Left Anterior Temporal Lobectomy Patients Research Articles

Rey–Osterrieth complex figure test: Comparison of traditional and qualitative scoring systems after unilateral temporal lobectomy

Objective We compared the performance on the Rey–Osterrieth Complex Figure Test (ROCF) of patients that had undergone unilateral anterior temporal lobectomy under both Taylor’s and Loring’s scoring systems to identify the sensitivity and specificity of each item for differentiating visuospatial memory deficits. Method We administered the ROCF to evaluate the visual memory of 37 left anterior temporal lobectomy (LATL) and 38 right anterior temporal lobectomy (RATL) patients with unilateral temporal lobe epilepsy who had undergone a standard unilateral anterior temporal lobectomy between 1996 and 2010. Fisher’s exact and Qui–Quadrado tests were used to analyze the relationships between the qualitative variables. The Mann–Whitney U test was used to compare the quantitative variables from the right and left sides. Results RATL patients performed worse than LATL patients based on the total score for delayed recall (DR) (p = 0.012). The scoring system’s showed a specificity of 97.2% & 78.9% and sensitivity of 10.5% & 62.2% on DR, for the Taylor and Loring systems respectively. Our detailed analysis of certain items showed that some differed between the groups in terms of the presence/absence, correct reproduction, and errors of those items. Loring’ errors I, IV, and X on DR and errors IV and X on immediate recall were more frequent in the RATL group. Conclusions The use of these two scoring systems combined may help maximize sensitivity and specificity with clinical populations. Further, our analyses showed that items could be clustered better and different weights could be given to them to maximize sensitivity and specificity.

Short-term neurocognitive outcomes following anterior temporal lobectomy.

Changes in cognitive function are a well established risk of anterior temporal lobectomy (ATL). Deficits in verbal memory are a common postoperative finding, though a small proportion of patients may improve. Postoperative evaluation typically occurs after six to 12months. Patients may benefit from earlier evaluation to identify potential needs; however, the results of a formal neuropsychological assessment at an early postoperative stage are not described in the literature. We compared pre- and postoperative cognitive function for 28 right ATL and 23 left ATL patients using repeated measures ANOVA. Changes in cognitive function were compared to ILAE seizure outcome. The mean time to postoperative neuropsychological testing was 11.1weeks (SD=6.7weeks). There was a side×surgery interaction for the verbal tasks: immediate memory recall (F(1,33)=20.68, p<0.001), short delay recall (F(1,29)=4.99, p=0.03), long delay recall (F(1,33)=10.36, p=0.003), recognition (F(1,33)=5.69, p=0.02), and naming (F(1,37)=15.86, p<0.001). This indicated that the left ATL group had a significant decrement in verbal memory following surgery, while the right ATL group experienced a small but significant improvement. For the right ATL group, there was a positive correlation between ILAE outcome and improvement in immediate recall (r=-0.62, p=0.02) and long delay recall (r=-0.57, p=0.03). There was no similar finding for the left ATL group. This study demonstrates that short-interval follow-up is effective in elucidating postoperative cognitive changes. Right ATL was associated with improvement in verbal memory, while left ATL resulted in a decrement in performance. Improvement in the right ATL group was related to improved seizure outcome. Short-interval follow-up may lend itself to the identification of patients who could benefit from early intervention.

Distinct types of white matter changes are observed after anterior temporal lobectomy in epilepsy.

Anterior temporal lobectomy (ATL) is commonly adopted to control medically intractable temporal lobe epilepsy (TLE). Depending on the side of resection, the degree to which Wallerian degeneration and adaptive plasticity occur after ATL has important implications for understanding cognitive and clinical outcome. We obtained diffusion tensor imaging from 24 TLE patients (12 left) before and after surgery, and 12 matched controls at comparable time intervals. Voxel-based analyses were performed on fractional anisotropy (FA) before and after surgery. Areas with postoperative FA increase were further investigated to distinguish between genuine plasticity and processes related to the degeneration of crossing fibers. Before surgery, both patient groups showed bilateral reduced FA in numerous tracts, but left TLE patients showed more extensive effects, including language tracts in the contralateral hemisphere (superior longitudinal fasciculus and uncinate). After surgery, FA decreased ipsilaterally in both ATL groups, affecting the fornix, uncinate, stria terminalis, and corpus callosum. FA increased ipsilaterally along the superior corona radiata in both left and right ATL groups, exceeding normal FA values. In these clusters, the mode of anisotropy increased as well, confirming fiber degeneration in an area with crossing fibers. In left ATL patients, pre-existing low FA values in right superior longitudinal and uncinate fasciculi normalized after surgery, while MO values did not change. Preoperative verbal fluency correlated with FA values in all areas that later increased FA in left TLE patients, but postoperative verbal fluency correlated only with FA of the right superior longitudinal fasciculus. Our results demonstrate that genuine reorganization occurs in non-dominant language tracts after dominant hemisphere resection, a process that may help implement the inter-hemispheric shift of language activation found in fMRI studies. The results indicate that left TLE patients, despite showing more initial white matter damage, have the potential for greater adaptive changes postoperatively than right TLE patients.

An investigation of implicit memory through left temporal lobectomy for epilepsy

Temporal lobe epilepsy patients have demonstrated a relative preservation in the integrity of implicit memory procedures. We examined performance in a verbal implicit and explicit memory task in left anterior temporal lobectomy patients (LATL) and healthy normal controls (NCs) while undergoing fMRI. We hypothesized that despite the relative integrity of implicit memory in both the LATL patients and normal controls, the two groups would show distinct functional neuroanatomic profiles during implicit memory. LATLs and NCs performed Jacoby’s Process Dissociation Process (PDP) procedure during fMRI, requiring completion of word stems based on the previously studied words or new/unseen words. Measures of automaticity and recollection provided uncontaminated indices of implicit and explicit memory, respectively. The behavioral data showed that in the face of temporal lobe pathology implicit memory can be carried out, suggesting implicit verbal memory retrieval is non-mesial temporal in nature. Compared to NCs, the LATL patients showed reliable activation, not deactivation, during implicit (automatic) responding. The regions mediating this response were cortical (left medial frontal and precuneus) and striatal. The active regions in LATL patients have the capacity to implement associative, conditioned responses that might otherwise be carried out by a healthy temporal lobe, suggesting this represented a compensatory activity. Because the precuneus has also been implicated in explicit memory, the data suggests this structure may have a highly flexible functionality, capable of supporting implementation of either explicit memory, or automatic processes such as implicit memory retrieval. Our data suggest that a healthy mesial/anterior temporal lobe may be needed for generating the posterior deactivation perceptual priming response seen in normals.

Discordance on FMRI and Wada Tests of Language Dominance in a Large Epilepsy Cohort (IN5-1.007)

Objective: To quantify discordance between fMRI and Wada language tests, identify factors associated with discordance, and compare the predictive value of each test in discordant cases. Background FMRI assessment of language dominance has begun to replace the traditional Wada test, but the incidence of discordance and factors underlying discordance between these tests have not been well defined. Design/Methods: Participants were 229 epilepsy patients who underwent both fMRI and Wada language testing. The fMRI protocol used a semantic decision task contrasted with a tone decision task. Patients were classified as left dominant, right dominant, or symmetric based on cutoff values applied to the lateralization index (LI, range -100 to +100) from each test. Results were discordant if the two tests failed to classify the patient in the same dominance category AND the LIs from the two tests differed by more than 50 units. A variety of Wada and fMRI quality measures were assessed for association with discordance. Regression formulas for predicting postoperative naming outcome were computed for each test based on data from the 56 left anterior temporal lobectomy patients in whom the tests were concordant, and these formulas were used to compare predicted and observed outcomes in patients with discordant fMRI and Wada. Results: Discordant results occurred in 30/229 patients (13.1%). The main predictor of discordance was the fMRI LI (p Conclusions: FMRI and Wada language dominance tests are generally concordant, though fMRI appears to be more sensitive for detecting atypical dominance. Overall, fMRI may provide a more accurate prediction of postoperative language outcome. Supported by: NIH grant R01 NS035929. Disclosure: Dr. Binder has nothing to disclose. Dr. Janecek has nothing to disclose. Dr. Swanson has nothing to disclose. Dr. Sabsevitz has nothing to disclose. Dr. Hammeke has nothing to disclose.

Use of preoperative functional MRI to predict verbal memory decline after temporal lobe epilepsy surgery

Verbal memory decline is a frequent complication of left anterior temporal lobectomy (L-ATL). The goal of this study was to determine whether preoperative language mapping using functional magnetic resonance imaging (fMRI) is useful for predicting which patients are likely to experience verbal memory decline after L-ATL. Sixty L-ATL patients underwent preoperative language mapping with fMRI, preoperative intracarotid amobarbital (Wada) testing for language and memory lateralization, and pre- and postoperative neuropsychological testing. Demographic, historical, neuropsychological, and imaging variables were examined for their ability to predict pre- to postoperative memory change. Verbal memory decline occurred in over 30% of patients. Good preoperative performance, late age at onset of epilepsy, left dominance on fMRI, and left dominance on the Wada test were each predictive of memory decline. Preoperative performance and age at onset together accounted for roughly 50% of the variance in memory outcome (p < 0.001), and fMRI explained an additional 10% of this variance (p <or= 0.003). Neither Wada memory asymmetry nor Wada language asymmetry added additional predictive power beyond these noninvasive measures. Preoperative fMRI is useful for identifying patients at high risk for verbal memory decline prior to L-ATL surgery. Lateralization of language is correlated with lateralization of verbal memory, whereas Wada memory testing is either insufficiently reliable or insufficiently material-specific to accurately localize verbal memory processes.

Limitations of Wada memory asymmetry as a predictor of outcomes after temporal lobectomy

The intracarotid amobarbital (Wada) test can be used to evaluate hemispheric memory capacity before anterior temporal lobectomy (ATL). Most patients demonstrate better memory with injection ipsilateral to planned resection (expected asymmetry [EA]), but a substantial minority show better memory with contralateral injection (unexpected asymmetry [UA]). Both degree and direction of Wada memory asymmetry (WMA) have been associated with worse surgical outcome in small series. Reports also suggest that UA is associated with greater decline in verbal memory after left ATL (L-ATL). The relationship between WMA and surgical outcome (at 3 months, 1 year, and last follow-up) was examined in a large group of ATL patients (108 L, 119 R) with both EA and UA. Also, memory in a subgroup (96 L, 108 R) was examined, comparing subscores of the Rey Auditory Verbal Learning Test obtained preoperatively, at 3 months, and at 1 year. Thirty-six percent of L-ATL and 8% of R-ATL patients had UA. UA was associated with worse surgical outcome at 1 year for R-ATL patients but was not associated with worse outcome for L-ATL patients. There was no correlation between WMA and persistent postoperative verbal memory change for patients with L- or R-ATL. Unexpected asymmetry is uncommon in patients with right anterior temporal lobectomy (R-ATL) and may be a risk marker of poor surgical outcome. This relationship may be obscured by language confounds in patients with L-ATL. The results suggest that Wada asymmetry (using mixed stimuli) does not predict postoperative verbal memory; it is unclear whether this finding is generalizable to centers using only nonverbal stimuli.

Validation of the WMS-III Facial Memory Subtest With the Graduate Hospital Facial Memory Test in a Sample of Right and Left Anterior Temporal Lobectomy Patients

A number of studies have shown visuospatial memory deficits following anterior temporal lobectomy (ATL) in the right, nondominant temporal lobe (RATL). The current study examines 26 patients with intractable temporal lobe epilepsy who underwent ATL in either the right (RATL, n = 16) or left temporal lobe (LATL, n = 10) on two tests of facial memory abilities, the Wechsler Memory Scale-III (WMS-III) Faces subtest and the Graduate Hospital Facial Memory Test (FMT). Repeated measures ANOVA on the FMT indicated a significant main effect of side of surgery. The RATL group performed significantly below the LATL group overall. Both groups showed a slight, but non-significant, improvement in performance from pre- to postsurgery on the FMT immediate memory, likely due to practice effects. Repeated measures ANOVA on the WMS-III Faces subtest revealed a significant interaction of group (RATL vs. LATL) by delay (immediate vs. delayed). Overall, the LATL group showed an improvement in recognition scores from immediate to delayed memory, whereas the RATL group performed similarly at both immediate and delayed testing. No effects of surgery were noted on the WMS-III. Following initial data analysis the WMS-III Faces I and II data were re-scored using the scoring suggested by Holdnack and Delis (2003), earlier in this issue. Repeated measures ANOVA revealed a trend toward significance in the three-way interaction of group (RATL vs. LATL) × time of testing (pre- versus postop) × delay (immediate vs. delayed memory). On the Faces I subtest, both the RATL and LATL groups showed a decline from preoperative to postoperative testing. However, on Faces II the LATL group showed an increase in performance from preoperative to postoperative testing, while the RALT group showed a decline in performance from preoperative to postoperative testing. While the FMT appears to be superior to the WMS-III Faces subtest in identifying deficits in facial memory prior to and following RATL, the application of the scoring methodology presented by Holdnack and Delis earlier in this issue does serve to increase the clinical utility of the WMS-III Faces subtest in this population.

Memory for faces dissociates from memory for location following anterior temporal lobectomy

It has been suggested that the right and left mesial temporal lobes are specialized for processing different types of information for long-term memory (LTM). Although findings have been consistent in regard to the dominant role of the left mesial temporal lobe (MTL) in verbal memory, the role of the right MTL in non-verbal memory remains debatable. Given the existence of two cortical pathways specialized for processing different types of visuospatial information, we examined whether memory processing for these two types of information might also be differentially localized. The effect of unilateral anterior temporal lobectomy (ATL) was compared for memory for unfamiliar faces and a novel sequence of spatial locations in 86 ATL patients (left ATL (LATL) = 35; right ATL (RATL) = 51) pre- and post-surgery to examine the contributions of right and left MTL structures to LTM for pattern and spatial information. Memory for spatial location was not related to side of ATL or time of testing. On the facial memory task, RATL patients showed impairments relative to LATL patients prior to surgery, which became magnified after surgery. These results extend the proposed dissociation between an occipitotemporal and an occipitoparietal pathway for processing visuospatial information by demonstrating dissociations in LTM systems for these two types of information. Lesions in the right MTL, adjacent to the cortical structures believed to be specialized for facial recognition, specifically impair the memory encoding of new faces, but not spatial locations.

Differences between nouns and verbs after anterior temporal lobectomy.

To test the claim that lesions of left anterior and middle temporal cortical structures specifically impair processing of nouns but not verbs, 56 left-hemisphere-language-dominant patients who had undergone anterior temporal lobectomy (ATL) completed tasks assessing confrontation naming of pictured objects and actions, generation of synonyms for nouns and verbs, and semantic lexical judgments about nouns and verbs. Compared with right ATL patients, left ATL patients were impaired across different tasks that assessed naming and comprehension of high-imageability as well as low-imageability nouns. These groups did not differ, however, in verb naming or comprehension on most tasks. Results are consistent with the hypothesized specialization of left temporal lobe structures for processing nouns and suggest that naming problems commonly seen after left ATL extend beyond difficulties with retrieving object names and may be related to subtle disturbances in comprehension of the meanings underlying nominal word forms.

Cognitive models of music psychology and the lateralisation of musical function within the brain

In this study, a computer-based musical composition task was used to access higher order musical representations of adult nonmusicians, and patients having undergone left- or right-sided anterior temporal lobectomy (ATL). Compositions were rated according to the main features of cognitive structuralist models of pitch, tonality, rhythm, and phrase structure (musical grouping), as well as in terms of their nontonal complexity. The results showed that all participants created compositions that contained features typical of Western tonal music. The a priori music-theoretical structure of the cognitive models, however, was not reflected in the data. Laterality effects were observed for the left and right ATL patients in comparison to the adult nonmusicians. Left ATL patients showed less use of tonal features in their compositions, whilst right ATL patients placed less emphasis on phrase structure and melodic contour. The right ATL patients also showed impaired melodic discrimination in comparison to the normal controls.

Confrontation naming after anterior temporal lobectomy is related to age of acquisition of the object names

Decline in visual confrontation naming ability may occur as a postacute complication of left anterior temporal lobectomy (ATL) for the treatment of intractable mesial temporal lobe epilepsy. In this study of 26 left ATL patients who demonstrated postsurgery decline on a standardized naming measure, it was hypothesized that naming performance would be significantly associated with specific attributes of the object names. We investigated the relation between performance on the Boston Naming Test (BNT) and the following attributes of the test items: living versus nonliving category (L/NL), word length (WL), written word frequency (WF), and age of acquisition (AoA). Regression analyses revealed that AoA and WF were significant predictors of preoperative group performance. AoA was the only significant predictor of performance after left ATL. For the 17 individuals who demonstrated a statistically meaningful decline on the BNT, as indicated by a Reliable Change Index, individual logistic regressions demonstrated that AoA was the strongest and most consistent predictor of postoperative success/failure for items that had been named correctly preoperatively. Consistent with the literature on naming errors in elderly normals and patients with aphasia or semantic dementia, the results provide evidence that object names learned in late childhood are among the most vulnerable when there is a decline in object naming ability. Investigation of additional attributes and semantic knowledge for the concepts represented by the pictured objects will be necessary to determine whether the naming deficit associated with TLE and ATL reflects an impairment of phonological word-form retrieval, semantics, or both.

Anterior temporal lobectomy, hippocampal sclerosis, and memory: recent neuropsychological findings.

Anterior temporal lobectomy (ATL) is an effective and increasingly utilized treatment for nonlesional, intractable mesial temporal lobe epilepsy. However, this surgery results in domain-specific neuropsychological morbidity for a subset of patients. Within the past decade, multidisciplinary studies have revealed that left ATL patients without significant sclerosis in the resected hippocampus are most at risk for a substantial postacute decline in the ability to encode new verbal information. These patients are also at risk for a significant decrement in confrontation naming and other retrieval-based language abilities. The memory deficit is not attributable to this disruption of language. A relationship between hippocampal sclerosis (HS) status and memory performance has not been identified consistently in right ATL patients, but investigation of new visuospatial measures continues. The influence of variables other than HS on neuropsychological outcome is also discussed.

Wada memory asymmetries predict verbal memory decline after anterior temporal lobectomy

We examined Wada memory and neuropsychological memory function in 34 nonlesional patients who underwent anterior temporal lobectomy (ATL) and who were seizure free at 1-year follow-up. Patients who displayed a decline on verbal memory measures that exceeded 1 SD after left ATL had significantly smaller left/right Wada memory asymmetries than left ATL patients without a significant verbal memory decline. When Wada memory asymmetries were used to predict verbal memory decline after left ATL in individual patients, similar statistically significant effects were present. No significant relationship between Wada memory and postoperative memory was present in right ATL patients, and postoperative memory function was not related to Wada memory performance after either left hemisphere or right hemisphere injection alone. We conclude that Wada memory asymmetries provide one measure of the risk to material-specific decline in verbal memory after left ATL.

Relationship of Age at Onset, Chronologic Age, and Adequacy of Preoperative Performance to Verbal Memory Change After Anterior Temporal Lobectomy

We examined the relationship of age of onset of epilepsy, chronological age at time of operation, and adequacy of preoperative memory performance to pre- to postoperative verbal memory decline. Patients who underwent left (n = 50) or right (n = 51) anterior temporal lobectomy (ATL) were administered tests of verbal episodic (list learning, paragraph recall) and semantic memory (visual naming, vocabulary), both preoperatively and 6 months postoperatively. As a group, left ATL patients showed the classic selective decrease on measures of episodic but not semantic memory. However, examination of episodic memory outcome showed considerable individual variability. Stepwise regression analyses indicated that both later age at onset and older chronologic age were significant and selective predictors of episodic memory decrease for left ATL patients. Adequacy of preoperative memory performance was a nonspecific predictor, associated with decrease in postoperative memory performance for both left and right ATL patients and for multiple types of memory indices. The clinical and theoretical implications are discussed.

Dysnomia after Left Anterior Temporal Lobectomy without Functional Mapping

The integrity of language function after a left (dominant) anterior temporal lobectomy performed without the use of functional mapping remains controversial. Much of the controversy concerns the degree to which analyses of group data obscure the identification of surgically induced dysnomia in individual patients. This study investigated postoperative language outcome in our entire series (n = 162) of nonretarded, left hemisphere speech dominant patients with intractable nonlesional epilepsy who underwent a left (n = 85) or right (n = 77) anterior temporal lobectomy without functional mapping. A comparison of preoperative to (6 mo) postoperative performance on a standardized test of nominal speech revealed the following: 1) a statistically significant but clinically modest difference in outcome between left and right anterior temporal lobectomy groups; 2) a subgroup (7%) of left anterior temporal lobectomy patients exhibited a postoperative dysnomia (a decline in nominal speech that exceeded the worst performance in the right anterior temporal lobectomy group); and 3) a postoperative decline in nominal speech after left anterior temporal lobectomy was specifically associated with a later age at the onset of epilepsy. Within the context of group data suggesting minimal risk to language function when functional mapping is not used, a small subgroup of individuals characterized by a later onset of epilepsy can be identified who exhibit a surgically induced dysnomia after a standard left anterior temporal lobectomy. Whether these results differ from the outcome of functional mapping remains to be determined.

Declarative memory following anterior temporal lobectomy in humans.

This study hypothesized that verbal memory decline following anterior temporal lobectomy (ATL) is associated with a lack of significant neuropathology in resected left, but not right, hippocampus and is limited to measures of episodic memory only. Tests of immediate (digit span), semantic (visual naming), and episodic memory as measured by the California Verbal Learning Test (CVLT) were administered before and 6 months after resection of the anterior left (n = 36) or right (n = 26) temporal lobe. There were no effects of hippocampal pathology on measures of immediate or semantic memory for either ATL group or for episodic memory for the right ATL group. Left ATL patients who demonstrated no/mild hippocampal sclerosis exhibited significantly greater postoperative decline in episodic memory compared with those with moderate/marked hippocampal sclerosis on multiple CVLT indices (recall measures, learning characteristics, and contrast measures).