Linguistic deficits following left selective amygdalohippocampectomy: a prospective study
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.
References (69)
- et al.
Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy
Surg. Neurol.
(1982) - et al.
Everyday memory after unilateral temporal lobectomy or amygdalohippocampectomy
Cortex
(1992) - et al.
Learning and retention of words and designs following excision from medial or lateral temporal-lobe structures
Neuropsychologia
(1997) - et al.
The hippocampal contribution to verbal fluency in patients with temporal lobe epilepsy
Cortex
(2001) - et al.
Adequacy of language function and verbal memory performance in unilateral temporal lobe epilepsy
Cortex
(1992) - et al.
Interictal language functions in chronic mesial temporal lobe epilepsy
Brain Lang
(2003) - et al.
Confrontation naming after anterior temporal lobectomy is related to age of acquisition of the object names
Neuropsychologia
(2000) - et al.
A category-specific naming impairment after temporal lobectomy
Neuropsychologia
(1996) - et al.
Medial temporal lobe activation during semantic language processing: fMRI findings in healthy left- and right-handers
Cogn. Brain Res.
(2003) The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
(1971)
Speed and flexibility on word fluency tasks after focal brain lesions
Neuropsychologia
The roles of semantic networks and search efficiency in verbal fluency performance in intractable temporal lobe epilepsy
Epilepsy Res.
Morphometry in temporal lobe epilepsy
Magn. Reson. Imaging
Effects of chronic epilepsy on intellectual functions
Prog. Brain Res.
Effects of chronic epilepsy on declarative memory systems
Prog. Brain Res.
Atypical hemispheric language dominance in left temporal lobe epilepsy as a result of the reorganization of language functions
Epilepsy Behav.
Patterns of language dominance in focal left and right hemisphere epilepsies: relation to MRI findings, EEG, sex, and age at onset of epilepsy
Brain Cogn.
Relationship of hippocampal sclerosis to duration and age of onset of epilepsy, and childhood febrile seizures in temporal lobectomy patients
Epilepsy Res.
Quantitative MRI hippocampal volumes: association with onset and duration of epilepsy, and febrile convulsions in temporal lobectomy patients
Epilepsy Res.
Selective amygdalohippocampectomy for temporal lobe epilepsy
Epilepsia
Mesial atrophy and outcome after amygdalohippocampectomy or temporal lobe removal
Ann. Neurol.
Interictal memory and language impairment in temporal lobe epilepsy
Neurology
Language before and after temporal lobectomy: specificity of acute changes and relation to early risk factors
Epilepsia
Visual confrontation naming outcome after standard left anterior temporal lobectomy with sparing versus resection of the superior temporal gyrus: a randomized prospective clinical trial
Epilepsia
Language function following anterior temporal lobectomy
J. Neurosurg.
Visual confrontation naming following left anterior temporal lobectomy: a comparison of surgical approaches
Neuropsychology
Language function after temporal lobectomy without stimulation mapping of cortical function
Epilepsia
Word-finding deficits persist after left anterotemporal lobectomy
Arch. Neurol.
Cognitive effects of resecting basal temporal language areas
Epilepsia
Acute naming deficits following dominant temporal lobectomy: prediction by age at 1st risk for seizures
Neurology
Cortical stimulation
Basal temporal language area
Brain
Basal temporal language area demonstrated by electrical stimulation
Neurology
Quantitative comparison of language deficits produced by extraoperative electrical stimulation of Broca's, Wernicke's, and basal temporal language areas
Epilepsia
Cited by (30)
Baseline neuropsychological characteristics in patients with epilepsy with left temporal lobe encephaloceles compared with left mesial temporal sclerosis
2020, Epilepsy and BehaviorCitation Excerpt :In this series, identification was aided by 3D variable flip angle turbo spin-echo (TSE) MR fluid-attenuated inversion recovery (FLAIR) sequence and a high index of suspicion. Epilepsy surgery in the language-dominant (usually left) temporal lobe has the potential to result in verbal memory and language dysfunction, either with standard temporal lobectomy or with selective amygdalohippocampectomy [4–6]. Early studies have pointed towards the material-specific nature of memory processing in dominant versus nondominant temporal lobes (verbal versus visual).
Knowledge of language function and underlying neural networks gained from focal seizures and epilepsy surgery
2019, Brain and LanguageCitation Excerpt :This study included patients with and without hippocampal sclerosis, again highlighting that even in cases with a normal-appearing hippocampus, visual confrontational naming was not harmed by destruction of this structure. It should be pointed out that selective open resection approaches have not been shown to be more efficacious in terms of cognitive outcome than standard ATL in most studies (Bartha et al., 2004; Kuang, Yang, Gu, Kong, & Cheng, 2014). The reason for the lack of difference between ATL and selective open resection approaches has been posited to result from the necessity to transect white matter in all of these open resection procedures, with most approaches disrupting the temporal stem (Gross, Willie, & Drane, 2016).
Surgical treatment for mesial temporal lobe epilepsy associated with hippocampal sclerosis
2015, Revue NeurologiqueCitation Excerpt :Whether this deficit can be attributed to the resection of lateral temporal neocortex [29] or to the resection of the mesial temporal lobe structures [73,74] is debated. Naming difficulties have been reported even after selective amygdalohippocampectomies [75,76]. However, postoperative seizure freedom may be associated with an improvement of language function [15,77].
Clinical significance and developmental changes of auditory-language-related gamma activity
2013, Clinical Neurophysiology