Left Temporal Resection Research Articles

Verbal and spatial learning after temporal lobe excisions in children: An adaptation of the Grober and Buschke procedure

Using an adaptation of Grober and Buschke’s procedure, we assessed verbal and visuospatial learning abilities in 16 children after left or right anteromesial temporal resection and 16 healthy controls to evaluate material-specific memory deficits. All children had relatively well-preserved verbal and spatial learning capacities after unilateral temporal resection. Children who had left temporal resection showed impaired verbal memory performance despite semantic control by cued recall. No memory deficits with visual material were detected in children who underwent right anteromesial temporal resection. Grober and Buschke’s procedure appears relevant for the detection of verbal memory disorders in children with left-sided temporal resection.

Evidence of lateralized anteromedial temporal structures involvement in musical emotion processing

The right and left anteromedial temporal lobes have been shown to participate in emotion processing. The aim of the study was to further address their role in music emotion perception/recognition, and assessment by two emotional determinants, i.e., arousal (relaxing versus stimulating aspects) and valence (pleasantness degree). Epileptic patients with right or left anterior mesio-temporal resection (including the amygdala), and control subjects were presented with happy musical (chosen highly stimulating) or sad excerpts (chosen to be relaxing), that were either consonant (pleasant) or dissonant (unpleasant). The patients demonstrated an abnormal perception of dissonant music disregarding of the side of the resection; thereby confirming the role of the parahippocampal gyrus in the perception of unpleasantness. Moreover, the pleasantness of musical excerpts, in particular the happy consonant ones, was overestimated by patients with right temporal damage. In contrast, the arousal rating for happy consonant excerpts was reduced only in the group with left-resections. This modified perception of arousal might be related to the decreased ability of those patients to recognize happy and sad music. Indeed, both right and left temporal resections impaired sadness recognition, whereas happiness recognition was only reduced by the left-resections. The main result was that for the first time, the mesio-temporal structures were demonstrated to be asymmetrically involved in positive musical emotion recognition.

Autonoetic Consciousness in Autobiographical Memories after Medial Temporal Lobe Resection

This study aims to investigate autonoetic consciousness associated with episodic autobiographical memory in patients who had undergone unilateral medial temporal lobe resection for intractable epilepsy. Autonoetic consciousness, defined as the conscious feeling of mentally travelling back in time to relive a specific event, was assessed using the Remember/Know (R/K) paradigm across different time periods as proposed in the autobiographical memory task developed by Piolino et al. (TEMPau task). Results revealed that the two patient groups (left and right temporal resection) gave reduced sense of reliving (R) responses and more familiarity (K) responses than healthy controls. This poor autonoetic consciousness was highlighted when patients were asked to justify their Remember responses by recalling sensory-perceptive, affective or spatiotemporal specific details across all life periods. These results support the bilateral MTL contribution to episodic autobiographical memory covering the entire lifespan, which is consistent with the multiple trace theory of MTL function [7,9]. This study also demonstrates the bilateral involvement of MTL structures in recalling specific details of personal events characterized by autonoetic consciousness.

Co-existence of cavernoma and cortical dysplasia in temporal lobe epilepsy

Cavernomas and cortical dysplasia are well-known causes of partial epilepsy. The association between cavernoma and cortical dysplasia in an epileptic patient has not yet been sufficiently documented. We report a case of long-term, drug-resistant, partial left temporal epilepsy associated with a cavernoma. According to the neurophysiological non-invasive presurgical study, the patient was submitted to a tailored left temporal resection. The histopathological study showed the coexistence of cavernoma and cortical dysplasia. This is an interesting combination of epilepsy-related pathologies that have so far not been documented.

Charles Bonnet syndrome in hemianopia, following antero‐mesial temporal lobectomy for drug‐resistant epilepsy

Charles Bonnet syndrome (CBS) is a disorder characterized by the occurrence of complex visual hallucinations in patients with acquired impairment of vision and without psychiatric disorders. In spite of the high incidence of visual field defects following antero-mesial temporal lobectomy for refractory temporal lobe epilepsy, reports of CBS in patients who underwent this surgical procedure are surprisingly rare. We describe a patient operated on for drug-resistant epilepsy. As a result of left antero-mesial temporal resection, she presented right homonymous hemianopia. A few days after surgery, she started complaining of visual hallucinations, such as static or moving "Lilliputian" human figures, or countryside scenes, restricted to the hemianopic field. The patient was fully aware of their fictitious nature. These disturbances disappeared progressively over a few weeks. The incidence of CBS associated with visual field defects following epilepsy surgery might be underestimated. Patients with post-surgical CBS should be reassured that it is not an epileptic phenomenon, and that it has a benign, self-limiting, course which does not usually require treatment.

Distribution of Auditory and Visual Naming Sites in Nonlesional Temporal Lobe Epilepsy Patients and Patients with Space‐Occupying Temporal Lobe Lesions

Current knowledge regarding the topography of essential language cortex is based primarily on stimulation mapping studies of nonlesional epilepsy patients. We sought to determine whether space-occupying temporal lobe lesions are associated with a similar topography of language sites, as this information would be useful in surgical planning. We retrospectively compared the topography of auditory and visual naming sites in 25 nonlesional temporal lobe epilepsy patients ("nonlesional") and 18 patients with space-occupying lesions ("lesional") who underwent cortical language mapping before left temporal resection. Both groups exhibited a similar pattern of auditory naming sites anterior to visual and dual (auditory-visual) naming sites; no group differences were specific to auditory or visual naming sites. However, significantly fewer lesional (10 of 20) compared with nonlesional patients (21 of 25) exhibited any naming sites in the temporal region (p=0.04). Although the proportion of naming sites on the superior temporal gyrus was similar between groups, naming sites were found on the middle temporal gyrus in 13 of 25 nonlesional patients, yet in only one of 18 lesional patients (p=0.002). Across groups, patients with visual naming sites were older than patients without visual naming sites identified (p=0.02). The precise location of essential language cortex cannot be reliably inferred from anatomic landmarks or patient-related variables. As time constraints are a common quandary in stimulation mapping, the different patterns reported here for patients with and without space-occupying lesions can be used to guide mapping strategies, thereby increasing the efficiency by which positive naming sites are identified.

Spatial Memory Following Temporal Lobe Resection

The present study sought a clearer understanding of spatial memory function consequent to temporal lobe resection, and, in particular, of spatial memory function with respect to two- as well as three-dimensional frames of reference. Relative to a group of 15 control participants, a group of 15 epilepsy patients with right temporal resections demonstrated deficits of memory for locations in a two-dimensional display. A group of 13 epilepsy patients with left temporal resections did not demonstrate such deficits. The right and the left resection groups both demonstrated deficits of memory for item-location relationships in a two-dimensional display. The right but not the left resection group demonstrated deficits of memory for item-location relationships in a three-dimensional display. The differing results that were observed for item-location relationships in two- and three-dimensional displays were attributed to differences in the way item information is bound with location information concerning two- and three-dimensional domains.

TEMPORAL LOBE SURGERY FOR INTRACTABLE EPILEPSY IN CHILDREN

Abstract OBJECTIVE Temporal lobectomy is a well-established neurosurgical procedure for temporal lobe epilepsy. In this study, we conducted a retrospective review of children with drug-resistant temporal lobe epilepsy to evaluate seizure outcome after temporal lobe surgery. METHODS We reviewed the medical records of 126 children who had surgery for temporal lobe epilepsy at The Hospital for Sick Children between 1983 and 2003. The records were examined for preoperative and intraoperative factors that could predict patient outcome after surgery. RESULTS The mean age at seizure onset was 5.9 years. The mean seizure duration before surgery was 5.6 years. All patients had preoperative computed tomographic scans, magnetic resonance imaging scans, or both. The mean age at the time of surgery was 13.5 years. Sixty-two patients underwent left temporal resections and 64 patients underwent right temporal resections. The histopathology of the temporal resections revealed low-grade brain tumors in 65 children (52%) and cavernous malformations in four children. Ganglioglioma and astrocytoma were the most common tumors encountered. Mesial temporal sclerosis was found in 16 patients (13%), astrogliosis in 15 patients (12%), and cortical dysplasia in eight patients (7%). Postoperative follow-up of at least 2 years was available for 106 patients and ranged up to 13.0 years. Seventy-four percent of patients had an Engel Class I or II outcome. Patients with temporal lobe lesions had better outcomes compared with those without lesions (P< 0.05). Patients without a history of secondary generalization of seizures also had a better outcome when compared with those with secondary generalization. Complications in the form of contralateral homonymous hemianopsia, dysphasia, and infection were found in 5% of patients. Twelve patients had a second temporal lobe procedure for intractable recurrent seizures. After a second procedure, seven patients returned to a seizure-free state. CONCLUSION Temporal lobe resections for epilepsy in children are effective and safe procedures, with a favorable impact on seizure control. Repeat temporal resections for recurrent seizures may also be effective in restoring a seizure-free outcome to children.

Cognitive functioning following epilepsy surgery

Temporal lobe resection is the most common surgery for intractable epilepsy because of its proven efficacy in seizure control. However, patients who may benefit from the procedure might be deterred from surgical evaluation due to concerns of postoperative cognitive decline. Recent reports on long-term follow-up indicate that, similar to findings within the year after surgery, cognition remains relatively stable in the years following right temporal resection. The verbal memory decline often observed 1 year after left temporal resection persists over time, yet is mitigated to some extent by good seizure outcome. Although memory decline observed on testing is not typically accompanied by functional decline, a small proportion of patients do experience reductions in occupational or academic status. Recent advances in functional imaging and refinements in preoperative mapping promise better prediction and protection of cognitive functioning. Additionally, results from studies comparing cognitive outcome among different surgical techniques suggest that more restricted resections benefit some patients, whereas more extended resections might be appropriate in a select group of well-defined patients. Preliminary reports on alternate treatments such as vagal nerve stimulation suggest no direct influence on cognition, although improvement in quality of life has been reported. The decision to pursue surgical treatment must balance the potential benefit of seizure control with the potential impact and probability of cognitive decline.

Naming ability after tailored left temporal resection with extraoperative language mapping: Increased risk of decline with later epilepsy onset age

Standard temporal resection in the left hemisphere carries the risk of postoperative naming ability decline, especially with later epilepsy onset age/absence of hippocampal sclerosis. Language mapping has been performed routinely at some centers to minimize postoperative primary language impairment, but its effect on changes in naming performance has not been explored. This study examined naming outcome in 24 patients with nonlesional epilepsy who had left temporal resection after extraoperative language mapping. The mean decline in Boston Naming Test (BNT) score was 7.8, and 13 (54%) patients had a BNT decline greater than the Reliable Change Index. Simple correlations found significant relationships between BNT score decline and: later onset age, higher preoperative BNT score, and resection of isolated language sites. A multiple regression analysis showed that onset age was the best predictor of BNT decline. Although naming ability in patients with early onset age is stable with language mapping, there is still a risk of decline for those with later onset age.

Effects of Trans‐sylvian Approach to Basal Forebrain Projection Fibers: Verbal Memory Decline after Selective Amygdalohippocampectomy

To the Editor: We read the manuscript by Gleissner et al. (1) with great interest. Verbal memory decline in patients with left temporal lobectomy is an important concern after epilepsy surgery, from the viewpoint of quality of life (QoL). The decrease reportedly was progressive for >10 years after surgery, and the degree of decrease was more than that of patients with left temporal lobe epilepsy treated with medication, according to the recent report (2). Initially, selective amygdalohippocampectomy (SAH) was thought to produce little or no verbal memory decrease (3), but Gleissner et al. (1) demonstrated that SAH caused a significant verbal memory decrease 1 year after surgery, similar to the deficits seen at 3 months after surgery (3). Does resection of the left hippocampus inevitably cause verbal memory decline? The authors (1, 3) reached the hippocampus by the trans-sylvian approach. Cholinergic pathways from the basal forebrain to the cerebral cortex mediate the effect that novel and relevant events have on attention and memory. The degeneration of the nucleus basalis of Meynert observed in Alzheimer's disease and dementia with Lewy bodies results in a depletion of cortical innervation and contributes to the cognitive hypofunction. The trajectories of cholinergic pathways from the nucleus basalis of Meynert recently was identified as two lateral pathways, with a capsular and a perisylvian division in humans by means of visualization of multiple cholinergic markers (4). The capsular division courses in the medial aspect of the external capsule, and it also travels ventrally in the white matter of the uncinate fasciculus, penetrates the substance of amygdala, and continues in a dense bundle in the temporal stem. The perisylvian division courses within the claustrum, curving laterally into the white matter of the inferior frontal and superior temporal gyri, and it also radiates to the frontoparietal and opercular cortices, the superior temporal gyrus, and the insula [Figs. 3C and D in Selden et al. (4)]. Furthermore, ischemic white matter lesions along those trajectories, such as subinsular lesions, can cause the cognitive dysfunction (5). Therefore a trans-sylvian approach may disconnect the cholinergic projection pathway from the nucleus basalis of Meynert, and if so, it may produce the additional effects on cognitive dysfunction besides the hippocampal resection. Fisher et al. (6) recently showed that donepezil, a reversible inhibitor of acetylcholine esterase that is used widely in patients with Alzheimer's disease, was effective for memory problems in patients with partial and generalized epilepsy. If verbal memory decline after left temporal resection was shown to be related to the involvement of the cholinergic system, a drug strategy such as donepezil could contribute to improving verbal memory.

Impaired recognition of scary music following unilateral temporal lobe excision

Music constitutes an ideal means to create a sense of suspense in films. However, there has been minimal investigation into the underlying cerebral organization for perceiving danger created by music. In comparison, the amygdala's role in recognition of fear in non-musical contexts has been well established. The present study sought to fill this gap in exploring how patients with amygdala resection recognize emotional expression in music. To this aim, we tested 16 patients with left (LTR; n = 8) or right (RTR; n = 8) medial temporal resection (including amygdala) for the relief of medically intractable seizures and 16 matched controls in an emotion recognition task involving instrumental music. The musical selections were purposely created to induce fear, peacefulness, happiness and sadness. Participants were asked to rate to what extent each musical passage expressed these four emotions on 10-point scales. In order to check for the presence of a perceptual problem, the same musical selections were presented to the participants in an error detection task. None of the patients was found to perform below controls in the perceptual task. In contrast, both LTR and RTR patients were found to be impaired in the recognition of scary music. Recognition of happy and sad music was normal. These findings suggest that the anteromedial temporal lobe (including the amygdala) plays a role in the recognition of danger in a musical context.

Changes in verbal and nonverbal memory following anterior temporal lobe surgery for refractory seizures: effects of sex and laterality

We studied the effects on verbal and nonverbal memory of anterior temporal lobe (ATL) surgery for epilepsy in 91 patients (46 men, 45 women), all of whom had left-hemisphere dominance for speech. Patients were divided into four groups according to sex and laterality of the excision. The memory tasks were administered shortly before surgery, 6 months postoperatively, and at a 2-year follow-up. Test scores were submitted to repeated-measures analyses of variance. We found that men treated with left temporal resection declined significantly in long-delay verbal memory after surgery, whereas no clear pre- to postoperative sex differences were found with respect to other verbal memory scores. Only the results on long-delay verbal memory confirm previous findings, showing a greater vulnerability of verbal memory to left ATL surgery in men than in women. Women with left temporal excisions obtained particularly poor scores on a long-delay nonverbal memory test preoperatively, but improved their performance on this test significantly after surgery. The seemingly gradual improvement during the 2-year follow-up suggests a plastic process.

Lateralization of Auditory Rhythm Length in Temporal Lobe Lesions

In the visual modality, short rhythmic stimuli have been proven to be better processed (sequentially) by the left hemisphere, while longer rhythms appear to be better (holistically) processed by the right hemisphere. This study was set up to see if the same holds in the auditory modality. The rhythm task as originally designed by Seashore was computerized and is part of the Fepsy Neuropsychological battery. This task was performed by 85 patients with intractable temporal lobe epilepsy (left TLE = 32; right TLE = 53) enrolled in the Dutch Collaborative Epilepsy Surgery Program. They performed the task before and 6 months after surgery. The task consists of 30 pairs of rhythmic patterns in 3 series of 10 items. The series contains patterns of 5, 6, or 7 notes. The purpose is to indicate whether the two patterns are the same or different. Reaction times are also measured. If the hypothesis is true, the short-item sequence will be better processed by patients with right temporal lobe epilepsy (nonimpaired left temporal lobe), the longer sequence will be better processed by the left temporal epilepsy group (nonimpaired right temporal lobe). No overall laterality effect on rhythm perception could be found and no difference was found between both test moments. IQ did not correlate with rhythm performance. However, there was an interaction effect of laterality and rhythm length on performance and reaction time. This effect can be explained by the increase after the operation of the score of the left focus group and a decrease in the right focus group on the longer rhythms. This effect was somewhat less strong in the reaction times: a clear tendency for faster reaction times after surgery in the left and longer reaction times in the right focus group. The effect could not be explained for by the difference in extent of resection in either temporal lobe. This study showed that memory for and discrimination of auditory rhythm is dependent on which hemisphere is used in processing. The effect could be demonstrated for the right hemisphere, which uses a holistic processing of stimuli, which outperforms the left in rhythms consisting of a long sequence. In left temporal resections an improvement occurs on the longer rhythms and in right temporal resections the performance on the longest rhythms decreases.

Spatial Localization after Excision of Human Auditory Cortex

Neurophysiological and animal ablation studies concur that primary auditory cortex is necessary for computation of the spatial coordinates of a sound source. Human studies have reported conflicting findings but have often suffered from inadequate psychophysical measures and/or poor lesion localization. We tested patients with unilateral temporal lobe excisions either encroaching on or sparing Heschl's gyrus (HG), quantifying lesion extent using anatomical magnetic resonance imaging measures. Subjects performed two tasks. In the localization task, they heard single clicks in a free-field spatial array subtending 180 degrees of azimuth and indicated the perceived location with a laser pointer. In the discrimination task, two clicks were presented, and subjects indicated if they were in the same or different position. As a group, patients with right temporal excision, either encroaching onto HG or not, were significantly impaired in both hemifields in both tasks, although this was not true for all individuals. Patients with left temporal resections generally performed normally, although some of the patients with left HG excision showed impaired performance bilaterally, especially in the discrimination task. This pattern stands in marked contrast to previous studies showing significant preservation of localization in hemispherectomized patients. We conclude that (1) contrary to hypotheses derived from animal studies, human auditory spatial processes are dependent primarily on cortical areas within right superior temporal cortex, which encompass both spatial hemifields; (2) functional reorganization may not take place after restricted focal damage but only after more extensive early damage; and (3) the existence of individual differences likely illustrates differential patterns of functional lateralization and/or recovery.

Increased intensity perception of aversive taste following right anteromedial temporal lobe removal in humans.

We used a modified version of the Spatial Taste Test to assess taste intensity perception in patients with either left or right temporal resection from the anteromedial temporal lobe (AMTL), and a group of control subjects. Sweet, sour, salty and bitter solutions were applied onto discrete locations of the tongue to stimulate either left or right fungiform, or left or right foliate papillae. Intensity ratings were assessed with the Labeled Magnitude Scale. Subjects also sipped 5 ml of each solution for whole mouth stimulation. Genetically based determinants of taste sensitivity were assessed with ratings of 6-n-propylthiouracil, and covaried from all analyses. As in previous studies, analysis of covariance indicated that the subjects in the right temporal group rated an aversive bitter taste as more intense than did subjects in the control group. In contrast, there were no group differences for sucrose ratings, suggesting that the AMTL may be involved preferentially in processing aversive compared with hedonic tastes. No group x side, or group x location effects were present. These results confirm that removal of the right AMTL in humans results in increased taste intensity/aversiveness perception. This finding complements existing literature indicating that the AMTL is important for processing aversive taste, and suggests that inhibitory mechanisms may play an important role in such processing.

Cognition and behavior after temporal lobectomy in pediatric patients with intractable epilepsy

The increased use of surgical intervention for intractable epilepsy during childhood has resulted in a critical need for information concerning possible cognitive and behavioral changes in pediatric patients after surgery. In this pilot study, comprehensive neuropsychologic evaluations were completed on nine children who had a temporal lobectomy for intractable epilepsy before 16 years of age. Performances before and after surgery were compared using cognitive and behavioral measures. Repeated measures analysis of variance did not indicate differences in performance on the basis of laterality of surgery, although the number of left (n = 5) vs right (n = 4) temporal resections was small. Paired comparison t tests, which included all patients, did not suggest marked changes in cognitive functioning after surgery, although decreases in delayed verbal memory were evident. Positive effects on quality of life during the first year after surgical intervention were suggested by reduced internalizing symptoms and increased social interaction. Replication of this study is recommended with a larger number of patients and multicenter collaboration.

Operant Conditioning after Temporal Lobe Lesions in Man: Conditional and Simple Discrimination Learning

Temporal lobe lesions have been found to impair the acquisition of classical conditional discrimination learning in an eyelid conditioning paradigm, with sparing of simple eyelid conditioning. In the present study, subjects with left or right temporal resections were compared with normal controls on two operant conditioning tasks using a conditional and a simple discrimination paradigm analogous to the previously reported classical conditioning tasks. Subjects with right temporal lesions, and to a lesser extent those with left temporal lesions were impaired relative to frontal lobe and control subjects in the acquisition of a conditional discrimination within an operant conditioning setting. A subsequent experiment showed that both left and right temporal lobe subjects were unimpaired on a simple oPerant discrimination task. These findings are compatible with theory relating hiPpocamPal function to the learning of if-then rules.

P300 Brain Activity in Seizure Patients Preceding Temporal Lobectomy

Event-related potentials were recorded over occipital and parietal scalp from 20 patients suffering from intractable partial complex seizures prior to undergoing a temporal lobectomy. Subjects were presented with language and nonlanguage visual stimuli using a divided-field, "odd-ball" paradigm. Although behavioral performance (button-press accuracy, reaction time, and running counts) was comparable across all groups (although accuracy was worse for those in the left temporal group), patients showed tremendous variability in both the amplitude and latency of the P300 response. Particularly notable was the observation that more slow wave activity was present among the patients than among the control subjects, and those scheduled for a left temporal resection evinced more amplitude reduction than those scheduled for a right temporal resection. In addition, a number of patients appeared not to show a P300 response at all. These results are discussed in the context of the utility of using noninvasive event-related potential measures to examine both memory impairment and the integrity of the neural structures that mediate memory functioning in certain patient populations.

Intracarotid Amobarbital (Wada) Test for Language Dominance: Correlation with Results of Cortical Stimulation

Eighty-eight patients had bilateral intracarotid amobarbital (Wada) testing to determine hemispheric dominance for language in preparation for epilepsy surgery, as well as unilateral extraoperative cortical electrical stimulation using subdural electrode arrays. In none of the patients with left dominance by Wada testing were language areas found with right-sided stimulation, but two patients with right dominance by Wada testing had language areas mapped on the left side. These findings suggest that left dominance by Wada testing is strong evidence for exclusive lateralization of language function in the left hemisphere, but there is concern about the ability of the Wada test to exclude the possibility of some left-sided language function despite apparent right-sided dominance. Patients with left dominance on Wada testing do not need cortical stimulation before extensive right temporal lobectomy, but we believe that patients with right or bilateral dominance on Wada testing should have cortical stimulation for localization of language areas if extensive left or right temporal or frontal resection is planned.