Neurol Sci (2010) 31:471–481 DOI 10.1007/s10072-010-0309-2
ORIGINAL ARTICLE
Language abilities and gestural communication in a girl with bilateral perisylvian syndrome: a clinical and rehabilitative follow-up Bruna Molteni • Daniela Sarti • Gloria Airaghi • Chiara Falcone Giulia Mantegazza • Giovanni Baranello • Federica Riva • Veronica Saletti • Nicoletta Paruta • Daria Riva
•
Received: 16 January 2009 / Accepted: 9 April 2010 / Published online: 2 June 2010 Springer-Verlag 2010
Abstract We present the neuropsychological and linguistic follow-up of a girl with bilateral perisylvian polymicrogyria during 4 years of gestural and verbal speech therapy. Some researchers have suggested that children with bilateral perisylvian polymicrogyria mentally fail to reach the syntactic phase and do not acquire a productive morphology. This patient achieved a mean length of utterance in signs/gestures of 3.4, a syntactic phase of completion of the nuclear sentence and the use of morphological modifications. We discuss the link between gesture and language and formulate hypotheses on the role of gestural input on the reorganization of compensatory synaptic circuits. Keywords Bilateral perisylvian polymicrogyria Gestural communication Neuropsychological follow-up
Introduction There is plenty of information in literature to support the close relationships between gesture and language [1–8]. The comprehension and production of gestures and language evolve in typically developing children in a close
B. Molteni (&) D. Sarti G. Airaghi G. Mantegazza G. Baranello F. Riva V. Saletti N. Paruta D. Riva Developmental Neurology Division, Fondazione I.R.C.C.S. Istituto Neurologico ‘‘Carlo Besta’’, via Celoria, 11, 20133 Milan, Italy e-mail:
[email protected] C. Falcone Neuroepidemiology Unit, Fondazione I.R.C.C.S. Istituto Neurologico ‘‘Carlo Besta’’, via Celoria, 11, 20133 Milan, Italy
temporal relationship and are mediated by adjacent and partially shared cortical regions. Many neuroimaging studies have demonstrated that the motor representations of oral and manual movements are adjacent and partially overlap in many frontal and parietal regions, including the primary motor and ventral pre-motor areas, and the intraparietal and inferior parietal sulci [9–12]. A complex neuronal ‘‘mirror’’ system has been demonstrated in some of these areas. According to Iacoboni and Wilson [13], the discovery of the mirror system strongly supports the close link between gesture and language because it provides the anatomical substrate that enables human beings to associate the observation and execution of actions of the mouth and hands, which is the first step toward imitation. In addition to Broca’s area, the mirror system also involves the superior temporal cortex, which overlaps with Wernicke’s area and has neurons that are activated with movements of the face and body, and an area in the parietal cortex that combines visuospatial information. This circuit enables imitation and amply overlaps with the well-known areas of language, suggesting a developmental continuity between action, observation, imitation and language. In addition, a few studies have recently shown that it might provide the neuronal substrate for an alternative functional reorganization, which could be stimulated in the rehabilitation setting in pathological conditions. In recent years, numerous studies have concentrated on the spontaneous gestural production in children with neurological disorders and language impairment [14, 15]. These papers had the purpose of establishing whether gestural development followed typical or atypical patterns in comparison with typically developing children, and whether gestures compensated for the deficiency in spoken language or facilitated language development in such infants.
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In the last two decades, augmentative communication systems relying on visual signs and/or symbols have been used in hearing children with a severely impaired capacity for oral expression. Analyzing language development in cognitively impaired children without hearing problems exposed to a systematic signed input, some authors [16, 17] found that the mean length of utterance (MLU) remained below 3, the utterances did not become more complex as they increased in length and the semantic relationships expressed were generally very simple, with a large proportion of utterances produced by juxtaposing words or ‘‘chaining items’’ [18]. They also reported that lexical categories mainly consisted of open-class elements (nouns, verbs, adjectives and adverbs). In contrast to the study by Grove and Dockrell [17], reporting that such children fail to reach morphological competences of language production, Rudd et al. [19] have recently conducted an experimental study consisting of teaching morphological changes in signs to a group of hearing children with cognitive impairment. Interestingly, they found that the children were capable of learning productive morphological rules of the signs. In relation to the development of pragmatic competences, a few longitudinal studies have examined the conversational acts produced by children who use augmentative communication systems. Some authors have identified a persistent impairment in the functional use of these systems and a tendency to adopt a passive role in the interaction [20]. Bilateral perisylvian polymicrogyria (BPP) is of particular interest among the neurological developmental disorders associated with severe language impairment. BPP was the first bilateral polymicrogyria syndrome to be described [21] and it is the most common [22]. It is clinically characterized by a pseudobulbar or supranuclear cortical palsy with facial, pharyngeal, glossal and masticatory diplegia, mental retardation and epilepsy, and by language difficulties that are often more severe than might be expected from the severity of the pseudobulbar palsy. Sans and Fernandez–Alvarez [23] suggested that the reason for these difficulties might lie both in the oro-motor dyspraxia and in a more extensive dysfunction of the cortical areas responsible for language. In a recent study [24] evaluating the neuropsychological characteristics, and language in particular, of six children with BPP, we found a globally impaired verbal and gestural communication and the inability to reach a primitive syntactic phase (i.e., incomplete and some nuclear sentences, according to the model of morphological language development proposed by Cipriani et al. [25]). In that study, however, all the children underwent different types of rehabilitation programs at different institutions and we were not able to formulate any hypotheses on the role of the gestural input in the language reorganization of these children with bilateral lesions.
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In the present study, we used signed Italian (SI), which combines lexicon from Italian sign language (ISL) with the grammar of spoken Italian (e.g., ball over table), and exact signed Italian (ESI), which in addition to SI uses ‘‘finger spelling’’ (a form of visual and manual alphabet), to ‘‘write’’, in space, those aspects that were missing or differently produced in the ISL. The aim of the study was to analyze the progress in lexical, syntactic, morphological and pragmatic terms the capabilities of a girl affected by BPP and exposed to signed Italian and later to exact signed Italian [26, 27] during a 4-year speech therapy at our institution.
Materials and methods Case description Clinical history The girl had no family history of neurological diseases and was the offspring of a reportedly normal pregnancy and delivery. At birth, she had tremors treated with phenobarbital. At 2 months, hematological tests revealed a recent cytomegalovirus infection. She had sucking/swallowing difficulties and delayed motor development, learning to walk independently at 2 years. She also had severely delayed language development with reduced vocalization and no babbling, as well as oro-motor problems with dribbling and eating difficulties. No epileptic seizures were reported. From the age of 12 months, she underwent psychomotor rehabilitation treatment. At the age of 3 years, she started speech therapy at another institution, using a system of visual symbols of augmentative alternative communication (AAC). Clinical examination and neuropsychological assessment The girl came to our observation at the age of 7 years and 4 months for an opinion on the rehabilitative program. She was attending the second year of primary school. MRI was performed using a 1.5-T scanner taking T1-weighted sagittal and T2-weighted axial views and scoring the extent of polymicrogyria and the degree of associated hemispheric distortion on the images according to the method used by Jansen and Andermann [22]. The images revealed diffuse bilateral asymmetrical (right [ left) polymicrogyria grade 3 [22] particularly evident at the perisylvian site (Fig. 1). The frontal regions were also affected. Lateral ventricles were asymmetrically enlarged (left [ right), mainly at the level of the trigons. The EEG showed interictal abnormalities with epileptiform activity, mainly over the temporal regions. Neurological assessment revealed
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We opted to use gestural communication in the rehabilitation setting to increase the girl’s language competences because of her severe dysarthria, cognitive impairment, spared manual praxic abilities and the spontaneous preference for mimicry and gestures. We formulated a speech therapy project aimed to develop all the language components, following the steps of typical language development. The creation of a communication network that also involved the girl’s family and her school was essential for this purpose. The features and goals of the treatment are illustrated in Table 2. Assessment of language development Fig. 1 MRI T1-weighted axial scans showing diffuse bilateral asymmetrical (right [ left) polymicrogyria grade 3 particularly evident at the perisylvian site
pseudobulbar palsy with anarthria and both general and fine motor difficulties. The girl was unable to close her mouth or move her tongue. Her phonation was limited to brief, raucous and unmodulated vocalizations. Velum mobility was reduced and swallowing was accompanied by a hyperextension of the head. Automatic chewing, coughing or vomiting reflexes were absent. She had bilateral tactile hypesthesia on her face, more marked on the left. The imitation of manual gestures was better on the right and the child could open her hand, extend her fingers, make a fist, point and bring thumb and index finger in a clamping action. School teachers and family members used oral communication modalities and AAC based on visual symbols, the latter however being poorly spontaneously used by the child. Her communication consisted of pointing and about 20 spontaneous isolated representational gestures made with difficulty and with one hand accompanied by rare vocalizations and facial mimicry. The girl underwent a cognitive and language assessment. Scholastic abilities were also assessed by means of a word spelling test. The results are shown in Table 1.
We analyzed the data collected five different times (T0, T1, T2, T3, T4) at 1-year intervals, starting from the age of 7 years and 4 months. The samples analyzed lasted 20 min and came from video-recorded sessions conducted in two different settings: a conversation with the therapist who communicated using SI and spoken language, and a figuredescribing task. In the conversational setting, the girl was encouraged to spontaneously communicate with the therapist about a present or past event or activity that she was interested in. For the figure-describing task, she was asked to describe 12 figures drawn from the childhood language assessment tests ‘‘PFLI, Prove per la valutazione del linguaggio infantile’’ [33]. The following gestural productions were considered: • •
• •
pointing: when the child used the hand to point to a particular object or event; representational gestures: gestures having a basic semantic content, relatively stable across different situations; some were conventional and culturally defined (e.g., HELLO, GREAT), while others appeared to be more directly action related (e.g., TO SLEEP) or object related (TELEPHONE); signs: from LIS lexicon used by the deaf community in Milan; finger spelling.
Table 1 Cognitive, language and scholastic assessment at T0 Test
Results
WISC-R [28]
PIQ 57
Italian version of MacArthur-Bates Communicative Developmental Inventory, gestures and words form [29]
Words produced: 0 (younger than 8 months old) Gestures produced: 45 (50th percentile of 17 months)
Language comprehension assessment tests: protocol 3 [30]
Words comprehended: all the 408 words Average score for children aged 42–48 months
PPVT [31] word comprehension test
QV \ 65 (QV 80 for age range 45–50 months)
Writing tests I elementary narration [32]
Poor (isolated, flat two-syllable words)
Self-dictated words in response to figurative stimulus (graduated internal test)
poor (three correct two-syllable words)
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Table 2 Characteristics and objectives of the treatment Type Twice-weekly individual sessions in the presence of a parent and/or school support teacher; regular sessions for teaching the signs to the adult and classmates Tools Vocabulary adapted from the Italian sign language; morpho-syntactic structure of the spoken Italian; all visual channels including videorecordings Short-term goals (7 years 4 months to 8 years 4 months)
Medium-term goals (8 years 4 months to 12 years 4 months)
Pragmatics
Visual contact; selection and introduction of the topic; taking turns; extension to different conversational partners
Maintaining and changing the topic; adjacency and contingency; cohesion; variation in communicative style; intelligibility and accuracy; facial expressions
Lexicon
Receptive: home and school lexical categories. Productive: mainly signs for nouns; acceptance of spontaneous gestures and expansion of categories already used on the strength of interests and motives Comprehension of coordinated phrases
Receptive: district, work, free time lexical categories. Productive: signs for verbs, adjectives and functors. Language decontextualization; gradual correction of all distinctive parameters; maintenance of a proper execution of the sign in progressively wider contexts and for increasingly long times Comprehension of subordinate phrases. Phrase production: from combining two signs to a complete simple nuclear phrase, first with one and then with two topics. Introduction of morphology with changes of gender and number; teaching of dactylology
Returning to exploring the girl’s own face; developing facial sensitivity; movement toward the mouth and eating unassisted
Biting, chewing and drinking in small sips; facial expressions; first significant vocalizations
Syntax
Oro-motor district
Gestural productions were recorded considering those between two pauses as a clause and noting not only the quantity per minute and their morphological and phonological changes, but also the non-manual components (e.g., facial mimicry). Non-manual elements such as gaze and facial mimicry were also recorded because they may contribute to the communicative efficacy of the gestural communication, amplifying or modifying the meaning of a given gesture/sign. Vocalizations with a prosodic value were all noted, but not counted. Double-meaning signs, e.g., signs that could have a meaning both as a verb and as a noun, were interpreted on the basis of the context. We calculated the MLU of the productions in SI as for spoken language and the mean number of gestural productions per utterance. As a reference for the MLU development stages, we used the model developed by Cipriani et al. [25] for Italian-speaking children. Inter-observer agreement in recording the sign samples was calculated on a 10-min sample drawn from the figure-describing scenario and considered as follows: the presence of the sign or of the gesture, the utterance boundaries and the length of the utterance produced as signs by the girl. One of the authors (Gloria Airaghi) was the first observer, and the girl’s signing school teacher was the second. The mean inter-observer agreement ranged from 85 to 90%. We examined the girl’s gestural linguistic abilities using our dynamic communication evaluation (DCE) grid [34], adapted to the clinical case considered. We analyzed the
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following language levels: syntactic (Table 3), lexical (Table 4), pragmatic (Table 5) and morphological. The gestures were classified according to the Italian version of MacArthur-Bates Communicative Development Inventories [29] into four semantic categories: nouns, actions/
Table 3 Adapted DCE grid: syntactic analysis Isolated gestures Syntax Pre-syntactic phase consisting mainly of single gestures in succession Syntactic phase consisting of incomplete and complete simple nuclear phrases Phrase expansion phase: incomplete and complete expanded and complex phrases Arrangement Conventional, unconventional, ambiguous, absent
Table 4 Adapted DCE grid: lexical analysis Nouns
Animals, vehicles, toys, food and drinks, clothing, body, furniture and rooms, familiar objects, outdoors
Predicates Verbs, adjectives Functors
Pronouns, wh questions, prepositions, conjunctions, articles, quantifiers
Other
Sounds and voices of nature, people, routines, time
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Table 5 Adapted DCE grid: pragmatic analysis Requests for attention, requests for action, requests for information, declarations on the object, declarations on the subject
Communicative role
Spontaneous, in response or in imitation
Communicative means
Gaze on the focus and on the other party, Please enter your comments here facial mimicry, deictic gestures, pointing, referential gestures, finger spelling
3
MLU
Communicative intentions
2
1
0 0
adjectives, functors and others (familial ‘‘routines’’, e.g., hello, great, thanks; people names). We coded the phrasal structure of the gestural utterances, drawing from the pattern of phrasal structure development identified by Cipriani et al. [25] in Italianspeaking children aged between 19 and 36–39 months. In our analysis, we recorded the frequency of use of each phrasal structure produced by the girl. We analyzed whether the sequence of the gestural productions in the utterance followed the sequence of the words in the sentence in the spoken Italian language, whether it could be well interpreted and whether it was absent because the sentence was composed of only one production. We also analyzed the sign modifications to see whether the girl was acquiring morphological rules enabling variations of meaning to be expressed. First, we recorded the different referential gestures produced by the girl on the five assessments. The gestures produced were classified according to the gesture production development model in speaking children and for communicative intentions according to recent models on the development of intentional communication [26, 35–38]. We calculated the percentages and 95% confidence intervals (CI) on the data recorded at the five assessments. We also performed the Cochraine Armitage test for trend, setting the level of significance at 5%. We assessed cognitive and scholastic abilities and neurological status again at T4. Cognitive development was assessed by means of the WISC-R scales. To administer the verbal scales, we used gestural communication as reinforcement for oral communication. Scholastic achievement was assessed by means of a word spelling test.
Results Syntactic structuring The MLU was 1.3 gestural productions at T0 and T1 and raised to 3.4 at T4 (Fig. 2). Data of the utterances are shown in Fig. 3. The proportions of isolated gestures/signs
1
2
3
4
Times
Fig. 2 Progress of the MLU
0%
10%
20%
30%
40%
0
68% (60-75)
1
68% (58-77)
34% (25-45)
2
3
4
60%
70%
80%
90%
29% (20-39)
3% (1-9)
27% (18-37)
4% (1-10)
76% (62-87)
21% (12-34)
100%
32% (25-40)
34% (25-45)
4% 14% (0-13) (6-26)
16% (8-28)
50%
51% (38-64)
6% (1-16)
11% (5-22)
Isolated gestures
Presyntactic phase
Syntactic phase
Extended and complexphrases
Fig. 3 Percentages and confidence intervals (95% CI) at the five assessments of syntactic levels: isolated gestures; presyntactic phase; syntactic phase; extended and complex phrases
and associations of gestures/signs, classified as belonging to the ‘‘pre-syntactic phase’’, significantly decreased over time (p \ 0.001). On the whole, this type of production represented 100% of the output at T0, but less than 40% at T4. In particular, the isolated gestures decreased from 68% at T0 and T1 to 4–16% at T3 and T4, while the pre-syntactic productions dropped from around 30% in the earlier assessments to around 15–20% at T3 and T4. There was a corresponding statistically significant increasing trend in the percentages of productions classified as belonging to the ‘‘syntactic phase’’, i.e., complete and incomplete nuclear sentences, and expanded and complex sentences, both complete and incomplete (p \ 0.001). The nuclear sentences (absent at T0) accounted for more than 50% of the productions at T3 and T4, while there was a more modest increase in the more complex structures, which reached 11% at T4. With the appearance of the phrasal structure, the sequence of the signs in the sentence
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100% 90%
10%
20%
30%
23% (8-45)
0
40%
50%
60%
70%
80%
14% (3-35)
36% (17-59)
90%
100%
27% (11-50)
80% 40% (26-56)
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61% (52-69)
70% 60% 50%
53% (44-62)
52% (41-63)
62% (53-70)
40%
33% (24-44)
2
16% (7-30)
13% (7-22)
44% (33-55)
37% (26-50)
3
13% (5-27)
31% (18-47)
10% (5-19)
49% (37-62)
4% 9% (1-13) (3-19)
37% (27-48)
15% (8-24)
30% 20% (13-29)
20%
44% (33-55)
4
5% (1-11)
10% Nouns
Predicates
Functors
Other
0% 0
1
2
3
4
Times
Fig. 5 Lexical categories: percentages and confidence intervals (95% CI) at the five assessments
Fig. 4 Different referential gestures/all gestures: percentages and confidence intervals (95% CI) at the five assessments
followed that of the Italian spoken language, instead of LIS (e.g., I’M NOT GOING HOME’’ instead of ‘‘I HOME GOING NOT’’).
100% 90% 80% 70% (58-81)
70%
Vocabulary
60% 50%
The girl showed a statistically significant rising trend (p \ 0.001) in the different referential gestures she produced (Fig. 4), starting from a percentage of 20% at T0 and settling at a percentage varying between 50 and 60% in the subsequent assessments. The analysis of the lexical categories (Fig. 5) showed a statistically significant declining trend (p \ 0.002) for the category ‘‘other’’. The remaining categories were represented in almost the same percentages over time, despite the increase in the production of different gestures. In the category ‘‘functors’’, the causal ‘‘why/because’’ and the indeterminate articles and possessive pronouns, which were missing at the earlier evaluations, were recorded at T4. At first, she started to produce WH-questions, pronouns and prepositions, respectively, by means of signs. Later, she started to use finger spelling to produce articles and to specify gender and number of possessive pronouns. Morphological sign modifications Morphological sign modifications (at first according to the grammar ISL rules expressed through specific alterations of the sign’s location and of some movement features, such as direction, duration, intensity or width: e.g., CHILD/ CHILDREN; I GIVE YOU/YOU GIVE ME; I GO/I WILL GO, and later in addition with finger spelling: e.g., LITTLE STREET/BIG STREET) were present in proportions below 4% on the first few assessments and occurred in sizeable percentages only at T4 (70%; 95% CI: 58–81) (Fig. 6).
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40% 30% 20% 0% (0-20)
10%
4% (1-11)
0% (0-9)
3% (0-11)
0% 0
1
2
3
4
Times
Fig. 6 Morphological modifications: percentages and confidence intervals (95% CI) at the five assessments
Communicative intentions (Fig. 7) The proportion of requests for attention significantly decreased while the proportion of declarations on the object (i.e., gestures/signs describing objects or facts: the ball is red; the weather is rainy) significantly increased from T0 to T4 (p \ 0.001). Declarations on the subject (i.e., gestures/signs describing her own action or wish—I ate everything; I want to play) and requests for information were absent throughout the period of observation. Communicative role The spontaneous productions significantly increased from T0 to T4 (p \ 0.001) (Fig. 8), reaching nearly 100% already at T2, while the productions in response and in imitation tended to disappear.
Neurol Sci (2010) 31:471–481 0%
10%
20%
30%
40%
477 50%
60%
63% (53-73)
0
70%
80%
19% (12-28)
100%
100% 90%
14% 8-23
74% (62-83)
1
90%
80% 70%
21% (12-32)
60% 50%
49% (38-60)
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51% (40-62)
38% 32-45
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31% 25-38
30% 6%
94% (84-99)
3 (1-16)
12% 7-18
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8% 4-12
10% 22% (12-34)
4
Req. attn
0%
75% (62-85)
Decl. obj.
Req. action
Decl. subj.
0
1
2
3
4
Times
Req. info
Fig. 7 Percentages and confidence intervals (95% CI) at the five assessments of communicative intentions: Req. attn requests for attention, Decl. obj. declarations on the object, Req. action requests for actions, Decl. subj. declarations on the subject, Req. info requests for information
Fig. 9 Pointing gestures: percentages and confidence intervals (95% CI) at the five assessments
100% 90% 80%
100% 95% 88-98
90%
100% 94-100
98% 91-100
80%
60%
51% 44-58
40%
65% 57-72
50%
67% 61-74
68% 61-74
67% 59-75
60% 50%
77% 67-84
70%
85% 78-90
70%
30% 20%
40%
10%
30%
0%
20% 10%
0
1
2
Times
3
4
0% 0
1
2
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4
Times
Fig. 10 Referential gestures: percentages and confidence intervals (95% CI) at the five assessments
Fig. 8 Spontaneous productions: percentages and confidence intervals (95% CI) at the five assessments
Cognitive and scholastic abilities and neurological status at T4 Means of communication Pointing significantly decreased (Fig. 9), while the use of referential gestures/signs (Fig. 10) significantly increased (p \ 0.001) from T0 to T4. Finger spelling also significantly increased over time (Fig. 11), ranging between 0 and 4% of the means of communication up to T3 and becoming 23% at T4 (95% CI: 18–30). Visual contact and gaze on the focus were normal since T0 as the girl did not avoid eye contact. Deictic gestures were recorded in very small proportions at T0 and further declined, disappearing by T2. At T4 we recorded an adequate use of facial mimicry, accompanied by vocalizations with a prosodic value.
The data are shown in Table 6. In particular, the results of the WISC-R scales were within the range of mild retardation according to the DSM IV. At T4, the girl was able to close her mouth for a few seconds without using her hands, bring her lips together, smile and, with considerable effort, close her eyes. She could slightly raise her eyebrows and managed to blow weakly; phonation was possible for a few seconds. The motility of her tongue was still severely impaired, but she could move the tip of her tongue to the left. Drooling was better controlled. The tactile sensitivity of her face remained deficient on the left, but improved in the region around the mouth.
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100% 90% 80%
Test for trend: p<0.001
70% 60% 50% 40% 30%
23% 18-30
20% 0% 0-1
10%
3% 1-7
1% 0-3
0% 0-4
0% 0
1
2
3
4
Times
Fig. 11 Finger spelling: percentages and confidence intervals (95% CI) at the five assessments
Discussion In the present study, we found that 4 years after the beginning of treatment, the phrasal structures produced by the girl could be placed at the end of phase III of nuclear sentence according to the classification by Cipriani et al. [25], with an MLU of 3.4. As reported in typically developing children [39], the increase in MLU in this child seemed to be related to the acquisition of morphological language competences. Although the category ‘‘functors’’ did not increase significantly over time, a qualitative improvement of language morphology was observed (e.g., ON THE/IN THE were produced by means of sign and finger spelling at the earlier assessments and exclusively by means of finger spelling later). At variance with the studies by Udwin and Yule [16] and by Grove and Dockrell [17], we found that the length of the utterance in the child seemed related not only to a higher use of open-class lexical categories (e.g., nouns, adjectives and verbs), but also to the appearance of functors enabling more complex semantic relations to be constructed, as at T4 fewer itemchaining pre-syntactic productions and complete, expanded nuclear sentences and complex sentences were recorded. Morphological sign modifications, many of which were correct, increased from T0 to T4, particularly concerning consistencies of number and gender, bearing witness to the emergence of a morpho-syntactic competence and a consequent switch to a grammatical phase. As reported in some linguistic studies of the sign, changes in meaning may be indicated using the visuospatial parameters of sign (i.e., hand shape, movement, location and direction) that are the equivalent to phonemes in the spoken language [26]. The patient was taught morphology with the aid of signed Italian and Italian sign language, adapting the signs and the changes in the signs to suit her motor impairment.
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This is in contrast to the studies by Udwin and Yule [16] and Grove and Dockrell [17], according to whom the sign input the children had received from the teachers seemed to be too limited in terms of quantity, lexical variety and morpho-syntactic content. As reported in the experimental study by Rudd et al. [19], our data confirm that children with mental impairment exposed to treatment using signs may learn productive morphological rules. Like typically developing infants, mentally retarded children with severe expressive language impairment seem to be able to learn morpho-syntax better from the more complex, contrastive context than from simple linguistic inputs [39], suggesting that rehabilitation projects should provide sufficiently varied morpho-syntactic models. As shown in Table 6, in parallel with the development of the gestural communication, there was evidence of an improvement in the girl’s writing abilities, as at follow-up she was able to write a simple and correct narrative text with sentences showing a syntactic structure similar to that of her gestural productions. Her learning of written language seemed to follow a parallel course with her learning of the signed linguistic input each benefiting from and facilitating the other’s development. With regard to pragmatic capabilities, we chose to analyze the girl’s progress in terms of communicative intentions in particular declarations and spontaneous productions, since previous studies [20, 40] reported them as being produced less often with respect to answers and requests for attention. Our aim was to be able to draw some conclusions on the communicative efficacy of the sign system used and on the input provided by the therapist, family and school. The growth in the spontaneous productions and the disappearance of the imitative productions demonstrated the adoption of an increasingly active role in the communicational exchange. The analysis of the communicative intentions also showed a consistent increase in the more well-developed and active intentions, such as declarations on the object, accompanied by a parallel consistent
Table 6 Cognitive, linguistic and scholastic assessment at T4 Test
Results
WISC-R
TIQ 54; VIQ 55; PIQ 58
Language comprehension assessment tests: protocol 6–7 [30]
Average score for children aged 6–7 years
QV \ 65 (QV 101 for age range 45–50 months) Writing tests III, elementary Simple narrative test; complete simple narration [32] and amplified nuclear and incomplete binuclear phrases were produced; rare spelling mistakes PPVT [31]
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reduction in the requests for attention. The means of communication became more evolved and decontextualized over time: at the last assessment, the girl mainly used referential gestures accompanied by finger spelling, while the primitive deictic gestures had disappeared. Our findings are in contrast with those by Udwin and Yule [20, 40] reporting a persistently limited use of augmentative communication systems in the children they analyzed, who tended to maintain a passive role in the communication. This may be related, however, to the type of rehabilitation the children received and to an insufficient exposure in the different environments where the children lived, i.e., at school and in the family. From the beginning, the aim of our rehabilitative program was to provide expertise in the use of signs to the principal parties for exchanging communication with the girl. We were able to count on the active involvement of her mother and her support teacher at school. Unlike the situation emerging from the study by Udwin and Yule [40], the adults believed in the emancipatory abilities that the girl could gain from using gestures/ signs, even though they tended to continue to interpret and anticipate her intentions and communicative output, as observed in parents of children with severe disabilities. Linguistic retest (Table 6) at T4 showed that the impairment mainly involved lexical rather than morphosyntactic abilities. These findings are consistent with our data in a previous study on children with BPP [24]. Bishop et al. [41] reported a similar pattern in children with cerebral palsy and severe expressive language impairments. According to the Liberman’s theory [42], the authors suggested that the lack of an articulatory feedback may interfere more with the children’s capacity of word discrimination and phonological memory, and thus with their word acquisition, rather than with the comprehension of semantic nexae. Although the neurological picture at follow-up was substantially unchanged, the functional assessment of the phono-articulatory muscles showed a motor and sensory improvement in the oral district. In our previous study on six children with BPP, we attributed the scarce progress in gestural linguistic capabilities to the fact that bilateral involvement of the perisylvian regions, having an anatomical substrate in common with the motor representation of mouth and hand movements, prevented any compensation for the general linguistic deficiency. Our present data seem to contradict our earlier assumption, although the six children previously studied underwent different and nonhomogeneous rehabilitative programs. Up until the 1980s, the relationship between neural structure and function was seen as being one-way: the development of the nervous system and the progressive acquisition of abilities were assumed to be determined strictly by the maturation of neural structures. Starting
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from the 1980s, however, many experimental studies demonstrated the role of environmental afferences in influencing the functional development and structural organization of the nervous system. In this light, the relationship between structure and function becomes two way, in that functional changes may induce structural modifications. The plasticity of the nervous system in the post-natal period is mainly due to modifications of the synaptic connections in response to afferences and this provides the basis for the learning process throughout life [43]. There are reports in literature [44, 45] on adult patients with focal lesions secondary to stroke, whose neuronal aggregates adjacent to lesions involving sensorimotor areas progressively acquired the function previously handled by the damaged neurons in response to training. These studies showed that the hemisphere affected by the stroke underwent a remodeling of the hand’s sensorimotor somatotopic representation beyond the normal areas, extending into adjacent areas of the hand’s representation. fMRI studies in children with perinatal brain lesions [46, 47] support the ‘‘interactive specialization’’ theory, which suggests that cognitive functions are mediated, in typical development, by a constellation of interconnected regions that acquire their specialized functional role in relation to function-related connections: this theory maintains that the typical developmental mechanisms interact with early-onset disease, giving rise to an atypical neurofunctional anatomy. If the balance of the regional competition is disrupted, as in the case of perinatal stroke or structural cortex anomalies, an alternative functional organization is possible. In a recent study performed on a group of children between 5.6 and 17.7 years of age surgically treated for left hemisphere refractory epilepsy [48], intrahemispheric reorganization was documented after surgery, with the displacement of the functional area assigned to producing oral movements toward more anterior frontal regions. Despite a bilateral impairment (which was prevalent in the frontal regions, but also extended posteriorly) and despite intensive rehabilitation treatment being started only when she was more than 7 years old, our patient developed her linguistic gestural abilities at morpho-syntactic level more than in other case reports in literature or in the six cases we had previously studied, and even had some, albeit marginal, improvement in her sensorimotor abilities in the orofacial region. In conclusion, our findings confirm the strict link between gesture and language, as established by the recent studies on the mirror system. It may also be interpreted as the outcome of a reorganization of the compensatory synaptic circuits stimulated by a sufficiently ample and intensive rehabilitative input.
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Acknowledgments We thank Dr. Tiziana Casalino for her help with data transcription and coding and Marina Denegri for editing. 21.
References
22.
1. Volterra V, Bates E, Benigni L, Bretherton I, Camaioni L (1979) First words in language and action: a qualitative look. In: Bates E, Benigni L, Bretherton I, Camaioni L, Volterra V (eds) The emergence of symbols: cognition and communication in infancy. Academic Press, New York, pp 141–222 2. Petitto LA, Marentette PF (1991) Babbling in the manual mode: evidence for the ontogeny of language. Science 251:1493–1496 3. Volterra V, Erting C (1994) From gesture to language in hearing and deaf children. Gallaudet University Press, Washington, DC 4. Capirci O, Iverson J, Pizzuto E, Volterra V (1996) Gestures and words during the transition to two-word speech. J Child Lang 23:645–673 5. Iverson JM, Goldin-Meadow S (1998) The nature and function of gesture in children’s communication. Jossey-Bass, San Francisco 6. Masataka N (2001) Why early linguistic milestones are delayed in children with Williams syndrome: late onset of hand banging as a possible rate-limiting constraint on the emergence of canonical babbling. Dev Sci 4:158–164 7. Stefanini S, Bello A, Caselli MC, Iverson JM, Volterra V (2009) Co-speech gestures in a naming task: developmental data. Lang Cogn process 24:168–189 8. Bates E, Dick F (2002) Language, gesture, and the developing brain. Dev Psychobiol 40:293–310 9. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609 10. Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21:188–194 11. Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661–670 12. Buccino C, Vogt S, Ritzl A, Zilles K, Freund HJ, Rizzolatti G (2004) Neural circuits underlying imitation learning of hand actions: an event-related study. Neuron 42:323–334 13. Iacoboni M, Wilson SM (2006) Beyond a single area: motor control and language within a neural architecture encompassing Broca’s area. Cortex 42:503–506 14. Iverson JM, Longobardi E, Caselli MC (2003) Relationship between gestures and words in children with Down’s syndrome and typically developing children in the early stages of communicative development. Int J Lang Commun Disord 38:179–197 15. Bello A, Capirci O, Volterra V (2004) Lexical production in children with Williams syndrome: spontaneous use of gesture in a naming task. Neuropsychologia 42:201–213 16. Udwin O, Yule W (1990) Augmentative communication systems taught to cerebral-palsied children—a longitudinal study I. The acquisition of signs and symbols, and syntactic aspects of their use over time. Br J Disord Commun 25:295–309 17. Grove N, Dockrell J (2000) Multisign combinations by children with intellectual impairments: an analysis of language skills. J Speech Hear Res 43:309–323 18. Veneziano E, Sinclair H, Berthoud I (1990) From one word to two words: repetition patterns on the way to structured speech. J Child Lang 17:633–650 19. Rudd H, Grove N, Pring T (2007) Teaching productive sign modifications to children with intellectual disabilities. Augment Altern Commun 23:154–163 20. Udwin O, Yule W (1991) Augmentative communication systems taught to cerebral-palsied children—a longitudinal study II.
23.
123
24.
25.
26.
27. 28. 29.
30. 31.
32.
33. 34.
35.
36. 37.
38. 39.
Pragmatic features of sign and symbol use. Br J Disord Commun 26:137–148 Kuzniecky R, Andermann F, Guerrini R (1994) The epileptic spectrum in the congenital bilateral perisylvian syndrome. CBPS multicenter collaborative study. Neurology 44:379–385 Jansen A, Anderman E (2005) Genetics of the polymicrogyria syndromes. J Med Genet 42:369–378 Sans A, Fernandez-Alvarez E (1996) Neuropsychological findings in congenital bilateral perisylvian syndrome versus early acquired opercular syndrome. In: Guerrini R, Andermann F, Canapicchi R, Roger J, Zifkin BG, Pfanner P (eds) Dysplasias of cerebral cortex and epilepsy. Lippincott-Raven, Philadelphia, pp 279–283 Saletti V, Bulgheroni S, D’Incerti L, Franceschetti S, Molteni B, Airaghi G, Pantaleoni C, D’Arrigo S, Riva D (2007) Verbal and gestural communication in children with bilateral perisylvian polymicrogyria. J Child Neurol 22:1090–1098 Cipriani P, Chilosi AM, Bottari P, Pfanner L (1993) L’acquisizione della morfosintassi in italiano: fasi e processi. Unipress, Padova Caselli MC, Maragna S, Volterra V (2006) Linguaggio e sordita`. Gesti, segni e parole nello sviluppo e nell’educazione. Il Mulino, Bologna Massoni P, Maragna S (1997) Manuale di logopedia per bambini sordi. Franco Angeli, Milano Wechsler D (1986) WISC-R Scala di Intelligenza Wechsler per bambini Riveduta. Organizzazioni Speciali, Firenze Caselli MC, Casadio P (1995) Il primo vocabolario del bambino. Guida all’uso del questionario MacArthur per la valutazione della comunicazione e del linguaggio nei primi anni di vita. Franco Angeli, Milano (Italian version of the MacArthur-Bates comunicative development inventories) Rustioni Metz Lancaster D (1994) Prove di valutazione della comprensione linguistica. Organizzazioni Speciali, Firenze Dunn LM, Dunn LM (1981) Peabody picture vocabulary testrevised. American Guidance Service, Circle Pines, MN. [Italian adaptation and standardization: Stella G, Pizzoli C, Tressoldi PE (2000) Peabody: Test di vocabolario recettivo. Omega edizioni, Torino] Tressoldi PE, Cornoldi C (1991) Batteria per la valutazione della scrittura e della competenza ortografica nella scuola dell’obbligo Organizzazioni Speciali, Firenze Bortolini U (1995) PFLI Prove per la valutazione fonologica del linguaggio infantile. Edit Master, Venezia Molteni B, Airaghi G, Mantegazza G, Sarti D (2006) Developmental language delay in early childhood: differential diagnosis between specific language delay and language delay secondary to other communication disorders. In: Riva D, Rapin I, Zardini G (eds) Language: normal and pathological development. Editions John Libbey Eurotext, Montrouge, pp 217–227 Caselli MC (1994) Communicative gestures and first words. In: Volterra V, Erting CJ (eds) From gesture to language in hearing and deaf children, 2nd edn. Gallaudet University Press, Washington, DC, pp 56–67 Goldin-Meadow S (2003) Hearing gesture: how our hands help us think. Harvard University Press, Cambridge Goldin-Meadow S, Butcher C (2003) Pointing toward two-word speech in young children. In: Kita S (ed) Pointing; where language, culture and cognition meet. Lawrence Erlbaum Associates, Mahwah, pp 85–107 Tommasello M, Carpenter M, Liszkowski U (2007) A new look at infant pointing. Child Dev 78:705–722 Pizzuto E, Caselli MC (1992) The acquisition of Italian morphology: implication for models of language development. J Child Lang 19:491–557
Neurol Sci (2010) 31:471–481 40. Udwin O, Yule W (1991) Augmentative communication systems taught to cerebral-palsied children–a longitudinal study. III. Teaching practices and exposure to sign and symbol use in schools and homes. Br J Disord Commun 26:149–162 41. Bishop DVM, Brown BB, Robson J (1990) The relationship between phoneme discrimination, speech production, and language comprehension in cerebral-palsied individuals. J Speech Hear Res 33:210–219 42. Liberman AM, Mattingly IG (1985) The motor theory of speech perception revised. Cognition 21:1–36 43. Bates E (1999) Language and infant brain. J Commun Dis 32:195–205 44. Rossini PM, Dal Forno G (2004) Integrated technology for evaluation of brain function and neural plasticity. Phys Med Rehabil Clin N Am 15:263–306 45. Rossini PM, Altamura C, Ferreri F, Melgari JM, Tecchio F, Tombini M, Pasqualetti P, Vernieri F (2007) Neuroimaging
481 experimental studies on brain plasticity in recovery from stroke. Eura Medicophys 43:241–254 46. Lie´geois F, Connelly J, Cross JH, Boyd SG, Gadian DG, VarghaKhadem F, Baldeweg T (2004) Language reorganization in children with early-onset lesions of the left hemisphere: an fMRI study. Brain 127:1229–1236 47. Fair DA, Brown TT, Petersen SE, Schlaggar BL (2006) fMRI reveals novel functional neuroanatomy in a child with perinatal stroke. Neurology 67:2246–2249 48. Kadis DS, Iida K, Kerr EN, Logan WJ, McAndrews MP, Ochi A, Otsubo H, Rutka JT, Snead OC 3rd, Weiss SK, Smith ML (2007) Intrahemispheric reorganization of language in children with medically intractable epilepsy of the left hemisphere. J Int Neuropsychol Soc 13:505–516
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