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Effects of left temporal lobectomy and amygdalohippocampectomy on memory
Effects of left temporal Iobectomy and amygdalohippocampectomy on memory
Teresa Lee M Psych, R o d e r i c k A. M a c k e n z i e MD FRACP, A. J. W a l k e r , M Psych, John M. M a t h e s o n FRACS, P. S a c h d e v MD PhD FRANZCP Neuropsychiatric Institute, Prince Henry Hospital, Sydney, NSW 2036, Australia
This study examined the effects of left (dominant) temporal lobe surgery on verbal and visual memory in 38 patients with temporal lobe epilepsy. Twenty-five patients had anterior temporal lobectomy (ATL)'rand 13 had selective amygdalohippocampectomy (AH). All were administered the Rey Auditory Verbal Learning Test and a Complex Figure Test preoperatively and 1 year after surgery. ATL resulted in better seizure control overall. The ATL group as a whole showed a greater postoperative decline of their verbal memory than the AH group. A closer examination of the ATL patients showed there was a subgroup (n = 11 ) with better preoperative memory functioning that had the most significant decline. In contrast, only three patients in the AH group had better preoperative memory, and the majority (n = 10) matched the 'memory impaired' ATL patients. The changes in memory performance of the 'memory impaired' ATL and AH patients did not reach statistical significance. Postoperatively all patient groups improved in their verbal fluency.
Journal of ClinicalNeuroscience 1997, 4(3): 314-319
© Pearson Professional Ltd 1997
Keywords: amygdalohippocampectomy, anterior temporal Iobectomy, verbal memory, neuropsychology, temporal lobe epilepsy
Introduction Resective surgery is now well established as a treatment for medically intractable epilepsy of temporal lobe origin. I The most c o m m o n surgical procedure is anterior temporal lobectomy (ATL) in which the anterior 4.5-6 cm of the temporal neocortex is removed, together with a variable portion of the hippocampus (2-3 cm) and the amygdala. 2 Considering the importance of these structures for cognition, the effects of ATL, especially of the dominant hemisphere, on m e m o r y and language functioning is of much theoretical interest and clinical c o n c e r n ? M e m o r y i m p a i r m e n t is frequently r e p o r t e d after ATL. 4 In general, left (dominant) temporal lobe resections p r o d u c e deficits in verbal m e m o r y and right (nondominant) temporal lobe resections p r o d u c e deficits in visual memory. 5 Novelly et al 6 r e p o r t e d that 1 year after surgery, left ATL patients had a significant reduction of verbal memory, but a significant i m p r o v e m e n t of nonverbal memory. O j e m a n n and Dodrill: r e p o r t e d a 92% m e a n reduction of verbal m e m o r y in 13 patients who u n d e r w e n t left ATL. T h e i r non-verbal m e m o r y scores increased slightly, although not significantly. H e r m a n n et aP c o m p a r e d learning and m e m o r y p e r f o r m a n c e of left and right ATL patients. They f o u n d that the left ATL group showed p o o r e r m e m o r y for both free and cued recall relative to preoperative levels, while the right ATL group showed less significant i m p a i r m e n t
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c o m p a r e d to their preoperative performances. Some studies, however, have f o u n d that visual m e m o r y was less lateralized than verbal memory. In Novelly et al's study, 6 the right ATL patients did not show significant reduction in visual memory. Rausch and Crandall, 8 in comparing left and right ATL patients, f o u n d that the visual m e m o r y measure did not reveal significant findings between the two groups. In a n o t h e r study the left ATL group was impaired on a visuo-spatial m e m o r y task. 9 T h e authors c o n c l u d e d that at least some aspects of visuo-spatial m e m o r y seem to be mediated by the left hemisphere. The m e m o r y impairment following ATL resection is generally attributed to partial removal of the hippocampus and the amygdala. 1° However, the lateral neocortex may also be involved in memory. For example, Ojemann and Dodrill 7 reported that large lateral, but not medial, temporal lobe resections were associated with significant postoperative m e m o r y deficits. More recent experimental studies suggest that cortical areas adjacent to the hippocampus such as the entorhinal, perirhinal and parahippoeampal cortices are also important for declarative memory. 11 It is therefore of theoretical as well as clinical importance to compare conventional ATL with procedures that selectively remove the anterior hippocampus and amygdala, and spare the lateral neocortex.
Left temporal Iobectomy and memory
Clinical studies
T h e technique of selective a m y g d a l o h i p p o c a m p e c tomy (AH) described by YasargiP 2 has b e e n used at our centre for patients with an epileptic focus clearly localized to the mesiobasal t e m p o r a l area. This p r o c e d u r e involves the removal of the anterior 3-4 cm of the hippocampus, the amygdala and the p a r a h i p p o c a m p a l gyrus. Selective A H was r e p o r t e d to have resulted in an i m p r o v e m e n t in learning and m e m o r y p e r f o r m a n c e , especially for material specific to the n o n - o p e r a t e d side) 3 Few studies have c o m p a r e d neuropsychological function after left ATL and AH. Goldstein and Polkey 14 c o m p a r e d 8 left ATL patients with 14 left AH patients a n d f o u n d that for logical memory, immediate recall o f verbal material and tests of non-verbal memory, there was little difference between the groups, while for verbal paired association, the AH g r o u p showed marginally less impairment. A g r o u p f r o m the Mayo Clinic 15 also e x a m i n e d the changes in m e m o r y and intellectual p e r f o r m a n c e s following various types of resection of mesial and lateral t e m p o r a l lobe structures and f o u n d no significant differences in the risk of cognitive i m p a i r m e n t . Clearly, the differential effects of extensive versus selective resection on m e m o r y are far f r o m established. A n o t h e r issue relating to m e m o r y in epilepsy patients is the relevance of m e m o r y test p e r f o r m a n c e to everyday memory. Goldstein and Polkey 5 d e m o n s t r a t e d that the differences in scores on traditional m e m o r y tests after surgery did not translate into behavioural measures of memory. T h o m p s o n and Corcoran 16 also drew attention to the discrepancies between m e m o r y test p e r f o r m a n c e (which tests only declarative m e m o r y ) and the complaints of everyday m e m o r y failure in some patients with epilepsy. They attributed this to the fact that the t e r m ' m e m o r y failure' was used to refer to some areas of cognitive dysfunction, such as n a m i n g difficulties, which may be aspects of language deficit. T h e present study c o m p a r e d the effects of left (dominant) AH versus ATL on m e m o r y in 38 patients with temporal lobe epilepsy. In addition to verbal and visual m e m o r y , we also e x a m i n e d the effects of the two operations on verbal generation (fluency).
Methods Subjects Thirty-eight patients who u n d e r w e n t left t e m p o r a l lobe surgery for epilepsy were included in this study. All subjects were of at least borderline intelligence (prorated verbal I Q scores of 70 or above). They were all left hemisphere d o m i n a n t for language, as d e t e r m i n e d by the sodium amytal ablation (Wada) test, a standard presurgical assessment p r o c e d u r e which has previously b e e n r e p o r t e d ) 7 T h e localization of the epileptogenic focus was d e t e r m i n e d f r o m the results of simultaneous video and scalp and sphenoidal e l e c t r o e n c e p h a l o g r a m (EEG) recordings, b o t h interictal and ictal, correlated with neuropsychological evaluation and results of magnetic resonance imaging (MRI) and ictal single p h o t o n emission c o m p u t e d t o m o g r a p h y (SPECT) scanning. W h e n results
were not definitely localizing, intracerebral or subdural strip EEG recordings were obtained. Selective A H was only p e r f o r m e d in patients whose invasive studies showed onset localized to one hippocampus. After these assessments, 25 subjects h a d conventional ATL and 13 had selective AH. T h e tissue r e m o v e d was e x a m i n e d histologically and classified as described previously):
Neuropsychological assessment Testing was carried out as part of the routine preoperative assessment, and 1 year after surgery. All patients were administered the Rey Auditory Verbal Learning Test (RAVLT) is (List A preoperatively and List B postoperatively) and a Complex Figure Test (CFT) is (Rey-Osterreith version preoperatively, the Taylor version postoperatively) as measures of their verbal and visual memory, respectively. T h e RAVLT consists of five presentations of a 15-word list with recall after every trial, one presentation of a seco n d 15-word list as a distractor, and a sixth recall trial (of the list presented five times). Trial 1 (RAVLT1) is a measure of immediate attention span; Trial 5 (RAVLT5) measures information acquired with repetition; and Trial 6 (RAVLT6) measures the a m o u n t of learned information retained following distraction. The CFT includes a copy trial and a 3 min delayed recall triM. Subjects were asked to copy the figure, which was scored on a unit scoring system, totalling 36 points (cited in ref 18). After the copy trial, a verbal fluency test, the Controlled Oral Word Association Test (COWAT),18 was given. This is a test of oral p r o d u c t i o n of spoken words beginning with three designated letters (F, A and S). Subjects were asked to say as m a n y words as they could think of that b e g a n with a given letter, excluding p r o p e r nouns, n u m b e r s and the same word with a different suffix. This was followed by a m e m o r y trial of the CFT that was scored in the same m a n n e r as the copy trial. T h e recall score (CFTR) was used as a measure of retention of visuo-spatial information.
Data analysis Neuropsychological test results were analysed using multivariate analysis of variance (MANOVA). T h e between-subjects factor was group (AH and ATL), and within-subjects factor was time (preoperative and postoperative). Age of onset of epilepsy was used as a covariate, as early onset of epilepsy has b e e n associated with p o o r cognitive functioning) 9 The four d e p e n d e n t variables were: RAVLT1, RAVLT5, RAVLT6 and the RCFT recall score. The ATL group showed a wide range of preoperative RAVLT6 scores, with a subgroup in the impaired range. The analysis was therefore repeated after dividing the ATL group into two subgroups, using 9 on RAVLT6 as the cut-off. This is one standard deviation below the m e a n score for the 20- to 29-year age group in an Australian normative study 2° (male: m e a n score = 11.1, s.d. = 1.7; female: m e a n score = 11.6, s.d. -- 2.5). Fourteen ATL patients had an RAVLT6 score < 9, suggesting a preoperative impairment, while nine patients had RAVLT6 score > 9. Ten AH patients had RAVLT6 scores < 9 and only three had scores > 9.
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Left temporal Iobectomy and memory
Table 1 Patient characteristics, surgical outcome and neuropathology Amygdalohippocampectomy (n = 13)
Anterior Temporal Lobectomy (n=25)
Age Mean (SD) Sex M/F IQ* Mean (SD)
26.9 (9.0) 4/9 88.8 (11.0)
27.0 (8.8) 17/8 84.3 (9.4)
Surgical outcome class** 1. SeizureFree 2. RareSeizures 3. Worthwile Improvement 4. No Wor~hwile Improvement
5 (38.5%) 3 (23.1%) 1 (7.7%) 4 (30.8%)
15 (60%) 4 (16%) 3 (12%) 3 (12%)
Neuropathologg Mesial Temporal Sclerosis Gliosis No Abnormality Turnout
5 (38.5%) 2 (15.4%) 6 (46.2%) 0
13 (52 %) 5 (20%) 6 (24%) 1 (4%)
*prorated Verbal IQ **from Enge121
Table 2 Comparison of preoperative and postoperative verbal and visual memory of two groups (AH and ATL ) AH (n=13)
REPEATED MEASURES MULTIVARIATE ANALYSES OF VARIANCE: EFFECTS
ATL (n=25)
Pre-op
Post-op
Pre-op
Post-op
Group
Time
RAVLT1
6.2 (1.8)
5.8 (1.6)
5.8 (1.5)
RAVLT5
10.5 (2.4)
9.4 (4.1)
RAVLT6
7.5 (2.3)
COWAT CFTR
Group & Time
5.3 (1.5)
NS
NS
NS
11.2 (2.6)
9.3 (2.2)
NS
0.001
NS
6.6 (3.8)
8.5 (3.3)
5.4 (3.1)
NS
0.001
0.04
24.6 (7.2)
29.5 (8.8)
31.6 (8.1)
34.3 (9.7)
0.049
0.006
NS
14.4 (7.1)
19.0 (8.9)
16.9 (8.6)
18.7 (6.8)
NS
0.04
NS
All scores shown are group means, with standard deviations in parentheses NS = not significant at the 0.05 level AH = Amygdalohippocampectomy ATL = Anterior Temporal Lobectomy RAVLT1,5,6 = Rey Auditory Verbal Learning Test scores on trials 1, 5 and 6 COWAT = Controlled Oral Word Association Test (total words produced) CFTR = Complex Figure Test recall scores.
Verbal memory
Results Patient characteristics, surgical o u t c o m e ropathology data are presented in Table 1.
and
neu-
Seizure outcome Seizure o u t c o m e at 1 year was graded into classes 1-4 according to Engel's classification. 21 T h e o u t c o m e results a p p e a r e d m o r e favourable in the ATL g r o u p (ATL: 60% seizure-free; AH: 38.5% seizure-free) although this did not reach statistical significance (Z2 analysis, P > 0.05). Seizure free o u t c o m e between ATL (n = 72, 60% seizurefree) and AH (n = 28, 21% seizure-free) groups in our larger series was statistically significant (P< 0.005).17 This difference was not explained by a difference in the neuropathology and is t h o u g h t to be related to the a m o u n t of tissue removed.
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Table 2 shows the g r o u p means and summarizes the results of the MANOVA. For RAVLT1, there was no significant difference either between the groups or over time. For RAVLTS, there was a significant effect for time (P < 0.001), in that b o t h groups showed a reduction in the n u m b e r of words learned postopelZatively. A significant effect for time ( P < 0.001) and g r o u p by time interaction (P < 0.04) was f o u n d for RAVLT6. A further analysis of variance revealed a significant deterioration (P < 0.005) between pre- and postoperative performances on RAVLT6 in the ATL g r o u p only. The covariate was f o u n d to be insignificant in all the analyses. T h e analyses were r e p e a t e d on each o f the four d e p e n d e n t measures: RAVLT1, RAVLT5, RAVLT6 and RCFTR, with comparisons carried out on three groups,
Left temporal Iobectomy and memory
Clinical studies
Table 3 Comparison of preoperative and postoperative verbal and visual memory of 3 groups (AH, ATL group 1 and group 2) AH (n=13)
ATE (n=25) Group 1 (n=14)
Pre-Op RAVLT1 RAVLT5 RAVLT6 COWAT CFTR
6.2 (1.8) 10.5 (2.4) 7.5 (2.3) 24,6 (7.2) 14.4 (7.1)
Post-Op 5.8 (1.6) 9.4 (4.1) 6.6 (3.8) 29.5 (8.8) 19.0 (8.9)
REPEATED MEASURES MULTIVARIATE ANALYSES OF VARIANCE EFFECTS Group 2 (n=11)
Pre-Op
Post-Op
Pre-Op
5.4 (1.3) 9.5 (2.0) 6.0 (1.4) 22.8 (8.3) 12.9 (7.3)
5.3 (1.7) 8.4 (2.2) 4.0 (2.4) 28.6 (10.4) 13.8 (4.2)
6.2 (1.6) ~3.4 (1.4) 11.7 (1.8) 26.9 (4.8) 20.5 (9.2)
Post-Op 5,4 (1.3) 10.4 (1.6) 7.2 (3.2) 30.6 (6.6) 24.5 (4.3)
Group
Time
Group & Time
NS
NS
NS
0.006
0.000
NS
0,000
0.000
0.013
NS
0,002
NS
0,003
0.05
NS
All scores are group means, w i t h standard deviations in parentheses NS = not significant at the 0.05 level AH = Amygdalohippocampectomy ATL = Anterior Temporal Lobectomy, Group 1:RAVLT6 scores <9, Group 2:RAVLT6 scores >9 RAVLT1,5,6 = Rey Auditory Verbal Learning Test scores on trials 1, 5 and 6 COWAT = Controlled Oral Word Association Test (total words produced) CFTR = Complex Figure Test recall scores.
the AIR g r o u p and the two ATL subgroups (< 9 and _> 9 RAVLT6 scores), over time (preoperatively and postoperatively), and are summarized in Table 3. Again, there was no significant group, time or interaction effects for RAVLT1. For RAVLT5, there were significant g r o u p (P < 0.006) and time (P < 0.000) effects, showing that, overall, there was a significant decrease in p e r f o r m a n c e over time. T h e r e was no g r o u p by time interaction effect. With RAVLT6, there was a significant g r o u p effect (P < 0.001) which was not u n e x p e c t e d as the two ATL subgroups were divided according to their presurgical RAVLT6 scores. However, there was also a significant time effect (P < 0.000) as well as g r o u p by time interaction effect (P < 0.013). Further analyses of variance revealed that there was a significant reduction in the postoperative RAVLT6 of the > 9 ATL g r o u p (P < 0.05), but not in the other two groups. Visual memory
No significant g r o u p effect or g r o u p by time interaction was f o u n d for recall on the RCFT when the two groups AH and ATL were considered. A significant time effect (P < 0.04) was f o u n d in that b o t h groups i m p r o v e d in their recall p e r f o r m a n c e s postoperatively. W h e n further analysis was carried out, c o m p a r i n g the p e r f o r m a n c e s of AH and the two ATL subgroups (< 9 and > 9) over time, significant main effects for g r o u p (P < 0.003) and time (P < 0.05) were f o u n d for RCFT recall. Further analyses revealed a significant difference between the two ATL subgroups, with the > 9 subjects recalling m o r e features than the < 9 g r o u p postoperatively. Verbal
fluency
Both the AH and the ATL groups i m p r o v e d in their verbal generation at postoperative follow-up. T h e r e was a significant g r o u p effect (P < 0.049) as well as time effect (P < 0.006). As for the three-group analysis, a significant main effect for time (P < 0.002) was found.
Discussion
In our study, the ATL g r o u p as a whole showed a greater postoperative i m p a i r m e n t of their verbal m e m o r y than the AH group. This is consistent with the few reports in the literature that have c o m p a r e d the two kinds of surgery, ls,~4T h e age of onset of epilepsy was not f o u n d to be a significant variable in cognitive o u t c o m e in this study, and previous studies have r e p o r t e d that seizure variables ( n u m b e r of seizures, age of onset, n u m b e r of medications) are of limited i m p o r t a n c e in neuropsychological p e r f o r m a n c e s . 22 T h e n u m b e r of words recalled in the first trial, being a measure of attention and immediate m e m o r y and involving anterior dorsal cortical areas, TM was u n c h a n g e d after b o t h procedures. T h e postoperative i m p a i r m e n t in verbal m e m o r y would be unlikely to be associated with a decline in language functioning, as all patient groups showed an i m p r o v e m e n t in verbal fluency. A closer examination of the ATL group revealed that it was the subgroup with better preoperative m e m o r y functioning that had the most significant change, with the preand postoperative differences between ' m e m o r y impaired' ATL and AH groups not reaching statistical significance. The former subgroup (ATL > 9) and the AH group demonstrated a trend towards improvement in their immediate recall of visual information, material specific to the nonoperated side. The fact that memory-impaired patients did not demonstrate significant additional worsening of their verbal recall may be because: firstly, the tissue removed was non-functional, explaining the p o o r preoperative function and a lack of further change; a n d / o r secondly, the test was insensitive to detect further mild decline in those with low m e m o r y functioning. Since our study did not include a better functioning AH group, we cannot conclude that ATL was necessarily worse than AH for p e r f o r m a n c e on verbal m e m o r y tasks in this group of higher functioning patients. Further studies, comparing AH and ATL groups with unimpaired m e m o r y function preoperatively, are necessary to clarify this issue.
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Clinical studies T h e clinical significance of verbal m e m o r y impairm e n t in a subgroup of patients is difficult to judge, although our clinical impression would suggest that such i m p a i r m e n t does not usually impact significantly on the person's functioning relative to the preoperative level. Many authors have shown that p e r f o r m a n c e on formal m e m o r y tasks that do not resemble daily tasks needing m e m o r y has a p o o r correlation with self-reports of m e m ory function. 2s'24 Assessment of behavioural memory, as suggested by Goldstein and Polkey, 5 is therefore of greater clinical relevance but our study did not include this measurement. T h e change in m e m o r y function must also be considered in the light of the degree of seizure control which is the p r i m a r y aim of the surgery. In our series, ATL was m u c h m o r e successful in this respect than AH, and even if it was marginally inferior on m e m o r y p e r f o r m a n c e , ATL could be j u d g e d to be superior to AH overall. It is i m p o r t a n t to take into account the difference in preoperative tests in the two groups, since the ATL g r o u p had a higher rate of c o n c o r d a n c e of all tests than the A H group, in w h o m invasive studies were necessary before surgery could be p e r f o r m e d . This almost certainly means that the A H patients were less likely to have a good result, whatever type of surgery was p e r f o r m e d . T h e results for visual m e m o r y bear further c o m m e n t . T h e 'verbal m e m o r y u n i m p a i r e d ' ATL patients and the AH patients showed a tendency towards a postoperative i m p r o v e m e n t in their visuo-spatial memory. This has previously b e e n explained as being due to the loss of the interference with n o r m a l function by the actively discharging focus. 12 This explanation would be m o r e applicable to our ATL group, as this was the g r o u p that showed the best seizure outcome. T h e A H and the 'verbal m e m o r y impaired' ATL g r o u p p e r f o r m e d relatively poorly (< 25th percentile) on immediate recall of visuospatial information preoperatively, even though their abnormalities were j u d g e d to be strongly lateralized to the d o m i n a n t hemisphere. This finding is consistent with earlier reports that delayed recall of the Rey Complex Figure did not distinguish between right- or left-sided surgical patients.19 Further, Goldstein and Polkey 14f o u n d in their study that patients who received left-sided surgery scored better than the right-sided cases on verbal learning preoperatively. Similarly, Zaidel et a125 recently r e p o r t e d their findings on effects of temporal lobectomy and f o u n d that the right medial temporal lobe regions are involved in verbal memory, though not as importantly as the left regions. These findings question the validity of the assumption of strong lateralization of m e m o r y function in temporal lobe epilepsy patients. In conclusion, o u r study showed that if verbal m e m ory was impaired preoperatively, left A H or ATL did not result in further significant deterioration of verbal m e m ory. In patients with u n i m p a i r e d verbal memory, ATL resulted in some decline in verbal m e m o r y and, paradoxically, some i m p r o v e m e n t in visuo-spatial memory. Patients who had good verbal m e m o r y may have had less decline in m e m o r y as a result of the selective procedure, but m o r e of these patients will n e e d to be operated in this way before a definite answer can be given. This study also
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Left temporal Iobectomy and memory supports previous work in raising doubts a b o u t the utility of verbal/non-verbal m e m o r y discrepancy in the lateralization of dysfunction in temporal lobe epilepsy patients. We suggest that future studies should assess diverse m e m ory functions, incorporating behavioural measures of memory.
Acknowledgements The authors acknowledge the assistance of Steven Cumming M Psych andJanine Klamus BAppSci. Secretarial assistance was provided by Doreen Hanlon. Received17 July 1995; Accepted 10 May 1996
Correspondence and offprint requests: Dr R. A. Mackenzie, NPI Prince Henry Hospital, Little Bay,NSW 2036, Australia, Tel: 61 2 525 8344, Fax: 61 2 524 1173 References 1. Binney CD, Polkey CE. Surgery for epilepsy. In: Kennard C (ed). Recent Advances in Clinical Neurology. Edinburgh: Churchill Livingstone, 1992: 55-93. 2. Olivier A. Commentary: cortical resections. In: Engel J(ed). Surgical Treatment of the Epilepsies. New York: Raven Press, 1987: 405-416. 3. Hermann BP, Wyler AR, Bush AJ, Tabatabai FR. Differential effects of left and right anterior temporal lobectomy on verbal learning and memory performance. Epilepsia 1992; 33: 289-297. 4. Channon S, Polkey CE. Memory and temporal lobe surgery: a review, J Roy Soc Med 1990; 83: 100-103. 5. Goldstein LH, Polkey CE. Behavioural memory after temporal lobectomy or amygdalo-hippocampectomy. BKJ Clin Psychol 1992; 31: 75-81. 6. Novelly RA, Augustine EA, Mattson RH et al. Selective memory improvement and impairment in temporal lobectomy for epilepsy. Ann Neurol 1984; 15: 64--67. 7. Ojemann GA, Dodrill CB. Verbal memory deficits after left temporal lobectomy for epilepsy: mechanism and intra-operative prediction.J Neurosurg 1985; 62: 101-107. 8. Rausch R, Crandall PH. Psychological status related to surgical control of temporal lobe seizures. Epilepsia 1982; 23: 191-202. 9. Tucker DM, Novelly RA, Isaac W, Spencer D. Effects of simultaneous vs sequential stimulus presentation on memory performance following temporal lobe resection in humans. Neuropsychologia 1986; 24(2): 277-281. 10. Mishkin iV[,Appenzeller T. The anatomy of memory. Sci Am 1987; 256: 80-89. 11. Zola-Morgan S, Squire LR. Neuroanatomy of memory. Annu Rev Neurosci 1993; 16: 547-563. 12. Yasargil MG, Wieser HG. Selective amygdalohippocampectomy at the University Hospital, Zurich. In: EngelJrJ(ed). Surgical Treatment of the Epilepsies. New York: Raven Press, 1987: 653-658. 13. Wieser HG. Selective amygdalohippocampectomy for temporal lobe epilepsy. Epilepsia 1988; 29 (Suppl,2): 100-113. 14. Goldstein LH, Polkey CE. Short-term cognitive changes after unilateral amygdalohippocampectomy for the relief of temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 1993; 56: 135-140. 15. Wolf RL, Ivnik RJ, Hirschorn KA, Sharbrough FW, Cascino GD, Marsh WR. Neurocognitive efficiency following left temporal lobectomy: standard versus limited resection. J Neurosurg 1993; 79: 76-83. 16. Thompson PJ, Corcoran R. Everyday memory failures in people with epilepsy. Epilepsia 1992; 33: S18-$20.
Left temporal Iobectomy and memory 17. Mackenzie RA, MathesonJM, Ellis M, KlamusJ. Selective versus non-selective temporal lobe surgery for epilepsy. J Clin Neurosci 1997; 4(2): 152-154. 18. Lezak MD. Neuropsychological Assessment, 3rd Edn. New York: Oxford University Press, 1995. 19. Powell GE, Polkey CE, McMillan TM. The new Maudsley series of temporal lobectomy: Short-term cognitive effects. BrJ Clin Psychol 1985; 24: 109-124. 20. Geffen G, Moar KJ, O'Hanlon AP, Clark CR, Geffen LB. The Auditory Verbal Learning Test (Rey) : performance of 16- to 86-year-olds of average intelligence. Clin Neuropsychol 1990; 4: 45-63. 21. EngelJrJ. Outcome with respect to epileptic seizures. In: EngelJrJ (ed) Surgical Treatment of the Epilepsies. New York: Raven Press, 1987: 553-572.
Clinical studies 22. Dodrill CB. Interictal cognitive aspects of epilepsy. Epilepsia 1992; 33(Suppl 6): 7-10. 23. Bennett-LevyJ, Powell GE. The subjective memory questionnaire (SMQ). An investigation into the selfreporting of 'real-life' memory skills. BrJ Soc Clin Psychol 1980; 19: 177-188. 24. Sunderland A, HarrisJE, Baddeley AD. Do laboratory tests predict everyday memory? A neuropsychological study. J Verbal Learning Verbal Behavior 1983; 22: 341-357. 25. Zaidel DW, Oxbury SM, OxburyJM. Effects of surgery in unilateral medial temporal lobe regions on verbal explicit and implicit memory. J Neuropsychiatry Neuropsychol Behav Neurol 1994; 7(2): 104-108.
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Teresa Lee M Psych, R o d e r i c k A. M a c k e n z i e MD FRACP, A. J. W a l k e r , M Psych, John M. M a t h e s o n FRACS, P. S a c h d e v MD PhD FRANZCP Neuropsychiatric Institute, Prince Henry Hospital, Sydney, NSW 2036, Australia
This study examined the effects of left (dominant) temporal lobe surgery on verbal and visual memory in 38 patients with temporal lobe epilepsy. Twenty-five patients had anterior temporal lobectomy (ATL)'rand 13 had selective amygdalohippocampectomy (AH). All were administered the Rey Auditory Verbal Learning Test and a Complex Figure Test preoperatively and 1 year after surgery. ATL resulted in better seizure control overall. The ATL group as a whole showed a greater postoperative decline of their verbal memory than the AH group. A closer examination of the ATL patients showed there was a subgroup (n = 11 ) with better preoperative memory functioning that had the most significant decline. In contrast, only three patients in the AH group had better preoperative memory, and the majority (n = 10) matched the 'memory impaired' ATL patients. The changes in memory performance of the 'memory impaired' ATL and AH patients did not reach statistical significance. Postoperatively all patient groups improved in their verbal fluency.
Journal of ClinicalNeuroscience 1997, 4(3): 314-319
© Pearson Professional Ltd 1997
Keywords: amygdalohippocampectomy, anterior temporal Iobectomy, verbal memory, neuropsychology, temporal lobe epilepsy
Introduction Resective surgery is now well established as a treatment for medically intractable epilepsy of temporal lobe origin. I The most c o m m o n surgical procedure is anterior temporal lobectomy (ATL) in which the anterior 4.5-6 cm of the temporal neocortex is removed, together with a variable portion of the hippocampus (2-3 cm) and the amygdala. 2 Considering the importance of these structures for cognition, the effects of ATL, especially of the dominant hemisphere, on m e m o r y and language functioning is of much theoretical interest and clinical c o n c e r n ? M e m o r y i m p a i r m e n t is frequently r e p o r t e d after ATL. 4 In general, left (dominant) temporal lobe resections p r o d u c e deficits in verbal m e m o r y and right (nondominant) temporal lobe resections p r o d u c e deficits in visual memory. 5 Novelly et al 6 r e p o r t e d that 1 year after surgery, left ATL patients had a significant reduction of verbal memory, but a significant i m p r o v e m e n t of nonverbal memory. O j e m a n n and Dodrill: r e p o r t e d a 92% m e a n reduction of verbal m e m o r y in 13 patients who u n d e r w e n t left ATL. T h e i r non-verbal m e m o r y scores increased slightly, although not significantly. H e r m a n n et aP c o m p a r e d learning and m e m o r y p e r f o r m a n c e of left and right ATL patients. They f o u n d that the left ATL group showed p o o r e r m e m o r y for both free and cued recall relative to preoperative levels, while the right ATL group showed less significant i m p a i r m e n t
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c o m p a r e d to their preoperative performances. Some studies, however, have f o u n d that visual m e m o r y was less lateralized than verbal memory. In Novelly et al's study, 6 the right ATL patients did not show significant reduction in visual memory. Rausch and Crandall, 8 in comparing left and right ATL patients, f o u n d that the visual m e m o r y measure did not reveal significant findings between the two groups. In a n o t h e r study the left ATL group was impaired on a visuo-spatial m e m o r y task. 9 T h e authors c o n c l u d e d that at least some aspects of visuo-spatial m e m o r y seem to be mediated by the left hemisphere. The m e m o r y impairment following ATL resection is generally attributed to partial removal of the hippocampus and the amygdala. 1° However, the lateral neocortex may also be involved in memory. For example, Ojemann and Dodrill 7 reported that large lateral, but not medial, temporal lobe resections were associated with significant postoperative m e m o r y deficits. More recent experimental studies suggest that cortical areas adjacent to the hippocampus such as the entorhinal, perirhinal and parahippoeampal cortices are also important for declarative memory. 11 It is therefore of theoretical as well as clinical importance to compare conventional ATL with procedures that selectively remove the anterior hippocampus and amygdala, and spare the lateral neocortex.
Left temporal Iobectomy and memory
Clinical studies
T h e technique of selective a m y g d a l o h i p p o c a m p e c tomy (AH) described by YasargiP 2 has b e e n used at our centre for patients with an epileptic focus clearly localized to the mesiobasal t e m p o r a l area. This p r o c e d u r e involves the removal of the anterior 3-4 cm of the hippocampus, the amygdala and the p a r a h i p p o c a m p a l gyrus. Selective A H was r e p o r t e d to have resulted in an i m p r o v e m e n t in learning and m e m o r y p e r f o r m a n c e , especially for material specific to the n o n - o p e r a t e d side) 3 Few studies have c o m p a r e d neuropsychological function after left ATL and AH. Goldstein and Polkey 14 c o m p a r e d 8 left ATL patients with 14 left AH patients a n d f o u n d that for logical memory, immediate recall o f verbal material and tests of non-verbal memory, there was little difference between the groups, while for verbal paired association, the AH g r o u p showed marginally less impairment. A g r o u p f r o m the Mayo Clinic 15 also e x a m i n e d the changes in m e m o r y and intellectual p e r f o r m a n c e s following various types of resection of mesial and lateral t e m p o r a l lobe structures and f o u n d no significant differences in the risk of cognitive i m p a i r m e n t . Clearly, the differential effects of extensive versus selective resection on m e m o r y are far f r o m established. A n o t h e r issue relating to m e m o r y in epilepsy patients is the relevance of m e m o r y test p e r f o r m a n c e to everyday memory. Goldstein and Polkey 5 d e m o n s t r a t e d that the differences in scores on traditional m e m o r y tests after surgery did not translate into behavioural measures of memory. T h o m p s o n and Corcoran 16 also drew attention to the discrepancies between m e m o r y test p e r f o r m a n c e (which tests only declarative m e m o r y ) and the complaints of everyday m e m o r y failure in some patients with epilepsy. They attributed this to the fact that the t e r m ' m e m o r y failure' was used to refer to some areas of cognitive dysfunction, such as n a m i n g difficulties, which may be aspects of language deficit. T h e present study c o m p a r e d the effects of left (dominant) AH versus ATL on m e m o r y in 38 patients with temporal lobe epilepsy. In addition to verbal and visual m e m o r y , we also e x a m i n e d the effects of the two operations on verbal generation (fluency).
Methods Subjects Thirty-eight patients who u n d e r w e n t left t e m p o r a l lobe surgery for epilepsy were included in this study. All subjects were of at least borderline intelligence (prorated verbal I Q scores of 70 or above). They were all left hemisphere d o m i n a n t for language, as d e t e r m i n e d by the sodium amytal ablation (Wada) test, a standard presurgical assessment p r o c e d u r e which has previously b e e n r e p o r t e d ) 7 T h e localization of the epileptogenic focus was d e t e r m i n e d f r o m the results of simultaneous video and scalp and sphenoidal e l e c t r o e n c e p h a l o g r a m (EEG) recordings, b o t h interictal and ictal, correlated with neuropsychological evaluation and results of magnetic resonance imaging (MRI) and ictal single p h o t o n emission c o m p u t e d t o m o g r a p h y (SPECT) scanning. W h e n results
were not definitely localizing, intracerebral or subdural strip EEG recordings were obtained. Selective A H was only p e r f o r m e d in patients whose invasive studies showed onset localized to one hippocampus. After these assessments, 25 subjects h a d conventional ATL and 13 had selective AH. T h e tissue r e m o v e d was e x a m i n e d histologically and classified as described previously):
Neuropsychological assessment Testing was carried out as part of the routine preoperative assessment, and 1 year after surgery. All patients were administered the Rey Auditory Verbal Learning Test (RAVLT) is (List A preoperatively and List B postoperatively) and a Complex Figure Test (CFT) is (Rey-Osterreith version preoperatively, the Taylor version postoperatively) as measures of their verbal and visual memory, respectively. T h e RAVLT consists of five presentations of a 15-word list with recall after every trial, one presentation of a seco n d 15-word list as a distractor, and a sixth recall trial (of the list presented five times). Trial 1 (RAVLT1) is a measure of immediate attention span; Trial 5 (RAVLT5) measures information acquired with repetition; and Trial 6 (RAVLT6) measures the a m o u n t of learned information retained following distraction. The CFT includes a copy trial and a 3 min delayed recall triM. Subjects were asked to copy the figure, which was scored on a unit scoring system, totalling 36 points (cited in ref 18). After the copy trial, a verbal fluency test, the Controlled Oral Word Association Test (COWAT),18 was given. This is a test of oral p r o d u c t i o n of spoken words beginning with three designated letters (F, A and S). Subjects were asked to say as m a n y words as they could think of that b e g a n with a given letter, excluding p r o p e r nouns, n u m b e r s and the same word with a different suffix. This was followed by a m e m o r y trial of the CFT that was scored in the same m a n n e r as the copy trial. T h e recall score (CFTR) was used as a measure of retention of visuo-spatial information.
Data analysis Neuropsychological test results were analysed using multivariate analysis of variance (MANOVA). T h e between-subjects factor was group (AH and ATL), and within-subjects factor was time (preoperative and postoperative). Age of onset of epilepsy was used as a covariate, as early onset of epilepsy has b e e n associated with p o o r cognitive functioning) 9 The four d e p e n d e n t variables were: RAVLT1, RAVLT5, RAVLT6 and the RCFT recall score. The ATL group showed a wide range of preoperative RAVLT6 scores, with a subgroup in the impaired range. The analysis was therefore repeated after dividing the ATL group into two subgroups, using 9 on RAVLT6 as the cut-off. This is one standard deviation below the m e a n score for the 20- to 29-year age group in an Australian normative study 2° (male: m e a n score = 11.1, s.d. = 1.7; female: m e a n score = 11.6, s.d. -- 2.5). Fourteen ATL patients had an RAVLT6 score < 9, suggesting a preoperative impairment, while nine patients had RAVLT6 score > 9. Ten AH patients had RAVLT6 scores < 9 and only three had scores > 9.
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Left temporal Iobectomy and memory
Table 1 Patient characteristics, surgical outcome and neuropathology Amygdalohippocampectomy (n = 13)
Anterior Temporal Lobectomy (n=25)
Age Mean (SD) Sex M/F IQ* Mean (SD)
26.9 (9.0) 4/9 88.8 (11.0)
27.0 (8.8) 17/8 84.3 (9.4)
Surgical outcome class** 1. SeizureFree 2. RareSeizures 3. Worthwile Improvement 4. No Wor~hwile Improvement
5 (38.5%) 3 (23.1%) 1 (7.7%) 4 (30.8%)
15 (60%) 4 (16%) 3 (12%) 3 (12%)
Neuropathologg Mesial Temporal Sclerosis Gliosis No Abnormality Turnout
5 (38.5%) 2 (15.4%) 6 (46.2%) 0
13 (52 %) 5 (20%) 6 (24%) 1 (4%)
*prorated Verbal IQ **from Enge121
Table 2 Comparison of preoperative and postoperative verbal and visual memory of two groups (AH and ATL ) AH (n=13)
REPEATED MEASURES MULTIVARIATE ANALYSES OF VARIANCE: EFFECTS
ATL (n=25)
Pre-op
Post-op
Pre-op
Post-op
Group
Time
RAVLT1
6.2 (1.8)
5.8 (1.6)
5.8 (1.5)
RAVLT5
10.5 (2.4)
9.4 (4.1)
RAVLT6
7.5 (2.3)
COWAT CFTR
Group & Time
5.3 (1.5)
NS
NS
NS
11.2 (2.6)
9.3 (2.2)
NS
0.001
NS
6.6 (3.8)
8.5 (3.3)
5.4 (3.1)
NS
0.001
0.04
24.6 (7.2)
29.5 (8.8)
31.6 (8.1)
34.3 (9.7)
0.049
0.006
NS
14.4 (7.1)
19.0 (8.9)
16.9 (8.6)
18.7 (6.8)
NS
0.04
NS
All scores shown are group means, with standard deviations in parentheses NS = not significant at the 0.05 level AH = Amygdalohippocampectomy ATL = Anterior Temporal Lobectomy RAVLT1,5,6 = Rey Auditory Verbal Learning Test scores on trials 1, 5 and 6 COWAT = Controlled Oral Word Association Test (total words produced) CFTR = Complex Figure Test recall scores.
Verbal memory
Results Patient characteristics, surgical o u t c o m e ropathology data are presented in Table 1.
and
neu-
Seizure outcome Seizure o u t c o m e at 1 year was graded into classes 1-4 according to Engel's classification. 21 T h e o u t c o m e results a p p e a r e d m o r e favourable in the ATL g r o u p (ATL: 60% seizure-free; AH: 38.5% seizure-free) although this did not reach statistical significance (Z2 analysis, P > 0.05). Seizure free o u t c o m e between ATL (n = 72, 60% seizurefree) and AH (n = 28, 21% seizure-free) groups in our larger series was statistically significant (P< 0.005).17 This difference was not explained by a difference in the neuropathology and is t h o u g h t to be related to the a m o u n t of tissue removed.
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Table 2 shows the g r o u p means and summarizes the results of the MANOVA. For RAVLT1, there was no significant difference either between the groups or over time. For RAVLTS, there was a significant effect for time (P < 0.001), in that b o t h groups showed a reduction in the n u m b e r of words learned postopelZatively. A significant effect for time ( P < 0.001) and g r o u p by time interaction (P < 0.04) was f o u n d for RAVLT6. A further analysis of variance revealed a significant deterioration (P < 0.005) between pre- and postoperative performances on RAVLT6 in the ATL g r o u p only. The covariate was f o u n d to be insignificant in all the analyses. T h e analyses were r e p e a t e d on each o f the four d e p e n d e n t measures: RAVLT1, RAVLT5, RAVLT6 and RCFTR, with comparisons carried out on three groups,
Left temporal Iobectomy and memory
Clinical studies
Table 3 Comparison of preoperative and postoperative verbal and visual memory of 3 groups (AH, ATL group 1 and group 2) AH (n=13)
ATE (n=25) Group 1 (n=14)
Pre-Op RAVLT1 RAVLT5 RAVLT6 COWAT CFTR
6.2 (1.8) 10.5 (2.4) 7.5 (2.3) 24,6 (7.2) 14.4 (7.1)
Post-Op 5.8 (1.6) 9.4 (4.1) 6.6 (3.8) 29.5 (8.8) 19.0 (8.9)
REPEATED MEASURES MULTIVARIATE ANALYSES OF VARIANCE EFFECTS Group 2 (n=11)
Pre-Op
Post-Op
Pre-Op
5.4 (1.3) 9.5 (2.0) 6.0 (1.4) 22.8 (8.3) 12.9 (7.3)
5.3 (1.7) 8.4 (2.2) 4.0 (2.4) 28.6 (10.4) 13.8 (4.2)
6.2 (1.6) ~3.4 (1.4) 11.7 (1.8) 26.9 (4.8) 20.5 (9.2)
Post-Op 5,4 (1.3) 10.4 (1.6) 7.2 (3.2) 30.6 (6.6) 24.5 (4.3)
Group
Time
Group & Time
NS
NS
NS
0.006
0.000
NS
0,000
0.000
0.013
NS
0,002
NS
0,003
0.05
NS
All scores are group means, w i t h standard deviations in parentheses NS = not significant at the 0.05 level AH = Amygdalohippocampectomy ATL = Anterior Temporal Lobectomy, Group 1:RAVLT6 scores <9, Group 2:RAVLT6 scores >9 RAVLT1,5,6 = Rey Auditory Verbal Learning Test scores on trials 1, 5 and 6 COWAT = Controlled Oral Word Association Test (total words produced) CFTR = Complex Figure Test recall scores.
the AIR g r o u p and the two ATL subgroups (< 9 and _> 9 RAVLT6 scores), over time (preoperatively and postoperatively), and are summarized in Table 3. Again, there was no significant group, time or interaction effects for RAVLT1. For RAVLT5, there were significant g r o u p (P < 0.006) and time (P < 0.000) effects, showing that, overall, there was a significant decrease in p e r f o r m a n c e over time. T h e r e was no g r o u p by time interaction effect. With RAVLT6, there was a significant g r o u p effect (P < 0.001) which was not u n e x p e c t e d as the two ATL subgroups were divided according to their presurgical RAVLT6 scores. However, there was also a significant time effect (P < 0.000) as well as g r o u p by time interaction effect (P < 0.013). Further analyses of variance revealed that there was a significant reduction in the postoperative RAVLT6 of the > 9 ATL g r o u p (P < 0.05), but not in the other two groups. Visual memory
No significant g r o u p effect or g r o u p by time interaction was f o u n d for recall on the RCFT when the two groups AH and ATL were considered. A significant time effect (P < 0.04) was f o u n d in that b o t h groups i m p r o v e d in their recall p e r f o r m a n c e s postoperatively. W h e n further analysis was carried out, c o m p a r i n g the p e r f o r m a n c e s of AH and the two ATL subgroups (< 9 and > 9) over time, significant main effects for g r o u p (P < 0.003) and time (P < 0.05) were f o u n d for RCFT recall. Further analyses revealed a significant difference between the two ATL subgroups, with the > 9 subjects recalling m o r e features than the < 9 g r o u p postoperatively. Verbal
fluency
Both the AH and the ATL groups i m p r o v e d in their verbal generation at postoperative follow-up. T h e r e was a significant g r o u p effect (P < 0.049) as well as time effect (P < 0.006). As for the three-group analysis, a significant main effect for time (P < 0.002) was found.
Discussion
In our study, the ATL g r o u p as a whole showed a greater postoperative i m p a i r m e n t of their verbal m e m o r y than the AH group. This is consistent with the few reports in the literature that have c o m p a r e d the two kinds of surgery, ls,~4T h e age of onset of epilepsy was not f o u n d to be a significant variable in cognitive o u t c o m e in this study, and previous studies have r e p o r t e d that seizure variables ( n u m b e r of seizures, age of onset, n u m b e r of medications) are of limited i m p o r t a n c e in neuropsychological p e r f o r m a n c e s . 22 T h e n u m b e r of words recalled in the first trial, being a measure of attention and immediate m e m o r y and involving anterior dorsal cortical areas, TM was u n c h a n g e d after b o t h procedures. T h e postoperative i m p a i r m e n t in verbal m e m o r y would be unlikely to be associated with a decline in language functioning, as all patient groups showed an i m p r o v e m e n t in verbal fluency. A closer examination of the ATL group revealed that it was the subgroup with better preoperative m e m o r y functioning that had the most significant change, with the preand postoperative differences between ' m e m o r y impaired' ATL and AH groups not reaching statistical significance. The former subgroup (ATL > 9) and the AH group demonstrated a trend towards improvement in their immediate recall of visual information, material specific to the nonoperated side. The fact that memory-impaired patients did not demonstrate significant additional worsening of their verbal recall may be because: firstly, the tissue removed was non-functional, explaining the p o o r preoperative function and a lack of further change; a n d / o r secondly, the test was insensitive to detect further mild decline in those with low m e m o r y functioning. Since our study did not include a better functioning AH group, we cannot conclude that ATL was necessarily worse than AH for p e r f o r m a n c e on verbal m e m o r y tasks in this group of higher functioning patients. Further studies, comparing AH and ATL groups with unimpaired m e m o r y function preoperatively, are necessary to clarify this issue.
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Clinical studies T h e clinical significance of verbal m e m o r y impairm e n t in a subgroup of patients is difficult to judge, although our clinical impression would suggest that such i m p a i r m e n t does not usually impact significantly on the person's functioning relative to the preoperative level. Many authors have shown that p e r f o r m a n c e on formal m e m o r y tasks that do not resemble daily tasks needing m e m o r y has a p o o r correlation with self-reports of m e m ory function. 2s'24 Assessment of behavioural memory, as suggested by Goldstein and Polkey, 5 is therefore of greater clinical relevance but our study did not include this measurement. T h e change in m e m o r y function must also be considered in the light of the degree of seizure control which is the p r i m a r y aim of the surgery. In our series, ATL was m u c h m o r e successful in this respect than AH, and even if it was marginally inferior on m e m o r y p e r f o r m a n c e , ATL could be j u d g e d to be superior to AH overall. It is i m p o r t a n t to take into account the difference in preoperative tests in the two groups, since the ATL g r o u p had a higher rate of c o n c o r d a n c e of all tests than the A H group, in w h o m invasive studies were necessary before surgery could be p e r f o r m e d . This almost certainly means that the A H patients were less likely to have a good result, whatever type of surgery was p e r f o r m e d . T h e results for visual m e m o r y bear further c o m m e n t . T h e 'verbal m e m o r y u n i m p a i r e d ' ATL patients and the AH patients showed a tendency towards a postoperative i m p r o v e m e n t in their visuo-spatial memory. This has previously b e e n explained as being due to the loss of the interference with n o r m a l function by the actively discharging focus. 12 This explanation would be m o r e applicable to our ATL group, as this was the g r o u p that showed the best seizure outcome. T h e A H and the 'verbal m e m o r y impaired' ATL g r o u p p e r f o r m e d relatively poorly (< 25th percentile) on immediate recall of visuospatial information preoperatively, even though their abnormalities were j u d g e d to be strongly lateralized to the d o m i n a n t hemisphere. This finding is consistent with earlier reports that delayed recall of the Rey Complex Figure did not distinguish between right- or left-sided surgical patients.19 Further, Goldstein and Polkey 14f o u n d in their study that patients who received left-sided surgery scored better than the right-sided cases on verbal learning preoperatively. Similarly, Zaidel et a125 recently r e p o r t e d their findings on effects of temporal lobectomy and f o u n d that the right medial temporal lobe regions are involved in verbal memory, though not as importantly as the left regions. These findings question the validity of the assumption of strong lateralization of m e m o r y function in temporal lobe epilepsy patients. In conclusion, o u r study showed that if verbal m e m ory was impaired preoperatively, left A H or ATL did not result in further significant deterioration of verbal m e m ory. In patients with u n i m p a i r e d verbal memory, ATL resulted in some decline in verbal m e m o r y and, paradoxically, some i m p r o v e m e n t in visuo-spatial memory. Patients who had good verbal m e m o r y may have had less decline in m e m o r y as a result of the selective procedure, but m o r e of these patients will n e e d to be operated in this way before a definite answer can be given. This study also
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Left temporal Iobectomy and memory supports previous work in raising doubts a b o u t the utility of verbal/non-verbal m e m o r y discrepancy in the lateralization of dysfunction in temporal lobe epilepsy patients. We suggest that future studies should assess diverse m e m ory functions, incorporating behavioural measures of memory.
Acknowledgements The authors acknowledge the assistance of Steven Cumming M Psych andJanine Klamus BAppSci. Secretarial assistance was provided by Doreen Hanlon. Received17 July 1995; Accepted 10 May 1996
Correspondence and offprint requests: Dr R. A. Mackenzie, NPI Prince Henry Hospital, Little Bay,NSW 2036, Australia, Tel: 61 2 525 8344, Fax: 61 2 524 1173 References 1. Binney CD, Polkey CE. Surgery for epilepsy. In: Kennard C (ed). Recent Advances in Clinical Neurology. Edinburgh: Churchill Livingstone, 1992: 55-93. 2. Olivier A. Commentary: cortical resections. In: Engel J(ed). Surgical Treatment of the Epilepsies. New York: Raven Press, 1987: 405-416. 3. Hermann BP, Wyler AR, Bush AJ, Tabatabai FR. Differential effects of left and right anterior temporal lobectomy on verbal learning and memory performance. Epilepsia 1992; 33: 289-297. 4. Channon S, Polkey CE. Memory and temporal lobe surgery: a review, J Roy Soc Med 1990; 83: 100-103. 5. Goldstein LH, Polkey CE. Behavioural memory after temporal lobectomy or amygdalo-hippocampectomy. BKJ Clin Psychol 1992; 31: 75-81. 6. Novelly RA, Augustine EA, Mattson RH et al. Selective memory improvement and impairment in temporal lobectomy for epilepsy. Ann Neurol 1984; 15: 64--67. 7. Ojemann GA, Dodrill CB. Verbal memory deficits after left temporal lobectomy for epilepsy: mechanism and intra-operative prediction.J Neurosurg 1985; 62: 101-107. 8. Rausch R, Crandall PH. Psychological status related to surgical control of temporal lobe seizures. Epilepsia 1982; 23: 191-202. 9. Tucker DM, Novelly RA, Isaac W, Spencer D. Effects of simultaneous vs sequential stimulus presentation on memory performance following temporal lobe resection in humans. Neuropsychologia 1986; 24(2): 277-281. 10. Mishkin iV[,Appenzeller T. The anatomy of memory. Sci Am 1987; 256: 80-89. 11. Zola-Morgan S, Squire LR. Neuroanatomy of memory. Annu Rev Neurosci 1993; 16: 547-563. 12. Yasargil MG, Wieser HG. Selective amygdalohippocampectomy at the University Hospital, Zurich. In: EngelJrJ(ed). Surgical Treatment of the Epilepsies. New York: Raven Press, 1987: 653-658. 13. Wieser HG. Selective amygdalohippocampectomy for temporal lobe epilepsy. Epilepsia 1988; 29 (Suppl,2): 100-113. 14. Goldstein LH, Polkey CE. Short-term cognitive changes after unilateral amygdalohippocampectomy for the relief of temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 1993; 56: 135-140. 15. Wolf RL, Ivnik RJ, Hirschorn KA, Sharbrough FW, Cascino GD, Marsh WR. Neurocognitive efficiency following left temporal lobectomy: standard versus limited resection. J Neurosurg 1993; 79: 76-83. 16. Thompson PJ, Corcoran R. Everyday memory failures in people with epilepsy. Epilepsia 1992; 33: S18-$20.
Left temporal Iobectomy and memory 17. Mackenzie RA, MathesonJM, Ellis M, KlamusJ. Selective versus non-selective temporal lobe surgery for epilepsy. J Clin Neurosci 1997; 4(2): 152-154. 18. Lezak MD. Neuropsychological Assessment, 3rd Edn. New York: Oxford University Press, 1995. 19. Powell GE, Polkey CE, McMillan TM. The new Maudsley series of temporal lobectomy: Short-term cognitive effects. BrJ Clin Psychol 1985; 24: 109-124. 20. Geffen G, Moar KJ, O'Hanlon AP, Clark CR, Geffen LB. The Auditory Verbal Learning Test (Rey) : performance of 16- to 86-year-olds of average intelligence. Clin Neuropsychol 1990; 4: 45-63. 21. EngelJrJ. Outcome with respect to epileptic seizures. In: EngelJrJ (ed) Surgical Treatment of the Epilepsies. New York: Raven Press, 1987: 553-572.
Clinical studies 22. Dodrill CB. Interictal cognitive aspects of epilepsy. Epilepsia 1992; 33(Suppl 6): 7-10. 23. Bennett-LevyJ, Powell GE. The subjective memory questionnaire (SMQ). An investigation into the selfreporting of 'real-life' memory skills. BrJ Soc Clin Psychol 1980; 19: 177-188. 24. Sunderland A, HarrisJE, Baddeley AD. Do laboratory tests predict everyday memory? A neuropsychological study. J Verbal Learning Verbal Behavior 1983; 22: 341-357. 25. Zaidel DW, Oxbury SM, OxburyJM. Effects of surgery in unilateral medial temporal lobe regions on verbal explicit and implicit memory. J Neuropsychiatry Neuropsychol Behav Neurol 1994; 7(2): 104-108.
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