ReviewNeural bases of childhood speech disorders: Lateralization and plasticity for speech functions during development
Highlights
► We reviewed the evidence linking childhood speech disorders and brain abnormalities. ► The brain basis for speech production in children and adults overlaps. ► The potential for brain plasticity however differs between adults and children. ► In children, unilateral lesions are not sufficient to result in speech disorders. ► Longterm severe speech disorders mainly arise from bilateral brain dysfunction.
Introduction
It has been known for centuries that brain lesions can affect the quality of speech production in adults (see Ackermann and Riecker, 2010, for a historical perspective). In contrast, little attention has been paid to speech in children, that is, to the motor aspects (as opposed to content) of language output. Research on language outcome after brain injury has led to a continuing debate over two seemingly opposing mechanisms. One hypothesis is that, with increasing age, language functions are less likely to be compensated for, due to decreasing brain plasticity. The second postulates that, in contrast, younger age is associated with increased vulnerability (e.g., Anderson et al., 2009). An alternative theory suggests that developmental plasticity follows a reverse U-shape function, with the highest phase of plasticity around the ages of three to six years (e.g., Anderson et al., 2009). This debate has mainly emerged from outcome data for language production and comprehension (see Chilosi et al., 2008, for a review on childhood aphasia). The lack of data linking brain lesion and motor speech outcome has made it difficult to explore the propensity for children and adolescents to recover speech function, and hence to provide long-term prognosis. This paucity of evidence also makes it difficult to address the question of hemispheric dominance for motor speech in the developing brain.
Current neuroanatomical models (e.g., Jürgens, 2002, see Fig. 1) confirm the crucial roles played by the pre- and primary motor cortices, the cerebellum, as well as subcortical control loops, for speech production. A recent model derived from fMRI data suggests that the planning and execution of speech movements may rely on distinct yet interlinked neural systems (Riecker et al., 2005). Speech planning would involve the supplementary motor area, anterior insula, dorsolateral frontal cortex, and the superior cerebellum, whereas speech execution would involve the primary motor cortex, putamen/globus pallidus, caudate nucleus, thalamus and inferior cerebellum (see Fig. 1 for an illustration). Computational modeling similarly emphasizes the important role of feedforward and feedback loops during speech learning, with crucial roles played by the premotor, sensorimotor cortices, and the cerebellum (Terband et al., 2009). Altogether, these models suggest that the neural basis of motor speech disorders affecting planning vs. execution may be distinct.
Whether acquired in adulthood or in childhood, motor speech disorders affect the quality of speech (where speech sounds are distorted or unusual) and also intelligibility (where people cannot be easily understood by the naïve listener). Two forms of motor speech disorders are classically recognized, namely dysarthria and apraxia of speech (or AOS, also termed verbal dyspraxia, speech dyspraxia, and most recently in children childhood apraxia of speech, or CAS). Dysarthria is a disorder of neuromuscular execution of the fine motor movements involved in speech sound production, that is, across the domains of articulation, resonance, vocal quality, prosody and respiration. For instance, dysarthric speech may sound imprecise or ‘slurred’ due to a failure of execution of the lips or tongue, or severely distorted as regards nasal resonance due to velopharyngeal dysfunction. Various sub-types of dysarthria have been reported to occur in isolation or combination depending on the neuroanatomical lesion site, as early as 1943 (Froeschels, see Duffy and Kent, 2001, for a historical perspective and Duffy, 2005, for an update on the widely used Mayo classification by Darley et al., 1969). In contrast, apraxia of speech is a disorder of planning and programming, where execution of individual speech sounds is reportedly mostly preserved but coarticulation and sequencing may be impaired.
Although “not a rare disorder … in paediatric neurology” (Van Mourik et al., 1997b, p. 299), dysarthria in conjunction with neuroimaging has mainly been reported in the adult population. Consistent with recent functional imaging studies during overt speech (see Price, 2010, for a recent review), unilateral damage to the pyramidal or extrapyramidal system and associated pathways is sufficient to result in dysarthria in adults (see review in Kent et al., 2001). A recent report (Urban et al., 2006) indicated that extracerebellar infarcts to the left hemisphere (irrespective of location) were not only more likely to result in dysarthria, but also resulted in more severe dysarthria than right hemisphere infarctions, especially for articulation and prosody, in the acute stage (within 72 h). Altogether, the findings therefore suggest a left hemisphere dominance for articulatory functions in the mature brain.
Apraxia of speech is the main symptom noted in adults with Broca's aphasia, resulting from infarcts to the left hemisphere and involving the inferior frontal region, including the posterior part of Broca's area (Hillis et al., 2004, Jordan and Hillis, 2006) and the insular cortex (Dronkers, 1996, Nagao et al., 1999) or adjacent white matter (Jaffe et al., 2003; see reviews Ackermann and Riecker, 2010, Ogar et al., 2005). It is also a feature of neurological degenerative diseases (e.g., Josephs et al., 2006), such as corticobasal degeneration (Josephs and Duffy, 2008), where pathology is bilateral. Since there is little evidence to suggest that right hemisphere damage alone is sufficient to result in apraxia of speech, the literature therefore suggests that the planning/programming of speech may also be predominantly subserved by left hemisphere networks in the mature brain.
Given that conditions such as infarcts and neurodegenerative diseases are rare in childhood, motor speech outcomes in children and adults with similar aetiologies have not been compared. Despite recent advances in neuroimaging data acquisition and analysis techniques that allow the detection of functional (e.g., functional MRI, PET) and subtle structural (e.g., voxel-brain morphometry or VBM, Ashburner and Friston, 2000) brain abnormalities, no neuroanatomical model of paediatric motor speech disorders is available. As a result, the question of a left hemispheric dominance for motor speech functions throughout development remains unanswered, and the potential for post-lesional functional reorganization remains difficult to predict in childhood.
In order to address these questions, the aim of the present article was to systematically review and describe recent evidence reporting on a link between motor speech disorders (apraxia of speech and dysarthria) and brain abnormalities in children and adolescents (16 years or younger) with developmental, progressive, or childhood-acquired neurological conditions.
Section snippets
Search strategy
Articles were searched using the OvidSP interface, which provides access to the following biomedical and health related databases: AMED; Biotechnology Abstracts; EMBASE; Health and Psychosocial Instruments; HMIC; Maternity and Infant Care; MEDLINE; PsycEXTRA; PsycINFO; PsycCRITIQUES; Social Policy and Practice.
For inclusion purposes, children and adolescents were defined as aged 16 or under, although adult cases were included if pathology onset was at or before the age of 16. The term brain
Results
Only 12 reports of CAS were accompanied by neuroimaging investigations. CAS was either associated with epilepsy disorders (five reports), metabolic disorders (two reports), syndromic conditions (two reports), idiopathic forms arising from FOXP2 disruption (two reports), or was of unknown origin (one report). When examining the number of cases (Fig. 2A), epilepsy and metabolic disorders accounted for about 70% of cases (31 individuals) altogether.
Neuroimaging correlates of dysarthria were
Discussion
Within the past 13 years, seventy-two articles have reported on motor speech disorder in the paediatric population together with neuroimaging data. Dysarthria and CAS were reported for numerous categories of neurological conditions (ten including our “miscellaneous” category). The human motor speech system therefore appears vulnerable to a wide range of neurological events arising in the pre- and post-natal period, although motor speech disorders were rarely the only symptoms for the cases
Concluding remarks
The present review confirms that the conditions associated with speech disorders differ between adults and children. However current adult models of the neural basis for speech seem to apply in childhood, whereby the perisylvian and perirolandic cortices, the basal ganglia, and the cerebellum all play a major role in both speech execution and planning. Yet one major difference is of critical note. Where uni-hemispheric damage in the adult population seems to be sufficient to result in chronic
Conflict of interest
The authors reported no conflict of interest.
Acknowledgements
We thank Cristina Mei for her assistance in retrieving and archiving abstracts and articles. We also thank Dr. Baldeweg and Dr. Vogel for their helpful comments on an earlier version of the manuscript, and Dr. Schulze for her assistance with illustrations. Dr. Morgan is supported by NHMRC Career Development Award 607315.
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