ADEQUACY OF LANGUAGE FUNCTION AND VERBAL MEMORY PERFORMANCE IN UNILATERAL TEMPORAL LOBE EPILEPSY Bruce P. Hermann l -4, Michael SeidenbergS, Allan Haltiner and Allen R. Wyler l •3•4 CEpi Care Center, Baptist Memorial Hospital; Departments of 2Psychiatry and 3Neurosurgery, University of Tennessee, Memphis; 4Semmes-Murphey Clinic; 5Department of Psychology, Chicago Medical School)

INTRODUCTION

Memory and learning abilities represent important domains of human cognitive function and are considered integral components of any comprehensive neuropsychological evaluation (Lezak, 1983). The classic material-specific model of memory function has played a prominent role in theoretical formulations of memory processes, and has also guided the content and selection of tests included in neuropsychological examinations. Broadly defined, the material-specific model attributes the learning and recall of verbal material to left (dominant) hemisphere function, and non-verbal or visuospatial material to right (nondominant) hemisphere function (Hecaen and Albert, 1978; Kolb and Whishaw, 1985; Squire, 1986). More specifically, the medial structures of the temporal lobe (amygdala and especially hippocampus) are assumed to playa vital role in the consolidation of material to long term store, with lateral cortical areas, particularly of the temporal lobe, contributing to memory processes in conjunction with diencephalic structures (Ojemann and Dodrill, 1985; Squire, 1986, 1987; Zola-Morgan and Squire, 1990). Temporal lobe epilepsy (complex partial seizures of temporal lobe origin in the current terminology) has played a critical role in the development and refinement of the material-specific model of memory (Delaney et aI., 1980; Frisk and Milner, 1990; Hecaen and Albert, 1978; Jones-Gotman, 1987; Jones-Gotman and Milner, 1978; Kolb and Whishaw, 1985; Loring et aI., 1989; Lee et aI., 1989; Milner, 1958, 1972; Novelly et aI., 1984; Rausch, 1985; Rausch and Babb, 1987; Smith and Milner, 1981). Invasive EEG monitoring of idiopathic temporallobe seizures has shown them to be predominantly of hippocampal origin (Spencer et aI., 1990; Wyler et aI., 1988), therefore providing a naturally occurring model of hippocampal pathology with which to evaluate the contributions of medial temporal lobe structures to human memory processes. It is generally unstated, but implicitly understood, that critical supportive cognitive systems must be intact in order to establish specific inferences concerning the functional integrity of memory systems. Coexisting deficits in stimulus reception or response output systems could distort findings in the evaluation of memory processes. For example, evaluation of verba/learning and memory ability is critically dependent upon the adequacy of the patient's language system. It is possible that impairment in specific language abilities such Cortex, (1992) 28, 423-433

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as auditory comprehension or retrieval of lexical codes could confound assessment of memory and learning ability. From a neural systems viewpoint, inferences concerning hippocampal functioning cannot take place without first establishing the integrity of the (primarily) cortically based language system of which the dominant temporal lobe is an integral part. Adequacy of basic language functioning is rarely explicitly controlled for in studies examining patient groups with significant memory impairments, and there is only modest understanding of the effects of temporal lobe epilepsy on language function. Patients with idiopathic (nonlesional) temporal lobe epilepsy rarely present with a frank aphasic disorder, and the issue of their language competence has not been of general interest. Because the disorder is primarily of hippocampal origin, one might not even expect to find significant compromise of language function. However, because of recent interest in the effects of temporal lobe resection (for treatment of intractable seizures) on postoperative language function, a few studies have examined and detected abnormalities in TLE patients' preoperative language ability (e.g., Hermann et aI., 1991). These findings raise the possibility that disturbances in language function may not be uncommon among nonaphasic patients with temporal lobe epilepsy. That compromised language function is relevant to the issue of memory function in epilepsy was suggested by Mayeux et aI. (1980). In a small sample of patients with left and right temporal lobe epilepsy they found word finding impairments to be related to poorer verbal memory and learning performance. Hermann et aI. (1988) used a broader assessment of language function and also found compromised language abilities to be associated with poorer memory and learning performance among temporal lobe patients. However, their sample size was modest, etiology varied among the subjects, a limited number of intercorrelated measures of memory were investigated, and only patients with left temporal lobe epilepsy were investigated. The purpose of this study is to build on these previous findings and further explore the language/memory relationship with a larger and more strictly defined sample of patients with both left and right temporal lobe epilepsy, a broader assessment of language function, and an empirically derived set of verbal memory indices. This investigation is composed of three parts. First, patients with unilateral left and right temporal lobe epilepsy are compared on a standardized aphasia battery in order to determine the impact of the disorder on their language functioning. Second, building on the findings of Mayeux et aI. (1980), the influence of nominal speech on verbal learning and memory ability is more closely examined in both temporal lobe epilepsy groups. Third, laterality of temporal lobe epilepsy and adequacy of language functions are directly compared to determine their relative effects on verbal learning and memory ability. MATERIALS AND METHOD

Subjects Ninety-nine consecutive patients over 16 years of age with intractable epilepsy of unilateral temporal lobe origin served as subjects. These individuals were referred to the epilepsy center for surgical consideration because of medication resistant epilepsy. As such, they un-

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· Memory and language in epilepsy TABLE I

Subject Characteristics

Chronological age Years of education Age at onset (yrs) Gender (Males:Females) Duration (yrs) WAIS-R VIQ* WAIS-R PIQ WAIS-R FSIQ

Left temporal (N=47)

Right temporal (N = 52)

30.4 (9.8) 12.5 (2.2) 11.9 (10.7) 23M:24F 18.6 (11.3) 87.2 (13 .3) 89.7 (13 .8) 87.4 (12.8)

30.4 (9.9) 12.5 (2.8) 13.1 (9.7) 26M:26F 17.3 (11.4) 92.0 (13 . 1) 91.9 (13 .0) 91.3 (11.98)

·p < O. IO.

derwent intensive neurophysiological investigation which permitted precise localization of their epileptogenic lesion. The pre-surgical work-up included continuous (24 hour) closed circuit TV I EEG monitoring with scalp electrodes in order to record several of the patients' typical spontaneous seizures for classification of seizure type and preliminary localization of seizure onset. All patients also underwent invasive EEG monitoring of spontaneous seizures with subdural strip electrodes in order to provide precise localization of the epileptogenic focus (Wyler et aI., 1984). Invasive monitoring involved implantation of six to eight strip electrodes. The most common electrode placements included bilateral, 6-cm (four-contact) electrodes from lateral to medial under the temporal lobe and a 5-cm (four-contact) electrode placed anterior to posterior along the middle temporal gyrus. In addition, four-contact electrodes were inserted down the interhemispheric fissure toward the corpus callosum and over the lateral frontal lobe. In some cases, a simpler frontal lobe examination was accomplished by deleting the frontal burr holes and sliding an eightcontact, 9-cm electrode over the lateral frontal cortex from the temporal burr hole. In all cases, electrodes were implanted bilaterally with attention made to positioning electrodes symmetrically. Immediately following surgery, patients had the electrode positions verified by CT. Generally, three seizures were recorded with invasive EEG procedures. All determinations as to the localization and lateralization of the ictal onset were made independently by the electroencephalographer who was blinded to the results of the psychological testing. To be included in the present investigation subjects had to have all invasively monitored seizures originating from one temporal lobe. One ictal event from the contralateral temporal lobe was a basis for exclusion. Patients underwent intracarotid amy tal testing to determine cerebral dominance for speech (Blume et aI., 1973). Individuals with anomalous organization of language function (e.g., bilateral speech, right hemisphere speech) were deleted from the subject pool. Patients underwent MRI imaging and those individuals with underlying structural lesions (e.g., tumor, infarction, arteriovenous malformation) were excluded from consideration. Mesial temporal sclerosis was not considered a structural lesion. An additional subject inclusion criterion was WAIS-R Full Scale IQ of 70 or greater. In summary , the final sample consisted of 99 consecutive non-retarded , left hemisphere dominant patients with intractable idiopathic (non-structural) epilepsy of left or right medial temporal lobe origin. The results of the EEG monitoring revealed that 47 patients had ictal onset from the left (dominant) temporal lobe, while 52 patients had ictal onset from the right (nondominant) temporal lobe. As shown in Table I, there were no statistically significant differences between the groups in demographic (age, education, gender) or seizure related variables (age at onset, duration of disorder). There was a trend for lower Verbal IQ in the left temporal lobe group (p