Rheumatol Int (2012) 32:1135–1142 DOI 10.1007/s00296-010-1762-1
ORIGINAL ARTICLE
Spatial versus verbal memory impairments in patients with fibromyalgia Seong-Ho Kim • Sang-Hyon Kim • Seong-Kyu Kim Eun Jung Nam • Seung Woo Han • Seung Jae Lee
•
Received: 20 August 2010 / Accepted: 30 December 2010 / Published online: 19 January 2011 Ó Springer-Verlag 2011
Abstract Mounting evidence suggests that individuals with fibromyalgia (FM) have impairments in general cognitive functions. However, few studies have explored the possibility of dissociation between verbal and visuospatial memory impairments in FM. Therefore, the purpose of this study was to investigate the asymmetrical impairment of cognitive functions between verbal and visuospatial memory and between short-term and long-term memory. Neuropsychological assessments were carried out on 23 female patients with FM and 24 healthy female controls. Verbal memory abilities were assessed using the Korean version of the Rey auditory verbal learning test (KAVLT)
S.-H. Kim Department of Internal Medicine, Inje University College of Medicine, Haeundae Paik Hospital, Busan, Korea S.-H. Kim Department of Internal Medicine, School of Medicine Keimyung University, Daegu, Korea S.-K. Kim Department of Internal Medicine, Catholic University of Daegu School of Medicine, Daegu, Korea E. J. Nam Division of Rheumatology, Department of Internal Medicine, School of Medicine, Kyungpook National University, Daegu, Korea S. W. Han Department of Internal Medicine, Daegu Fatima Hospital, Daegu, Korea S. J. Lee (&) Department of Psychiatry, Kyungpook National University School of Medicine, 200 Dongduk-ro, Jung-gu, Daegu 700-721, Korea e-mail:
[email protected]
and digit span task, and visuospatial memory abilities were assessed using the Korean version of the Rey complex figure test (KCFT) and spatial span task. The analysis of covariance was used to assess group differences in performance on cognitive tests after controlling for depression. The two groups did not significantly differ in terms of age, years of education, or in their estimated verbal and performance IQ, but FM patients reported more severe depressive symptoms than did controls on the Beck depression inventory. Significant group differences were found in immediate and delayed recall on the KCFT (F1,44 = 6.49, p = 0.014 and F1,44 = 6.96, p = 0.011, respectively), whereas no difference was found in immediate and delayed recall on the KAVLT. In terms of shortterm memory, neither the digit span task nor spatial span task showed any difference between groups, regardless of whether repetition was forward or backward. These findings suggest that spatial memory abilities may be more impaired than verbal memory abilities in patients with FM. Keywords Fibromyalgia Spatial memory Verbal memory Rey–Osterrieth complex figure
Introduction Fibromyalgia (FM) is characterized by chronic widespread musculoskeletal pain and the presence of at least 11 of 18 designated tender points distributed across soft tissues [1]. Other core symptoms, include fatigue, sleep disturbance, and frequently reported cognitive complaints or ‘‘fibrofog’’ [2, 3]. These cognitive complaints have been confirmed by objective measures, and those studies have revealed that patients with FM have impairments in psychomotor speed [4], attention [5], working memory [6] and long-term verbal memory [7].
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To date, psychological measures used in most studies have focused on verbal memory, and studies measuring visuospatial memory have been scarce [8, 9]. Two studies used the digit span test for short-term verbal memory and showed no differences compared with normal controls on a forward and backward digit span test even though they did not control for any confounding factors [10, 11]. However, one study using auditory verbal working memory items of the test of everyday attention (TEA) demonstrated impaired short-term verbal memory ability in patients with FM [6]. In their subsequent work, these authors replicated this finding using the same measure [12]. Other studies using different measures such as the paced auditory serial addition test [4, 5], and the reading span test [7], reported reduced performance in patients with FM. In terms of long-term verbal memory, Landro et al. [11] evaluated long-term verbal memory using the Randt memory test and found that the FM group differed significantly from the healthy controls. However, the subanalysis between the non-depressive FM group and healthy controls failed to show this difference. Park et al. reported reduced long-term verbal memory in free recall and recognition, but this result was from comparison without controlling for the depression score [7]. In contrast, recent studies controlling for confounding factors revealed that patients with FM did not perform more poorly than normal controls on long-term verbal memory tasks, such as the auditory verbal learning test (AVLT) [5, 13] and logical memory tests [5]. Moreover, Luerding et al. [14] reported no differences between patients with FM and normative data, even without considering any covariates. In contrast with the volume of work on verbal memory, not much attention has been paid to visuospatial memory. The Corsi block-tapping test is a prototypical test for shortterm visuospatial memory that requires reproducing an identical (or a reversed) sequence of tapped blocks immediately after the sequence has been shown to the subject; the process continues until the subject gives an inaccurate response [15]. The Corsi block test, a counterpart to the digit span test, measures spatial memory span. Two studies using this test reported opposite results; whereas Canovas et al. [10] reported no group difference when compared with normal controls, Luerding et al. [14, 15] found impaired performance on the backward Corsi block test among FM subjects. In terms of long-term visuospatial memory, different tasks testing delayed recall of non-verbal information have shown mixed results in FM subjects. Although no differences were found in the complex figure test (CFT) and 10/36 spatial recall test [10, 13], differences were shown in the Rey visual design learning test (RVDLT) [14]. However, recognition tests showed no differences between FM and normal subjects [11, 14]. Recently, using virtual reality
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spatial memory tasks, Canovas et al. [10] reported that FM patients performed significantly worse than controls on the spatial navigation tasks showing significantly more errors than their matched controls, whereas no significant differences were found between patients and controls using standard neuropsychological testing. Taken together, whether verbal or visuospatial function is assessed, simple short-term memory tests are unlikely to differentiate patients with FM from healthy subjects. More complicated tasks engaging greater cognitive load of attention and working memory are more likely to reveal impairment in patients with FM than is simple repetition of memorized words or locations. Second, patients with FM do not perform worse than normal controls on typical longterm verbal tests after controlling for confounding factors, such as depression and/or pain. Third, despite a paucity of studies using visuospatial tests, long-term visuospatial memory still may be a candidate for a cognitive domain that is specifically or at least, severely affected in FM patients. A plausible explanation for memory impairment, particularly spatial memory impairment, in patients with FM is that biological disruption in the function and integrity of the hippocampus [16–19] due to a chronic stress response [20, 21] may cause impairments in memory, as the hippocampus is substantially involved not only in memory and spatial orientation, but also in pain perception and modulation. The hippocampus also plays an important role in connecting the pathophysiologies of depression and pain [22]. Memory impairment may also develop secondary to more primary cognitive impairments, such as in attention and working memory [8]. On the cellular level, attention is critical for the stabilization of spatial representations [23]. Even though this biological evidence for the possibility of impairments in spatial memory exists, impairment in visuospatial memory has less been elucidated in patients with FM. The purpose of this study was to investigate the asymmetrical impairment of cognitive functions between verbal and visuospatial memory and between short-term and longterm memory. To assess cognitive functioning, a digit span task and the AVLT for short- and long-term verbal memory, and a spatial span task and the Rey complex figure test (RCFT) for short- and long-term visuospatial memory, were used.
Methods Subjects Twenty-three female patients with FM [age = 37.4 ± 7.1 (mean ± SD)] were recruited from the clinics of rheumatology at four university hospitals and one general hospital. All patients had been examined by experienced
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rheumatologists and met the diagnostic criteria for FM as defined by the American College of Rheumatology [1]. All patients were on stable doses of medication and asked to take no medication on the test day. The healthy control group consisted of 24 female volunteers [age = 37.4 ± 8.3 years (mean ± SD)] who were recruited using Internet advertisement and via the social networks of patients, such as their friends or relatives. To recruit subjects that would be similar in age to the patient groups, only subjects between the ages of 20 and 50 were recruited. To exclude the effects of the menstrual cycle on cognitive functions, all patients completed their tests between 4 days following the cessation of menstrual flow and 7 days prior to the onset of flow. None of the control subjects was taking psychoactive medication, nor did any have a current psychiatric diagnosis. Exclusion criteria for all subjects included: (a) a history of head injury or other neurological condition, (b) a history of a medical condition associated with cognitive dysfunction, and (c) a history of substance abuse. All participants gave informed consent. The study was approved by the Institutional Review Board at Kyungpook National University Hospital (No. 74005-1703). Clinical measures Current severity of fibromyalgia was measured by the Korean fibromyalgia impact questionnaire (KFIQ) [24] which is a self-completed measure comprising 10 subscales including 20 items developed originally for FM by Burckhardt et al. [25]. Tender points were surveyed by the use of a single manual application of pressure of 4 kg/cm2 for 18 specific tender point sites; the number of tender points was also used as another severity variable. Current level of depression was measured by the Korean version of the Beck depression inventory (BDI), which is a 21-item self-report questionnaire scored from 0 to 63 [26]. Scores of 10–19, 20–25 and [25 indicate mild, moderate, and severe depressive symptoms, respectively. Current levels of fatigue were measured by the Korean version of the brief fatigue inventory (BFI-K) [27, 28]. Neuropsychological measures Intelligence Two subtests of the Wechsler Adult Intelligence Scale Revised (WAIS-R), the vocabulary test and the block design test, were administered in a standardized way to assess general verbal and performance intelligence, respectively [29].
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Digit span task The forward digit span task involves repeating in forward order sequences of single numerals that are presented orally. It was originally included in conventional intelligence tests. The test proceeds by adding one more number to the sequence until two failures are made at a given span length. The task is conceptualized as a measure of immediate auditory (short-term) memory span. The backward digit span task involves in repeating backward orally presented sequences of single numerals. Thus, the task demands exact mental reversing of the perceived sequence: these requirements have some similarity to the ‘‘working memory’’ concept. The test proceeds by adding one more number to the sequence until two failures are made at a given span length. A digit span subset of the WAIS-R was carried out for this test [29]. Spatial span task The forward/backward spatial span task is a computerized version of the Corsi blocks task that assesses working memory capacity. The subject must choose each of the circles among nine circles flicked by the computer in the same or reverse order as they were originally presented. This test is part of the computerized cognitive test, which is a computerized cognitive test battery that was developed and standardized for Korean adults [30]. Rey–Kim memory test The Rey–Kim memory test (RKMT) [31] was also administered. In the RKMT, verbal memory performance is assessed by the KAVLT, a Korean version of the Rey auditory verbal learning test, and nonverbal memory performance is assessed by the K-complex figure test (KCFT), a Korean version of the RCFT. The KAVLT requires serial learning of a list of 15 unrelated words over five consecutive trials, each trial followed by immediate recall. After a delay period of 20 min, the patient is again required to recall the 15 words and then to choose the 15 words from a list of 50 words. The KCFT is essentially identical to a standard version of the RCFT. For the purposes of this investigation, the following four measures were examined: the KAVLT immediate recall (KAVLT-IR; sum of trials 1–5), the KAVLT delayed recall (KAVLT-DR), the KCFT immediate recall (KCFT-IR), and the KCFT delayed recall (KCFT-DR). Raw scores were used for these four measures.
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Continuous performance test The continuous performance test (CPT) presents target and non-target stimuli in random order at regular intervals. The CPT tests task vigilance and distractibility by allowing the subject to react in the presence of a prescribed specific target. In this study, visual stimuli incorporating shapes were given. This test is also a subtest of the computerized cognitive test [30].
BDI as a covariate. To control for the inflation of alpha, planned comparisons were performed. Pearson’s correlation analysis was used to test the relationships between clinical and neuropsychological variables. To examine the impact of attention and working memory abilities on verbal or visuospatial memory which was significant in the comparison analysis, regression analysis was carried out. Data were analyzed using the Statistical Package for the Social Sciences for Windows, Version 11.0.1(SPSS, Inc.; Chicago, IL). Significance was set at p \ 0.05.
Wisconsin card sorting test The Wisconsin card sorting test (WCST) [32] assesses the ability to solve problems in response to changing stimuli, the ability to shift and maintain a set of stimuli, and the ability to utilize feedback. In this task, participants are required to sort cards according to the several different dimensions (i.e., color, form, and number); the sorting principle must be deduced from verbal feedback provided by the computer. Once a particular response mode is established (i.e., 10 consecutive correct responses), a new sorting principle (concept) is instituted without warning and must be deduced by the participant. Measures of performance included the number of categories completed, and total and perseverative errors. Statistical analysis An independent samples t test was used for comparisons between groups on the demographic and clinical variables. The memory tests were analyzed using analyses of covariance (ANCOVA) with the depression score of the
Results Demographic characteristics and psychological symptoms As indicated in Table 1, no significant differences existed between groups on measures of age (t = -0.01, p = 0.990) or years of education (t = -1.49, p = 0.144). The groups were not different in estimated intelligence, as measured by the vocabulary subset for verbal IQ (t = -1.73, p = 0.091) and the block design test for performance IQ (t = -2.00, p = 0.052). Not surprisingly, patients with FA had higher depressive scores than did normal controls (t = 6.28, p \ 0.001); mean scores of BDI on the FM group indicated a moderate level of depression. Verbal memory ANOVA revealed no significant group differences on forward or backward digit span tests. Scores on the KAVLT
Table 1 Demographic and clinical information for fibromyalgia and control group Fibromyalgia
Healthy controls
Statistics
N = 23
N = 24
t
df
Age (years)
37.4 ± 7.1
37.4 ± 8.3
-0.01
45
0.990
Education (years)
12.8 ± 2.2
13.8 ± 2.2
-1.49
46
0.144
p
Demographic data
Psychological data IQ, verbal
11.0 ± 1.9
12.0 ± 2.1
-1.73
46
0.091
IQ, performance
11.6 ± 3.1
13.4 ± 3.0
-2.00
46
0.052
23.5 ± 10.7
8.6 ± 4.4
6.28
46
\0.001
BDI Clinical data Tender point (number)
12.2 ± 5.3
–
FIQ
59.0 ± 18.9
–
6.6 ± 2.4
–
34.3 ± 41.2
–
BFI Duration of illness (months)a
Values are represented as mean ± standard deviation BDI Beck Depression Inventory, FIQ Fibromyalgia Impact Questionnaire, BFI Brief Fatigue Inventory a
Median 13.0 months
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Rheumatol Int (2012) 32:1135–1142 Table 2 Neuropsychological data
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Measure
Fibromyalgia
Healthy controls
ANOVA
N = 23
N = 24
F
ANCOVAa p
F
p
Verbal Digit span Forward
8.4 ± 2.5
9.0 ± 2.6
0.68
0.414
0.19
0.666
Backward
6.4 ± 2.4
7.0 ± 2.1
0.76
0.390
0.15
0.703
KAVLT a
ANCOVA with scores of Beck depression inventory as a covariate
ANOVA analysis of variance, ANCOVA analysis of covariance, KAVLT Korean version of auditory verbal learning test, KCFT Korean version of Rey Complex Figure Test, IR immediate recall, DR delayed recall
IR
55.9 ± 9.6
60.9 ± 8.6
3.57
0.650
0.03
0.857
DR
11.7 ± 2.5
13.4 ± 1.6
4.04
0.011
0.57
0.453
Forward
6.0 ± 1.0
6.2 ± 1.0
0.85
0.360
0.001
0.978
Backward KCFT
5.5 ± 1.2
6.1 ± 0.8
4.19
0.046
0.63
0.432
Visuospatial Spatial span
IR
16.0 ± 7.4
24.3 ± 5.6
19.20
\0.001
6.49
0.014
DR
16.5 ± 7.3
23.8 ± 5.5
15.16
\0.001
6.96
0.011
revealed significant differences between groups in both immediate and delayed recall. However, ANCOVA with depressive scores as a covariate showed non-significant results for these four variables (Table 2). Visuospatial memory As shown in Table 2, ANOVA revealed a significant difference on the backward, but not on the forward spatial span test (F1,45 = 4.19, p = 0.046). The analysis of scores on the KCFT, a measure of visuospatial long-term memory, revealed that patients with fibromyalgia performed significantly more poorly than healthy controls on both immediate and delayed recall (F1,45 = 19.20, p \ 0.001, F1,45 = 15.16, p \ 0.001, respectively). After conducting the ANCOVA with depressive scores as a covariate, the significance with respect to backward spatial span disappeared, but differences in immediate and in delayed recall on the KCFT were still significant (F1,44 = 6.59, p \ 0.014, F1,44 = 6.96, p \ 0.011, respectively). Figure 1 presents examples of performance on the KCFT. Relationships between clinical variables and neuropsychological performance within the fibromyalgia group. The duration of illness was negatively related to performances on the backward digit span test and the KAVLT-IR. No significant correlations were shown for any other clinical variables (Table 3). Regression analysis Multiple regression analyses were carried out using the simultaneous entry method (see Tables 4, 5). The first analysis of the KAVLT-IR with a dependent variable
revealed no significant model (F5,17 = 1.42, p = 0.27) or independent variables. Furthermore, the analysis of the KCFT-IR with a dependent variable resulted in no significant model (F5,17 = 2.60, p = 0.06). However, one independent variable, namely attention, revealed as a significant predictor of performance on the KCFT-IR (t = 2.19, p = 0.04). Further simple regression analysis between KCFT-IR and CPT produced a value of 0.279 for R2 indicating that approximately 28% of the variance was accounted for by attentional ability (adjusted R2 = 0.245). The F value for the regression equation was significant (F1,21 = 8.13, p = 0.01).
Discussion The main finding of this study was that patients with FM showed poorer performance on a long-term visuospatial memory test, a KCFT, compared with normal controls, even after controlling for depression. However, between-group differences in the long-term verbal memory test, the AVLTDR, disappeared after controlling for depression. In terms of short-term memory, neither the digit span, nor the spatial span test showed any difference between groups, regardless of whether items were repeated forward or backward. Visuospatial impairment was not correlated with any clinical variables in the present study. Further regression analysis revealed that immediate recall on the KCFT was accounted for by attentional abilities in patients with FM. The RCFT task is one of the most widely used neuropsychological tests for the evaluation of visuospatial constructional ability and nonverbal memory skills. Reproducing the RCFT is a complex cognitive task,
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Fig. 1 Examples of performances on the Rey complex figure test. a The figures drawn by a 45-year-old healthy female with an estimated IQ of 126 and BDI score of 3. b The figures drawn by a 42-year-old female fibromyalgia patient with an estimated IQ of 127 and BDI score of 10
Table 3 Relationships between clinical variables and neuropsychological performance within fibromyalgia group (N = 23) FIQ
BFI
DOI
BDI
Table 5 Regression analysis between immediate recall in the KCFT and other variables within fibromyalgia group (N = 23) Variable
Regression analysis B (SE)
Beta
t
0.06 (0.13)
0.08
0.43
DSF
-0.165
-0.197
-0.359
-0.131
DSB
-0.089
-0.025
-0.451*
-0.045
BDI
KAVLT-IR
-0.246
-0.221
-0.460*
-0.280
IQ, verbal
0.21 (0.85)
0.06
0.25
KAVLT-DR
-0.145
-0.178
-0.268
-0.242
IQ, performance
0.90 (0.51)
0.38
1.76
SSF
0.108
0.061
-0.231
-0.189
WCST, perseverative errors
0.06 (0.19)
0.06
0.32
SSB
-0.073
-0.084
-0.401
-0.245
CPT, correct responses
0.96 (0.44)
0.45
2.19*
KCFT-IR
0.130
0.083
-0.372
-0.069
KCFT-DR
0.167
0.095
-0.258
-0.040
FIQ fibromyalgia impact questionnaire, BFI brief fatigue inventory, DOI duration of illness, BDI Beck depression inventory, DSF/B digit span test forward/backward, KAVLT-IR/DR Korean Version of Rey auditory verbal learning test-immediate/delayed recall, SSF/B spatial span test forward/backward, KCFT-IR/DR Korean Version of Rey Complex Figure Test-immediate/delayed recall *p \ 0.05
Table 4 Regression analysis between immediate recall in the KAVLT and other variables within fibromyalgia group (N = 23) Variable
BDI
Regression analysis B (SE)
Beta
t
-0.18 (0.19)
-0.20
-0.94
IQ, verbal
1.69 (1.24)
0.34
1.36
IQ, performance
0.34 (0.74)
0.11
0.46
WCST, perseverative errors
0.16 (0.28)
0.13
0.58
CPT, correct responses
0.39 (0.63)
0.14
0.62
R2 = 0.29, F = 1.42, p = 0.27 Constant: B(SE) = -16.78 (83.19), t = -0.20 BDI Beck depression inventory, WCST Wisconsin card sorting test, CPT continuous performance test
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R2 = 0.42, F = 2.60, p = 0.06 Constant: B (SE) = -126.25 (57.25), t = -0.21 BDI Beck depression inventory, WCST Wisconsin card sorting test, CPT continuous performance test *p \ 0.05
consisting of three test conditions: copy, immediate recall and delayed recall. In the copy condition, successful copying of the figure requires sufficient attention and concentration; visuospatial perception; visual-motor function; and planning and organizational abilities. When comparing performance between the immediate recall and the delayed recall, conditions enables differentiation of the encoding and storage phases of the memory process. In this study, no difference between groups was found in the copy condition (for examples, see Fig. 1). However, patients with FM showed poorer performance in the immediate recall condition, and their performance level was maintained in the delayed recall condition. These findings suggest that patients with FM may have some deficits in the encoding phase rather than the storage phase of their memory process. To our knowledge, this is a novel finding because previous studies using similar visual memory tasks only measured delayed recall of visual stimuli.
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On the other hand, the long-term verbal memory test, a Korean version of the AVLT, did not show differences between groups in performance on the immediate recall task, and significant differences between groups in the delayed recall task disappeared after controlling for depression. Using the same test, Grace et al. [5] found no significant differences in the total number of words recalled across the five learning trials, equivalent to the immediate recall task in this study, leading to the hypothesis that the repetitive nature of this task may compensate for the difficulties with attention. However, these authors did not report their results for delayed recall on the AVLT. Shur et al. [13] using the same test, found no significant difference in scores on the immediate and delayed recall tests of the AVLT after controlling for depression, pain, and fatigue. Thus, our findings that these variables were not significantly different between groups largely corroborate the previous observations. How can we explain the domain specific impairment of long-term memory? First, the cognitive load required to perform the given task should be considered. The RCFT reflects not only visuoperceptual ability and visuoconstructional ability, but also executive function, especially planning and organization [33]. Thus, additional cognitive load may be needed to perform the RCFT properly, relative to other tests in this study. However, regression analysis in this study revealed that performance on the RCFT was not significantly related to executive function as evaluated by the WCST, and was related to attentional ability as measured by the CPT only with 28% of accountability. These findings lead to the second possibility, namely that irrespective of factors affecting performance on these tests, visuospatial memory per se may be more severely impaired than verbal memory in FM. Third, different factors such as depression, pain, attention, and working memory may differentially affect the performance of verbal or visuospatial memory tasks. Shur et al. [13] reported that depression was related to performance on the AVLT-IR, and AVLT-DR, but not on the CFT-DR. Although two variables on the AVLT did not reach significance, our research showed the same trend in the correlation analysis. In addition, attentional ability had a great effect on performance on the RCFT than on the AVLT in the present study. With regards to short-term memory, in the present study, neither digit span nor spatial span test showed any difference between groups, regardless of whether the task involved forward or backward repetition. These findings are largely consistent with the previous studies [10, 11]. Although significance was weak, a significant betweengroup difference was shown on the backward spatial span test before controlling for depression, implying the possibility of differential impairment in spatial memory. In fact,
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Luerding et al. reported that ability on the Corsi block span test in patients with FM was significantly reduced, when performance scores were transformed into z scores [14]. Although those FM patients with longer chronicity had lower verbal memory spans and long-term verbal memory compared with others in the FM group, no correlations between clinical variables and the KCFT-IR or DR were found. These findings were exactly consistent with those of Canova et al. [10]. In contrast with verbal memory, impaired visuospatial memory may manifest itself in the early stage of the disease and persist across the course of the disease. Speculatively, this could be a potential candidate for a vulnerability marker. Further studies with patients in the early stages of FM and non-affected relatives are needed. This study had several limitations. First, due to the considerable variability in types and doses of medication taken, it was not possible to fully control for the putative effects of medication. Second, variables, such as sleep disturbance, fatigue, and pain can affect cognitive performance, but were not controlled in this study. In conclusion, using the RCFT, a conventional paper and pencil test, we demonstrated that female patients with FM showed poorer performance than normal controls on the long-term visuospatial memory test, especially during the encoding and further delayed recall phase, and this impairment was more pronounced than those in other domains of memory, such as short-term memory or longterm verbal memory. These findings suggest that visuospatial memory abilities may be more impaired than verbal memory abilities in patients with FM. Acknowledgments This research was supported by Kyungpook National University Research Fund, 2009. Conflict of interest of interest.
The authors declare that they have no conflict
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