Toddling into language: precocious language development in motor-impaired children with spinal muscular atrophy

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1 Lingua 112 (2002) Toddling into language: precocious language development in motor-impaired children with spinal muscular atrophy Jechil S. Sieratzki a,1, Bencie Woll b, * a Human Communication Sciences, University College London, Chandler House, Wakefield Street, London WC1N 1PG, UK b Language and Communication Science, City University, Northampton Square, London EC1V 0HB, UK Received 9 March 2001; received in revised form 4 June 2001; accepted 6 June 2001 Abstract One of the most compelling topics of neurolinguistic debate is whether language has its own domain or is mediated by the same network that processes other cognitive, perceptual, and sensorimotor functions. To examine the relation between motor and language development we have collected data on motor-impaired children with Spinal Muscular Atrophy (SMA) aged months. Analysis shows normal progress in vocabulary but marked precocity in overregularisation, a sign of early grammar development. Our finding supports the view of a separate learning system for grammar but cannot be explained by the classical account of a grammar module. It rather appears as if children with SMA explore language in place of a world they cannot reach, building grammatical knowledge while able-bodied toddlers are engaged with the physical environment. We propose that procedural learning which serves the acquisition of sensorimotor skills also has a role in language development. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Spinal muscular atrophy; Motor-impairment; Language acquisition; Language evolution; Over-regularisations; Procedural learning; MacArthur CDI We thank the children and their parents, and the Jennifer Trust for Spinal Muscular Atrophy for taking part in this study. We are indebted to Professor Victor Dubowitz of the Royal Post-Graduate Medical School and Hammersmith Hospital, London, for bringing the language development of children with SMA to our attention; to Professor Janet Atkinson of University College London for allowing us to use a pre-publication British version of the CDI; to Professor James Law of City University London; Professor Annette Karmiloff-Smith of the Institute of Child Health, University of London, and Dr. Brian MacWhinney, Carnegie-Mellon University, Pittsburgh for discussion and guidance. * Corresponding author. b.woll@city.ac.uk (B. Woll), sieratzki@vff.uni-frankfurt.de (J.S. Sieratzki). 1 Previously at the Department of Paediatrics, Hammersmith Hospital, London, UK /02/$ - see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S (01)

2 424 J.S. Sieratzki, B. Woll / Lingua 112 (2002) Introduction During the second year of life, usually following a toddler s first independent steps, language abilities expand dramatically: vocabulary increases rapidly to several hundred words and the first markers of grammatical structure become apparent. Like motor milestones, language achievements are attained in a predictable sequence but it is unclear whether there is any relation between these two principal components of early development. Piagetian theory regards motor actions as necessary precursors for the child s development of internal cognitive representation (Bebko et al., 1992). Development occurs in a fixed sequence of qualitatively different stages, with language constructed upon abstractions from sensorimotor schemata (Piattelli-Palmarini, 1994). More recent thinking within the Piagetian school, however, has ascribed a lesser role to external actions and a greater role to internal processing and innate capabilities. In contrast to Piagetian approaches, Chomskyan theory postulates that language is not directly connected to other aspects of development. In the historical debate between Piaget and Chomsky, which highlighted their opposing opinions on language acquisition, the question was raised as to whether one could expect a child born paraplegic...(to) have very great difficulties in developing language (Piattelli-Palmarini, 1980: 140). In the ensuing discussion, Chomsky made the prediction, it would turn out that there is no relation whatsoever, or at least the most marginal relation, between even extreme defects that would make it virtually impossible to develop and do all the things that Piaget was discussing, and [the child s] acquisition of language (p. 171). Spinal Muscular Atrophy (SMA), an autosomal recessive disease which affects about 1 in 30,000 births, provides a test case for the above question. SMA is characterised by an involution ( apoptosis ) of spinal motor-neurones, which does not involve cortical areas of the brain (Roy et al., 1995). Clinically, it manifests as a nonprogressive motor weakness of variable severity. Children with the most severe form (SMA-I) show practically generalised paralysis of the limbs and trunk, and severe respiratory weakness; they rarely survive beyond the first year of life. Children with intermediate SMA (SMA-II), our subject group, usually progress quite normally in the first 6 months, are able to sit unaided, but never achieve the ability to stand and walk. Those with the mild form (SMA-III) walk independently, though they may lose ambulation at a later age (Dubowitz, 1995). Children with SMA are typically exceptionally alert, with bright facial expression and confident communication skills, a sharp contrast to boys with Duchenne muscular dystrophy (DMD). Comparative psychometric studies have demonstrated that the motor impairment which occurs in both conditions could not explain the abnormally slow language development in DMD (Whelan, 1987; Billard et al., 1992). It appears rather that this deficit is connected to a synaptic defect at particular cerebral neurons (Lidov et al., 1990). Dubowitz (1995) has claimed that children with SMA show unusually early onset of language and make long sentences by the age of 2 years. Though systematic testing of SMA-patients at age 6 16 years has shown only average verbal abilities

3 J.S. Sieratzki, B. Woll / Lingua 112 (2002) (Whelan, 1987; Billard et al., 1992), this observation raises the compelling question of whether motor impairment could advance language development. 2. Subjects, methods, and results With the assistance of the Jennifer Trust for Spinal Muscular Atrophy, a United Kingdom family support association, we have collected data on 10 children with SMA-II aged months; in four children repeat data were obtained within intervals of 3 7 months. All children were able to sit without support and to use their hands to feed themselves and hold a toy or pen but none was able to crawl or walk independently. Speaking and swallowing were not affected. Language development was assessed with the MacArthur Communicative Development Inventory (CDI), a contemporary parental report using a recognition format (Fenson et al., 1991, 1994), which was modified in the vocabulary subtest with regard to differences between American and British vocabulary. The test offers norms for children aged months (child 1 6) and has in large studies proved reliable for defining typicality and exceptionality of language development. Percentiles for children over 30 months (child 7 10) were graphically extrapolated but not included in the statistical analysis. The MacArthur CDI has a proven record for the comparison of vocabulary and over-regularisations (OR) (Marchman and Bates, 1994), which is central to our study. OR are errors in word form and significant milestones of early grammar development. During the first stage of language acquisition, a child learns all forms of a word as separate units, but then begins a transition to systematic treatment of words. From about age 2 years incorrect forms of irregular past tenses and plurals appear such as ated and eated, foots and footses side by side with the correct irregular forms ate and feet. These errors are not present in normal parental input. They indicate that the child independently applies regular patterns to irregular items, i.e. the child has knowledge of inflectional rules for past tenses and plurals. Results are summarised in Table 1; Figs. 1 and 2 show the graphic distribution of the scores for normal children between the 10th and 90th percentile for vocabulary and OR, with those for our subjects plotted onto the graph. Vocabulary scores of SMA-children are close to those of average children, with the mean at the 52nd percentile. They are slightly lower in the four youngest subjects, due to relatively low results on words for actions, outside things, and places to go. Scores for OR are far above the average range, with the mean at the 78th percentile. Three children are above the 90th percentile, with scores up to 10 times the norm. A paired-samples t-test of vocabulary production and OR of children 1 6 (first tests) returns a probability of , very close to a statistically significant difference. Scores in the 2 subtests of irregular nouns and verbs and of sentence complexity average at the 65th percentile, approximately half way between vocabulary and OR. The subtest for sentence length returns an average at the 55th percentile.

4 426 J.S. Sieratzki, B. Woll / Lingua 112 (2002) Table 1 Performance of children with SMA in different sub-tests of the CDI Child Age (months) Vocabulary production Irregular nouns/verbs Sentence length Sentence complexity Overregularisation Score %ile Score %ile Score %ile Score %ile Score %ile 1 (F) nd *(F) (M) nd *(M) >90 3 (F) *(F) (F) >90 4*(F) e 24 80e 13 75e ns (F) >90 6 (M) (F) e 25 90e 6 <25e ns 27 >90e 8 (M) e 12 25e 15 90e ns 7 50e 9 (M) e 17 40e 6 <25e ns 27 90e 10(M) e 18 45e 10 50e ns 2 ++ Percentiles are from the original CDI. Values above 30 months have been graphically extrapolated. (*) repeat data sets. (nd) no data provided by parent. (ns) not scored over 30 months. (e) extrapolated percentile. (++) the high-score-low-score sequence in child 4 suggests very rapid early development of over-regularisations. The low score of child 10 at 35 months might thus be interpreted as either very rapid or very slow development as earlier measurements are not available. Fig. 1. Vocabulary production.

5 J.S. Sieratzki, B. Woll / Lingua 112 (2002) Fig. 2. Over-regularisations. 3. Discussion Though our sample is small, our findings raise fundamental questions regarding language development. The fact that children with SMA learn language so well is incompatible with the most naive version of Piaget s position; the fact that their language acquisition has unique aspects does not accord with Chomsky s strict separation of language from other aspects of development. The most striking linguistic finding in children with SMA is a marked precocity in OR relative to vocabulary production, which contrasts with the synchronous development seen in normal children (Marchman and Bates, 1994). However, our subjects seem to follow the normal developmental model: OR usually appear around age 2, peak at age 3 4, and disappear around age 5 years (Marcus et al., 1992). This inverted U-shaped pattern can be recognised in child 4 who was assessed twice (Fig. 3): at 27 months, she had an OR score of 15 items (to match the percentile of her vocabulary score of 433 items she would have needed only 1 OR). At 34 months, however, only four OR were recorded. This turn-around confirms that her high score for OR at age 27 months does not result from parental over-reporting, and suggests a normal developmental curve for OR which is shifted leftwards. It is possible that children with SMA receive a richer parental verbal input than their peers but such support could be expected to manifest across the board in all aspects of language development. Indeed, an isolated precocity in OR is difficult to explain under prevailing neuro-linguistic theories. The Chomskyan model implies a dual learning system for language. A modular device for grammar extracts morphological patterns from the language environment and transforms them into productive grammatical rules, independently of vocabulary

6 428 J.S. Sieratzki, B. Woll / Lingua 112 (2002) Fig. 3. Child 4, vocabulary (above) and over-regularisations (below) at 27 and 34 months. learning. Observations in children with Specific Language Impairment, who cannot master grammatical form correctly despite adequate vocabulary, have been used as evidence pro (Leonard, 1998) and contra (Bishop, 2000) an independent system for grammar. In a dual learning system, OR would either result from inefficient retrieval of irregular forms (explaining the occurrence of OR in young children: Marcus et al., 1992) or from abnormal operation of the grammar module. It has been suggested that impaired lexical retrieval may be responsible for an increased occurrence of OR in patients with posterior aphasia and Alzheimer s disease (Ullman et al., 1997). The same study also found abnormal OR occurrence in patients with extrapyramidal motor disorders (increased in Huntington s disease reduced in Parkinson s disease), leading to the suggestion of a role of the basal ganglia in the processing of grammatical rules. Clearly, neither mechanism applies to our subjects, who have good vocabulary and produce irregular and over-regularised forms of the same word item concurrently,

7 J.S. Sieratzki, B. Woll / Lingua 112 (2002) with a normal mixture of rote memory and rule production (Table 2). The classical Chomskyan account of a grammar module therefore does not offer a direct explanation for the precocious OR in our subjects. Connectionist theory, like the Piagetian school, puts language acquisition in the context of general cognitive development. It rejects Chomsky s language organ and proposes that language can be acquired by an associative network of neural systems which serve various cognitive and perceptual functions (Plunkett and Marchman, 1993; Bishop, 2000). The learning process is purely vocabulary-based; morphological rules gradually emerge from computation of phonological variation, in direct relation to overall language experience. Connectionists point to computer simulations of language development which produce normal OR-curves; and they use the observation in normal children of a close temporal connection between a critical mass of vocabulary and the onset of OR as important empirical support (Marchman and Bates, 1994). The dissociation between OR and vocabulary in our subjects may therefore be inconsistent with the basis of the connectionist model. It could be suggested that grammar learning by children with SMA may be enhanced by reassignment to grammatical processing of pre-frontal areas ordinarily claimed by the motor system. Cortical re-mapping does occur in response to sensory de-afferentation, and has been observed across somatic regions (Buonomano and Merzenich, 1997) and perceptual modalities (Sadato et al., 1996). It is not known whether such re-organisation can also occur in motor cortices and whether the apoptosis of spinal motor neurones in SMA may stimulate such a process. In fact, children with SMA have adequate fine motor control and are able to plan movements in space but they do not have sufficient power to execute them. Table 2 Examples of co-occurrence of irregulars and over-regularisations 1 1* 2 2* 3 3* 4 4* Feet p p p p p p p p p p p Feets/foots p p p p p p p p Men Mans/mens p p p p p p p p p p Teeth p Teeths/tooths p p p p p Ate p Ated/eated p p p p p p Blew Blewed/blowed p p p p p p p p p Broke Braked/broked p p p p p p p Drank Dranked/drinked p p p p p p Went p Goed/wented * Repeat data set; p correct irregular; over-regularisation.

8 430 J.S. Sieratzki, B. Woll / Lingua 112 (2002) While the concept of cortical re-mapping is theoretically challenging, a developmental explanation may fit better with our findings. It appears as if children with SMA explore language in place of a world they cannot reach, advancing in grammar while able-bodied toddlers are engaged with the physical environment. This early advance in language is no longer manifested in older children with SMA, as normal peers soon catch up (Whelan, 1987; Billard et al., 1992). Children with SMA appear, however, to maintain and refine their exquisite communication skills and their ability to manipulate the social environment. Further, more detailed studies of children with SMA and comparable disorders are required for a full description of language development under conditions of restricted mobility. 4. Toddling into language Progress in language usually remains slow until the child has learned walking. Alhough usually, vocabulary spurt and beginnings of grammar follow closely on the heels of the baby, quite literally (Pinker, 1994: 290), it would not be surprising that children who are unable to walk turn their attention to other learning tasks, especially language. This shift would, however, not predict an advance in OR relative to vocabulary unless it involved a learning mode which is somehow also related to the mechanisms serving motor development. The acquisition of knowledge involves two fundamentally different systems: declarative memory, which derives from conscious experiences (and serves the mental lexicon); and implicit or procedural memory, which derives from non-intentional abstraction of general patterns from encounters with the particular (Schacter, 1995). A toddler s acquisition of sensorimotor skills is typical of procedural learning. It involves a system which comprises the frontal and pre-frontal cortex, the basal ganglia, and the cerebellum. There is strong evidence that this system is not limited to motor functions, as was classically thought, but also contributes to non-motor operations, including language. For example, learning to read mirror-reversed text, a skill which requires repetition priming and procedural memory, produces activation of left basal ganglia and right cerebellar regions 2 in healthy adults (Poldrack and Gabrieli, 2001); and is impaired in patients with basal ganglial (Parkinson s disease) or spinocerebellar disorders, while declarative memory tasks such as word learning and recognition remain normal (Yamadori et al., 1996). In line with this evidence, Ullman et al. (1997), in their report mentioned previously, have suggested that grammatical rules are processed by the frontal-basal ganglia-procedural system. We expand on this concept by proposing that procedural learning serves the development of grammar. More recently, Ullman (2001) has also implicated the procedural system in the acquisition of grammatical rules. 3 However, he relates this to frontal/basal ganglia circuits only, ignoring the crucial role of the cerebellum in procedural learning. 2 The laterality of the cerebellum is the opposite of the laterality of the cortex and the basal ganglia. 3 A suggestion we made in the original presentation of this study (Sieratzki and Woll, 1998).

9 J.S. Sieratzki, B. Woll / Lingua 112 (2002) There is strong evidence that the cerebellum not only transforms sensory information as a means of guiding motor activity (Ito, 2000) but is also important for non-motor exploratory learning behaviour (Pierce and Courchesne, 2001) and development of speech and language functions (Riva and Giorgi, 2000; for broader reviews see Gordon, 1996; Thach, 1998). From a computational viewpoint, the cerebellum, basal ganglia, and cerebral cortex appear to have complementary roles, each area specialised for different types of learning: supervised learning, reinforcement learning, and unsupervised learning, respectively (Doya, 2000). Cerebellar projections to the prefrontal cortex provide the anatomical substrate for an involvement in rule-based learning in the cognitive domain (Middleton and Strick, 2001). We believe that in a child who is unable to walk, the enormous unused learning capacity of the cerebellum may be a factor in the advance of grammar relative to vocabulary. The developmental primacy of procedural learning might explain the strikingly early and efficient mastery of complicated grammatical rules by young children, well in advance of other intellectual achievements. An abundance of non-committed synapses in the pre-frontal cortex (Goldman-Rakic, 1987) provides a time-limited opportunity for a system of enormous learning capacity to be formatted by grammatical parameters. Children have a unique ability to learn any grammar without formal education and even to generate a new grammar out of incomplete linguistic structures. It has been suggested that this task requires preformed concepts of admissible linguistic form (Nowak, 2001). We would, however, postulate that the learning task may be sufficiently guided by an intrinsic preference of the procedural system for uniformity, i.e. for regular, repetitive primers. What may be required is an innate sensitivity for linguistic parameters. Human evolution and the genesis of language are connected to neo-cortical, in particular pre-frontal, enlargement (Leonard, 1997) which, interestingly, appears to have been paralleled by an expansion of the neo-cerebellum (Leiner et al., 1993). However, quantitative changes in total brain size and in relative proportions of brain regions (Deacon, 2000) may not be sufficient to account for the dynamic of language. What appears to be of crucial importance in both ontogenetic and phylogenetic development of language, is the degree and duration of cerebral plasticity. 4 The prolonged maturation period of the human brain (Armstrong, 1990) provides a window of opportunity for the youngest members of a community to explore the existing communication stock and for the speech and language cortices to be remodelled. In a sufficiently large cohort of language-ready hominids a process of co-operative interaction could transform a static system of calls and affective signals into a new, dynamic system with grammatical and semantic organisation (Kegl, 1998). Language took off when communication became the object of procedural learning. Once this first leap was taken language advanced with each generation, source of its own perpetual progress, tool and target in one, and the bridge early hominids crossed to become Homo Sapiens. Toddling into language may be paradigmatic 4 Neocortical expansion appears to be directly related to the duration of neurogenesis (Kornack and Rakic, 1998).

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