Elsevier

NeuroImage

Volume 24, Issue 3, 1 February 2005, Pages 841-851
NeuroImage

Productive and perceptive language reorganization in temporal lobe epilepsy

https://doi.org/10.1016/j.neuroimage.2004.10.001Get rights and content

Abstract

The aim of this work was to determine whether productive and perceptive language functions are differentially affected in homogeneous groups of epilepsy patients with right and left temporal lobe epilepsy (TLE). Eighteen patients with left TLE, 18 with right TLE, and 17 healthy volunteers were studied using fMRI during performance of three tasks assessing the productive and perceptive aspects of language (covert semantic verbal fluency, covert sentence repetition, and story listening). Hemispheric dominance for language was calculated in the frontal and temporal regions using laterality indices (LI). Atypical lateralization was defined as a right-sided LI (LI < −0.20) in the frontal lobes during the verbal fluency task or in the temporal lobes during the story listening task. Control subjects and right TLE patients demonstrated a strong left lateralization for language in the frontal lobes during the fluency task, whereas activation was less lateralized to the left hemisphere in left TLE patients, although the difference did not reach significance. In the story listening and the repetition tasks, activation was significantly more right sided in the temporal lobes of patients with left TLE. Atypical language representation was found in 19% of TLE patients (five left and two right TLE). The shift toward the right hemisphere was significantly larger in the temporal than the frontal lobes in patients with atypical language lateralization compared to TLE patients with a typical language lateralization. Neuropsychological performances of patients with atypical language patterns were better than those of patients with typical patterns, suggesting that this reorganization may represent a compensatory mechanism.

Introduction

Studies using the intracarotid amobarbital procedure (IAP), or Wada test, show that the incidence of atypical language lateralization, defined as right hemisphere dominance or bilateral representation, is higher in patients with evidence of early injury in the left hemisphere (Helmstaedter et al., 1997, Kurthen et al., 1994, Loring et al., 1990, Powell et al., 1987, Rasmussen and Milner, 1977, Rausch and Walsh, 1984, Rey et al., 1988, Risse et al., 1997, Staudt et al., 2002, Woods et al., 1988, Zatorre, 1989). The location and size of the lesion may also influence language lateralization (Rausch and Walsh, 1984, Woods et al., 1988). Functional MRI (fMRI) has shown a high concordance between the degree of asymmetry of activation during appropriately selected language tasks and hemispheric dominance as determined with the Wada test (Bahn et al., 1997, Benson et al., 1999, Binder et al., 1996, Desmond et al., 1995, Gaillard et al., 2002, Hertz-Pannier et al., 1997, Lehéricy et al., 2000, Sabbah et al., 2003, Woermann et al., 2003). In agreement with IAP data, several fMRI studies have suggested that atypical dominance patterns are more frequent in epilepsy patients (Springer et al., 1999, Woermann et al., 2003) and may predominate in patients with epilepsy of left hemispheric origin (Adcock et al., 2003, Billingsley et al., 2001, Carpentier et al., 2001, Sabbah et al., 2003). Other work found no difference in patients with left temporal lobe epilepsy (TLE) without any macroscopic lesion on MRI (Van der Kallen et al., 1998). In large series, atypical dominance was associated with an early age of brain injury and onset of intractable epilepsy (Springer et al., 1999, Woermann et al., 2003).

Language areas are located at distance from the epileptogenic lesion in patients with medial temporal lobe epilepsy, suggesting that brain dysfunctions occur in areas beyond this epileptic zone and in the absence of structural abnormality. Indeed, metabolic disturbances have been observed in temporal and frontal areas beyond the damaged temporal lobe (Engel et al., 1982, Jokeit et al., 1997). In patients with TLE, decreased metabolism predominates on the side of the epileptogenic focus and is greater in the temporal than the frontal lobes (Jokeit et al., 1997). Similarly, reorganization of language areas may also predominate in temporal as compared to frontal language areas. Most imaging studies in patients with epilepsy have focused on productive tasks, which did not allow assessment of how frontotemporal networks contribute to other aspects of language processing. Reorganization of language affecting differently productive and perceptive language functions was reported using fMRI in several types of lesions, such as periventricular white matter lesions (Staudt et al., 2001), tumor and schizencephaly (Ries et al., 2004) and brain arteriovenous malformations (Lehéricy et al., 2002). The same dissociation was initially described with IAP in epilepsy patients (Kurthen et al., 1992). A separate analysis of productive and perceptive functions would allow more detailed observation of frontal and temporal reorganization patterns in epilepsy patients. The clinical relevance of reorganization of language circuits in TLE patients also remains to be fully explored. If the reorganization of these circuits functions as an adaptive mechanism, atypical language patterns might be associated with better neuropsychological performances.

This study was thus performed to ask whether atypical language representation equally affects productive and perceptive language functions or whether it predominates in the temporal lobe in TLE patients. We also examined whether atypical language patterns were associated with better neuropsychological performances. Thirty-six patients with TLE were tested with both expressive and receptive tasks designed to encompass a large range of language functions, which are thought to involve both frontal and temporal areas. Patients were subdivided in two homogeneous groups of epilepsy patients with right and left TLE, balanced for age, gender, severity of epilepsy, and neuropsychological performances. It was expected that patients with left TLE would show increased activation in their right hemisphere and thus a greater probability of atypical language lateralization than both control subjects and patients with right TLE, as suggested by previous studies, and that atypical language lateralization would predominate in the temporal lobes of these patients.

Section snippets

Patients and controls

The population included 18 patients with left temporal lobe epilepsy (8 men and 10 women), 18 patients with right temporal lobe epilepsy (9 men and 9 women), and 17 healthy volunteers (7 men and 10 women). Thirty-one patients had hippocampal sclerosis ipsilateral to the epileptogenic focus, two had medial temporal dysplasia including the hippocampus, and three had laterobasal temporal dysplasia (Table 1).

Mean age (±SD) at assessment was 30.8 ± 8.3 years in left TLE patients (range 18–47 years),

Cerebral regions activated in individual subjects

The regions involved in each task were very similar for the three groups in terms of cerebral areas. The main differences between subjects were the lateralization of activation and the magnitude of signal increase. Overall, epilepsy patients exhibited less activation in all tasks than healthy volunteers.

In the semantic fluency task, activation was found in the dorsolateral and ventrolateral frontal areas, mainly in the left hemisphere. Activation was located in the precentral (BA 6) and middle

Brain regions activated in control subjects and patients

The tasks used in this study were designed to examine both perceptive and expressive aspects of language function (Lehéricy et al., 2000). In control subjects, the semantic fluency task which reflects the productive contribution to language processing mainly activated frontal language areas in agreement with previous studies (Binder et al., 1995, Binder et al., 1996, Cuenod et al., 1995, Pihlajamaki et al., 2000). In the repetition task, which engages both receptive and expressive components of

Acknowledgments

We are indebted to Drs. Emmanuelle Volle and Bertrand Bazin for contributing to MR examination in patients. We are grateful to Richard Miles for comments on the manuscript.

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