Research in Developmental Disabilities 35 (2014) 761–775

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Research in Developmental Disabilities

Nouns and predicates comprehension and production in children with Down syndrome A. Bello a,*, D. Onofrio b, M.C. Caselli b a b

Department of Neuroscience, University of Parma, Parma, Italy Institute of Cognitive Sciences and Technologies, National Research, Council, Rome, Italy

A R T I C L E I N F O

A B S T R A C T

Article history: Received 5 July 2013 Received in revised form 21 January 2014 Accepted 22 January 2014 Available online 14 February 2014

Our study investigated the lexical comprehension and production abilities as well as gestural production taking into account different lexical categories, namely nouns and predicates. Fourteen children with DS (34 months of developmental age) and a comparison group of 14 typically developing children (TD) matched for gender and developmental age were assessed through a test of lexical comprehension and production (PiNG) and the Italian MB-CDI. Children with DS showed a general weakness in lexical comprehension and production that appeared more evident when the lexicon was assessed through a structured test such as the PiNG that requires general cognitive skills that are impaired in children with DS. As for the composition of the lexical repertoire, for both groups of children, nouns are understood and produced in higher percentages compared to predicates. Children with DS produced more representational gestures than TD children in the comprehension tasks and above all with predicates; on the contrary, both groups of children exhibited the same number of gestures on the MB-CDI and during the subtests of PiNG production. Children with DS produced more unimodal gestural answers than the control group. Theoretical implications of these results are discussed. ß 2014 Elsevier Ltd. All rights reserved.

Keywords: Vocabulary comprehension Vocabulary production Nouns and predicates Down syndrome Gestures

1. Introduction Down syndrome (DS) is the most frequent genetic cause of intellectual disability and involves about one child in a thousand live births (Morris & Alberman, 2009). Besides generalized cognitive delay that affects approximately 80% of individuals with DS, the neuropsychological profile of children with DS is characterized by a lack of developmental homogeneity between cognitive and linguistics abilities, with a greater impairment of the latter. In fact, despite rare exceptions (Papagno & Vallar, 2001), many authors have observed that the linguistic abilities of children with DS are poorer than what is expected on the basis of their overall cognitive level. Furthermore, some authors highlighted that language ability in this population is not uniform with morphosyntax more impaired than lexicon (Chapman, 1997; Fabbretti, Pizzuto, Vicari, & Volterra, 1997; Galeote, Soto, Sebastia´n, Checa, & Sa´nchez-Palacios, 2013; Martin, Klusek, Estigarribia, & Roberts, 2009; Vicari, Caselli, Gagliardi, Tonucci, & Volterra, 2002). Some researchers also highlighted that children with DS show a preference for nonverbal communication using more gestures with respect to typically developing (TD) children (Chan & Iacono, 2001; Hattier, Matson, Sipes, & Turygin, 2011; Maltese, Rappo, Scifo, & Pepi, 2012). However, the findings on lexical skills and on the use of communicative gestures lead to contrasting results and many questions remain open.

* Corresponding author at: Department of Neuroscience, University of Parma, Via Volturno 39/E, 43125 Parma, Italy. Tel.: +39 0521 903945; fax: +39 0521 903900. E-mail address: [email protected] (A. Bello). 0891-4222/$ – see front matter ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ridd.2014.01.023

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1.1. Lexical comprehension and production Different studies on typically developing toddlers have shown that word comprehension is closely linked to the development of non-verbal cognitive skills (Ellis & Thal, 2008); moreover word comprehension emerges before word production and children have a greater repertoire of words comprehended compared with words produced (Bello, Giannantoni, Pettenati, Stefanini, & Caselli, 2012; Caselli, Rinaldi, Stefanini, & Volterra, 2012; Gershkoff-Stowe & Hahn, 2013). Some studies (Caselli, Casadio, & Bates, 1999; Tardif, Shatz, & Naigles, 1997; Waxman, Fu, Arunachalam, Leddon, & Geraghty, 2013) have also shown that the increase in vocabulary size is accompanied by important qualitative changes in both comprehension and production: nouns are acquired before predicates (i.e. verbs and adjectives) and, although they continue to be the most common category of words in children’s early vocabulary, when the lexical repertoire increases, the number of predicates progressively increases as well, in terms of both quantity and frequency. Both relationships between comprehension and production as well as between nouns and predicates are rarely investigated in children with DS. Receptive vocabulary is consistently observed as a relative strength among the various aspects of language function in Down syndrome, although it is often delayed relative to chronological age (CA) (Næss, Halaas Lyster, Hulme, & Melby Leverag, 2011; Roberts, Price, & Malkin, 2007 for a review on this topic). However, contrasting results emerge in studies on children and adolescents with DS in which different types of assessment (direct vs indirect) were used. Previous studies on 3 year old (CA) toddlers with DS, have found that receptive vocabulary levels measured by MacArthurBates Communicative Development Inventory (MB-CDI) are less delayed than expressive vocabulary levels (Caselli et al., 1998; Singer Harris, Bellugi, Bates, Jones, & Rossen, 1997). In both these studies mental ages of children was not available. In a more recent study the same questionnaire was used with parents of 186 children with DS (CA ranging from 1 to 6 years). The sample was divided in 7 subgroups according to the different mental ages (MA) (ranging from 8 to 29 months). The results of this study highlighted that in children with DS the size of lexical comprehension vocabulary was greater than TD children matched for MA (Galeote, Sebastia´n, Checa, Rey, & Soto, 2011). Similar results emerged in the study by La´zaro, Garayza´bal, and Moraleda (2013) which shows (although it is not the central point of the paper) that, in older children with DS, receptive vocabulary, directly assessed through the Spanish version of the Peabody Picture Vocabulary test (PPVT) is lower than expected for CA (12.2 years) but higher than expected for MA (6.5 years). In agreement with Chapman (2006), authors suggest that lexical comprehension exceeds non-verbal cognitive levels because of more life experience due to the greater chronological age of children with DS. On the contrary, some authors have found a weakness in receptive vocabulary both in children (CA: 9 years; MA: 4 years) (Caselli, Monaco, Trasciani, & Vicari, 2008; Price, Roberts, Vandergrift, & Martin, 2007) as well as in adolescents (CA: 14 years; MA: 6 years) (Ypsilanti, Grouios, Alevriadou, & Tsapkini, 2005). A previous longitudinal study on children with DS (CA: 9.9 years) showed an interesting developmental trend: similar levels of vocabulary to TD children matched on mental age only at the first point of observation (MA: 4.3 years) but non at the subsequent time-points: as they grow older, the vocabulary comprehension skills in children with SD are progressively lower compared with ST control groups (Hick, Botting, & ContiRamsden, 2005). Overall, these data support that verbal comprehension is coherent with more general cognitive abilities in the early years, becoming progressively poorer with respect to the children’s stage of cognitive development, although it remains better than their production capacity. As for vocabulary production, several studies on children with DS younger than 36 months (MA) have highlighted similarities with TD children matched for MA in expressive vocabulary when the MB-CDI was used (Galeote, Soto, Checa, Go´mez, & Lamela, 2008; Galeote et al., 2011; Vicari, Caselli, & Tonucci, 2000). However, considering the spontaneous production of children during a free-play session with their mothers, Zampini and D’Odorico (2011b) reported that children with DS (MA: 30 months) tended to use their acquired words with a lower frequency than the vocabulary-size matched TD children. Analyzing the vocabulary composition, the study showed that nouns are more frequently used than predicates both in children with DS and in TD controls. The proportion of adverbs and function words was significantly lower in children with DS, whereas the percentage of simpler word classes, such as routines and names for people, was higher. The authors suggested that their findings support the hypothesis that once children have reached a specific linguistic stage, they usually tend to persist in it (Zampini & D’Odorico, 2011b). However the results could indicate that children with DS have a different language profile than TD children, rather than a delay (Chapman & Hesketh, 2001; Fowler, 1990; Miller, 1988; Miller, Laddy, & Leavett, 1999). Different results emerged in studies on Italian children and adolescents with DS where expressive lexical skills were assessed through structured tasks. Using the Boston naming task, Vicari, Bates, et al. (2004) showed lower performance of participants with DS in lexical production with respect to control group matched for MA (5.2 years). More recently, two studies of our group confirmed this finding on younger children with DS (MA 3.10 years). In both studies a preliminary version of the picture naming test – PiNG (Bello et al., 2012) was used. Results confirmed that children with DS produced fewer correct and more incorrect spoken answers with respect to both groups of TD controls matched for chronological and mental age (Stefanini, Caselli, & Volterra, 2007) or for mental and language age (LA) (Stefanini, Recchia, & Caselli, 2008). These results suggested that not specific asynchrony emerged between cognitive and expressive vocabulary when an indirect instrument of language was used, whereas a weakness in language with respect to non verbal cognition was evident when expressive lexical skills were assessed through direct tasks.

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1.2. Relationship between gesture and spoken vocabulary Several researchers have shown that gestural and vocal productions are closely linked in typically developing children (Capirci & Volterra, 2008; Goldin-Meadow & Alibali, 2013; Stefanini, Bello, Caselli, Iverson, & Volterra, 2009). Words and gestures produced with the explicit intent to communicate with caregivers emerge at about 12 months: at this age infants show a preference for using gestures over words (Iverson, Capirci, & Caselli, 1994). Shortly after, at about 16 months, they become able to map both words and gestures to objects, actions or events with the same ease, resulting in a substantial ‘‘equipotentiality’’ between the two modalities (Abrahamsen, 2000; Volterra, Caselli, Capirci, & Pizzuto, 2005). Then, near the end of the second year of life, at about 20 months, it is possible to observe a decline in the frequency in using gestures, together with a rapid increase in the production of words. Gestures may not only be considered as scaffolding early language development but also as a predictor of progress in verbal language abilities (Capirci, Iverson, Pizzuto, & Volterra, 1996; Iverson & Goldin-Meadow, 2005; Longobardi, Rossi-Arnaud, & Spataro, 2012). Thus, for example, onset of pointing is a reliable predictor of the appearance of first words (Bates, Benigni, Bretherton, Camaioni, & Volterra, 1979; Tomasello, Carpenter, & Lizskowski, 2007), and in particular of nouns (Ozcaliskan, Gentner, & Goldin-Meadow, 2013); in addition, the production of gesture-word combinations that convey two distinct pieces of information predicts the emergence of twoword speech (Butcher & Goldin-Meadow, 2000; Fasolo & D’Odorico, 2012; Pizzuto & Capobianco, 2005). Different theories have been proposed to explain the relationship between gesture and spoken language. In a traditional theoretical approach gestures were considered as relevant features of the ‘prelinguistic’ stage, as behaviors that preceded and prepared for the emergence of language (Bates et al., 1979). More recent studies support the view that there is a remarkable continuity between prelinguistic and linguistic development, and that symbolic skills that are most evident in vocal linguistic productions, co-evolve with more general representational abilities, as is most apparent in the tight relationship between actions, gestures and words (Caselli et al., 2012). Today, a new theoretical framework emerging from different disciplines makes this approach to ontogeny of language extremely interesting and relevant. Recent findings on the neurophysiological basis of the motor system have provided a neural basis to this claim (Rizzolatti & Arbib, 1998; Rizzolatti & Luppino, 2001), supporting the hypothesis of a close link between motor programs associated to actions and gestures, and spoken linguistic representations in children (Capirci, Caselli, & De Angelis, 2010). Some interesting results on the relationship between gesture and language come from researches on children with developmental disorders involving delayed or impaired linguistic abilities. Most of these studies reported that, when children are limited in cognitive, linguistic, metalinguistic, and articulatory skills, they may compensate for some of these limitations with gestures (Capone & McGregor, 2004 for a review). As for children with Down syndrome, a greater percentage of actions and gestures was found in studies conducted on this population with the MB-CDI and strong correlation between lexical comprehension and gesture production was identified when assessed through questionnaires (Caselli et al., 1998; Galeote et al., 2011; Singer Harris et al., 1997) or during free interaction (Zampini & D’Odorico, 2009). A greater number of gestures than verbal productions was also found in a study where an experimental setting was used to elicit non verbal responses (Jackson-Maldonado, de Santiago Badillo, & Sa´nchez Aguliar, 2012). However, other studies did not find a gestural advantage in children with DS. Iverson, Longobardi, and Caselli (2003) analyzed gestures and speech production during mother–child spontaneous interactions in children with DS (CA: 3.9 years; MA: 1.8 years) and TD children matched for expressive language age (LA: 1.6 years). They found that children with DS displayed a smaller repertoire of deictic (e.g. POINTING) and representational gestures (e.g. COMB: the child moves his fingers near his head as if combing his hair in front a picture of a comb). However gestures were produced with similar frequency by children with DS and the TD controls. High variability in the spontaneous use of gestures has been observed. A recent study analyzed individual developmental trajectories of 8 children with DS longitudinally followed. Children’s spontaneous verbal and gestural productions were assessed during mother–child interaction from the age to two to four. The results highlighted two distinct patterns of development: some children showed an increasing profile of gesture production, whereas others showed an inverted U-shaped profile or a stable production of gestures. Only the latter group of children showed a remarkable growth in their spoken production (Zampini & D’Odorico, 2011a). Using a more structured situation, namely a picture naming task, the relationship between gestures and word production has been investigated in Italian children with TD, as well as in children with DS. A preliminary version of the PiNG test was used with a sample of TD children between 2 and 7 years of age (Pettenati, Stefanini, & Volterra, 2010; Stefanini et al., 2009). Results have shown that, when children are requested to label simple pictures of objects and/or actions, but no instruction regarding gesture production is given, they are likely to spontaneously accompany their spoken naming responses with pointing and/or representational gestures. Gesture production declined as a function of increasing age and spoken lexical competence. According with Capone (2007), the authors suggested that the function of these co-speech gestures may be to recreate a ‘direct link’ with the object or the action to be labeled and the production of a gesture may recreate the context in which the word was initially acquired, specifically when that word is not yet fully conceptualized. As for studies on children with Down syndrome in which the same structured task was used, the results on the relationship between gesture and word evidenced that children with DS (CA: 6.1 years; MA: 3.10 years) produced a significantly higher percentage of representational gestures without speech compared with the TD control groups (matched for CA, MA, or LA). The representational gestures produced were semantically related to the meaning represented in the

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pictures. With representational gestures children performed or reproduced the action usually executed with that object in hand or usually performed by the character depicted or represented in the picture itself. The authors suggested that these gestures might help children display ideas that they do not succeed in expressing in the verbal modality, conveying a substantial proportion of their knowledge (Stefanini et al., 2007, 2008). As evident from this background, results on lexical comprehension and production, and on the use of communicative gestures do not lead to unequivocal conclusions and further investigations are needed. Moreover, further studies are necessary in order to analyze, in preschoolers with DS, the lexical composition evaluated through direct tools and the use of spontaneous gestures when the child is requested to comprehend and produced nouns and predicates. The first aim of the current study is to evaluate comprehension and production of nouns and predicates in preschool children with DS, using both indirect and direct assessment tools. In particular we intend to investigate SD children of 2–3 years of developmental age since changes in the use of co-speech gestures between 2 year old children and children over 3 or 4 years of age were observed in typical development. Our second aim is to analyze the spontaneous gestures exhibited by children in comprehension and production, taking into account different lexical categories, namely nouns and predicates. Although a picture naming task may seem an unlikely context in which to examine gestures, it provides a common set of referents for communication, referents that are known to the experimenter and the coder. Moreover a naming task appears to be quite useful as a tool for exploring the link between gestural production and spoken linguistic representations. 2. Methods 2.1. Participants Eighteen DS children were asked to take part in this study: four of these children were excluded owing to their serious attention and collaboration problems which emerged while performing tasks. Thus the study included 14 Italian children with DS (6 boys, 8 girls), with a diagnosis of free trisomy 21 documented by karyotyping. At the moment of observation, they were attending specific speech and language therapy twice a week. None of the children were exposed to sign language. Children exposed to other spoken languages, children with auditory impairment, and children with epilepsy and psychopathological disorders were excluded from this study. The mean chronological age (CA) of children with DS was 54 months and the mean developmental age (DA), assessed by the Leiter International Performance Scale-Revised – Leiter R (Roid & Miller, 1997) or by Griffiths Mental Development Scales – Performance Scale E (Griffith, 2006), was 34 months. The participants with DS were matched one-to-one with typically developing (TD) children on the basis of their gender and DA: the same cognitive scale was used for each DS and relative TD control child. The same inclusion criteria adopted for children with DS were followed. The mean DA of TD children was 38 months and their CA was 29 months (see Table 1). A statistical analysis showed that the two groups did not differ in DA (x2(N = 28) = 16.67, p = .28) confirming that the matching was appropriated. The participants were included after the local Ethics Committee approved the protocol, and parents signed an informed consent. 2.2. Materials 2.2.1. The Italian MB-CDI The Italian version of the MacArthur-Bates Communicative Development Inventories MB-CDI – Words and Gestures Form (Caselli & Casadio, 1995) was filled in by the parents. The validity of the MB-CDI with parents of children with DS was demonstrated in a study by Miller, Sedey, and Miolo (1995); the questionnaire was also used, in different countries, with large populations of children with DS (Berglund, Eriksson, & Johansson, 2001; Caselli et al., 1998; Galeote et al., 2008, 2011; Zampini & D’Odorico, 2013).

Table 1 Mean (M), standard deviation (SD) and range (in months) of chronological and developmental age of children with Down syndrome (DS) and developmental age matched typically (TD) controls. Groups

Chronological age (months)

Developmental age (months)

DS children (n = 14)

M = 54 SD = 12 Range = 34–73

M = 34 SD = 4 Range = 23–39

TD children (n = 14)

M = 29 SD = 3 Range = 24–34

M = 38 SD = 6 Range = 23–42

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The questionnaire includes: 1. A checklist of 408 words divided into 19 semantic categories including items for nominals (e.g. animals, vehicles, toys), routines (e.g. people, games), predicates (i.e. verbs, adjectives) and function words (e.g. pronouns, prepositions, quantifiers). Each parent was asked if the child understood and produced each word. 2. An ActionGesture checklist, including 63 communicative and/or symbolic action-gestures (e.g. POINTING, BYE-BYE, COMB). Each parent was asked if the child habitually produced the actions and gestures included in the questionnaire. At the end of the questionnaire, there is a basic information sheet for collecting information on gender and birth order, the child’s medical history, exposure to languages other than Italian, on parental education and occupation. The questionnaire was completed by the parents the same day during which their child was assessed. 2.2.2. The Picture Naming Game (PiNG) The Picture Naming Game (PiNG) was used with children to assess lexical comprehension and production. This instrument is validated for Italian TD toddlers aged from 19 to 37 months (Bello, Caselli, Pettenati, & Stefanini, 2010; Bello et al., 2012). As reported in the Introduction, a preliminary version of the PiNG test was used in previous studies with older TD children (up to 7.6 years, Stefanini et al., 2009) and with children with DS (Stefanini et al., 2007, 2008), although it was not validated for this atypical population. The PiNG test is divided into four subtests: Noun Comprehension (NC), Production (NP), Predicate Comprehension (PC) and Predicate Production (PP). Each PiNG subtest consists of 20 lexical targets and 2 training items: the noun subtests (NC; NP) represent objects and tools and the predicate subtests (PC; PP) represent actions, adjectives and locative adverbs. The PiNG test was administrated to all children following the instructions provided in the validation study (Bello et al., 2012). In the comprehension subtests, three pictures were presented (the lexical target, the semantically related distractor and the semantically unrelated distractor): for example, in the NC subtest, the test administrator asked ‘‘Where is the cat?’’ presenting photographs of a cat, a dog and a television; in the PC subtest, the question was ‘‘Who is drinking?’’ presenting photographs of a child drinking, eating and grasping. The child was asked to point to or to touch the corresponding picture. The spatial arrangement of the photographs was random. In the production subtests, only one of the above pictures was presented: for example, in the NP the test administrator asked ‘‘What is this?’’ presenting the dog picture; in the PP the test administrator asked ‘‘What is he/she doing?’’ presenting the action word eating picture, and ‘‘What is it like?’’ for the descriptive words (e.g. small) and ‘‘Where is it?’’ for the locative adverbs (e.g. inside). The child was supposed to provide an answer. The NC and NP were combined, followed by the combined administration of the PC and PP. In particular, once the child provided an answer to the item in the comprehension subtest, the adult removed the photographs of the comprehension item and the semantically unrelated distractor, and the remaining photograph (i.e. the semantically related distractor) was used to test production. The two sets of pictures (nouns and predicates) were presented separately in random order, but order of picture presentation within each set was fixed (for a more detailed description of the instrument and test procedure see Bello et al., 2012). All children were tested individually in a quiet room by two trained psychologists after a brief period of familiarization. Following the procedures applied in the validation study, the PiNG test was administered to all 14 TD children and to 11 children with DS in one session. Three children with DS required two sessions. One or two breaks were given to TD and children with DS when needed during Noun task (NC and PN) and during Predicate task (PC and PP). The mean time of PiNG administration was about 34 min for children with DS and 24 min for TD children. All sessions were videotaped for later transcription. 3. Coding 3.1. The Italian MB-CDI For both comprehension and production, each item was given a score of 1 when the parent affirmed the child could understand/produce that item and 0 in the negative case. All the parents’ answers concerning the 408 words proposed were summed in the Total word Comprehension and Total word Production. For the analysis of lexical repertoire we only considered the Noun and Predicate categories (301 words). For the Noun category, all the answers given by the parents to the list of 209 items referring to the 9 different semantic groups (animals, vehicles, games, food, clothing articles, body parts, furniture items, household objects, outdoor items and places) were calculated. Likewise, for the Predicate category, all the answers given by the parents to the list of 92 items, referring to the 2 semantic groups (verbs and adjectives) were considered. As for Action-Gesture section, all the answers given by the parents to the list of the 63 items included were calculated. 3.2. The Picture Naming Game (PiNG) With regard to the comprehension subtests (NC and PC) only the first answer was analyzed. With regard to the production subtests (NP and PP), when a child did not provide the target spoken answer on the first attempt, he/she was given a second chance: the administrator, without explicitly correcting the child, repeated the question ‘‘What is this?’’ in the NP subtest, or ‘‘What is he/she doing?’’ in the PP subtest, encouraging the child to provide a second answer. In these cases, a ‘‘best response’’

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criterion was adopted, that is, if the child provided a correct spoken response on the second attempt, he/she was given credit for providing a correct response. If neither answer was correct, the first answer was tallied. We examined children responses in both comprehension (NC; PC) and production (NP; PP) subtests in terms of accuracy and strategies of answers, following the coding procedures provided in the validation study. In the present research we also analyzed the use of the gestures in both lexical comprehension and production tasks. For each item administered, we coded only one gesture, namely the one produced with the answer codified as ‘‘best response’’. In the production subtests, if the child produced a gesture without speech at the first attempt and a gesture associated with a word in the second attempt, we only coded the latter. 3.2.1. Vocal accuracy Correct answers as well as errors were considered in the present study. With regard to comprehension, the answer was coded as correct when the child showed, indicated or chose the photograph corresponding to the target labeled by the adult. With regard to production, a vocal answer was coded as correct when the child provided the expected word for the photograph. Phonologically altered forms, (e.g. ‘‘ompello’’ instead of ‘‘ombrello - umbrella’’) as well as onomatopoeia (e.g. ‘‘cocode`’’ instead of ‘‘gallina - hen’’) corresponding to the expected word were considered as correct answers. Errors included incorrect spoken answers and no spoken responses. Incorrect spoken answers were coded when both words inconsistent with the expected word and unintelligible answers (e.g., ‘‘tita’’ instead of ‘‘pettine - comb’’) were provided. No-response was coded when children declared they did not know the word corresponding to a photograph or did not provide an answer. As shown in a previous study on TD children from 23 to 37 months where the PiNG was used (Bello, Giannatoni, Pettenati, Stefanini, & Caselli, 2011), the two different types of errors show different developmental patterns: whereas the percentage of incorrect answers increases depending on lexical skills, the no-responses proportionally diminish. For this reason we also considered incorrect answers and no-response separately. 3.2.2. Gestures and modality of expression In comprehension subtests (CN and CP) we coded only the representational gestures produced after the experimenter had produced the required item (e.g. when the child hears the word ‘‘big’’, he extends the arms for BIG). The deictic gestures were not considered. In production subtests (PN and PP) we coded gestural production, including deictic gestures (e.g. POINTING) and representational gestures (e.g. for the picture ‘‘lion’’ the child imitated the lion’s attack with his arm). Regarding the modality of expression, the responses in the production task were coded as unimodal spoken when the child answered only in the spoken modality. They were coded as bimodal when the child answered using both spoken and gestural modalities. Deictic and representational gestures associated with a spoken response (correct as well as incorrect) were coded (e.g. the child said ‘‘dog’’ POINTING to the dog; the child said ‘‘bum’’ – onomatopoeia meaning to fall and made with his hand the gesture of FALLING DOWN). If the child produced two gestures, one deictic and one representational, for the same item, we coded the representational gesture. Responses were coded as unimodal gestural when the child did not produce any spoken response (no-response) and the meaning (related or not with respect to the item proposed) was produced only through the representational gestures (e.g. for the picture ‘‘comb’’ the child moves his fingers near his head as if COMBING his hair but no words were produced). 3.2.3. Reliability Data of all children with DS and TD children (i.e. 100% of all trials) were independently coded from tape by two coders (the first and second author). For all participants, the reliability between the coders (for the comprehension and production, for the gestural production, as well as, for the modality of expression) was assessed. Agreement between coders was 98% and 93.3% for the comprehension and production respectively, 92.5% for gestures, and 98% for modality of expression. The instances of disagreement were identified and a third coder was requested to code all these instances, choosing one of the two classifications proposed by the first two coders.

4. Data analysis All analyses have been performed using the statistical software SPSS (version 20.0). A p value of .05). 5.2. Lexical comprehension and lexical production at the PiNG test For each subtest the data of the children who completed more than half of the total items were considered for the analysis. Following this criterion, the data of 1 child with DS was excluded from the PN analysis and data of 2 children with DS was excluded from the PP analysis. Fig. 1 displays the percentages of correct answers exhibited during the comprehension and production tasks by children with DS and TD controls. We conducted four separate analyses of variance (ANOVAs) with the group (DS; TD) as independent variables and the percentage of correct answers and errors in comprehension and in production subtests as dependent variables respectively. Significant differences between children with DS and TD controls were found in comprehension (correct spoken answers: F(1,27) = 20.383, p < .001, h2 = .44; errors: F(1,27) = 19.274, p < .001, h2 = .43) and in production (correct spoken answers: F(1,25) = 29.830, p < .001, h2 = .55; errors: F(1,25) = 29.842, p < .001, h2 = .55). Children with DS produced fewer correct answers and a higher number of errors than TD children in comprehension subtests and in production subtests. In addition, a difference between comprehension and production emerged within each group. Two separate ANOVA tests (independent variable: type of task, comprehension and production; dependent variable: percentages of correct answers) were performed, respectively for each group of children. Children with DS and TD children produced significantly more correct answers in comprehension than in production task (DS: F(1,25) = 29.529, p < .001, h2 = .55; TD: F(1,27) = 29.302, p < .001, h2 = .53). We analyzed in detail the linguistic profiles of children with DS and TD controls, considering separately the specific trends of responses during the comprehension and production tasks for Nouns and Predicates.

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Fig. 1. Mean percentage of correct answers at PiNG comprehension and production tasks by children with DS and TD controls.

Four separate ANOVA tests (independent variable: lexical category, Nouns and Predicates; dependent variable: percentage of correct answers) were performed, respectively in comprehension and production, in order to evaluate the lexical category in each group of children. Our results showed that the percentage of correct answers is higher in Nouns than in Predicates for children with DS, both in the comprehension (F(1,26) = 12.708, p = .001, h2 = .32) and in the production tasks (F(1,26) = 7.078, p = .013, h2 = .21). Also TD children produced more correct answers in the Nouns, whereas the difference between Nouns and Predicates is significantly evident only in the comprehension subtest (comprehension F(1,26) = 11.410, p = .002, h2 = .30; production F(1,26) < 1, p > .05). In order to analyze similarities and differences between the two groups of children, we conducted four separate analyses of variance (ANOVAs) with the group (DS; TD) as independent variable and correct answers for four subtests as dependent variables respectively. For both the comprehension and the production subtests, the correct answers provided by children with DS were significantly lower with respect to those provided by TD children (CN: F(1,27) = 14.873, p < .001, h2 = .36; CP: F(1,27) = 17.330, p < .001, h2 = .40; PN: F(1,26) = 17.598, p < .001, h2 = .41; PP: F(1,25) = 18.813, p < .001, h2 = .44). We also considered the errors (no-response and incorrect answers) provided by children during the comprehension and production tasks, separately for Nouns and Predicates. The mean percentages of incorrect answers and no-responses exhibited at the PiNG subtests by children with DS and TD children are presented in Fig. 2. Four separate analyses of variance (ANOVAs) with the group (DS; TD) as independent variable and error for four subtests as dependent variables respectively were performed. For both the comprehension subtests and the production subtests, the errors provided by children with DS were significantly higher with respect to those provided by TD children (CN: F(1,26) = 14.708, p < .001, h2 = .36; CP: F(1,26) = 17.189, p < .001, h2 = .39; PN: F(1,25) = 17.614, p < .001, h2 = .41; PP: F(1,24) = 18.840, p < .001, h2 = .44). An analysis of types of errors

Fig. 2. Mean percentages of incorrect answers and no-responses for the four PiNG subtests by children with DS and TD controls.

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performed by the children was also conducted using separate analyses of variance (ANOVAs) with the group (DS; TD) as independent variable, and incorrect spoken answers and no-responses separately, for four subtests, as dependent variables respectively. Results showed that in the comprehension subtests the no-responses exhibited by children with DS were significantly higher with respect to those provided by children with TD (Nouns: F(1,27) = 9.773, p = .004, h2 = .27; Predicates: F(1,27) = 32.773, p < .001, h2 = .55). Relative to the incorrect spoken answers, no significant differences were found in Nouns and in Predicates (F(1,27) < 1, p > .05). For the production subtests, the no-responses provided by children with DS were significantly higher with respect to those provided by TD children (Nouns: F(1,26) = 8.879, p = .006, h2 = .26; Predicates: F(1,25) = 35.953, p < .001, h2 = .60). The number of incorrect answers exhibited by children with DS was significantly higher with respect to those exhibited by TD controls only in the Noun subtest (F(1,26) = 5.772, p = .024, h2 = .19); by contrast, the difference between the two groups did not emerge in the Predicate subtest (F(1,26) < 1, p > .05). 5.3. The use of gestures in lexical comprehension and production tasks The gestures spontaneously produced by the children during the four PiNG subtests were analyzed in this study. We considered the use of representational gestures in the comprehension subtests and the use of deictic and representational gestures in production subtests. Fig. 3 reports the percentages of items where the children produced gestures. In comprehension subtests, children with DS produced a greater number of representational gestures compared with TD children. ANOVA analysis confirms a significant difference between two groups (F(1,26) = 7.715, p = .012; h2 = .23). We carried out two separate ANOVA tests with the group (DS; TD) as independent variable and the representational gestures produced in NC and PC subtests as dependent variables respectively (percentages of gestures on administrated total items). Children with DS produced a significantly higher representational gestures percentage during PC subtest (F(1,26) = 14.217, p < .001; h2 = .35), but not in NC subtest (F(1,26) < 1, p > .05). In production subtests an ANOVA test with the group (DS; TD) as independent variable was carried out, taking into consideration the total number of spontaneously produced gestures. Our results do not show a significant difference between the two groups concerning the overall gesture production (deictic and representational) in the PiNG test (F(1,25) < 1, p > .05). We analyzed separately the two gesture types (deictic and representational) in NP and PP subtests. Four separate ANOVA tests with the group (DS; TD) as independent variable and the percentage of gestures types, deictic and representational, as dependent variables respectively were carried out. The results did not show a significant difference between children with DS and TD controls concerning deictic gestures (Nouns and Predicates: F(1,25) < 1, p > .05) or representational gestures (Nouns and Predicates: F(1,25) < 1, p > .05). We analyzed within each group the difference between the deictic and the representational gestures, separately for Nouns and Predicates. Within each group we conducted four separate analyses of variance (ANOVAs) with the type of gesture (deictic; representational) as independent variable and the percentage of gestures in the NP and PP subtests as dependent variables respectively.

Fig. 3. Mean percentage of PiNG items accompanied by deictic and/or representational gestures by children with DS and TD controls.

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Fig. 4. Mean percentages of answers by modality of expression for PiNG production tasks by children with DS and TD controls.

Results showed that children with DS and TD controls tend to produce more frequently the deictic gestures in NP subtest (DS: F(1,23) = 3.826, p = .06, h2 = .14; TD: F(1,26) = 3.739, p = .06, h2 = .13). As for the representational gestures, in children with DS there was not a significant difference in NP and in PP subtests (F(1,23) < 1, p > .05), whereas the TD controls more frequently produced representational gestures in PP subtest (F(1,27) = 8.404, p < .001, h2 = .24). The modality of expression was considered only in PiNG production subtests. Fig. 4 shows the percentage of unimodal spoken, bimodal, unimodal gestural answers exhibited by the two groups of children, separately in Nouns and Predicates. We conducted separate analyses of variance (ANOVAs) with the group (DS; TD) as independent variable and the percentage of type of answers, unimodal spoken, bimodal and unimodal gestural, as dependent variables, in the NP and PP subtests respectively. No differences were found in unimodal spoken answers and in bimodal answers for NP subtest and for PP subtest (F(1,25) < 1, p > .05, respectively). Significant differences between groups were instead found in unimodal gestural answers only for PP subtest (Nouns: F(1,26) < 1, p > .05; Predicates: F(1,25) = 5.491, p = .028, h2 = .18). 6. Discussion The current study aimed to investigate, for the first time in children with DS with a developmental age of 3 years, both lexical receptive and expressive skills using indirect and direct assessment tools. The modality of expression was also considered. This age represents in fact a privileged period to study the linguistic abilities in children, given the developmental changes that occur in the spoken vocabulary (both size and lexical repertoire) and in the use of co-speech gestures. The results of the study may be summarized in two main points that concern: first, lexical comprehension and production, considering nouns and predicates as two different lexical categories, and second, the use of gestures in both lexical comprehension and production of nouns and predicates. 6.1. Spoken lexical comprehension and production of nouns and predicates In the present study, children with DS showed a general weakness in lexical abilities compared to TD children of the same developmental age; the delay was evident in parental report (MB-CDI), as well as through a structured test (PiNG). Our results indicate that preschool children with DS have lower performance on lexical comprehension tasks compared to TD children. This confirms findings reported in previous studies on school-aged children and adolescent with DS, in which lower performance on lexical comprehension in this population has also been reported (Caselli et al., 2008; Price et al., 2007; Ypsilanti et al., 2005). By contrast, our data do not confirm results by Galeote et al. (2011) and by La´zaro et al. (2013). These authors found that the size of lexical comprehension vocabulary was greater in children with DS than in children with TD. As for lexical production, children with DS showed a smaller vocabulary size with the MB-CDI as well as with the PiNG test. On both tests the children with DS provided significantly fewer correct answers than the TD children. These data confirm and extend the results of previous studies on older children observed during spontaneous interactions with their mothers (Zampini & D’Odorico, 2011b) or through structured tests (Caselli et al., 2008; Stefanini et al., 2007, 2008). For the first time, our data provide evidence of a delay in expressive lexicon that emerges when indirect measures are considered. In fact, previous studies using the same MB-CDI questionnaire with parents of comparatively younger children have reported no differences in expressive lexicon (Berglund et al., 2001; Galeote et al., 2008; Vicari et al., 2000). At the age considered in the present study, the asynchrony between language and general cognitive abilities emerges. Language delay

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of children with DS might then be explained as a cascading effect determined by specific language skills and cognitive deficits, as documented in this population. Many studies report in fact serious phono-articulatory deficits together with verbal short-term memory impairment (Costanzo et al., 2013; Jarrold, Baddeley, & Phillips, 2007; Lanfranchi, Jerman, Dal Pont, Alberti, & Vianello, 2010; Vicari, Marotta, & Carlesimo, 2004). These deficits could be responsible for a more difficult and slow increase of vocabulary compared with TD children at a comparable developmental stage. In our study, the differences between lexical skills in children with DS and TD matched controls appeared more evident when the lexicon is assessed through a structured test such as PiNG. Parental reports, such as the MB-CDI, offer a parent’s extensive knowledge of their children and provide data on the entire repertoire of words comprehended and produced in a wide range of spontaneous and familiar contexts. Nevertheless, questionnaires are not suitable for capturing lexical organization or access, attention, accuracy in pronunciation, or level of decontextualization in understanding and producing words. On the contrary, a structured task, such as PiNG, requires general cognitive skills and executive functions (e.g., attention, planning, categorization, shifting, inhibition, etc.) that are impaired in people with DS, as reported in several studies (Costanzo et al., 2013; Lanfranchi et al., 2010 among others). These functions are involved both in production and in comprehension subtests of PiNG. However, during the comprehension subtests lower demands are posited on executive functions, since part of the cognitive load is supported by the subtest’s structure, as suggested by Næss et al. (2011). In particular, the PiNG test requires lexical retrieval abilities both for comprehension and production tasks. Picture naming necessarily involves a lexical-semantic encoding process during which one lexical unit is selected from a set of conceptually similar candidates (Caramazza, 1997). Huttenlocher (1974) proposed that even shallow and incomplete storage of an existing word form might be ‘‘good enough’’ to permit access to its meaning. In contrast, word production requires the retrieval of phonological information that might not be needed in similar levels of detail in comprehension. These disparities may affect how lexical information is selected and retrieved (Belke, Brysbaert, Meyer, & Ghyselinck, 2005). Specific difficulties in lexical retrieval are reported in children with DS whose lower general levels of intelligence might interfere with the ability to categorize objects and actions and, as a result, hinder further semantic representation and lexical development. Different studies have found a relationship between semantic representation and successful word retrieval both in typical (McGregor, Friedman, Reilly, & Newman, 2002) and atypical populations (Bello, Capirci, & Volterra, 2004; McGregor, Newman, Reilly, & Capone, 2002; van der Schuit, Segers, van Balkom, & Verhoeven, 2011). The type of mistakes children make (incorrect vs no-response) during a naming task provides a large amount of information on the quality, complexity and the stability of the semantic-conceptual representations. Many studies have shown that accurate naming is correlated to a rich semantic representation; on the contrary, the mistakes are linked to a weak semantic representation of words (Barsalou, 1999; Belacchi & Benelli, 2007; Borghi, 2002). A weakness in semantic representation affecting lexical access and retrieval might explain the significantly higher number of no-responses that emerged in our study, both in the comprehension and in the production subtests in children with DS compared with TD children. The greater frequency of no-responses in children with DS may be linked to the smaller vocabulary size, according to the normative data of the PiNG test that show a higher number of no-responses at a younger developmental age in TD children (Bello et al., 2012). As for the composition of the lexical repertoire, our results show that in both groups, nouns are understood and produced in higher percentages compared to predicates, confirming previous findings on typical population (Caselli et al., 1999; D’Odorico & Fasolo, 2007; Tardif et al., 1997; Waxman et al., 2013) and on children with DS (Zampini & D’Odorico, 2011b). The asymmetry in the acquisition of nouns and predicates is evident in the child’s vocabulary until the third year of age and reflects a different organization of these lexical categories which may depend on different cognitive mechanisms involved in the association of meaning to nouns and predicates (Hall & Waxman, 2004). Concrete nouns map onto the perceptual world in a direct way; they refer to objects and entities that naturally stand out as separate in the world (Gentner & Boroditsky, 2001; Markman, 1989). In the first stages of lexical development, children associate nouns to objects and generalize them to objects of the same category by employing mainly extra-linguistic indexes (e.g. the socio-communicative context, the use of gaze following, actions and gestures). By contrast, verbs select from a diffuse set of relational concepts for their referents that vary across different contexts. The relations that verbs convey vary also across languages and therefore, in order to learn verbs, children must discover how the language they are learning selects and combines relations. Verbs also requires linguistic guidance (e.g. morphosyntactic indexes), as to which relations in the world map onto the verbs in the language the child is learning (Bowerman & Choi, 2003; Gentner, 2006; Ozcaliskan et al., 2013). With regard to the Italian language, the earlier prevalence of nouns over verbs could depend also on specific language factors, such as a higher number of nouns than verbs, a more salient (initial or final) position of nouns inside sentences than predicates, and a lower morphosyntactic variability for nouns than predicates (Caselli et al., 1999). 6.2. The use of gestures in lexical comprehension and production The second aim of the present research was to examine the relationship between spontaneous gesture production and lexical skills. For the first time, this study explores the relationship between gestures and the comprehension and production of nouns and predicates through a structured task. Our results highlight that the total number of representational gestures produced in the comprehension task was higher in children with DS compared with TD controls; the latter exhibited few gestures. Considering separately the two lexical categories, children with DS showed more gestures compared to TD controls in Predicate Comprehension, whereas the two

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groups did not differ in total number of gestures in Nouns Comprehension. As for production, results on the Italian MB-CDI showed that children with DS and TD controls exhibited the same total number of actions and gestures. Our data do not confirm those of previous studies (Caselli et al., 1998; Galeote et al., 2011; Singer Harris et al., 1997). We suggest that this finding may depend on the different chronological ages of participants and the instrument used is no longer appropriate to highlight the differences at the age considered in the present study. In the PiNG production subtests, in agreement with Stefanini et al. (2007), children with DS and TD developmental age matched controls produced the same number of gestures. No differences emerged considering the overall task, and the two separate subtests. Moreover in both groups of children more deictic (i.e. pointing) than representational gesture were produced and deictic gestures were more frequently used in the production of nouns. As suggested in previous studies, pointing gestures may help children focus their attention on the object that must be named and allow them to create a link between the perceived object or action and its spoken label (Butterworth, 2003; Goldin-Meadow, 2007). The representational gestures are distributed quite differently in the two groups of children across the two lexical categories: children with DS have the same percentage of representational gestures for both Nouns and Predicates; on the contrary, typically developing children produced a higher percentage of representational gestures on the Predicate Production subtest. This different distribution of representational gestures might depend on the different development level of semantic representations linked to the lexical categories in each group. Owing to their phone-articular deficits, children with DS still show a weak association between sematic representation and lexical item in both lexical categories. As suggested by Capone (2007) if a child’s meaning representation is intact, but poorly linked to his/her phonological representation, the child may express such representation more readily in gestures. On the contrary, TD children already have a more consolidated semantic representation of Nouns and therefore the link with the word is more direct; this link is not yet consolidated for Predicates, owing to the above mentioned more complex cognitive mechanisms. The weakness of the link between the concept and the linguistic referent can be seen through the more frequent representational gestures in Predicates than in Nouns in children with DS. In fact, gesture production may help create a more precise and concrete image linked to the word. Moreover it is an essential characteristic of predicates to refer to actions and representational gestures reproduce these actions. This speculation is consistent with results of Marentette and Nicoladis (2011) who demonstrated that preschool children consider representational gestures as action-associated rather than as labels for objects. Evidence for a language–action link come from studies on parallel processing of words and actions in normal adults: meanings of action words or adjectives were automatically associated with the corresponding property of the object and activated a reach and/or a grasp motor plan influenced by the word (Gentilucci, Benuzzi, Bertolani, Daprati, & Gangitano, 2000; Glover, Rosenbaum, Graham, & Dixon, 2004). Considering the modality of expression, we found that the percentage of unimodal spoken answers and bimodal productions (speech and gesture) did not differ between the two groups. However children with DS produced higher unimodal gestural answers than the control group in the Predicate Production subtest, and all of them are representational gestures. These data may be interpreted as indicating that representational gestures are used by DS children to express those meanings that may not be conveyed verbally as also suggested by Stefanini et al. (2007). With representational gestures children performed or reproduced actions observed or linked to the referent in the picture and this may be considered an important step in the process of lexical retrieval (Krauss, Chen, & Gottesman, 2000). In fact, when speakers encounter difficulties in lexical retrieval the production of gestures activates the concept to be expressed and representational gestures manifests the child’s knowledge of semantic content of the expected word (Kita, 2000). Thus to consider co-speech gestures in a naming task represents a good window to highlight the cognitive function of gestures not only for their more evident communicative function, when gestural production is observed in contexts of child– mother interaction.

7. Summary and conclusions As for spoken lexical skills, our results showed a general delay in both comprehension and production of nouns and predicates in children with DS compared to TD controls matched for developmental age. The asynchrony between language and general cognitive abilities that emerges in our study supports the hypothesis that lexical comprehension and production become progressively poorer in relation to the stage of cognitive development (Næss et al., 2011). However strong similarities between the two groups of children also emerged. In children with DS, as in TD children, lexical comprehension was more developed than lexical production, and nouns are understood and produced better than predicates. As for gestural production, our data, for the first time, demonstrate that representational gestures not only serve as a potential means of expression, but also appear to facilitate the processing of words produced by the administrator, and the access of semantic representation in comprehension of words. Children may produce gestures not only to communicate with others but also for ‘‘thinking’’. Future investigations, based on longitudinal observations, are crucial to better understand the relationships among different language domains and the links between action, gesture and language, and the ways in which these may change during development. In addition, it will be important to investigate how gestural production, compared with vocal, changes in the same child comparing data collected during mother–child spontaneous interaction and structured tasks adapted and validated for this population.

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Our results encourage early language intervention on children with DS focused on comprehension abilities, often considered by practitioners as strength in this population. Moreover, the observation of gestures in a structured task may allow researchers and clinicians to obtain a better view of semantic knowledge of children, behind their lexical spoken skills, in particular in those with cognitive and/or language impairment. Acknowledgments This research was supported by the National Research Grant PRIN 2008 ‘‘Gestures and Language in Children with Atypical and at Risk Developmental Profiles: Relationships among Competences, Mother–Child Interaction Modalities and Proposals of Intervention’’, the Fondazione Monte of Parma and the Peretti Foundation. We wish to thank Paula Marentette and Virginia Volterra for their insightful comments and for the revision of the English language. References Abrahamsen, A. (2000). 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