Elsevier

Epilepsy & Behavior

Volume 5, Issue 3, June 2004, Pages 348-357
Epilepsy & Behavior

Linguistic deficits following left selective amygdalohippocampectomy: a prospective study

https://doi.org/10.1016/j.yebeh.2004.02.004Get rights and content

Abstract

Language deficits in 10 patients with medically intractable left-sided temporal lobe epilepsy prior to and following selective amygdalohippocampectomy are described. Preoperatively, a pattern of minor linguistic deficits was observed in three patients; isolated minor naming deficits were detectable in one additional patient. Three months after surgery, six patients' linguistic functions were unchanged, whereas in four patients, a significant decline in linguistic functions could be observed. All four patients revealed a very similar language syndrome characterized by reduced language comprehension and fluency, well-articulated speech, frequent word-finding difficulties, circumlocutions, and semantic paraphasias in the absence of any phonological disorder. These deficits remained stable during the 12-month follow-up period. However, magnetic resonance imaging did not show any neocortical lesions outside the resection area. Possible explanations for these findings include neuronal cell loss and deafferentiation in cortical areas, disruption of the basal temporal language area pathways, reorganization of the language network in chronic temporal lobe epilepsy, and neocortical lesions due to the surgical intervention. Furthermore, correlations between linguistic and demographic data for our patients suggest that patients older at epilepsy onset are at greater risk for developing postoperative language deficits.

Introduction

Selective amygdalohippocampectomy (sAHE) is a widely used surgical procedure in the treatment of medically intractable temporal lobe epilepsy (TLE) [1]. Compared with anterior temporal lobectomy, in which both temporal neocortex and mesial structures are removed, sAHE is a more restricted surgical procedure with the advantage that minimal amounts of cortical tissue are destroyed. Several studies have reported an advantage of sAHE with respect to postoperative neuropsychological and seizure outcome [2], [3], whereas others have not confirmed these results [4], [5], [6].

Little information is available regarding interictal language functions in TLE [7], [8], [9], and limited attention has been paid so far to possible language deficits following sAHE. Previous studies described language deficits prior to and following anterior temporal lobectomy [10], [11], [12], [13], [14], [15], [16], [17], and two investigations reported language functions after combined anterior temporal lobectomy and amygdalohippocampectomy [18], [19]. To our knowledge, there are no reports on linguistic functions or linguistic deficits following sAHE. This is not surprising because, according to the classic view, mesiobasal structures do not belong to the standard language areas, which include the speech-dominant temporal, frontal, and inferior parietal neocortex [20]. Therefore, language deficits are not expected after resection of mesiobasal structures.

There is, however, some evidence from lesion, stimulation, and neuroimaging studies of a basal temporal language area (BTLA). Lüders and co-workers showed that electrical stimulation of the fusiform gyrus of the language-dominant hemisphere at high intensity caused a transient aphasia with both language comprehension and production deficits, whereas electrical stimulation at lower intensity induced anomia [21], [22], [23]. Surgical resection of left basal temporal areas in patients with TLE is reported to carry the risk of naming deficits [18]. Functional imaging studies underline these findings, as they found the left fusiform gyrus active during picture naming [24]. In addition, several studies suggested a role for hippocampal formation in some aspects of language processing. Burnstine and co-workers used a combination of electrocortical stimulation and three-dimensional computerized axial tomography of the BTLA and reported that not only the fusiform gyrus, but also parts of inferior temporal and parahippocampal gyri were associated with language processing [25]. Snyder and co-workers [26] and Shear and co-workers [27] found that left hippocampal volume correlates significantly with naming deficits in patients with temporal lobe epilepsy. Davies and co-workers [28] demonstrated that both preoperative naming deficits and postoperative change in naming abilities are associated with the pathological status of the hippocampus. Martin and co-workers [29] measured neuronal loss and glial abnormality in the mesial temporal lobe with proton magnetic resonance spectroscopy and found significant associations between hippocampal neuronal integrity and confrontation naming. Gadian and co-workers [30] used proton magnetic resonance spectroscopy and found significant correlations between left-sided pathology and verbal functions, as well as between right-sided pathology and nonverbal functions. Sawrie and co-workers [31] studied confrontation naming after temporal lobe resection in adult patients with intractable mesial temporal lobe epilepsy and showed that naming performance correlated significantly with left hippocampal ratios measured by magnetic resonance spectroscopy. In addition, recent advances in functional magnetic resonance imaging (fMRI) have demonstrated a correlation between activation of the hippocampal formation and language processing in healthy adults [32], [33], [34], [35], [36].

Therefore, this study aims at the assessment of linguistic functions in patients with TLE and the influence of sAHE on language. Ten patients with medically intractable left-sided TLE were investigated prospectively with pre- and postoperative formal neurolinguistic assessment and neuropsychological background testing.

Section snippets

Patients

Ten patients were recruited consecutively between 2000 and 2001 during a presurgical evaluation program including detailed clinical and neurological examination, high-resolution MRI, video-EEG monitoring, Wada test, neuropsychological examination, and neurolinguistic examination. All patients had medically intractable unilateral TLE with seizure onset zone in the left mesial temporal lobe. Edinburgh Handedness Inventory laterality quotients [37] revealed a strong right-handedness in all

Preoperative neurolinguistic findings

Preoperative language assessment showed fluent, well-articulated spontaneous speech without semantic or phonemic paraphasias, neologisms, or perseverations in all patients (Table 2). However, two patients (E, G) had word-finding difficulties in spontaneous speech preoperatively. All patients had intact language comprehension in the semistandardized interview. In formal linguistic assessment, nine patients showed intact auditory language comprehension as assessed with the Token Test and the AAT

Discussion

In this study we analyzed language functions in patients with medically intractable left-sided TLE prior to and following sAHE. For this purpose a comprehensive neurolinguistic test battery was administered pre- and postoperatively to 10 patients with medically intractable left-sided mesial TLE. Some patients exhibited linguistic deficits when specifically tested. Furthermore, postoperative examination revealed that sAHE can significantly worsen linguistic abilities and produce persistent

Acknowledgements

This work was supported by the Österreichische Nationalbank Jubiläumsfonds No. 8741.

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