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Usefulness of verbal selective reminding in distinguishing frontal lobe memory disorders in epilepsy
Epilepsy & Behavior 22 (2011) 313–317
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Epilepsy & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h
Usefulness of verbal selective reminding in distinguishing frontal lobe memory disorders in epilepsy Benjamin L. Johnson-Markve a, Gregory P. Lee a,⁎, David W. Loring b, Kathryn M. Viner a a b
Department of Neurology, Medical College of Georgia, Augusta, GA, USA Department of Neurology, Emory University School of Medicine, Atlanta, GA, USA
a r t i c l e
i n f o
Article history: Received 24 January 2011 Revised 24 May 2011 Accepted 30 June 2011 Available online 8 September 2011 Keywords: Learning and memory Executive functions Epilepsy Assessment
a b s t r a c t Frontal lobe memory disorders are distinguished from hippocampal memory disorders by poor organization of encoding and retrieval, among other things. Because the verbal Selective Reminding Test (SRT) has a metamemory (“remembering-to-remember”) component, it may be useful in distinguishing frontal from temporal lobe memory disorders in patients with intractable epilepsy. Thirty-four patients with frontal lobe epilepsy (FLE) and 34 with temporal lobe epilepsy (TLE) underwent a comprehensive neuropsychological evaluation that included multiple memory and executive function tests. Patients with FLE performed significantly worse than those with TLE on SRT measures and Wechsler Memory Scale, Third Edition, Logical Memory (LM II), but not on other verbal and nonverbal memory tests. Furthermore, SRT and LM-II were significantly correlated with executive function measures. These findings have both theoretical and practical implications: (1) the memory impairment observed in frontal lobe disorders may be due, in part, to deficits in organizational strategy, monitoring, and remembering-to-remember, and (2) SRT and LM-II may be useful tests to differentiate frontal from temporal lobe memory disorders. © 2011 Elsevier Inc. All rights reserved.
1. Introduction As frontal lobe epilepsy (FLE) is the second most common onset site in localization-related epilepsy, the issue of accurately detecting frontal executive impairments, including so-called frontal lobe memory deficits, is important. Patients with frontal lobe memory disorders have been differentiated from those with temporal lobe memory disorders across several dimensions of learning and memory. Individuals with frontal lobe memory disorders reportedly have poor organization during the encoding phase [1], disturbed temporal order judgments [2], proactive interference [3], haphazard retrieval from long-term storage [4], and impairments in complex memory tasks often referred to as “metamemory” [5]. Metamemory refers to knowledge about one's memory capabilities and strategies that can aid memory in addition to the processes involved in memory self-monitoring. Studies in neurological patients have implicated the prefrontal cortex as an essential anatomical region in metamemory [6,7; summarized by 8]. Several researchers have explored the relationship between executive functions and verbal and visual–spatial new learning and memory in an attempt to describe how frontal lobe functions interact with hippocampal memory systems [9–13]. These investigations have, for the most part, found robust correlations between various executive function measures and tests of verbal and visual memory ⁎ Corresponding author at: Department of Neurology, Medical College of Georgia, Augusta, GA 30912, USA. Fax: + 1 706 721 7588. E-mail address: [email protected] (G.P. Lee). 1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.06.039
across indices of both immediate and delayed recall when including patients with a variety of neurological conditions. As temporal lobe epilepsy (TLE) is the most common type of seizure disorder for which epilepsy surgery is performed, and the frontal lobe is the second most common site of epilepsy surgery, some research has attempted to delineate the differences in memory dysfunction between patients with epilepsy with frontal lobe and those with temporal lobe lesions. For example, Incisa della Rocchetta and Milner evaluated post-resection verbal memory in patients who had undergone FLE and TLE surgery using a categorized list learning task and prose passage created specifically for the study [3]. Patients with frontal lobe resections performed better than patients with temporal lobe resections in recalling contextualized verbal information (prose passages), whereas both groups demonstrated equally poor free recall of words from the list learning task. McDonald et al. [1] investigated the memory impairment characteristics of patients with FLE and TLE using the California Verbal Learning Test II (CVLT-II) [14], Logical Memory (LM) and Visual Reproduction from the Wechsler Memory Scales—Revised (WMS-R) [15], and the Rey–Osterrieth Complex Figure (ROCF) [16]. The temporal lobe group demonstrated significantly worse recall of verbal information on both the CVLT-II and LM and percentage retention of the ROCF, and the frontal lobe group demonstrated significantly weaker release from proactive interference. Unexpectedly, there were no differences in semantic organization of verbal information. Results of these two studies showed that individuals with TLE perform worse on list learning and prose passage memory tasks compared with patients with FLE.
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B.L. Johnson-Markve et al. / Epilepsy & Behavior 22 (2011) 313–317
Although these studies provide some information about specific tests, there continues to be only limited information as to which standardized memory tests are most beneficial in distinguishing frontal lobe and temporal lobe memory disorders. Most of the literature in this area has covered the more common verbal list learning measures, such as the Rey Auditory Verbal Learning Test (RAVLT) and CVLT-II. Although these two tests contain a working memory component, both the RAVLT and CVLT-II present the entire tobe-learned word list on every trial. Moreover, the CVLT-II incorporates a semantically related categorization of words. After several years of informally observing that the verbal Selective Reminding Test (SRT) appeared to be sensitive to frontal lobe memory disorders, we undertook a more formal review of the technical requirements of various memory tests. In contrast to the most commonly used verbal list learning memory tests, the verbal SRT only selectively reminds patients of the words they did not recall on the previous trial. In other words, the SRT examiner repeats only those words not produced on the immediately previous recall trial, which appears on the face of it to tap into the concept of “remembering to remember.” Remembering to remember is often referred to as “metamemory” in cognitive psychology circles, and through its requirement to engage a higher level of cognitive functioning, it is considered an executive frontal lobe function. This suggests the verbal SRT may be more sensitive in detecting executive dysfunction and the presence of frontal lobe disease than other word list learning measures because it also has a metamemory requirement for successful learning and later recall. Thus, for the purposes of this study, it was hypothesized that the verbal SRT would be superior in identifying executive dysfunction and in differentiating between patients with FLE and those with TLE compared with other commonly used verbal and nonverbal memory tests because of its metamemory component. 2. Method 2.1. Participants Sixty-eight patients with intractable epilepsy who either were being considered for possible epilepsy surgery (N = 56) or had undergone surgery approximately 1 year before testing (N = 12) were identified by retrospective review of consecutive epilepsy surgery patients referred for neuropsychological evaluation at the Medical College of Georgia. Seizures were localization-related complex partial seizures of idiopathic or cryptogenic etiology (nonlesional) in most cases. Seizure focus localization was confirmed using ictal and interictal EEG recordings with simultaneous video recording of seizure activity in all cases. For 21 of the patients with FLE, their seizure focus was localized from chronically implanted subdural grid and/or depth electrodes. Exclusion criteria included Full Scale IQ b70, age b18 years, non-unilateral frontal or temporal epileptic etiology (e.g., bilateral, parietal, occipital), other neurological condition unrelated to the seizure disorder, significant history of substance use, and significant psychiatric history. Thirty-four (21 males, 13 females) patients with epilepsy had unilateral (17 left, 17 right) frontal lobe seizure onset, and 34 (19 males, 15 females) had unilateral (17 left, 17 right) temporal lobe seizure onset. Table 1 summarizes the demographics of the two groups. As may be seen in Table 1, there were no significant differences between patients with FLE and patients with TLE with respect to gender [F(2,66) = 0.237, P = 0.628), handedness (F = 0.268, P = 0.606), epilepsy surgery status [χ 2(1) = 0.101, P = 0.750], age (F = 3.232, P = 0.077), education (F = 2.678, P = 0.107), Full Scale IQ (F = 2.629, P = .110), seizure onset (F = 0.198, P = 0.658), or duration of seizure disorder (F = 2.315, P = 0.133). Of the 6 patients who underwent frontal lobectomy, 5 (83%) were seizure free (Engel I), and 1 (17%) had greater than 90% seizure reduction (Engel II) at the 1 year follow-up. All 6 of the patients
Table 1 Demographic statistics.
Gender Male Female Handedness Right Other Surgery status Pre Post Age Education Full Scale IQ Seizure onset Seizure duration a
Frontal lobe Epilepsy
Temporal lobe epilepsy
P
21 13
19 15
0.63
32 2
29 5
0.61
28 6 29.65 12.65 87.15 15.56 14.03
28 6 34.35 13.53 92.59 16.71 17.74
0.75
(11.50)a (1.95) (12.61) (10.86) (10.47)
(10.03) (2.46) (14.96) (10.38) (9.59)
0.08 0.11 0.11 0.66 0.13
Mean (SD).
who had temporal lobectomies were seizure free (Engel I) at the 1-year follow-up. 2.2. Procedures All patients underwent a neuropsychological evaluation using tests of verbal memory, including the SRT [17] and WMS-III [18] Logical Memory (LM) and Verbal Paired Associates (VPA), and tests of nonverbal memory, including the WMS-III Faces and ROCF [16]. All patients were also administered tests of executive functioning, including the Wisconsin Card Sorting Test (WCST) [19], Controlled Oral Word Association (COWA) [20], Trail Making Test Trial B (TMT-B) [21], Figure Fluency (FF) [22] from the Five-Point Test, and Wechsler Intelligence Scales for Children, Third Edition (WISC-III) [23], Mazes. Analysis of various memory scores included SRT long-term storage (LTS) raw score, SRT consistent long-term retrieval (CLTR) raw score, SRT delayed free recall (DFR) raw score, WMS-III LM-I scaled score, WMS-III LM-II scaled score, WMS-III VPA-I scaled score, WMS-III VPA-II scaled score, WMS-III Faces I scaled score, WMS-III Faces II scaled score, and ROCF immediate recall (IR) raw score. Specific variables from the executive measures were WCST categories complete (CC), WCST perseverative errors (PE), COWA total words, TMT-B total time, Figural Fluency (FF) unique designs (UD), FF perseverative designs (PD), and WISC-III Mazes total score. Administration of the SRT consisted of reading a list of 12 unrelated words to subjects and requesting that they repeat back as many words as they could recall over six trials using Form 2 of Hannay
Table 2 Performance on verbal and nonverbal memory tests (mean scores).
SRT CLTRb SRT LTSb SRT DFRb LM-Ic LM-IIc VPA-Ic VPA-IIc Faces Ic Faces IIc ROCF-IRb
FLE
TLE
Difference
P
21.38 29.32 5.15 8.41 7.97 7.65 7.91 8.21 8.26 18.19
29.38 37.18 6.82 9.85 9.82 9.18 9.18 8.09 7.62 17.66
–8.00 –7.86 –1.67 –1.44 –1.85 –1.53 –1.27 0.12 0.64 0.53
0.02d 0.04d 0.04d 0.06 0.04d 0.06 0.15 0.85 0.36 0.79
a SRT, Selective Reminding Test; CLTR, consistent long-term retrieval; LTS, long-term storage; DFR, delayed free recall; LM, Logical Memory; VPA, Verbal Paired Associates; ROCF-IR, Rey–Osterrieth Complex Figure immediate recall. b Raw score. c Scaled scores. d Significant at the 0.05 level (two-tailed).
B.L. Johnson-Markve et al. / Epilepsy & Behavior 22 (2011) 313–317
Fig. 1. Significant group mean differences on verbal memory tests. CLTR, consistent longterm retrieval; LTS, long-term storage; DFR, delayed free recall; LM, logical memory.
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One-way ANOVAs and t tests were conducted to determine if there were any differences between patients with FLE and those with TLE across the 10 memory tests. To determine if any laterality effects exist among those memory tests found to differ between groups, ANOVAs with follow-up Tukey HSD statistics were used to compare the results of individual memory test variables. To examine group differences on the executive function tests, t tests were used to compare each test individually. Finally, Pearson product–moment correlational statistics were applied to examine whether any of the memory tests are significantly correlated with any of the executive function measures. Statview for Windows (SAS Institute), Version 5.01, was used for all statistical analyses, and the significance level was set at 0.05. No adjustments for multiple comparisons were applied at this time because this was a preliminary exploratory study, and we did not want to miss any potentially important results that could identify variables that warrant future investigation [28]. 3. Results
and Levin's [24] word list. On subsequent trials, the examiner repeated only words not recalled by the subject on the preceding trial. The test was discontinued if the subject could recall all 12 words on three consecutive trials. The 6-trial version, which has shown high correlations on all test measures ranging from 0.51 to 0.96 with the 12-trial version, was used in the study to help combat patient fatigue and reduce the amount of time needed to complete the neuropsychological evaluations [25,26]. Three scores from the SRT were used to compare subjects with FLE to those with TLE. When a word is recalled on two or more consecutive trials, without intervening reminding, it is assumed to have entered LTS. When a subject begins to recall a word in LTS and continues to do so without prompting on all subsequent trials, it meets the operational criterion for CLTR; scoring starts with the first word recalled on the uninterrupted successful recall trials. After a 30minute delay, the total number of words freely recalled from the list is scored as DFR. 2.3. Data analysis Power analyses for each of the 10 memory test continuous variables, based on previous studies with independent experimental and control subjects whose scores were generally widely distributed, indicated the number of participants in this study (N = 68) was adequate to be able to reject the null hypothesis with 95% power probability [27]. The number of subjects required for adequate statistical power ranged from a low of 24 subjects per group (for LM-II) to a high of 31 subjects (for ROCF-IR). χ 2 analysis and simple one-way analyses of variance (ANOVAs) were used to compare demographic and seizure history variable characteristics of patients.
3.1. Verbal and nonverbal memory tests Patients with FLE performed significantly worse than those with TLE across all three SRT variables and on WMS-III LM delayed recall (LM-II). Specifically, patients with FLE obtained significantly poorer scores than those with TLE on SRT CLTR [t(1) = −2.32, P = 0.02], SRT LTS [t(1) = −2.13, P = 0.04], SRT DFR [t(1) = − 2.11, P = 0.04], and WMS-III LM-II [t(1) = −2.14, P = 0.04]. There were no statistically significant differences between patients with FLE and those with TLE on any other test of verbal memory studied including WMS-III LM immediate recall (LM-I) [t(1) = − 1.98, P = 0.06], WMS-III VPA immediate recall (VPA-I) [t(1) = − 1.97, P = 0.06], and WMS-III Verbal Paired Associates delayed recall (VPA-II [t(1) = − 1.46, P = 0.15]. In a similar vein, there were no significant differences between the FLE and TLE groups on any test measuring nonverbal memory including WMS-III Faces immediate recall (Faces I) [t(1) = 0.18, P = 0.85], WMS-III Faces delayed recall (Faces II) [t (1) = 0.92, P = 0.36], or ROCF-IR [t (1) = 0.27, P = 0.78]. These results are summarized in Table 2. Because different metrics were used to statistically analyze these results (i.e., some tests used raw scores, and others, scaled scores), scores across tests are not directly comparable. To assist with examining the magnitude of effects across tests, group means were converted to T scores and then plotted in the figures. As may be seen in Fig. 1, the T-score differences between patients with FLE and those with TLE are largest (mean = 6.5 T-score points) for the SRT measures and less evident on LM-II. Fig. 2 shows the similarity in performance between patients with FLE and those with TLE on the other verbal and nonverbal memory tests.
Fig. 2. Nonsignificant group mean differences on memory tests. LM, Logical Memory; VPA, Verbal Paired Associates; ROCF-IR; Rey–Osterrieth Complex Figure immediate recall.
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Table 3 Laterality effects on verbal memory tests (mean scores).
SRT CLTRa SRT LTS SRT DFR LM-II
Table 5 Correlations between verbal memory and executive function tests.
Right
Right
Left
Left
FLE
TLE
FLE
TLE
16.3 25.6 3.88 8.29
28.0 37.9 5.94 9.59
26.5 33.1 6.41 7.65
30.8 36.4 7.71 10.06
P
0.02b 0.09 0.007c 0.21
a SRT, Selective Reminding Test; CLTR, consistent long-term retrieval; LTS, long-term storage; DFR, delayed free recall; LM, Logical Memory. b Significant at the 0.05 level (two-tailed). c Significant at the 0.01 level (two-tailed).
3.2. Laterality effects Additional analyses were performed to determine if side of epileptogenic lesion affected memory test performance. To further evaluate the differences found between the FLE and TLE groups on the SRT and LM-II measures, a multivariate analysis of variance was performed comparing patients with FLE and those with TLE across all memory tests by laterality of seizure onset (left or right). Significant group differences were obtained for SRT CLTR [F(3,64) = 3.48, P = 0.021] and SRT DFR [F(3,64) = 4.37, P = 0.007] but not for SRT LTS [F(3,64) = 2.24, P = 0.092]. There were also no group differences for LM-II [F(3,64) = 1.55, P = 0.21]. Follow-up post hoc analysis of SRT scores using Tukey's HSD demonstrated that the patients with right FLE performed significantly worse than those with left TLE on SRT CLTR (P = 0.018) and SRT DFR (P b 0.01). Refer to Table 3 for a summary of these laterality results. 3.3. Executive function tests As may be seen in Table 4, frontal executive tests were selectively impaired in patients with FLE relative to those with TLE. In assessing the associations between the SRT and frontal executive measures, Table 5 shows that SRT CLTR, SRT LTS, SRT DFR, and WMS-III LM-II were modestly, but significantly, correlated with measures of executive function (ranging from 0.25 to 0.41) including WCST-CC, WCST-PE, COWA, TMT-B, FF UD, FF PD, and WISC-III Mazes. 4. Discussion These findings are consistent with previous studies suggesting the memory impairment seen in patients with frontal executive dysfunction may be due, in part, to inadequate organizational and retrieval strategies resulting from faulty control and monitoring mechanisms (i.e., metamemory). Using a list learning task on which the patient must impose his or her own structure or strategy for successful encoding and retrieval, such as the SRT, may be useful in identifying
Table 4 Performance on executive function tests (mean scores).
WCST CC WCST PE COWA TMT-B FF UD FF PD Mazes
a
FLE
TLE
P
4.09 19.8 25.2 103.5 20.8 2.03 22.2
5.74 12.3 31.1 76.8 26.3 1.06 23.9
0.000b 0.01c 0.01c 0.007b 0.001b 0.04c 0.05c
a WCST, Wisconsin Card Sorting Test; CC, categories completed; PE, perseverative errors; COWA, Controlled Oral Word Association; TMT-B, Trail Making Test Trial B; FF, Figural Fluency; UD, unique designs; PD, perseverative designs. b Significant at the 0.01 level (two-tailed). c Significant at the 0.05 level (two-tailed).
WCST CCa WCST PE COWA TMT-B FF UD FF PD Mazes
CLTR
LTS
DFR
LM II
0.414b 0.255 c 0.385c 0.326b 0.355b 0.269c 0.287c
0.405b 0.410b 0.299c ns 0.325b 0.262c ns
0.266c ns 0.328b ns ns ns ns
0.241c 0.288c ns ns 0.321b ns ns
a CLTR, consistent long-term retrieval; LTS, long-term storage; DFR, delayed free recall; LM, Logical Memory; WCST, Wisconsin Card Sorting Test; CC, categories completed; PE, perseverative errors; COWA, Controlled Oral Word Association; TMT-B, Trail Making Test Trial B; FF, Figural Fluency; UD, unique designs; PD, perseverative designs; ns, not significant. b Significant at the 0.01 level (two-tailed). c Significant at the 0.05 level (two-tailed).
the memory disorders associated with frontal lobe dysfunction. Although the patients with FLE performed significantly worse than those with TLE on all three SRT summary measures (namely, CLTR, LTS, and DFR), SRT CLTR was the most sensitive to frontal dysfunction and showed the strongest associations with executive measures. Further solidifying the association between frontal executive dysfunction and SRT performance, all three SRT summary measures were significantly correlated with commonly used executive function measures. Although we did not directly compare the SRT with other list learning tests, the current results suggest that the SRT may be superior in differentiating frontal from temporal deficits because it has the additional unique requirement that subjects learn information without consistent reminding. In contrast to some previous research, the present study found that patients with FLE also performed significantly worse than those with TLE on WMS-III LM-II, a prose passage memory task. It is unclear whether this is an anomaly of this specific sample or is due to some cognitive and/or affective deficit associated with their frontal lobe dysfunction. Interestingly, compared with the other three groups, the patients with right FLE performed the worst on the SRT measures, and they performed significantly worse than the patients with left TLE. This runs counter to what would normally be assumed: patients with left temporal lobe lesions would be expected to display more severe verbal memory deficits than patients with frontal lobe dysfunction. This counterintuitive laterality finding raises several possibilities for the role of the frontal lobes and SRT performance. One possibility involves the nature of how metamemory is organized in the brain. Metamemory is thought to be a frontal lobe executive function requiring the participation of both the left and right dorsolateral prefrontal cortices. As the verbal SRT appears to require intact frontal executive functions (e.g., active organization, monitoring, switching mental sets) for successful performance, it is not necessarily surprising that patients with right FLE performed the worst on the SRT because right frontal regions participate in these functions. Moreover, patients may have used a visualization strategy to assist in learning the verbal items. That is, individuals may have created a visual mental representation of items to help them remember. Thus, as individuals attempted to organize and recall previously learned words on the SRT, the words that were most consistently recalled may have been associated with some type of visual mnemonic process, which may have preferentially recruited right frontal lobe processes. Results of this study should be interpreted cautiously and require replication for several reasons. There were a relatively small number of patients in each subgroup which, combined with our methodology of post hoc analyses, reduces the confidence with which these findings should be interpreted. Future studies need to be conducted to
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evaluate the specific utility of SRT relative to other commonly used verbal list learning memory tests, such as the California Verbal Learning Test II and Rey Auditory Verbal Learning Test, to determine which test is best at detecting frontal lobe memory disorders. References [1] McDonald CR, Bauer RM, Grande L, Gilmore R, Roper S. The role of the frontal lobes in memory: evidence from unilateral frontal resections for relief of intractable epilepsy. Arch Clin Neuropsychol 2001;16:571–85. [2] Butters MA, Kasniak AW, Glisky EL, Eslinger PJ, Schacter DL. Recency discrimination deficits in frontal lobe patients. Neuropsychology 1994;8:343–53. [3] Incisa della Rocchetta AI, Milner B. Strategic search and retrieval inhibition: the role of the frontal lobes. Neuropsychologia 1993;31:503–24. [4] Incisa della Rocchetta AI. Classification and recall of pictures after unilateral frontal or temporal lobectomy. Cortex 1986;22:189–211. [5] Moscovitch M. Memory and working-with-memory: a component process model based on modules and central systems. J Cogn Neurosci 1992;1:257–67. [6] McGlynn SM, Kaszniak AW. When metacognition fails: impaired awareness of deficit in Alzheimer's disease. J Cogn Neurosci 1991;3:183–9. [7] Shimamura AP. The neuropsychology of metacognition. In: Metcalfe J, Shimamura AP, editors. Metacognition: knowing about knowing. Cambridge, MA: MIT Press; 1994. p. 253–76. [8] Pannu JK, Kaszniak AW. Metamemory experiments in neurological populations: a review. Neuropsychol Rev 2007;15:105–30. [9] Alexander MP, Stuss DT, Fansabedian N. California Verbal Learning Test: performance by patients with focal frontal and non-frontal lesions. Brain 2003;126:1493–503. [10] Duff K, Schoenberg MR, Scott JG, Adams RL. The relationship between executive functioning and verbal and visual learning and memory. Arch Clin Neuropsychol 2005;20:111–2. [11] Kopelman MD, Stanhope N. Recall and recognition memory in patients with focal frontal, temporal lobe and diencephalic lesions. Neuropsychologia 1998;36: 785–95.
317
[12] Tremont G, Halpert S, Javorsky DJ, Stern RA. Differential impact of executive dysfunction on verbal learning and story recall. Clin Neuropsychol 2000;14:295–302. [13] Vanderploeg RD, Schinka JA, Retzlaff P. Relationships between measures of auditory verbal learning and executive functioning. J Clin Exp Neuropsychol 1994;16:243–52. [14] Delis DC, Kramer JH, Kaplan E, Ober BA. California Verbal Learning Test: adult version manual. San Antonio, TX: Psychological Corp.; 1987. [15] Wechsler D. Wechsler Memory Scale—Revised. San Antonio, TX: Psychological Corp.; 1987. [16] Rey A. L'examen psychologique dans les cas d'encephalopathie traumatique. Arch Psychol 1941;28:286–340. [17] Buschke H, Fuld PA. Evaluation of storage, retention, and retrieval in disordered memory and learning. Neurology 1974;11:1019–25. [18] Wechsler D. Wechsler, Memory Scale—Third Edition. San Antonio, TX: Psychological Corp.; 1997. [19] Heaton RK. Wisconsin Card Sorting Test. Odessa, FL: Psychological Assessment Resources; 1981. [20] Benton AL, Hamsher KdeS. Multilingual Aphasia Examination. Iowa City: AJA Associates; 1989. [21] Reitan RM. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills 1958;8:271–6. [22] Regard M, Strauss E, Knapp P. Children's production of verbal and nonverbal fluency tasks. Percept Mot Skills 1982;55:839–44. [23] Wechsler D. Wechsler Intelligence Scale for Children—Third Edition. San Antonio, TX: Psychological Corp.; 1991. [24] Hannay HJ, Levin H. Selective Reminding Test: an examination of the equivalence of four forms. J Clin Exp Neuropsychol 1985;7:251–63. [25] Drane DL, Loring DW, Lee GP, Meador KJ. Trial-length sensitivity of the Verbal Selective Reminding Test to lateralized temporal lobe impairment. Clin Psychol 1998;12:68–73. [26] Larrabee GJ, Trahan DE, Levin HS. Normative data for a six-trial administration of the Verbal Selective Reminding Test. Clin Neuropsychol 2000;14:110–8. [27] Dupont WD, Plummer WD. Power and sample size calculations: a review and computer program. Control Clin Trials 1990;11:116–28. [28] Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology 1990;1:43–6.
Contents lists available at ScienceDirect
Epilepsy & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h
Usefulness of verbal selective reminding in distinguishing frontal lobe memory disorders in epilepsy Benjamin L. Johnson-Markve a, Gregory P. Lee a,⁎, David W. Loring b, Kathryn M. Viner a a b
Department of Neurology, Medical College of Georgia, Augusta, GA, USA Department of Neurology, Emory University School of Medicine, Atlanta, GA, USA
a r t i c l e
i n f o
Article history: Received 24 January 2011 Revised 24 May 2011 Accepted 30 June 2011 Available online 8 September 2011 Keywords: Learning and memory Executive functions Epilepsy Assessment
a b s t r a c t Frontal lobe memory disorders are distinguished from hippocampal memory disorders by poor organization of encoding and retrieval, among other things. Because the verbal Selective Reminding Test (SRT) has a metamemory (“remembering-to-remember”) component, it may be useful in distinguishing frontal from temporal lobe memory disorders in patients with intractable epilepsy. Thirty-four patients with frontal lobe epilepsy (FLE) and 34 with temporal lobe epilepsy (TLE) underwent a comprehensive neuropsychological evaluation that included multiple memory and executive function tests. Patients with FLE performed significantly worse than those with TLE on SRT measures and Wechsler Memory Scale, Third Edition, Logical Memory (LM II), but not on other verbal and nonverbal memory tests. Furthermore, SRT and LM-II were significantly correlated with executive function measures. These findings have both theoretical and practical implications: (1) the memory impairment observed in frontal lobe disorders may be due, in part, to deficits in organizational strategy, monitoring, and remembering-to-remember, and (2) SRT and LM-II may be useful tests to differentiate frontal from temporal lobe memory disorders. © 2011 Elsevier Inc. All rights reserved.
1. Introduction As frontal lobe epilepsy (FLE) is the second most common onset site in localization-related epilepsy, the issue of accurately detecting frontal executive impairments, including so-called frontal lobe memory deficits, is important. Patients with frontal lobe memory disorders have been differentiated from those with temporal lobe memory disorders across several dimensions of learning and memory. Individuals with frontal lobe memory disorders reportedly have poor organization during the encoding phase [1], disturbed temporal order judgments [2], proactive interference [3], haphazard retrieval from long-term storage [4], and impairments in complex memory tasks often referred to as “metamemory” [5]. Metamemory refers to knowledge about one's memory capabilities and strategies that can aid memory in addition to the processes involved in memory self-monitoring. Studies in neurological patients have implicated the prefrontal cortex as an essential anatomical region in metamemory [6,7; summarized by 8]. Several researchers have explored the relationship between executive functions and verbal and visual–spatial new learning and memory in an attempt to describe how frontal lobe functions interact with hippocampal memory systems [9–13]. These investigations have, for the most part, found robust correlations between various executive function measures and tests of verbal and visual memory ⁎ Corresponding author at: Department of Neurology, Medical College of Georgia, Augusta, GA 30912, USA. Fax: + 1 706 721 7588. E-mail address: [email protected] (G.P. Lee). 1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.06.039
across indices of both immediate and delayed recall when including patients with a variety of neurological conditions. As temporal lobe epilepsy (TLE) is the most common type of seizure disorder for which epilepsy surgery is performed, and the frontal lobe is the second most common site of epilepsy surgery, some research has attempted to delineate the differences in memory dysfunction between patients with epilepsy with frontal lobe and those with temporal lobe lesions. For example, Incisa della Rocchetta and Milner evaluated post-resection verbal memory in patients who had undergone FLE and TLE surgery using a categorized list learning task and prose passage created specifically for the study [3]. Patients with frontal lobe resections performed better than patients with temporal lobe resections in recalling contextualized verbal information (prose passages), whereas both groups demonstrated equally poor free recall of words from the list learning task. McDonald et al. [1] investigated the memory impairment characteristics of patients with FLE and TLE using the California Verbal Learning Test II (CVLT-II) [14], Logical Memory (LM) and Visual Reproduction from the Wechsler Memory Scales—Revised (WMS-R) [15], and the Rey–Osterrieth Complex Figure (ROCF) [16]. The temporal lobe group demonstrated significantly worse recall of verbal information on both the CVLT-II and LM and percentage retention of the ROCF, and the frontal lobe group demonstrated significantly weaker release from proactive interference. Unexpectedly, there were no differences in semantic organization of verbal information. Results of these two studies showed that individuals with TLE perform worse on list learning and prose passage memory tasks compared with patients with FLE.
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Although these studies provide some information about specific tests, there continues to be only limited information as to which standardized memory tests are most beneficial in distinguishing frontal lobe and temporal lobe memory disorders. Most of the literature in this area has covered the more common verbal list learning measures, such as the Rey Auditory Verbal Learning Test (RAVLT) and CVLT-II. Although these two tests contain a working memory component, both the RAVLT and CVLT-II present the entire tobe-learned word list on every trial. Moreover, the CVLT-II incorporates a semantically related categorization of words. After several years of informally observing that the verbal Selective Reminding Test (SRT) appeared to be sensitive to frontal lobe memory disorders, we undertook a more formal review of the technical requirements of various memory tests. In contrast to the most commonly used verbal list learning memory tests, the verbal SRT only selectively reminds patients of the words they did not recall on the previous trial. In other words, the SRT examiner repeats only those words not produced on the immediately previous recall trial, which appears on the face of it to tap into the concept of “remembering to remember.” Remembering to remember is often referred to as “metamemory” in cognitive psychology circles, and through its requirement to engage a higher level of cognitive functioning, it is considered an executive frontal lobe function. This suggests the verbal SRT may be more sensitive in detecting executive dysfunction and the presence of frontal lobe disease than other word list learning measures because it also has a metamemory requirement for successful learning and later recall. Thus, for the purposes of this study, it was hypothesized that the verbal SRT would be superior in identifying executive dysfunction and in differentiating between patients with FLE and those with TLE compared with other commonly used verbal and nonverbal memory tests because of its metamemory component. 2. Method 2.1. Participants Sixty-eight patients with intractable epilepsy who either were being considered for possible epilepsy surgery (N = 56) or had undergone surgery approximately 1 year before testing (N = 12) were identified by retrospective review of consecutive epilepsy surgery patients referred for neuropsychological evaluation at the Medical College of Georgia. Seizures were localization-related complex partial seizures of idiopathic or cryptogenic etiology (nonlesional) in most cases. Seizure focus localization was confirmed using ictal and interictal EEG recordings with simultaneous video recording of seizure activity in all cases. For 21 of the patients with FLE, their seizure focus was localized from chronically implanted subdural grid and/or depth electrodes. Exclusion criteria included Full Scale IQ b70, age b18 years, non-unilateral frontal or temporal epileptic etiology (e.g., bilateral, parietal, occipital), other neurological condition unrelated to the seizure disorder, significant history of substance use, and significant psychiatric history. Thirty-four (21 males, 13 females) patients with epilepsy had unilateral (17 left, 17 right) frontal lobe seizure onset, and 34 (19 males, 15 females) had unilateral (17 left, 17 right) temporal lobe seizure onset. Table 1 summarizes the demographics of the two groups. As may be seen in Table 1, there were no significant differences between patients with FLE and patients with TLE with respect to gender [F(2,66) = 0.237, P = 0.628), handedness (F = 0.268, P = 0.606), epilepsy surgery status [χ 2(1) = 0.101, P = 0.750], age (F = 3.232, P = 0.077), education (F = 2.678, P = 0.107), Full Scale IQ (F = 2.629, P = .110), seizure onset (F = 0.198, P = 0.658), or duration of seizure disorder (F = 2.315, P = 0.133). Of the 6 patients who underwent frontal lobectomy, 5 (83%) were seizure free (Engel I), and 1 (17%) had greater than 90% seizure reduction (Engel II) at the 1 year follow-up. All 6 of the patients
Table 1 Demographic statistics.
Gender Male Female Handedness Right Other Surgery status Pre Post Age Education Full Scale IQ Seizure onset Seizure duration a
Frontal lobe Epilepsy
Temporal lobe epilepsy
P
21 13
19 15
0.63
32 2
29 5
0.61
28 6 29.65 12.65 87.15 15.56 14.03
28 6 34.35 13.53 92.59 16.71 17.74
0.75
(11.50)a (1.95) (12.61) (10.86) (10.47)
(10.03) (2.46) (14.96) (10.38) (9.59)
0.08 0.11 0.11 0.66 0.13
Mean (SD).
who had temporal lobectomies were seizure free (Engel I) at the 1-year follow-up. 2.2. Procedures All patients underwent a neuropsychological evaluation using tests of verbal memory, including the SRT [17] and WMS-III [18] Logical Memory (LM) and Verbal Paired Associates (VPA), and tests of nonverbal memory, including the WMS-III Faces and ROCF [16]. All patients were also administered tests of executive functioning, including the Wisconsin Card Sorting Test (WCST) [19], Controlled Oral Word Association (COWA) [20], Trail Making Test Trial B (TMT-B) [21], Figure Fluency (FF) [22] from the Five-Point Test, and Wechsler Intelligence Scales for Children, Third Edition (WISC-III) [23], Mazes. Analysis of various memory scores included SRT long-term storage (LTS) raw score, SRT consistent long-term retrieval (CLTR) raw score, SRT delayed free recall (DFR) raw score, WMS-III LM-I scaled score, WMS-III LM-II scaled score, WMS-III VPA-I scaled score, WMS-III VPA-II scaled score, WMS-III Faces I scaled score, WMS-III Faces II scaled score, and ROCF immediate recall (IR) raw score. Specific variables from the executive measures were WCST categories complete (CC), WCST perseverative errors (PE), COWA total words, TMT-B total time, Figural Fluency (FF) unique designs (UD), FF perseverative designs (PD), and WISC-III Mazes total score. Administration of the SRT consisted of reading a list of 12 unrelated words to subjects and requesting that they repeat back as many words as they could recall over six trials using Form 2 of Hannay
Table 2 Performance on verbal and nonverbal memory tests (mean scores).
SRT CLTRb SRT LTSb SRT DFRb LM-Ic LM-IIc VPA-Ic VPA-IIc Faces Ic Faces IIc ROCF-IRb
FLE
TLE
Difference
P
21.38 29.32 5.15 8.41 7.97 7.65 7.91 8.21 8.26 18.19
29.38 37.18 6.82 9.85 9.82 9.18 9.18 8.09 7.62 17.66
–8.00 –7.86 –1.67 –1.44 –1.85 –1.53 –1.27 0.12 0.64 0.53
0.02d 0.04d 0.04d 0.06 0.04d 0.06 0.15 0.85 0.36 0.79
a SRT, Selective Reminding Test; CLTR, consistent long-term retrieval; LTS, long-term storage; DFR, delayed free recall; LM, Logical Memory; VPA, Verbal Paired Associates; ROCF-IR, Rey–Osterrieth Complex Figure immediate recall. b Raw score. c Scaled scores. d Significant at the 0.05 level (two-tailed).
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Fig. 1. Significant group mean differences on verbal memory tests. CLTR, consistent longterm retrieval; LTS, long-term storage; DFR, delayed free recall; LM, logical memory.
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One-way ANOVAs and t tests were conducted to determine if there were any differences between patients with FLE and those with TLE across the 10 memory tests. To determine if any laterality effects exist among those memory tests found to differ between groups, ANOVAs with follow-up Tukey HSD statistics were used to compare the results of individual memory test variables. To examine group differences on the executive function tests, t tests were used to compare each test individually. Finally, Pearson product–moment correlational statistics were applied to examine whether any of the memory tests are significantly correlated with any of the executive function measures. Statview for Windows (SAS Institute), Version 5.01, was used for all statistical analyses, and the significance level was set at 0.05. No adjustments for multiple comparisons were applied at this time because this was a preliminary exploratory study, and we did not want to miss any potentially important results that could identify variables that warrant future investigation [28]. 3. Results
and Levin's [24] word list. On subsequent trials, the examiner repeated only words not recalled by the subject on the preceding trial. The test was discontinued if the subject could recall all 12 words on three consecutive trials. The 6-trial version, which has shown high correlations on all test measures ranging from 0.51 to 0.96 with the 12-trial version, was used in the study to help combat patient fatigue and reduce the amount of time needed to complete the neuropsychological evaluations [25,26]. Three scores from the SRT were used to compare subjects with FLE to those with TLE. When a word is recalled on two or more consecutive trials, without intervening reminding, it is assumed to have entered LTS. When a subject begins to recall a word in LTS and continues to do so without prompting on all subsequent trials, it meets the operational criterion for CLTR; scoring starts with the first word recalled on the uninterrupted successful recall trials. After a 30minute delay, the total number of words freely recalled from the list is scored as DFR. 2.3. Data analysis Power analyses for each of the 10 memory test continuous variables, based on previous studies with independent experimental and control subjects whose scores were generally widely distributed, indicated the number of participants in this study (N = 68) was adequate to be able to reject the null hypothesis with 95% power probability [27]. The number of subjects required for adequate statistical power ranged from a low of 24 subjects per group (for LM-II) to a high of 31 subjects (for ROCF-IR). χ 2 analysis and simple one-way analyses of variance (ANOVAs) were used to compare demographic and seizure history variable characteristics of patients.
3.1. Verbal and nonverbal memory tests Patients with FLE performed significantly worse than those with TLE across all three SRT variables and on WMS-III LM delayed recall (LM-II). Specifically, patients with FLE obtained significantly poorer scores than those with TLE on SRT CLTR [t(1) = −2.32, P = 0.02], SRT LTS [t(1) = −2.13, P = 0.04], SRT DFR [t(1) = − 2.11, P = 0.04], and WMS-III LM-II [t(1) = −2.14, P = 0.04]. There were no statistically significant differences between patients with FLE and those with TLE on any other test of verbal memory studied including WMS-III LM immediate recall (LM-I) [t(1) = − 1.98, P = 0.06], WMS-III VPA immediate recall (VPA-I) [t(1) = − 1.97, P = 0.06], and WMS-III Verbal Paired Associates delayed recall (VPA-II [t(1) = − 1.46, P = 0.15]. In a similar vein, there were no significant differences between the FLE and TLE groups on any test measuring nonverbal memory including WMS-III Faces immediate recall (Faces I) [t(1) = 0.18, P = 0.85], WMS-III Faces delayed recall (Faces II) [t (1) = 0.92, P = 0.36], or ROCF-IR [t (1) = 0.27, P = 0.78]. These results are summarized in Table 2. Because different metrics were used to statistically analyze these results (i.e., some tests used raw scores, and others, scaled scores), scores across tests are not directly comparable. To assist with examining the magnitude of effects across tests, group means were converted to T scores and then plotted in the figures. As may be seen in Fig. 1, the T-score differences between patients with FLE and those with TLE are largest (mean = 6.5 T-score points) for the SRT measures and less evident on LM-II. Fig. 2 shows the similarity in performance between patients with FLE and those with TLE on the other verbal and nonverbal memory tests.
Fig. 2. Nonsignificant group mean differences on memory tests. LM, Logical Memory; VPA, Verbal Paired Associates; ROCF-IR; Rey–Osterrieth Complex Figure immediate recall.
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Table 3 Laterality effects on verbal memory tests (mean scores).
SRT CLTRa SRT LTS SRT DFR LM-II
Table 5 Correlations between verbal memory and executive function tests.
Right
Right
Left
Left
FLE
TLE
FLE
TLE
16.3 25.6 3.88 8.29
28.0 37.9 5.94 9.59
26.5 33.1 6.41 7.65
30.8 36.4 7.71 10.06
P
0.02b 0.09 0.007c 0.21
a SRT, Selective Reminding Test; CLTR, consistent long-term retrieval; LTS, long-term storage; DFR, delayed free recall; LM, Logical Memory. b Significant at the 0.05 level (two-tailed). c Significant at the 0.01 level (two-tailed).
3.2. Laterality effects Additional analyses were performed to determine if side of epileptogenic lesion affected memory test performance. To further evaluate the differences found between the FLE and TLE groups on the SRT and LM-II measures, a multivariate analysis of variance was performed comparing patients with FLE and those with TLE across all memory tests by laterality of seizure onset (left or right). Significant group differences were obtained for SRT CLTR [F(3,64) = 3.48, P = 0.021] and SRT DFR [F(3,64) = 4.37, P = 0.007] but not for SRT LTS [F(3,64) = 2.24, P = 0.092]. There were also no group differences for LM-II [F(3,64) = 1.55, P = 0.21]. Follow-up post hoc analysis of SRT scores using Tukey's HSD demonstrated that the patients with right FLE performed significantly worse than those with left TLE on SRT CLTR (P = 0.018) and SRT DFR (P b 0.01). Refer to Table 3 for a summary of these laterality results. 3.3. Executive function tests As may be seen in Table 4, frontal executive tests were selectively impaired in patients with FLE relative to those with TLE. In assessing the associations between the SRT and frontal executive measures, Table 5 shows that SRT CLTR, SRT LTS, SRT DFR, and WMS-III LM-II were modestly, but significantly, correlated with measures of executive function (ranging from 0.25 to 0.41) including WCST-CC, WCST-PE, COWA, TMT-B, FF UD, FF PD, and WISC-III Mazes. 4. Discussion These findings are consistent with previous studies suggesting the memory impairment seen in patients with frontal executive dysfunction may be due, in part, to inadequate organizational and retrieval strategies resulting from faulty control and monitoring mechanisms (i.e., metamemory). Using a list learning task on which the patient must impose his or her own structure or strategy for successful encoding and retrieval, such as the SRT, may be useful in identifying
Table 4 Performance on executive function tests (mean scores).
WCST CC WCST PE COWA TMT-B FF UD FF PD Mazes
a
FLE
TLE
P
4.09 19.8 25.2 103.5 20.8 2.03 22.2
5.74 12.3 31.1 76.8 26.3 1.06 23.9
0.000b 0.01c 0.01c 0.007b 0.001b 0.04c 0.05c
a WCST, Wisconsin Card Sorting Test; CC, categories completed; PE, perseverative errors; COWA, Controlled Oral Word Association; TMT-B, Trail Making Test Trial B; FF, Figural Fluency; UD, unique designs; PD, perseverative designs. b Significant at the 0.01 level (two-tailed). c Significant at the 0.05 level (two-tailed).
WCST CCa WCST PE COWA TMT-B FF UD FF PD Mazes
CLTR
LTS
DFR
LM II
0.414b 0.255 c 0.385c 0.326b 0.355b 0.269c 0.287c
0.405b 0.410b 0.299c ns 0.325b 0.262c ns
0.266c ns 0.328b ns ns ns ns
0.241c 0.288c ns ns 0.321b ns ns
a CLTR, consistent long-term retrieval; LTS, long-term storage; DFR, delayed free recall; LM, Logical Memory; WCST, Wisconsin Card Sorting Test; CC, categories completed; PE, perseverative errors; COWA, Controlled Oral Word Association; TMT-B, Trail Making Test Trial B; FF, Figural Fluency; UD, unique designs; PD, perseverative designs; ns, not significant. b Significant at the 0.01 level (two-tailed). c Significant at the 0.05 level (two-tailed).
the memory disorders associated with frontal lobe dysfunction. Although the patients with FLE performed significantly worse than those with TLE on all three SRT summary measures (namely, CLTR, LTS, and DFR), SRT CLTR was the most sensitive to frontal dysfunction and showed the strongest associations with executive measures. Further solidifying the association between frontal executive dysfunction and SRT performance, all three SRT summary measures were significantly correlated with commonly used executive function measures. Although we did not directly compare the SRT with other list learning tests, the current results suggest that the SRT may be superior in differentiating frontal from temporal deficits because it has the additional unique requirement that subjects learn information without consistent reminding. In contrast to some previous research, the present study found that patients with FLE also performed significantly worse than those with TLE on WMS-III LM-II, a prose passage memory task. It is unclear whether this is an anomaly of this specific sample or is due to some cognitive and/or affective deficit associated with their frontal lobe dysfunction. Interestingly, compared with the other three groups, the patients with right FLE performed the worst on the SRT measures, and they performed significantly worse than the patients with left TLE. This runs counter to what would normally be assumed: patients with left temporal lobe lesions would be expected to display more severe verbal memory deficits than patients with frontal lobe dysfunction. This counterintuitive laterality finding raises several possibilities for the role of the frontal lobes and SRT performance. One possibility involves the nature of how metamemory is organized in the brain. Metamemory is thought to be a frontal lobe executive function requiring the participation of both the left and right dorsolateral prefrontal cortices. As the verbal SRT appears to require intact frontal executive functions (e.g., active organization, monitoring, switching mental sets) for successful performance, it is not necessarily surprising that patients with right FLE performed the worst on the SRT because right frontal regions participate in these functions. Moreover, patients may have used a visualization strategy to assist in learning the verbal items. That is, individuals may have created a visual mental representation of items to help them remember. Thus, as individuals attempted to organize and recall previously learned words on the SRT, the words that were most consistently recalled may have been associated with some type of visual mnemonic process, which may have preferentially recruited right frontal lobe processes. Results of this study should be interpreted cautiously and require replication for several reasons. There were a relatively small number of patients in each subgroup which, combined with our methodology of post hoc analyses, reduces the confidence with which these findings should be interpreted. Future studies need to be conducted to
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evaluate the specific utility of SRT relative to other commonly used verbal list learning memory tests, such as the California Verbal Learning Test II and Rey Auditory Verbal Learning Test, to determine which test is best at detecting frontal lobe memory disorders. References [1] McDonald CR, Bauer RM, Grande L, Gilmore R, Roper S. The role of the frontal lobes in memory: evidence from unilateral frontal resections for relief of intractable epilepsy. Arch Clin Neuropsychol 2001;16:571–85. [2] Butters MA, Kasniak AW, Glisky EL, Eslinger PJ, Schacter DL. Recency discrimination deficits in frontal lobe patients. Neuropsychology 1994;8:343–53. [3] Incisa della Rocchetta AI, Milner B. Strategic search and retrieval inhibition: the role of the frontal lobes. Neuropsychologia 1993;31:503–24. [4] Incisa della Rocchetta AI. Classification and recall of pictures after unilateral frontal or temporal lobectomy. Cortex 1986;22:189–211. [5] Moscovitch M. Memory and working-with-memory: a component process model based on modules and central systems. J Cogn Neurosci 1992;1:257–67. [6] McGlynn SM, Kaszniak AW. When metacognition fails: impaired awareness of deficit in Alzheimer's disease. J Cogn Neurosci 1991;3:183–9. [7] Shimamura AP. The neuropsychology of metacognition. In: Metcalfe J, Shimamura AP, editors. Metacognition: knowing about knowing. Cambridge, MA: MIT Press; 1994. p. 253–76. [8] Pannu JK, Kaszniak AW. Metamemory experiments in neurological populations: a review. Neuropsychol Rev 2007;15:105–30. [9] Alexander MP, Stuss DT, Fansabedian N. California Verbal Learning Test: performance by patients with focal frontal and non-frontal lesions. Brain 2003;126:1493–503. [10] Duff K, Schoenberg MR, Scott JG, Adams RL. The relationship between executive functioning and verbal and visual learning and memory. Arch Clin Neuropsychol 2005;20:111–2. [11] Kopelman MD, Stanhope N. Recall and recognition memory in patients with focal frontal, temporal lobe and diencephalic lesions. Neuropsychologia 1998;36: 785–95.
317
[12] Tremont G, Halpert S, Javorsky DJ, Stern RA. Differential impact of executive dysfunction on verbal learning and story recall. Clin Neuropsychol 2000;14:295–302. [13] Vanderploeg RD, Schinka JA, Retzlaff P. Relationships between measures of auditory verbal learning and executive functioning. J Clin Exp Neuropsychol 1994;16:243–52. [14] Delis DC, Kramer JH, Kaplan E, Ober BA. California Verbal Learning Test: adult version manual. San Antonio, TX: Psychological Corp.; 1987. [15] Wechsler D. Wechsler Memory Scale—Revised. San Antonio, TX: Psychological Corp.; 1987. [16] Rey A. L'examen psychologique dans les cas d'encephalopathie traumatique. Arch Psychol 1941;28:286–340. [17] Buschke H, Fuld PA. Evaluation of storage, retention, and retrieval in disordered memory and learning. Neurology 1974;11:1019–25. [18] Wechsler D. Wechsler, Memory Scale—Third Edition. San Antonio, TX: Psychological Corp.; 1997. [19] Heaton RK. Wisconsin Card Sorting Test. Odessa, FL: Psychological Assessment Resources; 1981. [20] Benton AL, Hamsher KdeS. Multilingual Aphasia Examination. Iowa City: AJA Associates; 1989. [21] Reitan RM. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills 1958;8:271–6. [22] Regard M, Strauss E, Knapp P. Children's production of verbal and nonverbal fluency tasks. Percept Mot Skills 1982;55:839–44. [23] Wechsler D. Wechsler Intelligence Scale for Children—Third Edition. San Antonio, TX: Psychological Corp.; 1991. [24] Hannay HJ, Levin H. Selective Reminding Test: an examination of the equivalence of four forms. J Clin Exp Neuropsychol 1985;7:251–63. [25] Drane DL, Loring DW, Lee GP, Meador KJ. Trial-length sensitivity of the Verbal Selective Reminding Test to lateralized temporal lobe impairment. Clin Psychol 1998;12:68–73. [26] Larrabee GJ, Trahan DE, Levin HS. Normative data for a six-trial administration of the Verbal Selective Reminding Test. Clin Neuropsychol 2000;14:110–8. [27] Dupont WD, Plummer WD. Power and sample size calculations: a review and computer program. Control Clin Trials 1990;11:116–28. [28] Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology 1990;1:43–6.