three different groups.

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Table 5. Combined responses for each expression at the emotional task in developmental age-matched groups Emotion pointed to Group/Target emotion Down syndrome Happiness (H) Sadness (S) Anger (A) Disgust (D) Surprise (Su) Fear (F) No answer Nonspecific ID Happiness (H) Sadness (S) Anger (A) Disgust (D) Surprise (Su) Fear (F) No answer Cross-sectional TDa Happiness (H) Sadness (S) Anger (A) Disgust (D) Surprise (Su) Fear (F) No answer

H

S

A

D

Su

F

53 3 3 2 2 9 0

1 61 0 5 3 2 0

4 21 31 7 6 2 1

7 7 2 29 2 25 0

2 6 3 14 30 17 0

8 28 1 6 7 22 0

51 1 4 1 5 10 0

2 57 3 6 0 4 0

6 9 34 14 7 2 0

2 11 3 32 3 20 1

6 2 4 16 27 17 0

10 14 2 12 7 27 0

51 5 1 2 2 11 0

2 52 7 3 3 5 0

5 12 34 10 7 4 0

8 7 1 36 3 17 0

4 6 4 15 27 15 1

13 19 0 7 8 24 1

Note. Correct responses are in bold type. Maximum number of correct responses possible = 72. ID = intellectual disability; TD = typically developing. a Combined scores of three different groups.

Relationships between assessment measures and experimental task scores A series of correlations were performed on the mean results from the three sessions, for each assessment measure and each task score (see Table 6). In all three groups, success at the experimental task was weakly correlated with CA. This is comprehensible for the groups with developmental delay but somewhat surprising for the typical group, whose CA is theoretically equivalent to their DA. For the other

measures, which applied only to groups with intellectual disability, there was a different correlational pattern between the DS and NSID groups: stronger correlations were observed between the control task and cognitive measures in the DS group, while stronger correlations were observed between the emotional task and cognitive measures in the NSID group. We noted the absence of any significant correlation between Face Recognition and the emotional task in the DS group (r = .34, NS), while there was a relatively high correlation, with a large effect size, in the

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Table 6. Correlations among experimental task scores and assessment measures by developmental age-matched group Group Down syndrome Variable/Task CA DA Face Recognition Hand Movements Triangles

Control ∗

.51 .70∗∗∗ .64∗∗ .57∗∗ .75∗∗

Emotional .24 .41∗ .34 .46∗ .47∗

Nonspecific ID Control .39 .55∗∗ .53∗∗ .36 .57∗∗

Emotional .27 .68∗∗∗ .61∗∗ .49∗ .57∗∗

Longitudinal TD Control ∗

.46 – – – –

Emotional .38 – – – –

Note. n = 24 in each group. ID = intellectual disability; TD = typically developing; CA = chronological age; DA = developmental age. p < .05. ∗∗ p < .01. ∗∗∗ p < .001.

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∗

NSID group (r = .61, p < .001, 95% CI [0.27, 0.81]). Moreover, in the DS group, Face Recognition correlated significantly with the control task; a large effect size is noted (r = .64, p < .001, 95% CI [0.32, 0.83]). As regards the relationships between the two experimental measures, correlations were significant in all groups: DS group, medium effect size (r = .45, p = .029, 95% CI [0.06, 0.72]); NSID group, large effect size (r = .55, p = .006, 95% CI [0.19, 0.78]); TD group, large effect size (r = .61, p = .001, 95% CI [0.27, 0.81]). In summary, different correlational patterns were observed in the children with DS and the children with NSID. We noted in particular in the DS group an absence of relationship between the K-ABC subtest, which required recognition of identity, and performance on the emotional task. Discussion Our experiment aimed to assess the abilities of children with DS to recognise six basic emotions, in comparison with NSID and TD children, and from a longitudinal perspective. This issue is essential for understanding the development of emotional competence in these children (Denham et al., 2003; Saarni, 1999). Emotional competence implies that they are able to recognise emotional signals in other people. In order to avoid differences due to verbal labelling abilities, a strictly nonverbal procedure was used. We hypothesised that children with DS would have more difficulties and that their recognition abilities would develop more slowly. The data do not support these hypotheses. First, the results did not reveal significant differences at any session in the DS group’s abilities to discriminate basic emotions compared to other children with and without intellectual disability. They showed a significant change with a magnitude similar to that observed in other children: on the one hand, the children with DS and the children with NSID did

progress more slowly than TD children, but, on the other hand, when children with DS were matched with TD children in terms of DA, the results demonstrated no significant difference. This finding is not consistent with previous studies in which overall scores were different between groups (Williams et al., 2005; Wishart et al., 2007), and the DS group had lower scores. Second, analysis by individual emotion produced no significant result despite some subtle descriptive difference in the recognition of anger and disgust, emotions whose recognition reflects a developmental change around four years of age (Camras & Allison, 1985; Gosselin, 1995). Finally, the correlations between DA and the experimental measures, for the DS and NSID groups, were always significant and sometimes high. Yet we noticed an absence of relationship in the DS group between performance on the emotional task and performance on the Face Recognition subtest of the KABC, unlike the NSID group for which a high correlation existed. This corroborates Williams et al.’s (2005) finding of an absence of correlation between scores on the identity and emotion-matching tasks in the DS group. The main information provided by this study is that, when presented with six facial expressions simultaneously, children with DS are as well able to identify a basic emotion on the basis of its vocal expression as their peers with similar DA. This finding tends to show that the emotion recognition difficulties noted in children with DS in other studies must not be interpreted as indicating an overall deficit but rather as expressing a particular difficulty in recognising certain expressions, such as fear. Moreover, the neurological explanation proposed by Wishart et al. (2007) to explain these children’s fear recognition deficit invoked a reduced development of the temporal limbic system, especially the amygdala, a structure that is critical for the emotion of fear (Adolphs, 2001; Calder

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Emotion recognition by children with DS et al., 1996; Dolan & Morris, 2000; LeDoux, 1998; Wishart et al., 2007). Thus, future research could focus on the recognition of negative emotions, especially fear, in children with DS. It seems necessary to analyse the recognition of these emotions more closely and specifically. This study raises the question of the influence of the emotional lexicon on emotion recognition abilities. Russell and Widen (2002a) have shown a greater label effect than facial effect on the categorisation of happiness, anger, and sadness by children aged 2–7 years. Better performance with labels was also found by Russell and Widen (2002b) for fear and disgust. Despite many precautions to minimise the linguistic demands of experimental tasks, most past studies made use of emotional labels in their instructions. However, it is not clear whether this would induce specific categorical processing (Lindquist et al., 2006), in which case children with DS would be disadvantaged even when participants’ verbal level is controlled for. This question needs to be more accurately investigated using strictly nonverbal emotion recognition tasks. Furthermore, Salmon et al. (2013) showed the importance of language ability as a component of emotional knowledge, which raises questions for future studies in DS. Thus, it seems important to question the absence in children with DS of any relationship between facial emotion recognition (emotional task) and facial identity recognition (Face Recognition subtest of the K-ABC). Such an absence had been observed previously by Williams et al. (2005) in which no significant correlation was found in their DS group between emotion matching scores and Benton Facial Recognition Test measures. This could signify that children with DS develop their facial emotion recognition abilities relatively independently from facial identity recognition skills, which would be in line with Williams et al.’s (2005) suggestion that a particular developmental pathway exists in children with DS. This issue is important and requires further study in order to add to the knowledge of a specific behavioural phenotype in individuals with DS (Fidler et al., 2009), and contribute to a better understanding of early sociocognitive development in DS (Cebula et al., 2010). The findings of this study must be understood in the context of several limitations. First, there was only one trial per emotion at each age of testing, which could affect the reliability of the measure of children’s emotion recognition ability. As indicated before, however, the task showed quite acceptable developmental sensitivity in all groups and consistent results from one session to the other. For instance, the longitudinal design of this study makes it possible

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to show that low recognition scores for a given expression at the first session are not the result of chance but indicate the emergence of a new ability that will have increased by the following sessions. Overall, therefore, the developmental sequence of basic emotion recognition in children with DS followed the typical pattern described by Pochon and Mellier (2012) with the same tasks. The data obtained in our experiment demonstrated the good developmental sensitivity of the emotional task we used. During the 2 years of observation (from age 4 to 6), which corresponded to a crucial period for emotional regulation development (Kochanska, Murray, Jacques, Koenig, & Vandegeest, 1996; Rothbart, Ahadi, Hershey, & Fisher, 2001), the TD children acquired, on average, the ability to recognise two additional basic emotions. The children with intellectual disability also increased their recognition capabilities to a similar extent in terms of DA. During the period of the study, these children gained an average of 10 months of DA and developed the ability to recognise, on average, more than one additional emotional expression. This showed that the nonverbal task was able to take account of the increase in the children’s understanding of emotions. For the children with intellectual disability, this was attested by the positive relation between their performance and their cognitive level, as assessed by the K-ABC subtests. The longitudinal design of the study shows that better emotion recognition is associated with the development of nonverbal abilities. This corroborates the findings of Albanese, De Stasio, Di Chiacchio, Fiorilli, and Pons (2010), who showed a link between nonverbal intelligence and the ability to recognise emotions. Another possible limitation is that one of the KABC tasks used to determine the DA was a face identity recognition task, which could present an advantage for children with DS, given that they are often claimed to be particularly proficient in this area. However, the results of previous research are unclear. Wishart and Pitcairn (2000), using the same K-ABC task, found better performance in children with DS, whereas Williams et al. (2005) found that these children scored lower in an identity-matching task (explained by task disengagement), and Wishart et al. (2007) found no difference. The recognition of identity has been studied in more detail by Annaz, Karmiloff-Smith, Johnson, and Thomas (2009). These authors reported poor face recognition skills in children with DS on the Benton Test of Facial Recognition, and an anomalous pattern in a task requiring holistic face processing. Given these data, it seems difficult to conclude that children with DS are superior at recognising faces.

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Finally, the issue of the method used to assess the emotional knowledge of children could be raised. The capacity to associate a facial expression with a vocalisation is very far from representing all of the skills involved, in real life, in the identification of emotion expressed by others. As emphasised by Widen and Russell (2010), facial expressions, but also other nonverbal clues, including context, comprehension of causes and consequences, and verbal labelling, underlie the understanding of emotion. The current study addressed a basic component of emotion knowledge and should be complemented by the study of other aspects of emotional understanding. Despite these limitations, our study provided developmental data based on the longitudinal observation of children with DS, which is relatively rare in the study of emotional abilities in children with intellectual disability. The results obtained with the use of multimodal emotional material are of interest, and this kind of nonverbal method should be further developed, in particular by introducing dynamic stimuli (video sequences). Increasing the sample size, the number of trials for each emotion, and the number of point measurements is also necessary to improve the reliability of the longitudinal design in future research. By contributing to our knowledge of social cognition in children with DS, such studies may allow more targeted and appropriate educational and psychological support for these children. Acknowledgement The authors have no conflicts of interest. Note 1.

For 5-year-old children, the nonverbal scale of the K-ABC has four subtests (Hand Movements, Triangles, Matrix Analogies, Spatial Memory), while there are five subtests for 6-year-olds (Hand Movements, Triangles, Matrix Analogies, Spatial Memory, Photo Series).

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