460

Journal of the Royal Society of Medicine Volume 84 August 1991

Neuropsychological investigation of temporal lobe epilepsy

L H Goldstein PhD MPhil

Institute of Psychiatry, De Crespigny Park, London SE5 8AF

Keywords. temporal lobe epilepsy; cognition; neuropsychology-, seizure variables; neuropathology

Formal neuropsychological testing of patients with neurological disorders has been accepted for some 40 years or more as contributing valuable information to their diagnosis and treatment. The emphasis of neuropsychological assessments has shifted somewhat over the years' and their role now includes the provision of a functional description of the patient's cognitive strengths and weaknesses, the identification of rehabilitation goals and the establishment of baseline measures against which to evaluate the effects of pharmacological, neurosurgical or radiological measures. The neuropsychological approach of particular relevance to the assessment of temporal lobe epilepsy (TLE) patients is the delineation of cognitive deficits associated with a particular brain lesion. Consequently, neuropsychological assessments ofTLE patients have generally focused on the assessment of memory, in view ofthe body of knowledge which has accumulated concerning the role of temporal lobe structures (in particular temporal neocortex, hippocampus and amygdala) in learning and memory2 3. Such knowledge has accumulated largely from the study of memory in patients who have undergone temporal lobectomy (TL) for intractable epilepsy. The earliest suggestion that the temporal lobes were critically involved in human memory dates from a report by Bekhterev4 who described a patient who had exhibited a severe memory impairment and who on autopsy was shown to have bilateral softening in the region of the uncus, hippocampus and adjoining medial temporal cortex. In the 1950s, the importance ofthe hippocampus and amygdala in human memory was clearly demonstrated in patients with bilateral damage. Scoville & Milner's patient5 HM is the most extensively studied, having now been followed up for more than 30 years. In 1953 a bilateral medial temporal lobe resection, for intractable epilepsy, produced a severe anterograde memory impairment in this man, which has persisted with little improvement to this day. He is impaired in any memory test where there is a delay between the presentation of material and its recall, especially if given an interpolated distractor task. New motor skills can be acquired, and other instances of procedural learning have been documented67. At least one other patient has been described whose severe memory deficits were attributed to bilateral

hippocampal damage'. The evidence concerning memory impairment in patients with unilateral temporal lobe lesions has also come, for the greater part, from neurosurgicallytreated patients. Attempts have been made to relate memory deficits to the extent of hippocampal and neocortical removal. Jones-Gotman8 compiled a table

of tasks eliciting material-specific memory deficits after unilateral TL, classifying results according to whether small or large hippocampal excisions were performed. Three patterns ofresults emerge after TL. Firstly there are tasks on which the deficit is not exacerbated by encroachment on hippocampal tissue. In a second subgroup, there are tests sensitive to both large and small hippocampal removals, with the large excisions producing greater deficits than the smaller ones. In the third subgroup, deficits are only found with large hippocampal removals. Jones-Gotman's summary of data reflects the well accepted pattern of material-specific memory deficits seen after left and right TLs with in general, verbal learning and memory affected by a left TL-and nonverbal learning and memory by a right TL9-17. Clearly, when conducting a neuropsychological assessment on non-operated patients however, it is uncertain whether the effect of hippocampal or more widespread pathology is being measured. Thus to some extent the assessment leads to the description of the functional abilities of patients, in the context of what else is known on the basis of history, EEGs, scans, medication, etc. It is well accepted that a combination of neuropsychological tests is more effective than any single test in detecting organic dysfunction, and the use of many tests for the patients may be especially important as such patients may only show subtle, if any, overt indications of cognitive impairment. Although reports may exist of single, particularly sensitive tests with the patients18, it is still preferable to administer a selection of tests in order to demonstrate that a circumscribed area of dysfunction exists. As indicated by Rausch'9, interpretation of neuropsychological assessment results in a complex, multistage process. Absolute test scores do not reveal the complete picture, although raw or derived scores must indeed be related to age and IQ normative data, so that an initial impression can be gained of which scores are impaired. The pattern of scores obtained on a variety of tests must then be examined to see whether a subgroup of scores suggest impairments in specific functions. This is in order to be able to identify the key impairment. For example, a low score on a test of auditory verbal memory may be explained by deficits in verbal memory, auditory comprehension attention or learning, and the use of multiple tests may reveal the underlying deficit. The qualitative nature of the patient's responses must also be considered. For example patients with either left temporal or left frontal lobe impairment may perform poorly on a verbal learning task, although the pattern of impairment will differ. Correct interpretation of results therefore depends on clinical experience of

Paper read to Section of

Psychiatry, 13 November 1990

01410768/91/

080460-6/02900/

< 1991 The Royal Society of Medicine

Journal of the Royal Society of Medicine Volume 84 August 1991

patients with varying pathologies. Although not included by Rausch'9, patient-related variables other than age and IQ may also be relevant to neuropsychological interpretation. In particular, seizurerelated variables, such as age of onset and duration of seizures, and seizure frequency will be shown below to be of considerable importance in evaluating test scores. Intellectual assessment: IQ measures Although much of the emphasis of neuropsychological evaluations of TLE patients has been on memory functions, the intellectual level of such patients as measured on IQ tests, and the discrepancy between Verbal and Performance IQ on the Wechsler scales have attracted much attention. In unselected groups of epileptic patients the mean IQ falls within or just below the normal sample, unless epilepsy is associated with more widespread brain damage2O. Even in selected groups, such as a series of 59 patients undergoing unilateral TL for intractable epilepsy, preoperative Performance and Verbal IQs were within the normal range and did not differ significantly between the right and left sided pathology groups21; this reflects, however, the bias in patient selection for surgery since an IQ of less than 70 will contraindicate surgery as it may reflect the presence of generalized brain damage. Debate exists as to whether IQ tests are particularly informative about cognitive functioning in epileptic patients20'22 unless one takes into account factors other than the derived scores. This is because any factor such as medication or subclinical epileptic activity which decreases the speed of performance and efficiency of information processing is likely to depress scores on the timed, Performance subtests. In addition, at high values of Full Scale IQ, Verbal IQ is likely to be greater than Performance IQ whereas the converse applies for low values of Full Scale IQ. In preference to global statements about Verbal-Performance IQ differences in epileptic patients, one should look instead at measures of learning and memory to begin to obtain meaningful information about the cognitive functioning in patients with TLE.

Learning and memory Evidence has amassed which associates memory deficits with temporal lobe foci, in unoperated patients, although findings are not always consistent, and most data have been collected on patients with refractory seizures who were undergoing temporal lobe surgery. For example, Quadfasel & Pruyser23 reported no relationship between verbal memory deficit in TLE patients and the lateralization of the focus, although only six ofthe 30 patients had consistently unilateral spike discharge on the EEG. Glowinski24 also failed to establish a significant relationship between the side of lesion and impairment in verbal and non-verbal memory, although for many individual cases the predictions held in the expected direction. Berent et al.25 were unable to detect non-verbal memory deficits in patients with right sided temporal lobe foci, which may reflect the natural tendency to verbalize the stimulus material and the difficulties in devising tasks which cannot be verbalized'6'26'27. Loiseau et al.28'29 failed to report differences between right and left TLE patients on tests of verbal learning and memory. They explained their initial findings on the

basis of having used too simple test materials; but there was still no effect of lateralization of epileptic focus on memory tasks when a more complex test battery was used. On a more positive note, Ladavas et aL30 found that whilst short-term memory tasks failed to distinguish between the performance of right and left TLE groups, long-term memory tasks did, and in the predicted direction. Similarly, Delaney et al.31 reported that whilst differences were not apparent between right and left TLE on the immediate recall of materials, they were detected on delayed recall. This was a well-designed study, with patients matched on age at onset of epilepsy, duration of epilepsy and seizure frequency. Their tests included the Logical Memory stories, word list learning and the visual reproduction items ofthe Wechsler memory Scale32. Mungas et aL18 described the use of a verbal learning test, similar in structure to the Rey Auditory Verbal Learning Test33. This was administered to left TLE, right TLE and control subjects, with TLE defined on the basis of EEG findings. Performance was similar for all three groups during the immediate recall/learning trials. The performance of the left TLE groups, however, when averaged across three delayed recall trials (free recall, phoneme cued recall and semantic cued recall) was poorer than that ofthe other two groups. Hermann et al.4 reported poor verbal learning ability, impaired immediate memory and increased difficulty in the retrieval of verbal material as well as poor semantic organization in the new verbal learning and recall by left TLE patients whereas right TLE patients performed nearly as well as controls. Agnetti et aL.3 had also demonstrated verbal learning deficits- in patients with left temporal foci though no significant between-groups differences existed on non-verbal retention tests. In view of the emphasis placed earlier on the examination of pattern and quality of scores when interpreting the results of a neuropsychological study, Mayeux et aL's36 study is of interAet. They proposed that what patients and their relatives may experience as an interictal memory impairment may actually be an anomic deficit. The performance of 14 left TLE, seven right TLE and eight patients with generalized tonic-clonic seizures was compared on the WAIS, the Wechsler Memory Scale, the Benton Visual Retention Test37, the Rey Osterreith figure and on two naming tests, including the Boston Naming Test38. No between-groups differences were observed on the memory tests, but the left TLE patients performed very poorly on the confrontation-naming tests. Several measures of verbal learning and memory and intelligence were highly correlated with naming test scores. The studies raise the possibility that methodological factors may be important in determining whether positive or negative findings are reported in a study. The detection of a deficit may depend upon whether the test is sensitive enough to detect it, as well as whether or not the deficit exists in the first place. In addition, as stressed earlier and highlighted by Mayeux et aL's study, the demonstration and interpretation of a deficit will be determined partly by the range of tests administered. It may well be necessary to move from the use of traditional standardized tests, which were not developed for use with this population, to more 'experimental' tests which may have a more theoretical basis and which

461

462

Journal of the Royal Society of Medicine Volume 84 August 1991

may, as in the case of Mungas et at's study throw more light on the role of temporal lobe structures than will global measures of memory, such as are obtained using the Wechsler Memory Scale, for example.

Effect of some patient characteristics on cognitive status Neuropathology Since specific details concerning neuropathology only become available following surgical intervention little attention has been paid to the role of neuropathology in determining cognitive status. Recently, however, neuropathological findings were related to the preoperative cognitive st-atus of 40 Maudsley Hospital operated TLE patients39. Neuropathological findings were subdivided into hippocampal sclerosis (HS), other, tumour-like malformations (OP) and nonspecific findings (NS). HS was associated with febrile convulsions, an earlier onset of regular seizures and poorer preoperative intelligence, when compared with the other neuropathological groups. This was irrespective of the ultimate side of operation and held for Verbal and Performance IQ. For preoperative memory measures, there was an interaction between pathology and ultimate side of operation. Thus the left and right TLE case with HS scored at the same level on the immediate recall of the Logical Memory stores. The left TLE cases with OP had a poorer (below average) level of recall whereas the right TLE cases had an above average level of immediate recall. A similar pattern was found for the delayed recall measure. This interaction did not apply to the delayed recall of the Rey figure. For the NS group, verbal IQ was within the average range and lay mid-way between the scores of the HS and OP groups. The NS group scored similarly to the HS group on delayed recall of the Rey figure, with the scores being somewhat lower than for the OP group. Finally, of the 40 patients, 13 showed amygdalar damage. These patients were compared to those without such damage, and no differences were foundfor any verbal or non-verbal test preoperatively. Thus McMillan et al.'s39 study suggests that patients who had febrile convulsions, and later developed TLE may well be expected to show intellectual impairments when tested as adults. The possible interaction between the longer -term effect of seizures and the presence of HS, neither of which can be dissociated from occurrence of febrile convulsions, make it difflcult to decide on the cause of the lower preoperative IQ in this group. Increased severity of brain damage, a greater possibility of bilateral impairment and reduced capacity for functional reorganization might occur in patients with a longer duration of intractable epilepsy. McMillan et al.'s observations for the OP group, whereby the presence of a left temporal lesion was associated with especially poor verbal,memory, permits the teasing apart of the earlier findings2' of no preoperative differences on memory measures, where scores of all subjects, irrespective of pathology were pooled. In the OP group, onset of epilepsy was likely to have occurred when functions were already localized and fully functioning tissue is likely to have been affected by the disease process. Thus, in considering the presence of material specific memory deficits of ThE patients, the underlying cause of the epilepsy must be taken into account.

Seizure type and frequency As already noted, early age at onset of seizures appears to have a poorer prognosis with regard to intellectual ability, at least in those people who come to surgery as adults. There is some consensus40 that generalized seizures will produce impaired cognitive functioning, either -for the duration of their spikewave abnormality, or in comparison with patients who suffer from partial seizures41 (cf. refs 28 or 29 as far as memory is concerned). Frequent absence seizures may disrupt school performance and lead to educational underachievement. Seizure frequency appears to be related to cognitive status21. Dikmen and Matthews42 noted that a group of patients with a high frequency of motor seizures performed more poorly than patients with low seizure frequency on a variety of tasks, mainly from the WAIS and the Halstead Reitan battery. The worst scores however were in patients with a long seizure history and early age at onset. Decrease in seizure frequency has been seen to be related to improvements on IQ and memory tests, over a test-retest

interval43'". The relationship between the frequency of generalized tonic-clonic seizures and a variety of psychological variables has been examined in a large sample of epileptic patients5. An episode of status epilepticus or more than 100 individual convulsions were associated with decreased functioning in a number of areas. Wilkus and Dodrill46 noted that a group of patients with generalized EEG discharges performed poorest on a battery of psychological tests. In general, those with discharges occurring at a rate of more than one per minute did worse than those with fewer discharges. Thus, frequency of generalized seizures -is an important variable affecting cognitive processing and the rate of interictal EEG activity may also correlate with cognitive impairment. The rate of interictal discharges is relevant for partial as well as generalized epilepsy. Binnie47, reviewing evidence that sub-clinical spikewave discharges may affect performance on cognitive tests, indicated that the demonstration of such transitory cognitive impairment (TCI) depends on the psychological test employed and the nature of the EEG discharges. Intellectually demanding tests, which require high rates of information processing, are those most likely to permit the effects of TCI to be seen. TOI is also most often demonstrable during prolonged generalized, symmetrical and regular spike-wave discharges at about three per second. TCI has also now been shown to occur in focal epilepsy, and a signifcant association has been demonstrated between the locus of discharges and impairment on verbal and nonverbal tasks (which were affected by left and right sided discharges respectively). Discharges during stimulus presentation, rather than in the response phase, were most disruptive of performance. TCI was demonstrated most readily when the level of task performance was close, to the patient's individual limit. Binnie and associates have demonstrated the effects of subclinical discharges in children during performance on a general intelligence test and formal scholastic ability4849. Such finings should therefore call into question the validity of findings from neuropsychological testing of patients with TLE, unless one takes into account the possible effects of TCI. The practical difficulties,

Journal of the Royal Socety of Medicine Volume 84 August 1991

which include the time taken to analyse EEG/video telemetric data, necessary to evaluate the presence and effects of TCI on routine neuropsychological assessment mean that for the most part, the role of TCI in determining neuropsychological -test scores is uncertain. Careful observation of the patient during. testing may however provide some 'impression of whether cognitive functioning is being disrupted spasmodically in any way. Anticonvulsant medication Details exist of the relative effects of different anticonvulsants on a range of neuropsychological functions, derived from studies of drug effects both in patients and normal volunteers (see reviews, ref. 20, 50). In general studies have contrasted the least detrimental effects of carbamazepine with the more harmful effects (in terms of effect on cognitive ability) of phenytoin, with phenobarbitone and clonazepam being associated with the phenytoin end of the spectrum, and sodium valproate seeming to effect cognitive functioning somewhere in between. Factors such as blood serum level and poly versus monotherapy need also to be taken into account when evaluating cognitive performance2.

Interpretation of between- groups differences on neuropsychological measures with- respect to patient characteristics The importance of patient characteristics, and in particular those related to epilepsy, in evaluating between group differences on measures of cognitive functioning will be demonstrated on preoperative neuropsychological assessment results of 50 adult patients under the care of C E Polkey who have undergone surgery for TLE since April 1987, at the Maudsley Hospital. Patients ultimately underwent either a right or left temporal lobectomy (TL) or a right or left amygdalohippocampectomy (AH) the latter having been reported to be likely to produce less cognitive impairment than the traditional en bloc resection51 and being an operation for patients for whom the epileptic focus can be clearly localized in mesial temporal lobe structures rather than in temporal neocortex52. Patient characteristics are displayed in Table 1.

Again it must be noted that these are highly selected groups of patients, in whom there- is no indication of generalized br damage, and differ from Powell et al.'s21 sample in that the AH operation has only been performed relatively recently at the Maudaley. The -tests admin-istered include a short form of the WAISR54, the Logical Memory Passages and verbal paired associates from the Wechsler Memory Scale, the. Rey figure", the Benton Visual Retention Test, digit span (from the WAIS-R) and a spatial span!test, derived from the Corsi block tapping task55. All results here relate to preoperative scores. For prorated Verbal IQ, there are no significant effects of side of operation, even when age at onse of epilepsy, age at surgery, time betweexi onset of epilepsy and surgery and the frequency of preoperative:complex partial, seizures per. month are included as covariates in analyses of covariance (ANCOVA). A similar pattern of results- is obtained for prorated Performance IQ. Thus as with the earlier Maudsley series, Verbal and Performance IQ provide little inforxnation concerning the presence of a right or left temporal lobe focus. A measure derived from the IQ variables, a contrast between the Verbal and Performance IQ seores53, if subjected to simple analysis of variance (ANOVA) or ANCOVAs taking into account seizure-related variables fails to yield any significant main- effects or interactions. This is equally true for a measure termed General Ability IQ, similar but not identical to Full Scale IQ53. ANOVA ofthe immediate recall score ofthe Logical Memory Passages yields a significant interaction between the type of ultimate operation and side of surgery (F(1,44)-5.32, P=0.024). Thus the ultimate right AH group scored lower than did the right TL group, whereas the ultimate left AH group scored higher than did the left TL group. These interactions remain when epilepsy-related covariates are included in the analyses, so these particular patient-related variables cannot account for the significant sidexoperation interactions. The sidex operation interactions approached but did not reach statistical significance for any analysis, for the delayed verbal recall measures. As with Powell et aL's21 data then, preoperative verbal memory

Table 1. Characteristics of 50 patients ultimately receiving temporal lobe surgery for intractable epilepsy LTL (n=15) Sex

Age at onset of epilepsy Ageatonset of chronic epilepsy Age at surgery Neuropathology

7 F, 8 M 7 yr5 m (±4 yr 10 m)

8yr9m, (±5 yr 3 m) 28 yr 5 m (±7 yr 2 m) 8 MTS 4 tumour 1 hamartoma I CD 1 NS

RTL

(n=11) 5 F, 6 M 12 yr l m (±7 yr 8m) 14yr2m (±8 yr 5 m) 32 yr 6 m (±11 yr 1 m) 2 MTS 2 tumour 1 hamartoma 1 CD 5 NS

LAH (n=15)

RAH (n=9)

7 F, 8 M 6 yr 4 m (±6 yr& m) 7yr5m (±7 yr 4 m) 25 yr 4 m (±6 yr 1 m) 13 MTS 2 NS

6 F,3 M 12 yr 6 m (±10 yr 11 m) 13yr9m (±10 yr 9 m) 29 yr 5 m (±8 yr 5 m) 8 MTS 1NS

LTL, ultimate left temporal lobectomy; RTL, ultimate right temporal lobectomy; RAH, ultimate right amygdalohippocampectomy; LAH, ultimate left amygdalo-hippocampectomy; MS, mesial temporal sclerosis; CD, cortical dysplasia; NS, non-specific pathology; ±, standard deviation

463

464

Journal of the Royal Society of Medicine Volume 84 August 1991

scores, as compared simply for side of focus did not distinguish between groups of TLE patients. It may be that the different distribution of neuropathology reported for the AH -and TL groups (see Table 1) holds the explanation to these interactions, although numbers are too small to permit m l statistical analyses to be performed to test this hypothesis. An ANOVA on scores of verbal paired associate learning, not considered by Powell et aL21 failed to yield significant main effects or interactions. This was also the case for the ANCOVAs incorporating the epilepsy-related variables. Similar findings to those of Powell et al.21 were obtained for the percentage recall of the Rey figure in that no between groups differences were detected. On the Benton Visual Retention Test, a test of immediate visuospatial recall, two raw scores can be derived, a correct score, and an error score. For a simple ANOVA on correct scores, the sidexoperation interaction was a significant (F(1,44)=7.66, P=0.008). A similar result was obtained when the epilepsyrelated variables were included as covariates in the analyses. A similar sidexoperation interaction was found for the error scores (F(1,44)=5.27, P=0.026) and this was also significant both for raw scores alone and with the various covariates included, the inclusion of seizure frequency as covariate producing the highest level of significance (F(1,44)=7.28, P=0.011). Thus again these results cannot be explained by the seizure related variables, and suggest that other factors such as neuropathology may be important determinants of these effects. For digit span forwards, no main effects were found until preoperative seizure frequency was included as a covariate, when the side xoperation was significant (F(1,32)=7.58, P=0.01). No main effects or interactions were found on simple ANOVAs or ANCOVAs on measures of spatial span, using the Corsi block tapping task, either forwards or backwards. Thus from an assessment of an albeit highly selected group it can be seen that it is not particularly easy to elicit differences that reflect the side of the epileptogenic focus. Where differences were elicited they were generally of the nature of side xtype of ultimate operation, rather than reflecting clear leftright differences, and one sigaificant interaction only became apparent when an epilepsy-related variable was included in the analyses as a covariate. Thus looking for simple between-groups differences in patients with either left or right temporal lobe foci may be an oversimplification of the differences between patients, and epilepsy-related variables must be taken into account. Although it is not currently possible to verify the hypothesis that underlying neuropathology may in part determine level of cognitive functioning, this is strongly suggested both by current observations and those of McMillan

must be interpreted within the context of a model of cognitive functioning in TLE, and at present, the model proposed by Powell et al.21 and McMillan et al39 is of value, stressing as it does the importance of neuropathology, age of onset of epilepsy and frequency of seizures. Cognitive investigation of TLE therefore should in some -respects be an interdisciplinary process in that the data gathered by different disciplines in the general work-up of the patient must be taken into account in the interpretation of neuropsychological test results.

et al.39.

18 Mungas D, Ehlers C, Walton N, McCutchen CB. Verbal learning differences in epileptic patients with left and right temporal lobe foci. Epikpsia 1985;26:340-5 19 Rausch R. Psychological evaluation. In: Engel J, Jnr, ed. Surgical treatmnent ofthe epilepsies. New York: Raven Press, 1987:181-95 20 Trimble MP¢, Thompson PJ. Neuropsychological aspects of epilepsy. In: Grant I, Adams KM, eds. Neuropsychological assessment of neuropsychiatric disorders. New York: Oxford University Pre-ss, 1986:321-46 21 Powell GE,< Polkey CE, M^Millan TM.. Th!e new Maudsley sries of temporal loetmy, I: short term cognitive effects. Br J Clin Psy,chol 1986234:109-24

Conclusions Test sensitivity, range of tests administered and patient characteristics determine whether materialspecific memory and other cognitive deficits will be detected in patients with TLE. At present memory tests and possibly some tests of language functioning must continue to offer a major-tool in assesing patients with TLE, but more theoretically-based experimental measures must continue to be developed66. Neuropsychological assessment results

References 1 Kolb B, Whishaw IQ. Fundamentals of human neuropsychology, 3rd edn. San Francisco: WA Freeman, 1990 2 Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg 1972; 19:421-46 3 Mishkin M, Appenzeller T. The anatomy of memory. Sci Am 1987;25:80-9 4 Bekhterev VM. Demonstration eines Gehirns mit zerstor;ng der vordereu und inneren Theile der Hirrinde beider Schlafenlappen. Neurol Zbl 1900;19:990-1 5 Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957;20:11-21 6 Milner B, Corkin S, Teuber H-L. Further analysis of the hippocampal amnesic sndrome: 14 year follow-up study of H.M. Neuropsychologia 1968;6:215-34 7 Cohen NJ, Corkin S. The amnesic patient H.M: learning and retention of a cognitive skill. Neurosci Abst 1981;7:235 8 Jones-Gotman M. Commentary: psychological evaluation - testing hippocampal function. In: Engel J Jnr, ed. Surgical treatment of the epilepsies. New York: Raven Press, 1983:203-11 9 Prisko L. Short-term memory in focal cerebral damage. PhD Thesis, McGill University, 1963 10 Kimura D. Right temporal-lobe damage: perception of unfamiliar stimuli after damage. -h Neurol 1963;8: 264-71 11 Milner B. Brain mechanisms suggested by studies of temporal lobes. In: Millikan CH, Darley FL, eds. Brain mechanisms underlying speech and language. New York: Grune & Stratton, 1967:122-32 12 Warrington EK, James M. An investigation of facial recognition in patients with unilateral cerebral lesions. Cortex 1967;3:317-26 13 Milner B. Visual recognition and recall after right temporal-lobe excision in man. Neuropsychologia 1968;6:191-209 14 Taylor L. Localisation of cerebral lesions by psychological testing. Clin Neurosurg 1969;16:269-87 15 Corsi PM. Human memory and the medial temporal region ofthe brain. PhD Thesis, McGill University, 1972 16 Jones-Gotman M. Memory for designs: the hippocampal contribution. Neuropsychologia 1986;24:193-203 17 Frisk V, Milner B. The relationship of working memory to the immediate recall of stories following unilateral temporal or frontal lobectomy. Neuropsychologia

1990;28:121-35

Journal of the Royal Society of Medicine Volume 84 August 1991

22 Ossetin J. Methods and problems in the assessment of cognitive function in epileptic patients. In: Trimble MP, Reynolds EH, eds. Epilepsy, behaviour and cognitive function. Chichester: Wiley, 1988:9-26 23 Quadfasel AF, Pruyser PW. Cognitive deficits in patients with psychomotor epilepsy. Epilepsia 1955;4:80-90 24 Glowinski H. Cognitive deficits in temporal lobe epilepsy: An investigation of memory function. J Nerv Ment Dis 1973;137:129-37 25 Berent S, Bolt TJ, Giordani B. Hemispheric site of epileptogenic focus: Cognitive, perceptual and psychosocial implications for children and adults. In: Canger R, Angeleri F, Penry JK, eds. Advances in epileptology. New York: Raven Press, 1980 26 Goldstein LH, Canavan AGM, Polkey CE. Verbal and abstract designs paired associate learning after unilateral temporal lobectomy. Cortex 1988;24:41-52 27 Goldstein LH, Canavan AGM, Polkey CE. Cognitive mapping after unilateral temporal lobectomy. Neuropsychologia 1989;27:167-77 28 Loiseau P, Strube E, Broustet D, Battelochi S, Gomeni C, Morselli PL. Learning impairment in epileptic patients. Epilepsia 1983;24:183-92 29 Loiseau P, Strube E, Signoret J-L. Memory and epilepsy. In: Trimble MR, Reynolds EH, eds. Epilepsy, behaviour and cognitive function. Chichester: Wiley, 1985:165-76 30 Ladavas E, Umilta C, Provinciali L. Hemispheredependent cognitive performances in epileptic patients. Epilepsia 1979;20:493-502 31 Delaney RC, Rosen RJ, Mattson RH, Novelly RA. Memory function in focal epilepsy. A comparison of nonsurgical unilateral temporal lobe and frontal lobe samples. Cortex 1980;16:103-17 32 Wechsler D, Stone CP. The Wechsler Memory Scale. New York: Psychological Corporation, 1945 33 Rey A. L'Examen clinique en psychologie. Paris: Presses Universitaires de France, 1964 34 Hermann BP, Wyler AR, Richey ET, Rea JM. Memory function and verbal learning ability in patients with complex partial seizures of temporal lobe origin. Epilepsia 1987;28:547-54 35 Agnetti V, Ganga M, Murrigaile M, Piras MR, Ticca A. Memory assessment in temporal lobe epilepsy. Paper presented at the 11th Epilepsy International Symposium, Florence Italy, 1979. 36 Mayeux R, Brandt J, Rosen J, Benson DF. Interictal memory and language impairment in temporal lobe epilepsy. Neurology 1980;30:120-5 37 Benton AL. Revised visual retention test manual. New York: Psychological Corporation, 1974 38 Kaplan E, Goodglass H, Weintraub S. The Boston Naming Test. Philadelphia: Lee & Febiger, 1983 39 McMillan TM, Powell GE, Janota I, Polkey CE. Relationships between neuropathology and cognitive functioning in temporal lobectomy patients. J Neurol Neurosurg Psychiatry 1987;50:167-76 40 Trimble MR. Cognitive hazards of seizure disorders. In: Trimble MR, ed. Chronic epilepsy, its prognosis and management. Chichester: Wiley, 1989:103-11

41 Giordani B, Berent S, Sackellares JC, Rourke D, Seidenberg M, O'Leary DS, Dreifuss FE, Ball JT. Intelligence test performance of patients with partial and generalised seizures. Epilepsia 1985;26:37-42 42 Dickmen S, Matthews CG. Effects of major motor seizure frequency on cognitive-intellectual function in adults. Epilepsia 1977;18:21-9 43 Seidenberg M, O'Leary DC, Berent S, Boll T. Changes in seizure frequency and test-retest scores in the WAIS. Epilepsia 1981;22:75-83 44 Goldstein LH, Patel V, Aspinall P, Lishman WA. The effect of anticonvulsants on cognitive functioning following a probable encephalitic illness. Br JPsychiatry 1991 (in press) 45 Dodrill CB. Correlates of generalised tonic-clonic seizures with intellectual, neuropsychological, emotional and social function in patients with epilepsy. Epilepsia 1986;27:399-411 46 Wilkus RJ, Dodrill CB. Neuropsychological correlates of the EEG in epileptics. Epilepsia 1976;17:89-100 47 Binnie CD. Seizures, EEG discharges and cognition. In: Trimble MR, Reynolds EH, eds, Epilepsy, behaviour and cognitive function. Chichester: Wiley, 1988:45-9 48 Siebelink RM, Bakker DJ, Binnie CD, Kastelein-Nolst Trenith DGA. Psychological effects of sub-clinical epileptiform EEG discharges in children. II: General intelligence tests. Epilepsy Res 1988;2:117-21 49 Kasteleijn-Nolst Trenite DGA, Bakker DJ, Binnie CD, Buerman A, van RaaiJ M. Psychological effects of subclinical epileptiform discharges. I: Scholastic skills. Epilepsy Res 1988;2:111-16 50 Trimble MR. Anticonvulsant drugs: mood and cognitive function. In: Trimble MR, Reynolds EH, eds. Epilepsy, behaviour and cognitive function. Chichester: Wiley, 1988:135-43 51 Wieser HG, Yasargil MG. Selective amygdalo hippocampectomy as a surgical treatment of mediobasal limbic epilepsy. Surg Neurol 1982;17:445-57 52 Polkey CE, Binnie CD, Janota I. Acute hippocampal recording and pathology at temporal lobe resection and amygdalohippocampectomy for epilepsy. J Neurol Neurosurg Psychiatry 1989;52:1050-7 53 Canavan AGM, Dunn G, McMillan TM. Principle components of the WAIS-R. Br J Clin Psychol 1986; 25:81-5 54 Rey A. Le test de copie defigure complexe. Paris: Presses Universitaires de France, 1959 55 Canavan AGM, Passingham RE, Marsden CD, Quinn N, Wyke M, Polkey CE. Sequencing ability in parsonins, patients with frontal lobe lesions and patients who have undergone unilateral temporal lobectomies. Neuropsychologia 1989;27:787-98 56 Fenwick P, Anderson E. Lateralised cognitive tests and the CNV used to detect temporal lobe damage. Paper presented at the 17th Epilepsy International Congress, Jerusalem 1987.

(Accepted 29 April 1991)

465

Neuropsychological investigation of temporal lobe epilepsy.

460 Journal of the Royal Society of Medicine Volume 84 August 1991 Neuropsychological investigation of temporal lobe epilepsy L H Goldstein PhD MPh...
1MB Sizes 0 Downloads 0 Views