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Purpose: Benign childhood epilepsy with centrotemporal spikes (BECTS) is the most common epilepsy syndrome of childhood and can be associated with language difficulties. The exact profile of these difficulties and their neurofunctional underpinnings, however, are not yet clear.
Methods: To further understand the impact of the BECTS syndrome on language, we assessed language performance using standard neuropsychological measures, and patterns of language lateralization using functional magnetic resonance imaging (fMRI) in children with typical BECTS (n = 20) and healthy controls (n = 20).
Results: The fMRI analyses revealed that language-related activation was less lateralized to the left hemisphere in anterior brain regions in the patients relative to the control group. This finding was consistent with decreased performance in the BECTS group compared to the control group on the neuropsychological measure most dependent on the integrity of anterior aspects of the language axis, namely, sentence production.
Discussion: The converging lines of evidence from the neuropsychological and activation methodologies support the view that BECTS is associated with language difficulties that are regional, and anterior, in nature.
Benign childhood epilepsy with centrotemporal spikes (BECTS) is the most common epilepsy syndrome of childhood (Cavazzuti et al., 1980; Engel, 2001). The syndrome has a characteristic electroencephalography (EEG) signature of frequent focal interictal epileptiform discharges arising from the perirolandic region, and in its typical form occurs without underlying structural pathology or frequent seizures. The syndrome resolves spontaneously by adolescence and is defined as occurring in children of normal intellect without neuropsychological deficits (Loiseau & Duche, 1989). Recent studies, however, indicate that the syndrome can be associated with mild cognitive and learning difficulties. Poor performance is reported in a number of functional domains including language (Staden et al., 1998; Baglietto et al., 2001; Monjauze et al., 2005; Wolff et al., 2005; Riva et al., 2007), attention (D’alessandro et al., 1990; Piccirilli et al., 1994), spatial perception (Volkl-Kernstock et al., 2006), memory (Croona et al., 1999), executive function (Metz-Lutz et al., 1999; Baglietto et al., 2001), and academic achievement (Vinayan et al., 2005).
Given the proximity of the seizure focus to classical language areas in BECTS, several studies have attempted to clarify the nature of difficulties within the language sphere (Staden et al., 1998; Baglietto et al., 2001; Monjauze et al., 2005; Wolff et al., 2005; Riva et al., 2007), but a clear account of the effects of BECTS on language, and its neurofunctional underpinnings, is yet to emerge. Some studies indicate that language skills are broadly affected in children with BECTS (Baglietto et al., 2001; Wolff et al., 2005). Studies conducted within a psycholinguistic framework, on the other hand, describe a selective profile of language difficulties involving sentence formulation (Staden et al., 1998; Monjauze et al., 2005), or fluency (Riva et al., 2007), whereas comprehension (Deonna et al., 1993; Monjauze et al., 2005) and naming (Monjauze et al., 2005; Riva et al., 2007) are spared. This pattern suggests selective dysfunction within the language system in children with BECTS.
Lateral specialization for the processing of language is detectable at an early stage in healthy children (Kinsbourne & Hiscock, 1977). Behavioral studies suggest that basic systems for language perception and control are well lateralized by approximately 3 years of age, and that the degree of lateralization is stable until adulthood (Kimura, 1967; Hiscock & Kinsbourne, 1980; Hiscock et al., 1985). Functional neuroimaging studies further support this view: Activation associated with the processing of meaningful speech is left-hemisphere dominant, encompassing frontal and temporoparietal cortices in infants as young as 3 months of age (Dehaene-Lambertz et al., 2002). A similar pattern is seen in children aged 5–7 years (Ahmad et al., 2003). In middle to late childhood, patterns of activation associated with covert language production are also left lateralized (Holland et al., 2001; Wood et al., 2004; Szaflarski et al., 2006), and patterns of lateralization can be related to neuropsychological measures of language performance (Wood et al., 2004).
Childhood epilepsies with refractory focal seizures and structural lesions can be associated with alterations in the pattern of language lateralization, manifesting as bilateral recruitment of homologous regions, or right hemisphere dominance (Rasmussen & Milner, 1977; Liegeois et al., 2004; Anderson et al., 2006; Yuan et al., 2006). It is not clear, however, if idiopathic partial epilepsies such as BECTS exert similar effects.
To gain a better understanding of the impact of the BECTS syndrome on language, we characterized the language profile and assessed language lateralization by means of functional magnetic resonance imaging (fMRI) in children with BECTS and healthy controls. The relationship between performance on language tests and the indices of language lateralization was then explored.
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We would like to thank the children and their families for participating in our research as well as Janet Barchett and the neurophysiology teams at Austin Health, the Royal Children’s Hospital, and Monash Medical Centre for assistance with the identification of potential subjects. We also thank the radiographers involved in the project, Todd Little, Heather Ducie, and Shawna Farquharson, as well as Esther Hutchinson for testing some of the participants. The authors gratefully acknowledge the support of the National Health and Medical Research Council, Neurosciences Victoria, and the Brain Imaging Research Foundation, Australia. We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.
Disclosure: None of the authors has any conflict of interest to disclose.