Language-related hemispheric asymmetry in healthy subjects and patients with temporal lobe epilepsy as studied by event-related brain potentials and intracarotid amobarbital test

Abstract

There are current attempts to replace the WADA test for pre-surgical evaluation of hemispheric language capabilities by one of the methods of functional brain imaging. Recent PET and fMRI studies using verbal cognitive tasks like verb generation, semantic monitoring or semantic (`deep') encoding of words showed asymmetries of activation in the fronto-lateral cortex. In a previous ERP study subjects were required to indicate whether pronounceable non-words and abstract geometric figures were presented for the first time (`new item') or whether they had been shown before (`old item'). Group analyses of this study showed significant material-specific hemispheric asymmetries with ERPs being more negative-going in recordings of the posterior part of the left hemisphere with verbal material (CP5/6) but more negative-going in recordings of the right hemisphere with the spatial material (P7/8). The aim of the present study was to test statistically ERP lateralization effects in individual healthy subjects as well as WADA-tested patients suffering from seizures of the mesio-temporal lobe (MTL). In all subjects ERP lateralization with verbal material was tested in the electrode pair CP5/6, and ERP lateralization with figures in the electrode pair P7/8. Statistical analyses of single trials showed that in 20 out of 24 subjects ERPs with verbal material started to be more negative-going in CP5 as compared to CP6 in the period between 100 and 200 ms after stimulus onset or the subsequent time epoch (200–300 ms). In one subject not CP5/6 but the closely adjacent electrode pair P7/P8 showed this verbal material-related hemispheric effect. In patients language dominance as indicated by ERPs was not always consistent with the data of the WADA test. In one patient with left MTL seizures ERPs with verbal material and figures were found to be significantly lateralized to the right hemisphere although the WADA test assigned this patient to have a language-dominant left hemisphere.

Introduction

Intracarotid application of amobarbital (WADA test; Wada, 1949; Wada and Rasmussen, 1960) is a diagnostic tool in the pre-surgical evaluation of patients suffering from temporal lobe epilepsy. It is the standard technique to determine the language dominant hemisphere and to predict postoperative neuropsychological outcome, in particular impairment of verbal memory after partial resections of the temporal lobe (Chelune et al., 1991; Kurthen et al., 1994).

The WADA test is criticized because of its invasiveness, possible amobarbital cross-flow to the other hemisphere and because of the fact that the territory of the posterior cerebral artery remains unaffected (Snyder et al., 1990; Hart et al., 1991). Limited available time during the test procedure, sedation and the lack of test-retest reliability are methodological drawbacks (Malmgen et al., 1992; Bouwer et al., 1993).

There are attempts to replace the WADA test by methods of functional brain imaging. PET (positron emission tomography) and fMRI (functional magnetic resonance imaging) studies used verbal cognitive tasks like verb generation, semantic monitoring or semantic encoding of words (Pardo and Fox, 1993; Benson et al., 1994; Binder et al., 1996; Desmond et al., 1995; Swanson et al., 1995). When healthy, right-handed subjects performed these tasks there was focal activity in the area of Broca which was larger in the left hemisphere. In most patients results from functional imaging were consistent with those of the WADA test (Desmond et al., 1995). Event-related potentials (ERPs) were also used to determine language-related hemispheric asymmetries. Previous studies employed tasks of word fluency (Altenmüller et al., 1993; Jung et al., 1984) and semantic memory encoding (Lang et al., 1988; Uhl et al., 1990). Task performance caused a sustained, surface-negative brain potential which was significantly larger on the left as compared to the right hemisphere in recordings located above the frontal convexity (Uhl et al., 1990; Altenmüller et al., 1993).

In the present study EEG was recorded while subjects were presented with series of short readable non-words and abstract geometric figures and were asked to detect repetitions. The time interval between initial presentation of an item and its repetition was short (short-term memory task). Patients with lesions of the temporo-lateral and inferior parietal cortex are disabled in reading non-words (`phonological dyslexia'; Beauvois and Derouesne, 1979; Funnell, 1983) and retaining verbal material in short-term memory (for review see Della-Sala and Logie, 1993). Therefore it was assumed that task and verbal material as used in the present study critically involve the parieto-temporal cortex of the left hemisphere. The functionality of this part of the cortex is of particular interest for surgical treatment of temporal lobe epilepsy.

In a previous study, Beisteiner et al. (1996)recorded the EEG while healthy subjects were performing a continuous memory recognition task of readable non-words and abstract geometric figures. ERPs to verbal material were significantly lateralized to the left hemisphere in parieto-temporal recordings. In contrast, ERPs in response to figures were significantly lateralized to the right hemisphere in parieto-occipital recordings. A shortcoming of the previous study was that data processing did not offer the possibility of statistically testing language-related hemispheric asymmetry in single subjects. For the present study, the same paradigm was used to perform statistical analyses of single subjects. Subjects were either healthy (n=24) or suffered from temporal lobe epilepsy (n=20). Twelve patients underwent presurgical evaluation including the WADA test. Points of interest were: Is the method suitable to test the relative language-related hemispheric asymmetry in single subjects statistically? Are there differences between healthy subjects and patients? Do results of the WADA test and ERP agree or disagree?