Effect of age of onset of temporal lobe epilepsy on the severity and the nature of preoperative memory deficits

The nature and severity of pre-operative memory deficits observed in unilateral temporal lobe epilepsy depend upon a number of variables. Among these variables, age of seizure onset seems to be important. The age at which the lesion is sustained could modify the normal functional organization of the brain. Many studies have examined the effect of age of onset on the severity of memory deficits but have seldom focused on the nature of such deficits (verbal/nonverbal) as a function of epileptic focus laterality. This study investigates the effect of age of onset on the nature and severity of memory impairments. Fifty-six epileptics with unilateral temporal lobe epilepsy and 20 normal subjects were administered a neuropsychological evaluation. Four groups of patients were constituted: left or right temporal lobe epilepsy with early (0-5 years) or late (10 years and over) age of seizure onset. The early group showed major verbal and nonverbal memory deficits. The late group presented minor specific deficits: essentially verbal deficits with left temporal lobe seizures and nonverbal deficits with right temporal lobe seizures. These results may be interpreted in the framework of ontogenesis theories of hemispheric specialization.     

Postictal Courses of Cognitive Deficits in Focal Epilepsies

Summary: Patients with epileptic seizures frequently complain of long-lasting cognitive impairment after a seizure. We evaluated this issue in 31 patients with epileptic seizures of a frontal (n = 8) or temporal lobe origin [right temporal lobe (RTL) n = 8/left temporal lobe (LTL) n = 151. Seizures were secondarily generalized in 18 patients. Computerized testing of verbal and nonverbal recognition memory was performed before the seizure, directly after postictal reorientation, and 30 min and 1 h later. Repeated testing of 14 healthy persons served as control. The following results were obtained: Depending on seizure generalization, postictal reorientation times were 1–45 min. Frontal lobe seizures showed no effect on postictal memory performances, but verbal and visual recognition memory was significantly decreased after temporal lobe seizures. Decrease in either verbal or visual memory and time of recovery were related to lateralization of seizure onset. Functional recovery after reorientation lasted 30 min to 1 h. The decrease in performance was more severe after generalized seizures. Decision times during memory performance were not significantly affected by the seizures. Temporal lobe seizures lead to circumscribed and long-lasting memory deficits, which can be assumed to affect patients'capabilities seriously. Preand postictal testing is a useful tool for determining postictal cognitive impairment and in determining the site of seizure onset.     

Seizures During Cognitive Testing in Patients with Temporal Lobe Epilepsy: Possibility of Seizure Induction by Cognitive Activation

In 18 of 185 patients under consideration for epilepsy surgery, 20 seizures were observed during neuropsychological evaluation. We wished to determine whether the task at seizure onset corresponded neuropsychologically to lateralization of the epileptic focus. The patients' characteristics and the circumstances of the seizures were as follows: Fourteen patients had right temporal lobe epilepsy (RTE) and four had left temporal lobe epilepsy (LTE). Although a wide range of cognitive functions had been tested, all but one seizure occurred during assessment of memory performance. In the RTE patients, 12 of 16 seizures occurred during visual memory testing. Two seizures were observed during a verbal memory task, and one seizure was observed during mental rotation. In two LTE patients, seizures were elicited during verbal memory testing. Two LTE patients with seizures during visual memory testing had speech dominance of the right hemisphere. This high correspondence between the eliciting performance and the focus localization suggests that cognitive performances ipsilateral to the epileptic focus may affect seizure threshold in focal epilepsies.     

Comparison of neuropsychological outcomes after selective amygdalohippocampectomy versus anterior temporal lobectomy

Transsylvian selective amygdalohippocampectomy (TSA) is an operative technique designed to spare unaffected brain tissue during surgical treatment for mesial temporal lobe epilepsy. In contrast to standard anterior temporal lobectomy (ATL), the advantages of TSA with respect to postoperative cognitive outcome are equivocal. We compared cognitive function before and after surgery in 49 patients with unilateral mesial temporal lobe seizures who underwent either ATL (n=17) or TSA (n=32). All patients received neuropsychological testing before and 1 year after surgery. The intelligence quotient (IQ) increased postoperatively in both surgical groups. Memory evaluation in the ATL group revealed a postoperative decline in nonverbal memory after right-sided resection and a postoperative decline in verbal memory after left-sided resection. In the TSA group, there was a slight postoperative decline only in verbal memory after left-sided resection, but other memory function was well preserved. In particular, there was significant postoperative improvement in verbal memory after right-sided resection. Overall, memory function was better preserved in the TSA group than in the ATL group.     

Memory outcome after selective amygdalohippocampectomy: a study in 140 patients with temporal lobe epilepsy

PURPOSE: The technique of selective amygdalohippocampectomy (SAH) was originally developed in epilepsy surgery to spare unaffected brain tissue from surgery, thus minimizing the cognitive consequences of temporal lobe surgery. The results of previous studies, however, are equivocal in this regard. This study evaluated memory after SAH in a large sample of patients with mesial temporal lobe epilepsy. METHODS: The 140 patients received material-specific memory tests before and 3 months after unilateral SAH. RESULTS: Significant declines in all aspects of verbal learning and memory were found particularly for the left resected group. With reliability-of-change indices, a high number of patients showed postoperative verbal memory declines, < or = 51% in left SAH and < or = 32% in right SAH. For left SAH, a higher preoperative verbal memory performance, a lower preoperative nonverbal memory score, an older age at surgery, and a later onset of epilepsy predicted a stronger decline in verbal memory. After right SAH, the risk for a verbal memory decline was slightly increased when patients had surgical complications or a presurgical evaluation with bilateral intrahippocampal depth electrodes. Results concerning nonverbal memory were less clear. CONCLUSIONS: The results clearly indicate, that particularly left SAH can lead to a significant decline in memory functions. Predictors of postoperative verbal memory were similar to those reported for temporal lobectomy. Postoperative deteriorations were broader and stronger in our study than in previous studies. We discuss methodologic differences (sample size, retest interval, extent of resection) and other factors as possible reasons.     

Memory function in focal epilepsy: a comparison of non-surgical, unilateral temporal lobe and frontal lobe samples

Three well-matched groups of non-surgical, pharmacologically controlled epileptic patients with unilateral seizure foci in either the left temporal lobe, the right temporal lobe or a frontal lobe, and a normal control group were compared on several verbal and non-verbal memory tasks. Results revealed significant impairment of verbal memory in left temporal epileptic subjects, and significant impairment of non-verbal, visual memory in right temporal epileptic subjects. Seizure patients with unilateral frontal lobe foci did not differ from the control sample on any measure. Results support previous research which emphasizes the importance of temporal lobe systems in memory function. The findings are discussed with regard to the nature and specificity of the observed deficits.     

Usefulness of verbal selective reminding in distinguishing frontal lobe memory disorders in epilepsy

Frontal lobe memory disorders are distinguished from hippocampal memory disorders by poor organization of encoding and retrieval, among other things. Because the verbal Selective Reminding Test (SRT) has a metamemory ("remembering-to-remember") component, it may be useful in distinguishing frontal from temporal lobe memory disorders in patients with intractable epilepsy. Thirty-four patients with frontal lobe epilepsy (FLE) and 34 with temporal lobe epilepsy (TLE) underwent a comprehensive neuropsychological evaluation that included multiple memory and executive function tests. Patients with FLE performed significantly worse than those with TLE on SRT measures and Wechsler Memory Scale, Third Edition, Logical Memory (LM II), but not on other verbal and nonverbal memory tests. Furthermore, SRT and LM-II were significantly correlated with executive function measures. These findings have both theoretical and practical implications: (1) the memory impairment observed in frontal lobe disorders may be due, in part, to deficits in organizational strategy, monitoring, and remembering-to-remember, and (2) SRT and LM-II may be useful tests to differentiate frontal from temporal lobe memory disorders.     

Neuropsychological Effect of Temporal Lobe Resection in Preadolescent Children with Epilepsy

Summary: Purpose : Numerous studies have demonstrated changes in cognitive, memory, and language functioning in adults and adolescents after temporal lobectomy, yet little information is available regarding neuropsychological outcome in preadolescent children.
Methods : We studied pre-and postoperative neuropsychological test results from 14 children who underwent temporal lobe resection for intractable epilepsy at age 7–12 years (mean 9.4 years).
Results : Thirteen patients (93%) had no seizures or less than one seizure a year at follow-up 23-48 months (mean 34 months) after operation. Postoperative neuropsychological testing was performed 6–9 months (mean 7 months) after surgery in 13 patients and 36 months after the first operation in 1 patient who underwent two-stage resection of a tumor. Verbal, Performance, and Full Scale IQ were initially in the low-average range, with no significant change across the pre-and postoperative evaluations. Immediate verbal memory performance decreased significantly in children who initially performed above the median preoperatively and tended to decrease in children who had left rather than right temporal lobe resection. Significant postoperative decreases in delayed memory scores were independent of preoperative ability or side of resection.
Conclusions : Our small study suggests vulnerability to postoperative decline in immediate verbal memory scores in preadolescent children who have higher baseline immediate memory function or undergo left rather than right temporal lobe resection, similar to that observed in adolescents in adults. The entire group exhibited a statistically significant decrease in delayed verbal memory. Study of larger series of patients will be important to clarify further the short-and long-term risks and benefits of temporal lobe resection in childhood.     

Hemisphere memory of concrete and abstract information determined with the intracarotid Sodium Amytal test

An extended version of the bilateral intracarotid Sodium Amytal test was administered pre-operatively to 13 patients with intractable complex partial epileptic seizures, to determine cerebral hemisphere speech and memory. There were 6 patients with left temporal lobe lesions and 7 patients with right temporal lobe lesions. Amobarbital (175 mg, 10%), injected on 2 occasions, determined the left hemisphere to be speech dominant in all cases. Memory assessed with recall, cued recall, and recognition of concrete/abstract words and pictures, was studied on 3 occasions: in a baseline test considered to indicate the degree of patient cooperation and the bilateral hemisphere memory; in a right hemisphere Amytal test; and in a left hemisphere Amytal test. The specific data pattern obtained, that abstract pictorial information is most efficiently processed by an intact right hemisphere and that verbal information is processed best by an intact left hemisphere, demonstrates the reliability of the approach taken here to present abstract and concrete to be remembered information.     

Wada memory performance predicts seizure outcome after epilepsy surgery in children

PURPOSE: Wada memory asymmetries were examined in children from four comprehensive epilepsy surgery centers who subsequently underwent epilepsy surgery to determine whether Wada memory performance could predict degree of seizure relief in children. METHODS: One hundred fifty-six children (between ages 5 and 16 years) with intractable epilepsy underwent Wada testing before resective epilepsy surgery (93 within the left hemisphere, and 63 within the right hemisphere). Memory stimuli were presented soon after intracarotid amobarbital injection, and recognition memory for the items was assessed after return to neurologic baseline. Eighty-eight children underwent unilateral temporal lobe resection, and 68 had extratemporal lobe resections. One hundred four (67%) children were seizure free (Engel class I), and 52 (33%) were not seizure free (Engel classes II-IV) at follow-up (mean follow-up interval, 2.3 years). RESULTS: Seizure-free children recalled 19.3% more Wada memory items after ipsilateral injection than did non-seizure-free children (p = 0.008). If analysis was restricted to youngsters with temporal lobectomies (TLs), seizure-free children recalled 27.7% more items after ipsilateral injection than did non-seizure-free TL children (p = 0.004). With regard to individual patient prediction, 75% of children who had memory score asymmetries consistent with the seizure focus were seizure free. In contrast, only 56% of children whose memory score asymmetries were inconsistent with the seizure focus were seizure free (p = 0.01). CONCLUSIONS: Results suggest that Wada memory performance asymmetries are related to the degree of seizure relief after epilepsy surgery in children and adolescents.     

Efficacy of hippocampal transection for left temporal lobe epilepsy without hippocampal atrophy

We describe a case of left temporal lobe epilepsy without hippocampal atrophy. A 31-year-old woman presented with typical symptoms of complex partial seizures. Magnetic resonance imaging demonstrated slightly obscure internal structures in the left hippocampus. Scalp electroencephalography revealed interictal epileptiform discharges in the left temporal lobe. A Wada test with propofol determined the language-dominant hemisphere to be the left. Intraoperative electrocorticography revealed active epileptic discharges in the hippocampus and the anterior temporal basal area. The hippocampal epileptic area was treated with multiple transection, which led to the complete cessation of epileptic discharges. After surgery, the Rey Auditory Verbal Learning Test score decreased from 12 to 9. However, it returned to the preoperative level 6months after surgery. We describe this case as a typical example demonstrating the efficacy of hippocampal transection for seizure control and the preservation of verbal memory.     

Behavioral activation of human hippocampal EEG: Relationship to recent memory

Behaviorally activated EEG was recorded from each hippocampus in 17 epilepsy surgery patients with unilateral (11 left, 6 right) mesial temporal lobe (MTL) seizure onset and correlated with preoperative material-specific memory test performances. Whole-band power (1–30 Hz) was recorded and subjected to spectral analysis under three conditions: (a) eyes closed resting, (b) eyes open with a verbal task, and (c) eyes open with a nonverbal task. Significantly less EEG desynchronization was observed in the epileptogenic hippocampus during the verbal activation condition but not during the eyes-open nonverbal task. Decreased EEG reactivity in the left hippocampus during verbal activation was correlated significantly with verbal memory test impairment among patients with left MTL seizure onset. However, similar relationships were not obtained between right seizure focus patients and performance on a visuospatial learning test. Results confirm the association of left MTL structures with verbal memory functions and emphasize the difficulty in demonstrating a consistent relationship between right MTL structures and visuospatial memory performance.     

Intracarotid Amobarbital Procedure as a Predictor of Material-Specific Memory Change After Anterior Temporal Lobectomy

Summary: Memory testing during the intracarotid amobarbital procedure (IAP) is used extensively to identify temporal lobe surgery candidates "at risk" for developing severe postoperative anterograde amnesia. However, the utility of the IAP in predicting commonly observed material-specific memory deficits has not been thoroughly investigated. We examined the utility of contralateral IAP memory testing, as an index of the functional capacity of the surgical temporal lobe, to predict postoperative material-specific memory changes on the Wechsler Memory Scale-Revised (WMS-R) in patients with left hemisphere speech dominance undergoing left (n = 32) and right (n = 31) temporal lobectomy (TL). Left TL patients who "passed" contralateral IAP memory testing (368% recognition of memory items) had significantly greater verbal memory decrements than those who "failed" the IAP, presumably as a result of removal of functional tissue. A similar relationship between contralateral IAP performance and visual memory performance was not observed among right TL patients. Thus, the functional adequacy of the tissue to be resected appears to be inversely related to postoperative verbal memory decrement, at least among left TL patients. This relationship is consistent with results of recent studies demonstrating an inverse relationship between verbal memory decrements after left TL and preoperative neuropsychological verbal memory performance, magnetic resonance imaging (MRI) hippocampal volumes, and degree of mesiotemporal sclerosis (MTS).     

Memory performance following unilateral electrical stimulation of the hippocampus in a child with right temporal lobe epilepsy

Verbal and visual memory performance was evaluated during unilateral stimulation of the hippocampus in an 11-year-old child with complex partial epilepsy associated with a right mesial temporal lobe focus. Memory was assessed during left and right hippocampal stimulation as well as preoperatively and 6-months postoperatively following anterior temporal lobe resection including removal of the anterior portion of the hippocampus. Stimulation of the left hippocampus resulted in a mild to moderate decrement in both verbal and visual memory performance as compared with a right hippocampal stimulation. In addition, stable or improved performance on memory assessment as well as general neuropsychological evaluation was noted 6 months postoperatively. Taken together, these data suggest that, in this child with early seizure onset (8 months of age), visual learning/memory functions shifted to the contralateral hippocampus and associated structures following damage to the right mesial temporal lobe structures. In addition, verbal learning/memory continues to be mediated by the left hippocampus, as expected. Thus, it appears that, as in the case of language lateralization, there may be a distinct subset of temporal lobe seizure patients (i.e., early seizure onset, high seizure frequency, chronic duration) in whom the brain has the capacity to shift material-specific memory functions to the contralateral mesial temporal lobe structures.     

Cognitive changes in people with temporal lobe epilepsy over a 13-year period

ObjectivesThe aims of our study were to evaluate cognitive decline in people with temporal lobe epilepsy over a period of 13 years and to determine what clinical and treatment characteristics may have been associated with these.Materials and methodsThirty-three individuals with temporal lobe epilepsy underwent the same neuropsychological assessment of verbal and nonverbal memory, attention, and executive functions using the same cognitive test battery as one used 13 years ago. Long-term verbal and nonverbal memory was tested four weeks later. Results were compared with those carried out 13 years earlier.ResultsThere was no significant change in verbal and verbal–logical memory tests; however, nonverbal memory worsened significantly. Long-term verbal memory declined for 21.9% of participants, long-term verbal–logical memory for 34.4%, and long-term nonverbal memory for 56.3%. Worsening of working verbal and verbal–logical memory was associated with longer epilepsy duration and lower levels of patients' education; worsening of verbal delayed recall and long-term verbal–logical memory was associated with higher seizure frequency. Decline in long-term nonverbal memory had significant association with a longer duration of epilepsy. The worsening of reaction and attention inversely correlated with the symptoms of depression.ConclusionOver a 13-year period, cognitive functions did not change significantly. Good seizure control and reduced symptoms of depression in this sample of people with temporal lobe epilepsy were associated with better cognitive functioning. The predictors of change of cognitive functions could be complex and require further study.     

Can postictal memory predict postoperative memory in patients with temporal lobe epilepsy?

We investigated the contribution of postictal memory testing for lateralizing the epileptic focus and predicting memory outcome after surgery for temporal lobe epilepsy (TLE). Forty‐five patients with TLE underwent interictal, postictal, and postoperative assessment of verbal and nonverbal memory. Surgery consisted of anterior temporal lobectomy (36), selective isolated amygdalohippocampectomy (6), or amygdalohippocampectomy coupled to lesionectomy (3). Postictal and postoperative but not interictal memory were significantly lower in left TLE than in right TLE. Nonverbal memory showed no significant difference in left TLE versus right TLE in all conditions. Postictal memory was significantly correlated with postoperative memory, but the effect disappeared when the lateralization of the focus was considered. Postictal verbal memory is a useful bedside tool that can help lateralize the epileptic focus. Larger studies are needed to further estimate its predictive value of the postoperative outcome.     

The effects of duration of intractable epilepsy on memory function

We assessed whether duration (time since diagnosis) of intractable epilepsy is associated with progressive memory loss in 250 individuals with left or right temporal lobe epilepsy and those diagnosed with psychogenic nonepileptic seizures. Verbal and nonverbal memory function was assessed using several memory assessment measures administered to all individuals as part of a larger neuropsychological assessment. Multivariate multiple regression analyses demonstrated that duration of temporal lobe epilepsy and age of seizure onset are significantly related to verbal memory deficits in patients with epilepsy. The interaction between duration of epilepsy and diagnostic group was nonsignificant, as was the interaction between age at spell onset and diagnostic group. As measured by several neuropsychological memory tests, duration of disease adversely affects verbal memory performance in patients diagnosed with temporal lobe epilepsy. Our study also supports the notion that age at seizure onset significantly affects verbal memory performance in this population. These results have implications for the strategy of treatment and counseling of patients with intractable temporal lobe epilepsy.     

The effects of cognitive rehabilitation on memory outcome after temporal lobe epilepsy surgery

OBJECTIVE: Epilepsy surgery is a valuable treatment option for patients with pharmacoresistant epilepsy, but seizure freedom is often achieved at the cost of cognitive impairments caused by surgery. The aim of this study was to investigate the short-term effects of cognitive rehabilitation on memory outcome after temporal lobe epilepsy surgery. METHODS: Two groups of patients who underwent temporal lobe resection, one followed (n=55) and one not followed (n=57) by postoperative rehabilitation, were evaluated with respect to memory and attention before and 3 months after temporal lobe surgery. The groups came from different epilepsy centers, but were largely matched with respect to age, sex, type of surgery, and seizure outcome. RESULTS: After surgery, 78% of the patients were seizure-free. Repeated-measures MANOVA revealed a significant "side x surgery" effect on verbal recognition and a "rehabilitation x surgery" effect on verbal learning and recognition. There were no effects for loss in verbal delayed recall or figural memory. Detailed analyses indicated gains as a result of rehabilitation, particularly after right temporal lobe surgery. Attention generally improved. The risk of manifesting losses in verbal memory was about four times higher without than with rehabilitation. CONCLUSIONS: Rehabilitation can counteract the verbal memory decline that is normally seen after temporal lobe resection. Its positive effects were evident particularly with respect to the more cortically associated aspects of verbal learning rather than to the mesial aspects of long-term consolidation/retrieval. Figural memory was not affected at all, and attention improved independent of rehabilitation. Interestingly, left temporal lobe-resected patients, who were most in need of an efficacious rehabilitation, profited less than right temporal lobe-resected patients, indicating that left-sided surgery may reduce the capacity needed for efficient training of verbal memory. Thus, rehabilitation has a positive effect on memory outcome, but its usefulness for risk groups and the question of whether training should be performed after or possibly before surgery are debatable. Further research should also address different interventions, longer-term outcome, and the carryover effects on everyday functioning.     

Memory outcome after left anterior temporal lobectomy in patients with expected and reversed Wada memory asymmetry scores

PURPOSE: The ideal candidate for anterior temporal lobectomy surgery shows a Wada memory asymmetry (WMA) score characterized by better memory performance in the hemisphere contralateral to the seizure focus relative to the ipsilateral (surgical) hemisphere. However, some surgical candidates show a reversed WMA or better Wada memory performance in the hemisphere of surgical interest relative to the hemisphere contralateral to the seizure focus. To date, no data are available contrasting memory and seizure outcome for these two Wada groups. The present study compared memory and seizure outcome after left anterior temporal lobectomy (L-ATL) in patients showing expected and reversed WMA scores, and also examined the relationship of the individual hemisphere Wada memory scores for predicting verbal memory outcome after L-ATL. METHODS: We compared 6-month postoperative verbal memory change scores and seizure outcome in L-ATL patients with either an expected (n=12) or reversed WMA (n=9) pattern on Wada memory testing. RESULTS: L-ATL patients showing a reversed WMA score had a poorer verbal memory outcome and poorer seizure control after surgery compared with patients showing a WMA score in the expected direction. CONCLUSIONS: L-ATL patients with a reversed WMA score have a greater risk for memory morbidity and poorer seizure outcome than do patients with a WMA score in the expected direction. The WMA score was the best predictor of memory outcome after L-ATL. When the WMA score is not considered, both individual Wada hemisphere scores (contralateral and ipsilateral) provided significant and independent contribution to predicting postoperative verbal memory functioning. These findings are discussed in the context of the functional reserve and hippocampal adequacy models of memory change after temporal lobectomy.     

Pre- and postoperative neuropsychological profiles in children and adolescents with temporal lobe epilepsy

PURPOSE: To evaluate the neuropsychological performance of children before and after temporal lobe resection (TLR). METHODS: Memory, attention, language, and visuoconstructive abilities were examined in 20 children (age 10-16 years) before, and 3 and 12 months after TLR (right, n = 10; left, n = 10; two-thirds anterior resection, n = 16; amygdalohippocampectomy, n = 4). Preoperative performance was compared with data of 30 age-matched healthy children; changes in performance after surgery were determined by repeated-measurement multivariate analysis of variance (MANOVA) and by use of reliable change indices (RCI). RESULTS: Preoperatively, no differences were observed between patients and controls in verbal and figural memory performance. Children with temporal lobe epilepsy (TLE), however, and particularly those with a left temporal focus, showed significantly reduced language performance. Repeated-measurement statistics indicated that memory performance did not change after surgery, whereas language performance and attention significantly improved 3 months and 1 year after surgery, respectively. Individual evaluations of memory showed gains in five children and deterioration in four children. Poor seizure control appeared the decisive variable characterizing children with losses in memory. CONCLUSIONS: Compared with adults, pre- and postoperative memory data suggest less pronounced hemispheric differences in school-age children with TLE. The results raise the possibility that children have a lower risk of memory deterioration after TLR, which may be due to their larger potential for cerebral plasticity.