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.     

Memory outcome 2 years after anterior temporal lobectomy in patients with drug-resistant epilepsy

PURPOSE: Memory decline is often observed after anterior temporal lobectomy (ATL), particularly in patients with dominant hemisphere resections. However, the follow-up length has been 1 year or less in most studies. Our aims were to examine postoperative memory changes over a longer period and to identify baseline demographic and clinical predictors of memory outcome. METHODS: We administered material-specific memory tests at baseline, and 1 and 2 years after surgery to 82 consecutive right-handed patients (52% males) who underwent ATL for drug-resistant temporal lobe epilepsy (TLE) (35 left, 47 right) after a non-invasive presurgical protocol. Repeated measures multivariate analysis of variance (RM-MANOVA) was used to examine the relationship between changes in memory tests scores over time and side of TLE and pathology. Also, standardized residual change scores were calculated for each memory test and entered in multiple linear regression models aimed at identifying baseline predictors of better memory outcome. RESULTS: RM-MANOVA revealed a significant change in memory test scores over time, with an interaction between time and side of surgery, as 2 years after surgery patients with RTLE were improved while patients with LTLE were not worse as compared with baseline. Pathology was not associated with changes in memory scores. In multiple regression analysis, significant associations were found between right TLE and greater improvement in verbal memory, younger age and greater improvement in visuospatial memory, and male gender and greater improvement in both verbal and visuospatial memory. CONCLUSIONS: Our results suggest that the long-term memory outcome of TLE patients undergoing ATL without invasive presurgical assessment may be good in most cases not only for right-sided but also for left-sided resections.     

Memory outcome after selective amygdalohippocampectomy in patients with temporal lobe epilepsy: one-year follow-up

Summary:  Purpose: In a previous study we reported clinically significant memory declines 3 months after selective amygdalohippocampectomy (SAH) in 140 patients with mesial temporal lobe epilepsy, particularly if the resection was left-sided. We supposed that the observed postoperative impairments might have reflected acute effects of surgery. Therefore we evaluated in the present study whether a recovery can be found 1 year after surgery.
Methods: Verbal and nonverbal memory functions were assessed in 115 patients before and 3 and 12 months after unilateral SAH.
Results: No recovery of postoperative verbal memory declines was found in the left-SAH group. Clinically meaningful losses were still evident in 33 to 50% of patients. In right-SAH patients, a recovery of verbal memory was indicated, and effects of surgical complications were no longer evident. One year after surgery, the corresponding preoperative performance was the only significant predictor of a postoperative change in the left-SAH group.
Conclusions: Verbal memory decline observed 3 months after left SAH is persistent 1 year after surgery. Declines in verbal memory, which were observed in some right-SAH patients at the short-term follow-up, seem to be temporary.     

选择性杏仁核-海马切除术对内侧颞叶癫痫病人神经心理学的影响

目的 探讨选择性杏仁核-海马切除术（SAH）对内侧颞叶癫痫病人认知功能的影响。方法 回顾性分析2009年1月~2017年5月接受SAH治疗的67例内侧颞叶癫痫的临床资料,术前、术后3个月和术后1年均行详细的神经心理学评估,包括智商、记忆商和语言功能。结果 36例行左侧SAH,31例行右侧SAH。术后1年,癫痫控制效果达到Engel分级Ⅰ级50例,Ⅱ级7例,Ⅲ级8例,Ⅳ级2例。术后3个月,左侧手术病人言语功能、记忆商较术前明显降低（P<0.05）,右侧手术病人言语理解指数、语义流畅性测验明显改善（P<0.05）;术后1年,无论是左侧手术病人,还是右侧手术病人,智商、记忆商、言语功能较术后3个月略改善（P>0.05）;手术前后视觉记忆均无明显变化（P>0.05）。结论 海马硬化性内侧颞叶癫痫行SAH后,左侧手术病人会出现比较明显的言语和记忆功能减低。     

Visual memory deficits in temporal lobe epilepsy: toward a multifactorial approach.

Temporal lobe epilepsies (TLE) are associated with material-specific memory deficits depending on the side of seizure origin. However, while verbal memory deficits have been consistently reported in patients with left-sided TLE, the relationship between visual memory deficits and right-sided TLE is more complex. Here, we review factors that influence the pattern of lateralization and the nature of visual memory impairments in TLE and discuss the possible relationship between these deficits and perceptual impairments in TLE patients.     

Differential effects of temporal pole resection with amygdalohippocampectomy versus selective amygdalohippocampectomy on material-specific memory in patients with mesial temporal lobe epilepsy

PURPOSE: In the surgical treatment of mesial temporal lobe epilepsy, there is converging evidence that individually tailored or selective approaches have a favorable cognitive outcome compared to standard resections. There is, however, also evidence that due to collateral damage, selective surgery can be less selective than suggested. As part of a prospective transregional research project the present study evaluated the outcome in memory and nonmemory functions, following two selective approaches: a combined temporal pole resection with amygdalohippocampectomy (TPR+) and transsylvian selective amygdalohippocampectomy (SAH). METHODS: One year after surgery, cognitive outcomes of postoperatively seizure-free patients with mesial TLE and hippocampal sclerosis, who underwent either TPR+ (N = 35) or SAH (N = 62) in two German epilepsy centers (Bonn/Berlin), were compared. RESULTS: Repeated measurement MANOVA and separate post hoc testing indicated a double dissociation of verbal/figural memory outcome as dependent on side and type of surgery. Verbal memory outcome was worse after left-sided operation, but especially for SAH, whereas figural memory outcome was worse after right-sided operation, preferentially for TPR+. Attention improved independent of side or type of surgery, and language functions showed some improvement after right-sided surgeries. DISCUSSION: The results indicate a differential effect of left/right SAH versus TPR+ on material-specific memory insofar as transsylvian SAH appears to be favorable in right and TPR+ in left MTLE. The different outcomes are discussed in terms of a different surgical affection of the temporal pole and stem, and different roles of these structures for verbal and figural memory.     

Pre- and postoperative verbal memory in pediatric patients with temporal lobe epilepsy

Outcome studies concerning memory after pediatric temporal lobe surgery in the treatment of epilepsy are rare and have not yielded consistent results. In the present study, 55 children and adolescents with temporal lobe epilepsy (TLE; 26 left, 29 right, 6-17 years) performed a verbal memory test before and 3 as well as 12 months after different types of temporal lobe resections (anterior lobectomy, amygdalo-hippocampectomy (AH), lesionectomy (LX)). Groups did not significantly differ before surgery. Three months after surgery, the left resected group showed a decline in learning and delayed recall, and performed significantly lower than the right resected group. Recoveries were evident 1 year after surgery. The postoperative memory declines were associated with a left-sided resection and a higher preoperative performance. Comparisons on the different resection types suggest a special risk in patients undergoing a left-sided AH. In summary, our results indicate a functional association of verbal memory functions with the left temporal lobe similar to findings in adult patients. Declines after left-sided temporal resections seem to be reversible at least for part of the children, perhaps due to the greater plasticity of the immature brain.     

Memory functions following surgery for temporal lobe epilepsy in children

Surgical treatment appears to improve the cognitive prognosis in children undergoing surgery for temporal lobe epilepsy (TLE). The beneficial effects of surgery on memory functions, particularly on material-specific memory, are more difficult to assess because of potentially interacting factors such as age range, intellectual level, left-handedness, type of surgery and seizure outcome. This study investigated memory functions in 20 right-handed children who had left or right-temporal lobe surgery - including hippocampectomy - and became seizure-free. The neuropsychological evaluation included tests measuring verbally and visually mediated episodic memory, everyday memory as well as attention/working memory and language/semantic memory. We also assessed the relationships between age of seizure onset, general cognitive ability and memory functions. Children with TLE showed poor memory efficiency before surgery that tended to improve about 1 year after surgery. We found a material-specific memory effect, especially after surgery-9 (out of 12) children with left TLE had worse verbal memory results while 5 (out of 8) with right TLE had worse visual memory results. Post-operatively, most children had poor everyday memory performance on the Rivermead Behavioural Memory Test. No significant relationship was observed between episodic memory scores and age of epilepsy onset but children with early onset remained with lower Performance IQ values, Rey's figure copy scores and naming performances after surgery. Surgery significantly improved all the attention/working memory scores, some verbal episodic memory tasks and naming test performances. A different pattern of episodic and semantic memory limitations related to left or right TLE was observed.     

Bilateral hippocampal atrophy: consequences to verbal memory following temporal lobectomy

BACKGROUND: Bilateral hippocampal damage is a risk factor for memory decline after anterior temporal lobectomy (ATL). OBJECTIVE: To investigate verbal memory outcome in patients with temporal lobe epilepsy (TLE) with either unilateral or bilateral hippocampal atrophy as measured by MRI. METHODS: The authors selected 60 patients with TLE who had undergone ATL (left = 31, right = 29). They determined normalized MRI hippocampal volumes by cursor tracing 1.5-mm slices from three-dimensional MRI acquisition. Hippocampal volumes were defined as atrophic if the volumes were below 2 SD for control subjects. Bilateral hippocampal atrophy was present in 10 patients with left TLE and 11 patients with right TLE. The authors assessed acquisition, retrieval, and recognition components of verbal memory both before and after ATL. RESULTS: Groups did not differ across age, education, intelligence, age at seizure onset, or seizure duration. Seizure-free rates after ATL were 70% or higher for all groups. Before surgery, patients with left TLE displayed worse verbal acquisition performance compared with patients with right TLE. Patients with left TLE with bilateral hippocampal volume loss displayed the lowest performance across all three memory components. After surgery, both groups of patients with left TLE exhibited worse verbal memory outcome compared with patients with right TLE. Bilateral hippocampal atrophy did not worsen outcome in the patients with right TLE. A higher proportion of patients with left TLE with bilateral hippocampal atrophy experienced memory decline compared with the other TLE groups. CONCLUSION: Bilateral hippocampal atrophy in the presence of left TLE is associated with worse verbal memory before and after ATL compared with patients with unilateral hippocampal volume loss or right TLE with bilateral hippocampal volume loss.     

Verbal retention lateralizes patients with unilateral temporal lobe epilepsy and bilateral hippocampal atrophy

PURPOSE: To examine the lateralization utility of preoperative verbal retention in patients with and without bilateral hippocampal atrophy. METHODS: The sample consisted of 74 patients with EEG-defined unilateral temporal lobe epilepsy (TLE) who had also undergone volumetric magnetic resonance imaging (MRI). Verbal retention was operationalized by the Logical Memory percentage retention subtest (LM%) of the Wechsler Memory Scale. Patients were divided into groups with (a) bilaterally normal hippocampal volumes, (b) unilateral atrophy, or (c) bilateral atrophy. Two different thresholds (empirically derived vs. normative) were used to lateralize on the basis of LM%. LM% lateralization was then examined by group using chi2, sensitivity, positive predictive values, and odds ratios. Analyses were also conducted separately in the subset of patients who were seizure free after surgery. RESULTS: Mean LM% performance was significantly lower in patients with left versus right TLE in the subset with bilateral hippocampal atrophy (p = 0.018), but not in patients with a normal MRI (p = 0.918) or unilateral atrophy (p = 0.087). The odds of a correct lateralization by LM% increased from 1.67 in patients with normal MRI to 36.11 in patients with bilateral hippocampal atrophy. The power of a right and left lateralization prediction by LM% was 100% and 75%, respectively, in patients with bilateral hippocampal atrophy. Similar results were obtained when analysis was restricted to patients who were seizure free after surgery. CONCLUSIONS: Preoperative verbal retention as measured by LM% may provide meaningful lateralization information in patients who are difficult to lateralize via MRI.     

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.     

A comparison of two fMRI methods for predicting verbal memory decline after left temporal lobectomy: Language lateralization versus hippocampal activation asymmetry

Purpose: Language lateralization measured by preoperative functional magnetic resonance imaging (fMRI) was shown recently to be predictive of verbal memory outcome in patients undergoing left anterior temporal lobe (L‐ATL) resection. The aim of this study was to determine whether language lateralization or functional lateralization in the hippocampus is a better predictor of outcome in this setting. Methods: Thirty L‐ATL patients underwent preoperative language fMRI, preoperative hippocampal fMRI using a scene encoding task, and pre‐ and postoperative neuropsychological testing. A group of 37 right ATL (R‐ATL) surgery patients was included for comparison. Results: Verbal memory decline occurred in roughly half of the L‐ATL patients. Preoperative language lateralization was correlated with postoperative verbal memory change. Hippocampal activation asymmetry was strongly related to side of seizure focus and to Wada memory asymmetry but was unrelated to verbal memory outcome. Discussion: Preoperative hippocampal activation asymmetry elicited by a scene encoding task is not predictive of verbal memory outcome. Risk of verbal memory decline is likely to be related to lateralization of material‐specific verbal memory networks, which are more closely correlated with language lateralization than with overall asymmetry of episodic memory processes.     

Preserved memory in temporal lobe epilepsy patients after surgery for low-grade tumour. A pilot study

The objective was to carry out a pilot study exploring memory outcome in patients with temporal lobe epilepsy (TLE) and low-grade tumour. A prospective study using a competence-related memory assessment was carried out in the Laboratory of Neuropsychology, Epilepsy Center and Neurosurgical Department of the “C. Besta” National Neurological Institute in 24 TLE patients undergoing surgical resection for left (n=12) or right (n=12) low-grade tumours and 36 healthy subjects. Patients underwent mesial or lateral temporal lobe lesionectomy. Neuropsychological tests exploring verbal and visual short-term memory, learning, delayed recall and ability to control interference in memory were applied. Before and after surgery, significant verbal impairment was present in left TLE patients compared to controls and right TLE patients, and visual deficits were present in both groups compared to controls. After surgery, there was no significant decrease in mean verbal or visual memory scores related to the operated side. Some memory abilities subserved by the contralateral temporal lobe improved. Postoperative memory scores were related to preoperative scores, side of operation, age and education. In patients with TLE and low-grade tumour, temporal lobe surgery does not necessarily induce memory deficits. Improvement of memory abilities subserved by the unoperated temporal lobe may be expected.     

Clinical Applications of Magnetic Resonance Spectroscopy

Summary: Magnetic resonance spectroscopy (MRS) is a new tool for evaluation of patients with epilepsy, demonstrating abnormalities of energy and lipid metabolism ictally and, more recently, interictally. These metabolic abnormalities include increased inorganic phosphate, pH, and decreased phosphomono-esters as determined by ³¹P MRS, as well as decreased N- acetylaspartate determined by ¹H MRS. Furthermore, increased lactic acid has been detected postictally. These metabolic changes appear to be confined to the region of seizure origination and can be detected interictally. Therefore, they can be used for lateralization of the epileptogenic focus. Ongoing research suggests that these abnormalities may also be useful in localization of the focus, demonstrating metabolic alterations in temporal lobe epilepsy (TLE) similar to those in neocortical epilepsy. However, further technical development will be required before the goal of using these techniques for localization of the epileptogenic focus can be realized. For TLE lobe epilepsy at least, the clinical utility of 'H MRS to lateralize the seizure focus has clearly been demonstrated by several centers. The consistent findings in TLE suggest that 'H MRS is ready to become part of the evaluation process of patients with medically refractory epilepsy being evaluated for seizure surgery.     

The selective amobarbital test in the anterior choroidal artery: perfusion pattern assessed by intraarterial SPECT and prediction of postoperative verbal memory

To screen for patients at risk for memory decline after temporal lobe epilepsy (TLE) surgery, selective amobarbital procedures, such as injection into the anterior choroidal artery (ACA-IAT), are sometimes used. We investigated the extent of the territory affected during ACA-IAT and its predictive value with respect to postoperative memory. Seventeen patients with TLE underwent ACA-IAT. In 9 of 17 patients, intraarterial SPECT co-registrated to MRI allowed delineation of amobarbital-perfused structures. Another subgroup of 9 of 17 patients underwent anterior temporal lobectomy. Verbal memory was tested pre- and postoperatively and during ACA-IAT. Major variations in the ACA-IAT perfusion pattern occurred and were not correlated with the verbal memory scores during ACA-IAT. Postoperatively, no patient experienced a severe verbal memory decline, but individual postoperative performance was not correlated with results during ACA-IAT. Our study suggests that ACA-IAT can be used to screen for severe postoperative amnesia in inconclusive cases, but cannot predict individual outcome, even when the perfusion pattern is taken into account.     

导航引导下保留侧脑室完整的颞叶癫痫手术26例体会

目的探讨神经导航下保留侧脑室完整的前颞叶海马、杏仁核切除术治疗颞叶癫痫的效果。方法将26例神经导航下保留侧脑室完整的前颞叶海马切除术后患者的术前Wada试验评估、术后并发症及癫痫控制情况进行分析。结果术后随访时间24～36月,EngelⅠ级22例（85％）,EngelⅡ级3例（11％）,EngelⅢ例（4％）。术后1例（4％）患者出现记忆减退症状,4例患者发生视野缺损。结论同时切除海马、杏仁核的标准前颞叶切除术为外科治疗颞叶癫痫的有效术式,术前Wada试验评估能很好的预测手术对患者记忆功能的影响,保留侧脑室完整的术式可减少视野缺损的发生。     

Material-specific lateralization of working memory in the medial temporal lobe

Mnemonic deficits in patients with medial temporal lobe (MTL) damage arising from temporal lobe epilepsy (TLE) are traditionally constrained to long-term episodic memory, sparing short-term and working memory (WM). This view of WM as being independent of MTL structures has recently been challenged by a small number of patient and neuroimaging studies, which have focused primarily on visual and visuospatial WM. In the present study we investigated material-specific lateralization of WM in 96 patients with unilateral damage to MTL stemming from TLE (56 left) and 30 control subjects using a pair of matched verbal and visuospatial supraspan tasks. Patients with unilateral TLE were impaired on both verbal and visuospatial WM tasks irrespective of the affected hemisphere. Patients with unilateral right TLE showed an additional deficit for visuospatial WM capacity when contrasted with patients with left TLE, whereas patients with unilateral left TLE showed increased intrusion errors on the verbal task when compared to patients with right TLE. These findings suggest a material-specific lateralization of WM in the MTL.     

Influence of anxiety on memory performance in temporal lobe epilepsy

This study examined the degree to which anxiety contributed to inconsistent material-specific memory difficulties among 243 patients with temporal lobe epilepsy from the Multisite Epilepsy Study. Visual memory performance on the Rey Complex Figure Test (RCFT) was poorer for those with high versus low levels of anxiety but was not found to be related to the TLE side. The verbal memory score on the California Verbal Learning Test (CVLT) was significantly lower for patients with left-sided TLE than for patients with right-sided TLE with low anxiety levels but equally impaired for those with high anxiety levels. These results suggest that we can place more confidence in the ability of verbal memory tests like the CVLT to lateralize to left-sided TLE for those with low anxiety levels, but that verbal memory will be less likely to produce lateralizing information for those with high anxiety levels. This suggests that more caution is needed when interpreting verbal memory tests for those with high anxiety levels. These results indicated that RCFT performance was significantly affected by anxiety and did not lateralize to either side, regardless of anxiety levels. This study adds to the existing literature which suggests that drawing-based visual memory tests do not lateralize among patients with TLE, regardless of anxiety levels.     

Postictal stability of proton magnetic resonance spectroscopy imaging (1H-MRSI) ratios in temporal lobe epilepsy

Interictal proton (1H) MRS is increasingly used for seizure lateralization in patients with temporal lobe epilepsy (TLE). Studies reporting postictal 1H-MRS metabolite changes in patients with TLE are few and contradictory. The authors prospectively performed interictal and postictal proton magnetic resonance spectroscopy imaging (1H-MRSI) studies in seven patients with TLE. The authors found no consistent changes in metabolite peak area ratios between studies, suggesting that 1H-MRS ratios remain stable between interictal and postictal state in TLE.     

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

Purpose: 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.
Methods: 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.
Results: 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 ≤ 0.003). Neither Wada memory asymmetry nor Wada language asymmetry added additional predictive power beyond these noninvasive measures.
Discussion: 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.