Elsevier

Brain and Language

Volume 114, Issue 2, August 2010, Pages 126-134
Brain and Language

Speech and oral motor profile after childhood hemispherectomy

https://doi.org/10.1016/j.bandl.2009.12.004Get rights and content

Abstract

Hemispherectomy (disconnection or removal of an entire cerebral hemisphere) is a rare surgical procedure used for the relief of drug-resistant epilepsy in children. After hemispherectomy, contralateral hemiplegia persists whereas gross expressive and receptive language functions can be remarkably spared. Motor speech deficits have rarely been examined systematically, thus limiting the accuracy of postoperative prognosis. We describe the speech profiles of hemispherectomized participants characterizing their intelligibility, articulation, phonological speech errors, dysarthric features, and execution and sequencing of orofacial speech and non-speech movements. Thirteen participants who had undergone hemispherectomy (six left, seven right; nine with congenital, four with acquired hemiplegia; operated between four months and 13 years) were investigated. Results showed that all participants were intelligible but showed a mild dysarthric profile characterized by neuromuscular asymmetry and reduced quality and coordination of movements, features that are characteristic of adult-onset unilateral upper motor neuron dysarthria, flaccid-ataxic variant. In addition, one left and four right hemispherectomy cases presented with impaired production of speech and non-speech sequences. No participant showed evidence of verbal or oral dyspraxia. It is concluded that mild dysarthria is persistent after left or right hemispherectomy, irrespective of age at onset of hemiplegia. These results indicate incomplete functional re-organization for the control of fine speech motor movements throughout childhood, and provide no evidence of hemispheric differences.

Introduction

The smooth execution of finely controlled speech articulation is a uniquely human skill that requires precise and fast coordination of over 100 muscles (Ackermann & Riecker, 2004). Although motor speech deficits have been reported in a range of adult clinical populations with focal neuropathology, including strokes and degenerative diseases (see Kent, Duffy, Slama, Kent, and Clift (2001) for a review), similar studies in children are rare. The paucity of such reports limits our knowledge about the potential for re-organization of neural systems controlling motor speech, and therefore our ability to predict outcome after lesions affecting those systems during development. One extreme example of unilateral lesion is seen in children who have undergone hemispherectomy, that is, complete removal or disconnection of an entire cerebral hemisphere. Although a remarkable sparing of language after childhood hemispherectomy has been reported in numerous studies (e.g. Basser, 1962, Curtiss and de Bode, 1999, Gott, 1973, Liégeois et al., 2008b, Mariotti et al., 1998, Ogden, 1988) the motor speech profile of this patient group has rarely been described. The present study attempts to address this issue.

Behavioral and direct cortical stimulation studies in humans with focal pathology indicate that vocalization involves a wide network of cortical and subcortical regions, namely the supplementary motor area (SMA), the anterior cingulate, the premotor and primary motor cortices (face and trunk area) and Broca’s area, the putamen, substantia nigra, ventrolateral thalamus and cerebellum (see Jurgens (2002) for a comprehensive review). Neuroimaging studies on speech production have confirmed these findings and indicate a predominant left-lateralized system involving two circuits, one involved in planning, and another involved in “execution” or production of motor speech sounds. Using a functional connectivity approach to analyze fMRI data during syllable repetition for instance, Riecker et al. (2005) concluded that there was a speech “executive” and a “preparatory” loop. A recent study on basal ganglia connections using diffusion tensor imaging (Leh, Ptito, Chakravarty, & Strafella, 2007) suggests, however, that the two loops are interconnected. For example, some parts of the putamen are connected to the primary motor cortex (executive loop), while others are connected to the SMA (preparatory loop). Interestingly, most regions involved in the preparatory loop were left lateralized (apart from the cerebellum), whereas activation of the sensorimotor cortex was bilateral in the executive loop, but not in the basal ganglia (Riecker et al., 2005). How speech planning and execution is affected by unilateral lesions in children has rarely been reported.

Dysarthria is a collective term for disorders affecting the execution of speech sounds. It is commonly associated with weakness, paralysis, incoordination, reduced tone and/or poor control of the muscle groups that compose the speech mechanism (Duffy, 2005). Dysarthria may be classified into sub-categories (e.g., spastic, ataxic, flaccid, etc.) based upon the clinical speech features and the associated site of brain pathology (cerebellum, basal ganglia, etc.: Darley et al., 1969b, Darley et al., 1975, Duffy, 2005). Importantly, in relation to the present study, dysarthria may be detected after left or right hemisphere pathology (Duffy, 2005). Unfortunately, the dysarthria classifications are derived from studies of adults with neuropathology. Although the features encountered in adults and children may differ (Van Mourik, Catsman-Berrevoets, Paquier, Yousef-Bak, & Van Dongen, 1997), in the absence of a childhood speech disorder classification system, the adult classification is widely applied to paediatric cases in the literature. Most cases of acquired dysarthria are reported in children following posterior fossa tumor removal or traumatic brain injury (e.g., Cahill et al., 2005, Cornwell et al., 2003a, Cornwell et al., 2003b, Morgan et al., 2007). Cases of dysarthria in children after unilateral cortical lesions, such as infarcts, are rare (Van Mourik et al., 1997), often restricted to single-case studies, and do not describe detailed motor speech profiles (e.g., “dysarthria” in Chen, Zhu, Lin, Wu, and Feng (2008); “slurred speech” in Agrawal, Joharapurkar, and Gharde (2007)). Clinical studies on groups of children post-stroke have mainly focused on language outcome (e.g., Bates et al., 2001, Mosch et al., 2005) reporting motor speech outcome only briefly (nonspecific “articulation” in Mosch et al. (2005); phonological errors in Chilosi et al. (2008)). Here specific and quantitative methods were used to provide a comprehensive differential diagnosis of motor speech.

Hemispherectomy is a rare surgical procedure (see Nogueira, Marino, Aguiar, and Jacobsen (2006) and Schramm (2002) for reviews of the current techniques) used for the relief of intractable epilepsy of congenital or acquired origin. It involves complete removal (“anatomical” hemispherectomy) or partial resection and disconnection (“functional” hemispherectomy) of an entire cerebral hemisphere. It is noteworthy that both types of surgeries are functionally equivalent, since the remaining tissue in the functional hemispherectomy is disconnected from both deep and contralateral structures. In summary, the implications of hemispherectomy are that all functions are subserved by a single hemisphere. The study of participants who have undergone hemispherectomy therefore offers a unique opportunity to study speech motor functions of a single cerebral hemisphere, and to examine the potential for re-organization during development.

Overall, hemispherectomy in childhood results in favorable seizure, cognitive, and neurological outcomes (van Empelen, Jennekens-Schinkel, Buskens, Helders, & van Nieuwenhuizen, 2004), with gross language functions being remarkably preserved even after left hemispherectomy (Pulsifer et al., 2004), within limits of memory and intellectual abilities (Liégeois et al., 2008b). Language outcome is dependent upon age at onset of pathology and hemispheric side of surgery (Rankin and Vargha-Khadem, 2007, Vargha-Khadem et al., 1991) among other factors. In particular, near-normal every day language and fluent speech after left hemispherectomy is reported in children with congenital damage (Mariotti et al., 1998, Vargha-Khadem et al., 1991), whereas children with damage acquired after age five may show dysphasic symptoms such as word finding difficulties and short utterances (Boatman et al., 1999, Vargha-Khadem et al., 1991). Children who have undergone right hemispherectomy after postnatal pathology are likely to show age-appropriate language functions, whereas those with pre/perinatal pathology may show language deficits in line with more general intellectual limitations (Liégeois et al., 2008b). Whether this interaction between age at onset of pathology and side of surgery also applies to motor speech function remains to be determined.

One criterion often used for the decision to proceed to hemispherectomy is the presence of hemiplegia. After hemispherectomy, motor skills on the contralesional side may either worsen – if only mild hemiplegia was present prior to surgery- or fail to improve (Devlin et al., 2003, Leonhardt et al., 2001, Maehara et al., 2002, van Empelen et al., 2004, van Empelen et al., 2005). Although most individuals are able to walk without assistance (89% in one report: Kossoff et al., 2003) and move their arms, hand movements are limited (with spasticity and lack of sensation), and pincer grip and individual finger movements are severely restricted (Dijkerman et al., 2008, Holloway et al., 2000, Leonhardt et al., 2001, van Empelen et al., 2004). There is evidence of a distal–proximal gradient on the contralesional side, where motor functions of the proximal muscles are relatively preserved compared to those of the distal muscles (Dijkerman et al., 2008). The afore-mentioned motor disorders are seen after left as well as right hemispherectomy, and after congenital as well as late acquired hemiplegia, indicating little interhemispheric re-organization and compensation during childhood for contralesional sensorimotor control of the hand and fingers.

The main difference between the neural basis for control of finger vs. speech movements is cortical innervation. In the case of finger movements, the motor cortices project both directly (pyramidal tract) and indirectly (extrapyramidal tract) mainly to the contralateral limb. Therefore, a unilateral lesion is sufficient to result in hemiplegia. In contrast, most cranial nerves involved in speech receive bilateral input from the cortex, except cranial nerves XII (tongue movements) and VII (lower face). As a result, persistent deficits will be observed only for the latter nerves following unilateral lesions, while functions of the other cranial nerves should only be partly affected, since they will still receive input from ipsilateral and contralateral descending pathways. Although there is now evidence that unilateral lesion to the cortico-bulbar tract is sufficient to cause dysarthria in adults, for example after infarct (Kumral, Celebisoy, Celebisoy, Canbaz, & Calli, 2007), this hypothesis has never been explicitly tested in children with unilateral brain damage.

Despite the well-known differences between fine motor control and language outcome post-hemispherectomy, speech characteristics have not been systematically investigated. Here we describe motor speech abilities in a group of participants with hemispherectomy with a view to examine the effects of hemispheric side of surgery (left vs. right) and age at onset of hemiplegia (congenital vs. acquired after age five), including assessment of the execution and sequencing of oral non-speech and speech tasks, dysarthria, and speech intelligibility.

Section snippets

Participants

Participants were selected (see criteria below) from a group of individuals who underwent hemispherectomy (Fig. 1) at Great Ormond Street Hospital or King’s College Hospital, London, UK. Inclusionary criteria consisted of: seizure-free status (on or off medication), at least 1 year post-surgery, and over the age of seven (i.e. when articulation, phonological and oromotor skills are known to have matured). Thirteen (four males, nine females; six with left, seven with right hemispherectomy) of the

Intelligibility

At a single-word level, all participants except one (LP-2, who scored 79%) obtained a score between 85% and 100% (group mean 94%; SD = 6.05), indicating high single-word intelligibility, irrespective of side of injury or age at onset of pathology. A high level of intelligibility was also noted at the conversational speech level, with the majority of participants obtaining a score of 5 ‘Speech is completely intelligible’ (8/13, 61.54%), or 4 ‘Speech is intelligible with the exception of a few

Discussion

Here we report on the speech characteristics of participants who have undergone hemispherectomy for relief from intractable epilepsy. Because speech assessment was not carried out pre-operatively, it cannot be concluded that the reported deficits are a consequence of hemispherectomy per se. As in the case of well established hemiplegia prior to hemispherectomy, the motor speech deficits may have been a consequence of the brain pathology, emerging early during the evolution of the epileptic

Clinical implications

Although all participants were highly intelligible, they nevertheless presented with persistent dysarthria that affected the ‘precision’ or ‘naturalness’ of their speech, with these features prevailing up to 10 years post-surgery. This finding will lead to improvements in prognostic indicators of long term speech outcome in participants with hemispherectomy. Whether the type of dysarthria reported here can be remediated even partially with speech therapy intervention pre- or post-operatively

Disclosure

The authors reported no conflict of interest.

Acknowledgements

We thank all the participants and families who contributed to this research. This work was undertaken at GOSH/UCL Institute of Child Health which received part funding from the Department of Health’s NIHR Biomedical Research Centres scheme.

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    Present address: Language & Literacy Unit, Murdoch Childrens Research Institute, Parkville, Australia.

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