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Assessment of verbal memory in temporal lobe epilepsy using the selective reminding test: Equivalence and reliability of alternate forms
J Epilepsy 1994;7:57-63 © 1994 Butterworth-Heinemann
Assessment of Verbal Memory in Temporal Lobe Epilepsy Using the Selective Reminding Test: Equivalence and Reliability of Alternate Forms Michael Westerveld, Kimberlee J. Sass, Arlene Sass, and Hugh G. Henry
Each of four forms of the verbal Selective Reminding Test (vSRT) were administered in counterbalanced order to 24 patients with epilepsy. Results of repeatedmeasures analysis of variance indicated that the forms were equivalent in difficulty. Furthermore, no practice effect was detected, in that performance on the first administration did not differ significantly from the second, third or fourth administrations, regardless of form. Although the four forms were found to be equivalent in difficulty and without significant practice effect, intercorrelation of forms was modest in magnitude. The measures derived from standard scoring of the vSRT (Total Recall, Long-Term Storage, Long-Term Retrieval, and Consistent Long-Term Retrieval) were highly intercorrelated. Factor analysis of these indices yielded a single factor solution for each of the four forms. We recommend using a single composite measure and obtaining multiple baseline estimates. This may provide a more reliable and stable estimate of verbal memory impairment, resulting in improved identification of patients with dominant temporal lobe epilepsy. Key Words: Temporal lobe epilepsy--Verbal memory--Selective Reminding Test.
Assessment of verbal m e m o r y plays an important role in the selection and presurgical evaluation of patients with temporal lobe epilepsy. Various verbal m e m o r y measures are sensitive to disease within the dominant temporal lobe; however, the Selective Reminding procedure (1) is unique among verbal memory measures in that it is significantly correlated with hippocampal pyramidal cell density obtained from pathologic analysis of excised tissue from the left, but not the right, of left-speech-dominant adults (2). Using the four 12-item word lists presented by Hannay
Received June 9, 1993; accepted September 30, 1993. From the Section of Neurological Surgery, Yale University School of Medicine, New Haven, CT, U.S.A. Address correspondence and reprint requests to Dr. M. Westerveld at Section of Neurological Surgery, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, U.S.A.
and Levin (3), Sass et al. (2) demonstrated that the verbal Selective Reminding Test (vSRT) scores are correlated with hippocampal pyramidal cell density in CA3 and the hilar area of the dentate (2). Leftspeech-dominant patients with severe hippocampal neuron loss experience no significant decrement in vSRT performance followingtotal excision of the left hippocampus (4). However, those with mild or moderate neuron loss decline significantly. Although recent research demonstrates the utility of the vSRT as an index of hippocampal pathology, prior studies with healthy adults raise concerns about the psychometric properties of this test. Buschke (1) developed the selective reminding procedure to differentiate impairments of information storage, retention, and retrieval. The procedure has been criticized for its failure to do so (5). Significant correlations have been reported between the various indices obtained by standard scoring methods (5,6). Factor ] EPILEPSY, VOL. 7, NO. 1, 1994
57
M. WESTERVELD ET AL.
analysis of vSRT indicates that these indices reflect a single construct (6). Alternate word lists have been developed to facilitate research involving serial assessment (3,7), but the forms are not equivalent in difficulty, alternate form reliability is marginal and a practice effect hinders the interpretation of changes in test scores (3). The psychometric properties of the vSRT may differ when the test is administered to clinical samples. It is plausible that differentiation of storage and retrieval processes may not be possible for healthy adults with intact memory, but the distinction could be relevant for patients with memory disorders. It is also plausible that the apparent disparity in form difficulty results from the relative ease with which associations are made among the individual test stimuli. The four vSRT forms may be equally difficult for patients with clinical memory disorders, if they are less facile in forming such associations. Finally, patients with significant memory disorders may not benefit from practice, as healthy adults do. The present study was performed to examine the psychometric properties of the four vSRT forms when administered to a sample of patients with seizure disorders. It was hypothesized that the four forms would be of equivalent difficulty for this sample, and that there would be no significant practice effect with serial administration. It was further hypothesized that the five vSRT scores obtained by standard scoring practice would not correlate with each other to the degree previously reported for healthy adults.
Me~od Subjects
Twenty-four consecutive patients (13 women and 11 men) admitted to the Yale Epilepsy Surgery Program for evaluation of medically refractory epilepsy were examined using the procedures detailed below. The mean age of the sample was 30.2 years (SD = 9.6 years). The average education was 12.7 years (SD = 3.8), and the mean WAIS-R Verbal IQ score was 93.6 (SD = 16.3). All but one of the patients had partial complex seizures (one patient had generalized seizures). Eighteen of 24 had partial complex seizures of temporal lobe origin; 16 of these had unilateral temporal lobe origin (6 left temporal, 10 right temporal). Two additional patients had bilateral seizure onset by scalp EEG. Five patients had seizures of frontal lobe origin, and one patient's seizures were of unknown origin. The average age of onset of refractory seizures for the 58 J F_~ILEPSY, VOL. 7, NO. 1, 1994
entire sample was 13.23 (+ 10.3 years). Nine patients had histories of one or more febrile convulsions with refractory seizures beginning later in life. Only 2 patients were found to have structural lesions (one temporal lobe arteriovenous malformation and one frontal lobe tumor). One patient had documented history of encephalitic coma, and one patient had a history of traumatic brain injury with seizures beginning within 2 years postinjury. Material and Methods Each of the patients was randomly assigned to one of the 24 possible permutations of administration order (e.g., 1234, 1243, 1342, etc.). These patients were administered one form of the vSRT during each of the first 4 days of their hospitalization for audio/ video and EEG evaluation. The first administration was performed on the day of admission. The second and third administrations were performed in the context of our standard comprehensive neuropsychologic test battery. Like the first administration, the fourth administration was not in the context of other neuropsychological tests and was performed following completion of the full neuropsychologic test battery. Eight of the 24 patients had no seizures recorded during the first 3 days following admission; an additional 2 patients had seizures only nocturnally. Only 5 of the 24 patients had more than 3 seizures during the course of the 4 test administrations. However, no SRT administrations occurred within 2 h of a seizure. Patients were on a variety of medication regimens, and schedules for the tapering of medication for patients who did not have spontaneous seizures were done on an individual basis. The relatively large number of medication combinations and tapering schedules in relation to the number of patients precludes statistical analysis of this factor. The four word lists administered are those presented by Hannay and Levin (3). Testing with the vSRT was conducted at approximately the same time of day for each of the four forms. The test was administered and scored according to standard practice. The entire word list was presented on only the first trial. On subsequent trials, only those words that were not recalled on the immediately preceding trial were repeated. Administration was continued in this manner until the patient recalled the entire word list on 2 consecutive trials or until 12 trials had been completed. Total recall (TR), long-term storage (LTS), retrieval from long-term storage (LTR), consistent long-term retrieval (CLTR), and short-term recall (STR) were computed. TR was the total number of words recalled
VERBAL MEMORY ASSESSMENT on all trials throughout the test. When the patient achieved the termination criterion before 12 trials were completed, a score of 12 (full credit) was assigned for all trials not administered. A word was considered to have entered LTS when it was recalled on two consecutive trials. Consequently, this was calculated by s u m m i n g the n u m b e r of words that met the criterion of having entered LTS, regardless of subsequent recall. LTR (long-term retrieval) was defined as the total n u m b e r of words meeting the criterion for LTS that were actually recalled. CLTR was calculated by s u m m i n g the n u m b e r of words that were recalled from LTS without failure on all subsequent trials. STR was calculated by subtracting the n u m b e r of words that were recalled from long-term storage (LTR) from the total words recalled on any given trial (TR). Intact m e m o r y is shown by elevated scores on scales TR, LTS, LTR, and CLTR, and by lower scores on scale STR. Results Mean scores and SDs for this sample on each of the four forms are s u m m a r i z e d in Table 1. Repeatedmeasures analysis of variance (ANOVA) was used to evaluate the significance of m e a n differences between forms on each of the vSRT indices. The main effect for test form is not statistically significant. Average scores for each administration trial, regardless of form, are presented in Table 2. Performance i m p r o v e m e n t with successive trials was not observed. Indeed, the m e a n scores are suggestive of a mild performance decrement; however, the results of
Table 1.
VerbalSelective Reminding Test results (means and standard deviations) vSRT form
TR LTS LTR CLTR STR
1
2
3
4
Result
101.9 (17.6) 95.6 (25.3) 83.0 (28.0) 53.5 (36.0) 18.4 (11.67)
104.8 (19.6) 98.5 (26.6) 89.0 (28.5) 62.8 (35.3) 16.2 (11.45)
106.0 (16.7) 101.3 (20.8) 90.1 (25.0) 61.5 (33.4) 16.3 (10.42)
105.5 (16.9) 95.2 (22.0) 85.7 (25.0) 59.2 (32.9) 18.9 (9.60)
NS NS
Table 2.
Results for administration order (means and standard deviations) vSRT administration order
TR LTS LTR CLTR STR
1
2
3
4
Result
106.9 (16.1) 101.7 (20.9) 91.2 (24.3) 64.2 (34.2) 14.7 (9.48)
103.4 (18.4) 94.3 (27.2) 84.0 (29.9) 58.5 (35.8) 18.9 (12.7)
104.8 (16.6) 98.8 (19.1) 88.1 (22.9) 58.2 (30.6) 16.8 (7.7)
103.2 (18.4) 94.7 (26.8) 84.5 (28.7) 56.2 (36.9) 19.3 (12.2)
NS NS NS NS NS
For abbreviations, see Table 1. a repeated-measures ANOVA indicated that this was not statistically significant. The n u m b e r of intrusions from prior lists during administrations 2, 3, and 4 were negligible. Twelve of the 24 patients made no intrusions. In total, only 16 intrusions from previous lists were recorded for the other 12 patients. The m e a n n u m b e r of intrusions for the entire sample was 0.22 per person, per administration. Thus, each patient could be expected to make approximately one intrusion during either the second, third, or fourth administrations. Table 3 summarizes the differences between the m a x i m u m and m i n i m u m scores obtained by patients during the administration of the four vSRT forms. The differences were sometimes extreme, particularly for the measures of LTS, LTR, and CLTR. Five patients (21%) achieved LTS scores that varied by 50 points or more. Four patients achieved LTR scores that differed by 50 points, and this variability was observed with respect to CLTR for 6 patients. In contrast, differences between m a x i m u m and m i n i m u m performances never exceeded 40 points for TR.
Differences between maximum and minimum scores (numbers of patients)
Table 3.
NS
Range
Recall
LTS
LTR
CLTR
STR
NS
<10 10-19 20-29 30-39 40-49 50-59 >60
3 10 8 3 0 0 0
0 4 5 5 5 3 2
1 4 6 3 6 3 1
2 4 0 7 5 2 4
6 7 9 2 0 0 0
NS
Abbreviations: TR, total recall; LTS, long-term storage; LTR, long-term retrieval; CLTR, consistent long-term retrieval; STR, short-term recall; NS, not significant.
J EPILEPSY,VOL, 7, NO. 1, 1~94 59
M. WESTERVELDETAL. Table 4.
Correlations between forms
Table 6.
vSRT index
Factor loading of SRT indices on their respective factors a Form
Form with
TR
LTS
LTR
CLTR
STR
1/2 1/3 1/4 2/3 2/4 3/4
0.63b 0.69c 0.6¥ 0.78c 0.8¥ 0.75¢
0.38a 0.51b 0.48b 0.36a 0.54b 0.58b
0.49 b
0.58 b
0.61b 0.55b 0.66c 0.69~ 0.66c
0.66c 0.60b 0.81¢ 0.76¢ 0.68c
0.25 0.48b 0.40~ 0.37~
SRTindex
0.52 b 0.53 b
TR LTS LTR CLTR
1
2
3
4
0.964 0.977 0.997 0.954
0.946 0.958 0.998 0.904
0.940 0.982 0.997 0.964
0.955 0.973 0.991 0.962
°All four forms yielded single-factor solutions. One-tail significance levels: ap < 0.05, bp < 0.01, Cp < 0.001. Alternate forms reliability was examined by calculating the correlation coefficients of the vSRT indices for the four forms. These results are summarized in Table 4. All but one of these correlations were statistically significant (p < 0.05). The magnitude of the correlation coefficients ranged from 0.25 to 0.84. In general, correlation coefficients were greater in magnitude for TR (range, 0.63-0.84) and CLTR (range, 0.58-0.81), versus LTS (range, 0.36-0.58), LTR (range, 0.49-0.69), and STR (range, 0.25-0.53). Two analyses were conducted in order to evaluate the possible influence of seizure occurrence on SRT scores. Change in SRT performance from the first administration to the fourth was not correlated with
Table 5.
Form 1 Recall LTS LTR CLTR Form 2 Recall LTS LTR CLTR Form 3 Recall LTS LTR CLTR Form 4 Recall LTS LTR CLTR
Correlations of vSRT indices
LTS
LTR
CLTR
STR
0.94
0.97 0.98
0.92 0.88 0.94
-0.80 -0.90 -0.91 -0.86
0.88
0.95 0.96
0.92 0.75 0.89
-0.67 -0.89 -0.86 -0.67
0.89
0.95 0.98
0.96 0.90 0.96
-0.69 -0.93 -0.87 -0.78
0.91 0.89 0.94
-0.73 -0.83 -0.82 -0.84
0.92
0.97 0.98
All correlations are statistically significant (p • 0.001). 60
J EP/LEPSY, VOL. 7, NO. 1, 1994
seizures that occurred in the first 3 days following admission (r = 0.294; p > 0.15). Eight of the 24 patients had no seizures recorded during this period. The mean change in performance (factor score for the first form administered minus factor score for the fourth form administered) for these 8 patients is not significantly different from the mean change in performance for the 8 patients with the highest seizure frequency over the first 3 days following admission (t = 0.664; p = 0.517). The correlations of the vSRT indices with each other also were calculated for each of the four forms. The indices derived from standard scoring of the vSRT are highly intercorrelated (see Table 5). Factor analysis of forms 1, 3, and 4 indicated that a single factor solution accounted for more than 90% of the variance. A single factor solution accounted for 87.7% of the variance for form 2. The results of factor analysis are presented in Table 6. Two methods were employed to compute a single index for the vSRT, since factor analysis suggested that the individual scores measure the same construct. The first involved computation of factor scores, using the factor coefficients presented in Table 7. STR was not employed in the computation of the factor scores. The information it conveys is redundant, since it represents the difference between TR and LTR. The factor score coefficients for the vSRT scores are virtually identical. Therefore, each vSRT component contributes equally to the factor score. For this reason, essentially the same information is obtained by averaging the raw scores. The second Table 7.
Recall LTS LTR CLTR
Factor scores
Form1
Form2
Form3
Form4
0.25707 0.25486 0.26102 0.25019
0.26555 0.25462 0.26973 0.25194
0.25440 0.25226 0.26068 0.25612
0.25590 0.25530 0.26158 0.25137
VERBAL MEMORY ASSESSMENT Table 8.
Correlationsof summary scores Factor score
Form 1 Form 2 Form 3
Form 2
Form 3
Form 4
0.54°
0.64 b 0.68 b
0.58a 0.73b 0.69 b
Practice Effect and Equivalence of Forms
Sum of raw scores
Form 1 Form 2 Form 3
also found the vSRT indices to be highly intercorrelated; factor analysis yielded single factor solutions for each of the four forms. Our findings have important implications for the assessment of verbal memory in the presurgical evaluation of patients with epilepsy.
Form 2
Form 3
Form 4
0.53°
0.64 b
0.58° 0.72b 0.70~
0.70b
One-tail significance levels: "p • 0.01, bp ¢~ 0.001. summary score is the mean of TR, LTS, LTR, and CLTR. Table 8 presents the correlations of factor scores and mean scores for the four vSRT forms. The correlation coefficients for the factor scores range from 0.54 to 0.73. The correlation coefficients for raw score means are essentally the same. These coefficients are slightly lower than the coefficients for total recall (range, 0.63-0.84) and CLTR (range, 0.58-0.81). They are comparable to the coefficients for LTR (range, 0.49-0.69) and somewhat greater than the coefficients for LTS (range, 0.36-0.58) and STR (range, 0.250.53). Two computations were performed to" determine whether ~ultiple assessments of m e m o r y can reduce error variance. The first involved correlation of the mean of the first two administrations (regardless of form) with the mean of the last two administrations. The correlation coefficients were 0.75 when factor scores were employed and 0.74 for raw scores. Both coefficients were statistically significant (p < 0.001). The second involved correlation of the better score of the first two administrations (regardless of form) with the better of the second two administrations. The correlation coefficients were 0.82 when factor scores were employed and 0.75 for raw scores.
Discussion The results of the present study indicate that, for an unselected (i.e., consecutive) sample of patients undergoing inpatient evaluation of seizure disorders, the four forms of the vSRT were equally difficult. Furthermore, there was no significant practice effect when multiple administrations were performed. We
We did not confirm the practice effect that was previously reported by Hannay and Levin (3). These authors administered four vSRT forms to a sample of college studients at 1-week intervals using a Latin square experimental design. They found that performances during the third and fourth administrations surpassed that of the first administration, regardless of form. The authors inferred that experience with the task-enhanced performance. Scores obtained during the second, third, and fourth administrations did not differ significantly from one another. There are several possible explanations for the absence of a practice effect in our sample. The overall performance of our sample was impaired for all four forms of the test. This finding is unlikely to be a result of global cognitive impairment, since the mean VIQ was within the average range. Poor acquisition of novel information is asociated with some medically refractory seizure disorders, particularly those involving the temporal lobe. The failure to profit from experience with this test procedure may be a further reflection of this learning deficit. This interpretation would be consistent with the observations of other authors who failed to identify practice effects in patients with dementia (8). It is also possible that our sample's failure to profit from test experience was attributable to proactive interference. Hannay and Levin (3) administered the tests with 1-week intervals between administrations. Our patients completed the tests four consecutive days. Although it is plausible, this hypothesis is not supported by the data. A large number of intrusions would be expected, if proactive interference was responsible for the absence of a practice effect. The actual n u m b e r of intrusions from previous word lists was negligible. It is also plausible that a number of uncontrolled factors associated with hospitalization for seizure evaluation (e.g., p o o r sleep, medication changes, effects of seizures) hindered the patient's ability to profit from test experience. The relatively small sample size in relation to the number of medication combinations precluded statistical analysis of this as a source of error. However, it has been noted else-
J EPILEPSY,VOL. 7, NO. 1, 1994 61
M. WESTERVELD EF AL.
Table 9.
Difference between maximum and minimum scores
Hannay and Levin (3)°
Recall LTS LTR CLTR STR
Present sample =
Dif
Forms
Dif
Forms
5.85 9.30 9.50 10.63 4.05
2 -
4.1
3-
1
4- 1 4- 1 2- 1 1 - 4
6.1 7.1 9.3 2.7
3324-
4 1 1 2
1
=Dif,difference between highest and lowest scores; forms, test form of highest score - test form of lowest score.
where (9) that there is little evidence for selective effects of AEDs on memory. The effects of seizures during hospitalization is also a potential source of error. It is possible that increasing seizures over the course of hospitalization had an effect on performance, effectively negating any demonstration of practice effect that might otherwise be observed. We believe that this is not likely in our sample for several reasons. No patient was administered the SRT within 2 h of a seizure. Only 5 of the 24 patients had more than 3 seizures during the 4 days of SRT administration. Furthermore, change in SRT scores over the course of administration was not consistently related to the n u m b e r of seizures recorded. The correlation between change in test score from first to fourth administration was not significant. Many (33%) of the patients actually had no seizures during the 4 days of testing, and most patients did not have an increase in seizure activity relative to their baseline. Finally, the mean change in SRT performance for the 8 patients who had no seizures recorded during the period of test administration did not differ significantly from those patients w h o had the greatest n u m b e r of seizures recorded during the course of the four test administrations. Our sample also found each of the four forms equally difficult. This is in contrast to results obtained with healthy adults that indicate form I is more difficult than the other forms (3). Table 9 contrasts the range of scores reported by Hannay and Levin (3) and those obtained by our patients. The difference between the maximum and minimum scores obtained for our patients was less than that reported by Hannay and Levin. Ruff et al. (10) suggested that healthy adults who performed effectively on the vSRT had relatively more efficient strategies for making associations among the stimuli. These authors implied that lower associational values for items comprising form 1 account for its difficulty. Neurologically impaired 62 J EPILEPSY,VOL. 7, NO. 1, 1994
patients may find the vSRT forms equally difficult because they poorly utilize verbal association strategies. Therefore, they are unable to benefit from the higher associational values of stimuli that comprise the other forms. The demonstration that the four word lists of the verbal Selective Reminding Test are statistically equivalent for a sample of patients with epilepsy is important because there are few m e m o r y tests that provide alternate forms for assessment of change following some intervention (e.g., surgery, effects of AEDs). Demonstration that alternate forms are equivalent in difficulty and performance is not subject to significant practice effects facilitates assessment of meaningful change. However, the utility of the vSRT for serial assessment must be considered with respect to its reliability.
Alternate Forms Reliability We found significant correlations between the indices of all four forms. The results of our study are similar to those of Hannay and Levin (3), who reported statistically significant but modest reliability coefficients (Table 4). Variance in performance on alternate forms was sometimes extreme, particularly for the measures of LTS, LTR, and CLTR (Table 3). Modest reliability is a significant problem for the vSRT. It hinders the interpretation of change following intervention. Error variance may be reduced by administration of two forms and utilizing a composite vSRT index to demonstrate a patient's current memory functioning. As reported above, two computations were performed to evaluate this practice. The first involved computation of correlation between the mean of the first two administrations (regardless of form) with the mean of the last two administrations. The correlation coefficient obtained by this method (0.75 for factor scores and 0.74 for the mean of raw scores) surpassed all of the correlation coefficients between single forms (Table 8). The second computation involved correlation of the better score of the first two performances with the better of the latter two. This computation was based on the notion that patients may perform below their true level of ability for a n u m b e r of reasons (e.g., inattention, physical discomfort, fatigue, depression, etc.), but it is far less likely that coincidental events (e.g., presence of objects in the room that serve as obvious cues for test items) will result in a performance that exceeds the true level of ability. Therefore, the better of two performances is probably the more accurate. The correlation coefficients (0.82 for factor scores and 0.75 for raw scores) were comparable to those based on mean
VERBAL MEMORY ASSESSMENT values. A significant portion of error variance is not necessarily inherent in the test, but rather the patient; use of the mean or the better of two baseline assessments minimizes this source of error, thereby enhancing interpretation of change.
Interpretation of vSRT Indices The selective reminding procedure is intended to differentiate storage, retention, and retrieval in the assessment of verbal m e m o r y disorders. However, the scores that ostensibly reflect the relative efficiency at each stage are highly intercorrelated. Factor analyses of forms 1, 3, and 4 yielded single factor solutions that accounted for at least 90% of the variance; the single factor extracted from analysis of form 2 accounted for 87.5% of the variance. A single index from among those obtained using standard scoring methods should adequately convey the vSRT result, given the redundancy of the scores. However, it is unclear which of the indices one should use. TR and CLTR are the most reliable, but 25% of the sample obtained CLTR scores that differed by 50 points or more. These data favor use of TR, but the TR variance is relatively less than LTS, LTR, and CLTR, which suggests that it may be less sensitive than the other indices to clinically significant m e m o r y components. This would be expected because TR is the sum of words recalled from LTS and STS. Our results indicate that a summary score provides the best estimate of ability, given that the individual indices contribute to the total score. One summary score may be derived from the factor analytic data. However, since our results are based on a relatively small sample size for factor analysis, the results may be somewhat sample-specific. Alternatively, a summary score composed of the mean of the TR, LTR, LTS, and CLTR scores provides a similar measure of stability. The results of this study suggest that performing a minimum of two assessements of m e m o r y and utilizing a composite index of performance may improve the reliability of the vSRT, and consequently enhance its ability to identify patients with dominanthemisphere temporal lobe disease. The negligible number of intrusions from previous lists indicate that multiple examinations can be performed with as little as 24 h between assessments. Even so, it may often be difficult to obtain two measures in many clinical settings, and it could reasonably be argued that, since other measures require only one administration, obtaining two measures would be unnecessarily time-consuming. However, we believe that the relative value of the information obtained by utilizing two forms of the SRT justifies the expenditure of time.
Prior evidence indicates that the SRT is significantly correlated with hippocampal cell counts, and that preoperative assessments using the vSRT may be a measure of hippocampal pathology (2), and the SRT provides greater opportunity for assessment of change with minimal influence of practice. In conclusion, our study supports the use of the vSRT as a valid means of identifying patients with dominant temporal lobe epilepsy. Prior reports have established that the SRT can distinguish between dominant and nondominant temporallobe disease (2, 11). The present study addresses some of the perceived limitations of the SRT as an assessment technique. We conclude that the utility of the vSRT would be enhanced by interpreting a composite measure comprised of all the derived scores rather than interpreting one or more of these scores individually. When feasible, multiple baseline assessments should also be obtained. Finally, in patients with epilepsy, the four forms of the vSRT are equivalent and may be used interchangeably. References
1. Buschke H. Selective Reminding for analysis of memory and learning. ] VerbLearn VerbBehav 1973;12:54350. 2. Sass KJ, Spencer DD, Kim JH, Westerveld M, Novelly RA, Lencz T. Verbal memory impairment correlates with hippocampal pyramidal cell density. Neurology 1990;40:1694-7. 3. Hannay HJ, Levin HS. Selective Reminding Test: an examination of the equivalence of four forms. J ClinExp Neuropsychol 1985;7:251-63. 4. Sass KJ, Westerveld M, Spencer SS, Kim JH, Spencer DD. Degree of hippocampal neuron loss mediates verbal memory decline following left anteromedial temporal lobectomy. Epilepsia (in press). 5. Loring DW, Papanicolaou AC. Memory assessment in neuropsychology: theoretical considerations and practical utility. ] Clin Exp Neuropsychol 1987;9:34058. 6. Larrabee GJ, Trahan DJ, Curtiss G, Levin HS. Normative data for the Verbal Selective Reminding Test. Neuropsychology 1988;2:173-82. 7. Peters BH, Levin HS. Memory enhancement after physostigmine treatment in the amnesic syndrome. Arch Neurol 1977;34:215-9. 8. Peters BH, Levin HS. Effects of physostigmine and lecithin on memory in Alzheimer's disease. Ann Neurol 1979;6:219-21. 9. Thompson PJ. Antiepileptic drugs and memory. Epilepsia 1992;33(Suppl 6):$37-40. 10. Ruff RM, Light RH, Quayhagen M. Selective Reminding Tests: a normative study of verbal learning in adults. J Clin Exp Neuropsychol 1988;1:539-50. 11. Ribbler A, Rausch R. Performance of patients with unilateral temporal lobectomy on selective reminding procedures using either related or unrelated words. Cortex 1990;26:575-84.
j EPILF_~SY,VOL. 7, NO. 1, 1994 63
Assessment of Verbal Memory in Temporal Lobe Epilepsy Using the Selective Reminding Test: Equivalence and Reliability of Alternate Forms Michael Westerveld, Kimberlee J. Sass, Arlene Sass, and Hugh G. Henry
Each of four forms of the verbal Selective Reminding Test (vSRT) were administered in counterbalanced order to 24 patients with epilepsy. Results of repeatedmeasures analysis of variance indicated that the forms were equivalent in difficulty. Furthermore, no practice effect was detected, in that performance on the first administration did not differ significantly from the second, third or fourth administrations, regardless of form. Although the four forms were found to be equivalent in difficulty and without significant practice effect, intercorrelation of forms was modest in magnitude. The measures derived from standard scoring of the vSRT (Total Recall, Long-Term Storage, Long-Term Retrieval, and Consistent Long-Term Retrieval) were highly intercorrelated. Factor analysis of these indices yielded a single factor solution for each of the four forms. We recommend using a single composite measure and obtaining multiple baseline estimates. This may provide a more reliable and stable estimate of verbal memory impairment, resulting in improved identification of patients with dominant temporal lobe epilepsy. Key Words: Temporal lobe epilepsy--Verbal memory--Selective Reminding Test.
Assessment of verbal m e m o r y plays an important role in the selection and presurgical evaluation of patients with temporal lobe epilepsy. Various verbal m e m o r y measures are sensitive to disease within the dominant temporal lobe; however, the Selective Reminding procedure (1) is unique among verbal memory measures in that it is significantly correlated with hippocampal pyramidal cell density obtained from pathologic analysis of excised tissue from the left, but not the right, of left-speech-dominant adults (2). Using the four 12-item word lists presented by Hannay
Received June 9, 1993; accepted September 30, 1993. From the Section of Neurological Surgery, Yale University School of Medicine, New Haven, CT, U.S.A. Address correspondence and reprint requests to Dr. M. Westerveld at Section of Neurological Surgery, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, U.S.A.
and Levin (3), Sass et al. (2) demonstrated that the verbal Selective Reminding Test (vSRT) scores are correlated with hippocampal pyramidal cell density in CA3 and the hilar area of the dentate (2). Leftspeech-dominant patients with severe hippocampal neuron loss experience no significant decrement in vSRT performance followingtotal excision of the left hippocampus (4). However, those with mild or moderate neuron loss decline significantly. Although recent research demonstrates the utility of the vSRT as an index of hippocampal pathology, prior studies with healthy adults raise concerns about the psychometric properties of this test. Buschke (1) developed the selective reminding procedure to differentiate impairments of information storage, retention, and retrieval. The procedure has been criticized for its failure to do so (5). Significant correlations have been reported between the various indices obtained by standard scoring methods (5,6). Factor ] EPILEPSY, VOL. 7, NO. 1, 1994
57
M. WESTERVELD ET AL.
analysis of vSRT indicates that these indices reflect a single construct (6). Alternate word lists have been developed to facilitate research involving serial assessment (3,7), but the forms are not equivalent in difficulty, alternate form reliability is marginal and a practice effect hinders the interpretation of changes in test scores (3). The psychometric properties of the vSRT may differ when the test is administered to clinical samples. It is plausible that differentiation of storage and retrieval processes may not be possible for healthy adults with intact memory, but the distinction could be relevant for patients with memory disorders. It is also plausible that the apparent disparity in form difficulty results from the relative ease with which associations are made among the individual test stimuli. The four vSRT forms may be equally difficult for patients with clinical memory disorders, if they are less facile in forming such associations. Finally, patients with significant memory disorders may not benefit from practice, as healthy adults do. The present study was performed to examine the psychometric properties of the four vSRT forms when administered to a sample of patients with seizure disorders. It was hypothesized that the four forms would be of equivalent difficulty for this sample, and that there would be no significant practice effect with serial administration. It was further hypothesized that the five vSRT scores obtained by standard scoring practice would not correlate with each other to the degree previously reported for healthy adults.
Me~od Subjects
Twenty-four consecutive patients (13 women and 11 men) admitted to the Yale Epilepsy Surgery Program for evaluation of medically refractory epilepsy were examined using the procedures detailed below. The mean age of the sample was 30.2 years (SD = 9.6 years). The average education was 12.7 years (SD = 3.8), and the mean WAIS-R Verbal IQ score was 93.6 (SD = 16.3). All but one of the patients had partial complex seizures (one patient had generalized seizures). Eighteen of 24 had partial complex seizures of temporal lobe origin; 16 of these had unilateral temporal lobe origin (6 left temporal, 10 right temporal). Two additional patients had bilateral seizure onset by scalp EEG. Five patients had seizures of frontal lobe origin, and one patient's seizures were of unknown origin. The average age of onset of refractory seizures for the 58 J F_~ILEPSY, VOL. 7, NO. 1, 1994
entire sample was 13.23 (+ 10.3 years). Nine patients had histories of one or more febrile convulsions with refractory seizures beginning later in life. Only 2 patients were found to have structural lesions (one temporal lobe arteriovenous malformation and one frontal lobe tumor). One patient had documented history of encephalitic coma, and one patient had a history of traumatic brain injury with seizures beginning within 2 years postinjury. Material and Methods Each of the patients was randomly assigned to one of the 24 possible permutations of administration order (e.g., 1234, 1243, 1342, etc.). These patients were administered one form of the vSRT during each of the first 4 days of their hospitalization for audio/ video and EEG evaluation. The first administration was performed on the day of admission. The second and third administrations were performed in the context of our standard comprehensive neuropsychologic test battery. Like the first administration, the fourth administration was not in the context of other neuropsychological tests and was performed following completion of the full neuropsychologic test battery. Eight of the 24 patients had no seizures recorded during the first 3 days following admission; an additional 2 patients had seizures only nocturnally. Only 5 of the 24 patients had more than 3 seizures during the course of the 4 test administrations. However, no SRT administrations occurred within 2 h of a seizure. Patients were on a variety of medication regimens, and schedules for the tapering of medication for patients who did not have spontaneous seizures were done on an individual basis. The relatively large number of medication combinations and tapering schedules in relation to the number of patients precludes statistical analysis of this factor. The four word lists administered are those presented by Hannay and Levin (3). Testing with the vSRT was conducted at approximately the same time of day for each of the four forms. The test was administered and scored according to standard practice. The entire word list was presented on only the first trial. On subsequent trials, only those words that were not recalled on the immediately preceding trial were repeated. Administration was continued in this manner until the patient recalled the entire word list on 2 consecutive trials or until 12 trials had been completed. Total recall (TR), long-term storage (LTS), retrieval from long-term storage (LTR), consistent long-term retrieval (CLTR), and short-term recall (STR) were computed. TR was the total number of words recalled
VERBAL MEMORY ASSESSMENT on all trials throughout the test. When the patient achieved the termination criterion before 12 trials were completed, a score of 12 (full credit) was assigned for all trials not administered. A word was considered to have entered LTS when it was recalled on two consecutive trials. Consequently, this was calculated by s u m m i n g the n u m b e r of words that met the criterion of having entered LTS, regardless of subsequent recall. LTR (long-term retrieval) was defined as the total n u m b e r of words meeting the criterion for LTS that were actually recalled. CLTR was calculated by s u m m i n g the n u m b e r of words that were recalled from LTS without failure on all subsequent trials. STR was calculated by subtracting the n u m b e r of words that were recalled from long-term storage (LTR) from the total words recalled on any given trial (TR). Intact m e m o r y is shown by elevated scores on scales TR, LTS, LTR, and CLTR, and by lower scores on scale STR. Results Mean scores and SDs for this sample on each of the four forms are s u m m a r i z e d in Table 1. Repeatedmeasures analysis of variance (ANOVA) was used to evaluate the significance of m e a n differences between forms on each of the vSRT indices. The main effect for test form is not statistically significant. Average scores for each administration trial, regardless of form, are presented in Table 2. Performance i m p r o v e m e n t with successive trials was not observed. Indeed, the m e a n scores are suggestive of a mild performance decrement; however, the results of
Table 1.
VerbalSelective Reminding Test results (means and standard deviations) vSRT form
TR LTS LTR CLTR STR
1
2
3
4
Result
101.9 (17.6) 95.6 (25.3) 83.0 (28.0) 53.5 (36.0) 18.4 (11.67)
104.8 (19.6) 98.5 (26.6) 89.0 (28.5) 62.8 (35.3) 16.2 (11.45)
106.0 (16.7) 101.3 (20.8) 90.1 (25.0) 61.5 (33.4) 16.3 (10.42)
105.5 (16.9) 95.2 (22.0) 85.7 (25.0) 59.2 (32.9) 18.9 (9.60)
NS NS
Table 2.
Results for administration order (means and standard deviations) vSRT administration order
TR LTS LTR CLTR STR
1
2
3
4
Result
106.9 (16.1) 101.7 (20.9) 91.2 (24.3) 64.2 (34.2) 14.7 (9.48)
103.4 (18.4) 94.3 (27.2) 84.0 (29.9) 58.5 (35.8) 18.9 (12.7)
104.8 (16.6) 98.8 (19.1) 88.1 (22.9) 58.2 (30.6) 16.8 (7.7)
103.2 (18.4) 94.7 (26.8) 84.5 (28.7) 56.2 (36.9) 19.3 (12.2)
NS NS NS NS NS
For abbreviations, see Table 1. a repeated-measures ANOVA indicated that this was not statistically significant. The n u m b e r of intrusions from prior lists during administrations 2, 3, and 4 were negligible. Twelve of the 24 patients made no intrusions. In total, only 16 intrusions from previous lists were recorded for the other 12 patients. The m e a n n u m b e r of intrusions for the entire sample was 0.22 per person, per administration. Thus, each patient could be expected to make approximately one intrusion during either the second, third, or fourth administrations. Table 3 summarizes the differences between the m a x i m u m and m i n i m u m scores obtained by patients during the administration of the four vSRT forms. The differences were sometimes extreme, particularly for the measures of LTS, LTR, and CLTR. Five patients (21%) achieved LTS scores that varied by 50 points or more. Four patients achieved LTR scores that differed by 50 points, and this variability was observed with respect to CLTR for 6 patients. In contrast, differences between m a x i m u m and m i n i m u m performances never exceeded 40 points for TR.
Differences between maximum and minimum scores (numbers of patients)
Table 3.
NS
Range
Recall
LTS
LTR
CLTR
STR
NS
<10 10-19 20-29 30-39 40-49 50-59 >60
3 10 8 3 0 0 0
0 4 5 5 5 3 2
1 4 6 3 6 3 1
2 4 0 7 5 2 4
6 7 9 2 0 0 0
NS
Abbreviations: TR, total recall; LTS, long-term storage; LTR, long-term retrieval; CLTR, consistent long-term retrieval; STR, short-term recall; NS, not significant.
J EPILEPSY,VOL, 7, NO. 1, 1~94 59
M. WESTERVELDETAL. Table 4.
Correlations between forms
Table 6.
vSRT index
Factor loading of SRT indices on their respective factors a Form
Form with
TR
LTS
LTR
CLTR
STR
1/2 1/3 1/4 2/3 2/4 3/4
0.63b 0.69c 0.6¥ 0.78c 0.8¥ 0.75¢
0.38a 0.51b 0.48b 0.36a 0.54b 0.58b
0.49 b
0.58 b
0.61b 0.55b 0.66c 0.69~ 0.66c
0.66c 0.60b 0.81¢ 0.76¢ 0.68c
0.25 0.48b 0.40~ 0.37~
SRTindex
0.52 b 0.53 b
TR LTS LTR CLTR
1
2
3
4
0.964 0.977 0.997 0.954
0.946 0.958 0.998 0.904
0.940 0.982 0.997 0.964
0.955 0.973 0.991 0.962
°All four forms yielded single-factor solutions. One-tail significance levels: ap < 0.05, bp < 0.01, Cp < 0.001. Alternate forms reliability was examined by calculating the correlation coefficients of the vSRT indices for the four forms. These results are summarized in Table 4. All but one of these correlations were statistically significant (p < 0.05). The magnitude of the correlation coefficients ranged from 0.25 to 0.84. In general, correlation coefficients were greater in magnitude for TR (range, 0.63-0.84) and CLTR (range, 0.58-0.81), versus LTS (range, 0.36-0.58), LTR (range, 0.49-0.69), and STR (range, 0.25-0.53). Two analyses were conducted in order to evaluate the possible influence of seizure occurrence on SRT scores. Change in SRT performance from the first administration to the fourth was not correlated with
Table 5.
Form 1 Recall LTS LTR CLTR Form 2 Recall LTS LTR CLTR Form 3 Recall LTS LTR CLTR Form 4 Recall LTS LTR CLTR
Correlations of vSRT indices
LTS
LTR
CLTR
STR
0.94
0.97 0.98
0.92 0.88 0.94
-0.80 -0.90 -0.91 -0.86
0.88
0.95 0.96
0.92 0.75 0.89
-0.67 -0.89 -0.86 -0.67
0.89
0.95 0.98
0.96 0.90 0.96
-0.69 -0.93 -0.87 -0.78
0.91 0.89 0.94
-0.73 -0.83 -0.82 -0.84
0.92
0.97 0.98
All correlations are statistically significant (p • 0.001). 60
J EP/LEPSY, VOL. 7, NO. 1, 1994
seizures that occurred in the first 3 days following admission (r = 0.294; p > 0.15). Eight of the 24 patients had no seizures recorded during this period. The mean change in performance (factor score for the first form administered minus factor score for the fourth form administered) for these 8 patients is not significantly different from the mean change in performance for the 8 patients with the highest seizure frequency over the first 3 days following admission (t = 0.664; p = 0.517). The correlations of the vSRT indices with each other also were calculated for each of the four forms. The indices derived from standard scoring of the vSRT are highly intercorrelated (see Table 5). Factor analysis of forms 1, 3, and 4 indicated that a single factor solution accounted for more than 90% of the variance. A single factor solution accounted for 87.7% of the variance for form 2. The results of factor analysis are presented in Table 6. Two methods were employed to compute a single index for the vSRT, since factor analysis suggested that the individual scores measure the same construct. The first involved computation of factor scores, using the factor coefficients presented in Table 7. STR was not employed in the computation of the factor scores. The information it conveys is redundant, since it represents the difference between TR and LTR. The factor score coefficients for the vSRT scores are virtually identical. Therefore, each vSRT component contributes equally to the factor score. For this reason, essentially the same information is obtained by averaging the raw scores. The second Table 7.
Recall LTS LTR CLTR
Factor scores
Form1
Form2
Form3
Form4
0.25707 0.25486 0.26102 0.25019
0.26555 0.25462 0.26973 0.25194
0.25440 0.25226 0.26068 0.25612
0.25590 0.25530 0.26158 0.25137
VERBAL MEMORY ASSESSMENT Table 8.
Correlationsof summary scores Factor score
Form 1 Form 2 Form 3
Form 2
Form 3
Form 4
0.54°
0.64 b 0.68 b
0.58a 0.73b 0.69 b
Practice Effect and Equivalence of Forms
Sum of raw scores
Form 1 Form 2 Form 3
also found the vSRT indices to be highly intercorrelated; factor analysis yielded single factor solutions for each of the four forms. Our findings have important implications for the assessment of verbal memory in the presurgical evaluation of patients with epilepsy.
Form 2
Form 3
Form 4
0.53°
0.64 b
0.58° 0.72b 0.70~
0.70b
One-tail significance levels: "p • 0.01, bp ¢~ 0.001. summary score is the mean of TR, LTS, LTR, and CLTR. Table 8 presents the correlations of factor scores and mean scores for the four vSRT forms. The correlation coefficients for the factor scores range from 0.54 to 0.73. The correlation coefficients for raw score means are essentally the same. These coefficients are slightly lower than the coefficients for total recall (range, 0.63-0.84) and CLTR (range, 0.58-0.81). They are comparable to the coefficients for LTR (range, 0.49-0.69) and somewhat greater than the coefficients for LTS (range, 0.36-0.58) and STR (range, 0.250.53). Two computations were performed to" determine whether ~ultiple assessments of m e m o r y can reduce error variance. The first involved correlation of the mean of the first two administrations (regardless of form) with the mean of the last two administrations. The correlation coefficients were 0.75 when factor scores were employed and 0.74 for raw scores. Both coefficients were statistically significant (p < 0.001). The second involved correlation of the better score of the first two administrations (regardless of form) with the better of the second two administrations. The correlation coefficients were 0.82 when factor scores were employed and 0.75 for raw scores.
Discussion The results of the present study indicate that, for an unselected (i.e., consecutive) sample of patients undergoing inpatient evaluation of seizure disorders, the four forms of the vSRT were equally difficult. Furthermore, there was no significant practice effect when multiple administrations were performed. We
We did not confirm the practice effect that was previously reported by Hannay and Levin (3). These authors administered four vSRT forms to a sample of college studients at 1-week intervals using a Latin square experimental design. They found that performances during the third and fourth administrations surpassed that of the first administration, regardless of form. The authors inferred that experience with the task-enhanced performance. Scores obtained during the second, third, and fourth administrations did not differ significantly from one another. There are several possible explanations for the absence of a practice effect in our sample. The overall performance of our sample was impaired for all four forms of the test. This finding is unlikely to be a result of global cognitive impairment, since the mean VIQ was within the average range. Poor acquisition of novel information is asociated with some medically refractory seizure disorders, particularly those involving the temporal lobe. The failure to profit from experience with this test procedure may be a further reflection of this learning deficit. This interpretation would be consistent with the observations of other authors who failed to identify practice effects in patients with dementia (8). It is also possible that our sample's failure to profit from test experience was attributable to proactive interference. Hannay and Levin (3) administered the tests with 1-week intervals between administrations. Our patients completed the tests four consecutive days. Although it is plausible, this hypothesis is not supported by the data. A large number of intrusions would be expected, if proactive interference was responsible for the absence of a practice effect. The actual n u m b e r of intrusions from previous word lists was negligible. It is also plausible that a number of uncontrolled factors associated with hospitalization for seizure evaluation (e.g., p o o r sleep, medication changes, effects of seizures) hindered the patient's ability to profit from test experience. The relatively small sample size in relation to the number of medication combinations precluded statistical analysis of this as a source of error. However, it has been noted else-
J EPILEPSY,VOL. 7, NO. 1, 1994 61
M. WESTERVELD EF AL.
Table 9.
Difference between maximum and minimum scores
Hannay and Levin (3)°
Recall LTS LTR CLTR STR
Present sample =
Dif
Forms
Dif
Forms
5.85 9.30 9.50 10.63 4.05
2 -
4.1
3-
1
4- 1 4- 1 2- 1 1 - 4
6.1 7.1 9.3 2.7
3324-
4 1 1 2
1
=Dif,difference between highest and lowest scores; forms, test form of highest score - test form of lowest score.
where (9) that there is little evidence for selective effects of AEDs on memory. The effects of seizures during hospitalization is also a potential source of error. It is possible that increasing seizures over the course of hospitalization had an effect on performance, effectively negating any demonstration of practice effect that might otherwise be observed. We believe that this is not likely in our sample for several reasons. No patient was administered the SRT within 2 h of a seizure. Only 5 of the 24 patients had more than 3 seizures during the 4 days of SRT administration. Furthermore, change in SRT scores over the course of administration was not consistently related to the n u m b e r of seizures recorded. The correlation between change in test score from first to fourth administration was not significant. Many (33%) of the patients actually had no seizures during the 4 days of testing, and most patients did not have an increase in seizure activity relative to their baseline. Finally, the mean change in SRT performance for the 8 patients who had no seizures recorded during the period of test administration did not differ significantly from those patients w h o had the greatest n u m b e r of seizures recorded during the course of the four test administrations. Our sample also found each of the four forms equally difficult. This is in contrast to results obtained with healthy adults that indicate form I is more difficult than the other forms (3). Table 9 contrasts the range of scores reported by Hannay and Levin (3) and those obtained by our patients. The difference between the maximum and minimum scores obtained for our patients was less than that reported by Hannay and Levin. Ruff et al. (10) suggested that healthy adults who performed effectively on the vSRT had relatively more efficient strategies for making associations among the stimuli. These authors implied that lower associational values for items comprising form 1 account for its difficulty. Neurologically impaired 62 J EPILEPSY,VOL. 7, NO. 1, 1994
patients may find the vSRT forms equally difficult because they poorly utilize verbal association strategies. Therefore, they are unable to benefit from the higher associational values of stimuli that comprise the other forms. The demonstration that the four word lists of the verbal Selective Reminding Test are statistically equivalent for a sample of patients with epilepsy is important because there are few m e m o r y tests that provide alternate forms for assessment of change following some intervention (e.g., surgery, effects of AEDs). Demonstration that alternate forms are equivalent in difficulty and performance is not subject to significant practice effects facilitates assessment of meaningful change. However, the utility of the vSRT for serial assessment must be considered with respect to its reliability.
Alternate Forms Reliability We found significant correlations between the indices of all four forms. The results of our study are similar to those of Hannay and Levin (3), who reported statistically significant but modest reliability coefficients (Table 4). Variance in performance on alternate forms was sometimes extreme, particularly for the measures of LTS, LTR, and CLTR (Table 3). Modest reliability is a significant problem for the vSRT. It hinders the interpretation of change following intervention. Error variance may be reduced by administration of two forms and utilizing a composite vSRT index to demonstrate a patient's current memory functioning. As reported above, two computations were performed to evaluate this practice. The first involved computation of correlation between the mean of the first two administrations (regardless of form) with the mean of the last two administrations. The correlation coefficient obtained by this method (0.75 for factor scores and 0.74 for the mean of raw scores) surpassed all of the correlation coefficients between single forms (Table 8). The second computation involved correlation of the better score of the first two performances with the better of the latter two. This computation was based on the notion that patients may perform below their true level of ability for a n u m b e r of reasons (e.g., inattention, physical discomfort, fatigue, depression, etc.), but it is far less likely that coincidental events (e.g., presence of objects in the room that serve as obvious cues for test items) will result in a performance that exceeds the true level of ability. Therefore, the better of two performances is probably the more accurate. The correlation coefficients (0.82 for factor scores and 0.75 for raw scores) were comparable to those based on mean
VERBAL MEMORY ASSESSMENT values. A significant portion of error variance is not necessarily inherent in the test, but rather the patient; use of the mean or the better of two baseline assessments minimizes this source of error, thereby enhancing interpretation of change.
Interpretation of vSRT Indices The selective reminding procedure is intended to differentiate storage, retention, and retrieval in the assessment of verbal m e m o r y disorders. However, the scores that ostensibly reflect the relative efficiency at each stage are highly intercorrelated. Factor analyses of forms 1, 3, and 4 yielded single factor solutions that accounted for at least 90% of the variance; the single factor extracted from analysis of form 2 accounted for 87.5% of the variance. A single index from among those obtained using standard scoring methods should adequately convey the vSRT result, given the redundancy of the scores. However, it is unclear which of the indices one should use. TR and CLTR are the most reliable, but 25% of the sample obtained CLTR scores that differed by 50 points or more. These data favor use of TR, but the TR variance is relatively less than LTS, LTR, and CLTR, which suggests that it may be less sensitive than the other indices to clinically significant m e m o r y components. This would be expected because TR is the sum of words recalled from LTS and STS. Our results indicate that a summary score provides the best estimate of ability, given that the individual indices contribute to the total score. One summary score may be derived from the factor analytic data. However, since our results are based on a relatively small sample size for factor analysis, the results may be somewhat sample-specific. Alternatively, a summary score composed of the mean of the TR, LTR, LTS, and CLTR scores provides a similar measure of stability. The results of this study suggest that performing a minimum of two assessements of m e m o r y and utilizing a composite index of performance may improve the reliability of the vSRT, and consequently enhance its ability to identify patients with dominanthemisphere temporal lobe disease. The negligible number of intrusions from previous lists indicate that multiple examinations can be performed with as little as 24 h between assessments. Even so, it may often be difficult to obtain two measures in many clinical settings, and it could reasonably be argued that, since other measures require only one administration, obtaining two measures would be unnecessarily time-consuming. However, we believe that the relative value of the information obtained by utilizing two forms of the SRT justifies the expenditure of time.
Prior evidence indicates that the SRT is significantly correlated with hippocampal cell counts, and that preoperative assessments using the vSRT may be a measure of hippocampal pathology (2), and the SRT provides greater opportunity for assessment of change with minimal influence of practice. In conclusion, our study supports the use of the vSRT as a valid means of identifying patients with dominant temporal lobe epilepsy. Prior reports have established that the SRT can distinguish between dominant and nondominant temporallobe disease (2, 11). The present study addresses some of the perceived limitations of the SRT as an assessment technique. We conclude that the utility of the vSRT would be enhanced by interpreting a composite measure comprised of all the derived scores rather than interpreting one or more of these scores individually. When feasible, multiple baseline assessments should also be obtained. Finally, in patients with epilepsy, the four forms of the vSRT are equivalent and may be used interchangeably. References
1. Buschke H. Selective Reminding for analysis of memory and learning. ] VerbLearn VerbBehav 1973;12:54350. 2. Sass KJ, Spencer DD, Kim JH, Westerveld M, Novelly RA, Lencz T. Verbal memory impairment correlates with hippocampal pyramidal cell density. Neurology 1990;40:1694-7. 3. Hannay HJ, Levin HS. Selective Reminding Test: an examination of the equivalence of four forms. J ClinExp Neuropsychol 1985;7:251-63. 4. Sass KJ, Westerveld M, Spencer SS, Kim JH, Spencer DD. Degree of hippocampal neuron loss mediates verbal memory decline following left anteromedial temporal lobectomy. Epilepsia (in press). 5. Loring DW, Papanicolaou AC. Memory assessment in neuropsychology: theoretical considerations and practical utility. ] Clin Exp Neuropsychol 1987;9:34058. 6. Larrabee GJ, Trahan DJ, Curtiss G, Levin HS. Normative data for the Verbal Selective Reminding Test. Neuropsychology 1988;2:173-82. 7. Peters BH, Levin HS. Memory enhancement after physostigmine treatment in the amnesic syndrome. Arch Neurol 1977;34:215-9. 8. Peters BH, Levin HS. Effects of physostigmine and lecithin on memory in Alzheimer's disease. Ann Neurol 1979;6:219-21. 9. Thompson PJ. Antiepileptic drugs and memory. Epilepsia 1992;33(Suppl 6):$37-40. 10. Ruff RM, Light RH, Quayhagen M. Selective Reminding Tests: a normative study of verbal learning in adults. J Clin Exp Neuropsychol 1988;1:539-50. 11. Ribbler A, Rausch R. Performance of patients with unilateral temporal lobectomy on selective reminding procedures using either related or unrelated words. Cortex 1990;26:575-84.
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