Word-finding difficulties confound performance on verbal cognitive measures in adults with intractable left temporal lobe epilepsy
Address correspondence to Robyn M. Busch, Cleveland Clinic Epilepsy Center, Neurological Institute, 9500 Euclid Avenue, P57, Cleveland, OH 44195, U.S.A. E-mail: email@example.com
This study sought to determine if word-finding difficulties (WFDs), which are common in adults with dominant temporal lobe epilepsy (TLE), are related to performance on verbal cognitive measures, including memory. One hundred six individuals with left TLE and pathologically confirmed mesial temporal sclerosis completed comprehensive preoperative neuropsychological evaluations. Patients were divided into two groups based on the degree of benefit received from phonemic cueing on a confrontation naming task. Cognitive performance was then compared between patients with greater and fewer WFDs. Patients with greater WFDs demonstrated poorer performance on many verbal cognitive measures compared to those with fewer WFDs. In contrast, there were no significant differences between groups on any of the nonverbal cognitive measures. Chi-square analyses indicated that below average verbal memory performance occurred at a significantly higher rate for patients with greater WFDs (42–46%) as compared to patients with fewer WFDs (18–24%). Results showed that WFDs confound performance on verbal cognitive measures in adult patients with left TLE, particularly on measures with high demands for lexical retrieval. This suggests that when patients have word-retrieval difficulties, measures of verbal memory and verbal intelligence may be underestimated and potentially lead to misinterpretation of test performance and misinformation regarding risk of declines after surgical resection.
Patients with dominant temporal lobe epilepsy (TLE) often experience visual naming and verbal memory difficulties, and prior research has suggested that deficits in these two abilities are significantly related. Mayeux et al. (1980) found that visual naming performance was highly correlated with verbal learning and memory in patients with left TLE, leading them to hypothesize that anomia may underlie impaired performance on learning and memory measures in these patients. Subsequent studies revealed deficits in phonemic cued delayed recall in patients with TLE (Mungas et al., 1985) and a relationship between postoperative aphasia and memory loss after dominant temporal lobectomy (Ojemann & Dodrill, 1985), further suggesting that language processing plays a role in the verbal memory deficits commonly observed in patients with TLE. In 1988, Hermann et al.1988 directly tested this hypothesis and found that impaired retrieval, as assessed by visual naming and verbal fluency, predicted verbal memory impairment on a word-list learning task in patients with dominant temporal lobe epilepsy. These authors concluded that language and other cognitive skills should always be evaluated when assessing verbal memory and learning in patients with epilepsy as dysnomia, or retrieval difficulties more broadly defined, appears to contribute to reduced learning and memory performance in patients with dominant TLE.
Since these initial studies were published, a number of investigators have examined the relationship between semantic and episodic memory in patients with epilepsy with inconsistent results across studies, likely due to differences in the measures and methodology employed (Chelune et al., 1989; Hermann et al., 1992; Perrine et al., 1992; Giovagnoli, 1999; Bell et al., 2001; Smith & Lah, 2011). The majority of studies to date have used total score on the Boston Naming Test (BNT) or the Visual Naming subtest of the Multilingual Aphasia Examination as the primary index of visual naming. Problematically, total naming score does not provide specific information regarding the possible cause of poor performance as deficits may be due to retrieval-based difficulty or a loss of knowledge from semantic store for a particular word. The goal of the current study was to extend prior research by examining the degree to which retrieval-based word-finding difficulties (WFDs) affect performance on measures of verbal memory, as well as on other verbal cognitive tasks, in adults with left TLE.
This study involved an institutional review board–approved, retrospective review of previously collected and archived data from 106 adult patients (60.4% female; 97.2% Caucasian, 2.8% African American) with medically intractable left TLE who completed comprehensive preoperative neuropsychological evaluations. All patients underwent left temporal lobe resections that included resection of mesial temporal structures and had pathologically confirmed mesial temporal sclerosis (MTS). Participants ranged in age from 17 to 73 years (mean 36.83, standard deviation [SD] 12.05) and in education from 11 to 20 years (mean 13.28, SD 1.99). The mean age at seizure onset for the group was 13.89 years (SD 11.95), and the mean duration of epilepsy was 22.79 years (SD 12.19).
To determine which patients were experiencing reduced visual naming performance due primarily to word-retrieval difficulties, patients were divided into two groups based on the degree of benefit received from phonemic cueing on a confrontation naming task. This was determined by dividing each patient's total raw score on the BNT (Kaplan et al., 1983) by the total raw BNT score plus the number of items correct when provided with phonemic cues. Patients were considered to have greater WFDs if this ratio was <0.90 (the median value) and fewer WFDs if this ratio was ≥0.90. Test scores were then examined to identify univariate outliers on the neuropsychological variables separately for the two patient groups. To reduce the impact of outlying scores, they were replaced with a score one standard score point higher or lower than the next closest score (Tabachnick & Fidell, 2001). Demographic and seizure data for the two patient groups are provided in Table 1. WFDs occurred at a higher rate for men (64%) as compared to women (43%), = 4.28, p = 0.038. There were no other differences between the groups on relevant demographic or seizure variables (see Table 1).
Table 1. Demographic and seizure data for study patients
|Age||35.47 (12.17)||38.29 (11.86)|
|Education||12.95 (1.66)||13.65 (2.25)|
|Age at seizure onset||13.79 (12.12)||14.00 (11.89)|
|Duration of seizures||21.51 (11.70)||24.18 (12.67)|
|Sex||Male = 27 (49%)||Male = 15 (29%)|
|Female = 28 (51%)||Female = 36 (71%)|
|Race||Caucasian = 54 (98%)||Caucasian = 49 (96%)|
|African American = 1 (2%)||African American = 2 (4%)|
As part of their standard presurgical evaluations, participants completed a comprehensive neuropsychological battery that included the following subset of measures used in this study: Boston Naming Test (Kaplan et al., 1983), Wechsler Adult Intelligence Scale – Third Edition (WAIS-III; Wechsler, 1997a), Word Reading Subtest from the Wide Range Achievement Test – Third Edition (WRAT-3; Wilkinson, 1993), Controlled Oral Word Association Test (COWAT; Benton & Hamsher, 1989), Ruff Figural Fluency Test (Ruff, 1988), and Wechsler Memory Scale – Third Edition (WMS-III; Wechsler, 1997b).
One-way analyses of variance (ANOVAs) were conducted on the cognitive measures as a function of WFD group. Results revealed that patients with greater WFDs demonstrated poorer performance on many verbal cognitive measures than those with fewer WFDs. Specifically, patients with greater WFDs performed significantly more poorly on measures of verbal intelligence (i.e., vocabulary, verbal abstract reasoning, and fund of information), single-word reading, phonemic verbal fluency, and select verbal memory subtests (i.e., word-pairs immediate and delayed, word-list delayed). Effect sizes for these variables were generally in the moderate range (Cohen's d = 0.465–0.643). There were no differences in performance between patients with greater and fewer WFDs on nonverbal cognitive measures including nonverbal intelligence (i.e., attention to visual detail, block construction, nonverbal reasoning), figural fluency, face recognition memory, and visual scene recall (Cohen's d = 0.211–0.351) (see Table 2). All analyses were rerun using sex as a covariate, and the pattern of results remained largely unchanged.
Table 2. Summary of performance on all cognitive measures reported separately for patients with and without word-finding difficulties
|Verbal measures|| || || || || |
|WAIS-III verbal comprehension index||85.82 (11.42)||93.08 (13.37)|| 9.075 || 0.003 || 0.581 |
|Vocabulary||7.35 (2.52)||8.57 (2.72)|| 5.775 || 0.018 || 0.465 |
|Similarities||7.62 (2.35)||9.00 (2.85)|| 7.454 || 0.007 || 0.528 |
|Information||7.42 (2.41)||8.65 (2.42)|| 6.846 || 0.010 || 0.509 |
|WRAT-4 reading subtest||90.13 (12.40)||95.08 (11.22)|| 4.625 || 0.034 || 0.419 |
|COWAT||76.98 (13.38)||86.55 (18.99)|| 9.098 || 0.003 || 0.583 |
|WMS-III auditory immediate memory index||83.67 (15.81)||91.02 (13.30)|| 6.647 || 0.011 || 0.503 |
|Logical memory I||7.71 (3.26)||8.25 (2.66)||0.882||0.350||0.182|
|Verbal paired associates I||6.69 (2.94)||8.61 (3.03)|| 10.922 || 0.001 || 0.643 |
|Word list I||7.29 (2.77)||7.69 (3.40)||0.434||0.511||0.129|
|WMS-III auditory delayed memory index||81.20 (15.76)||89.16 (14.02)|| 7.497 || 0.007 || 0.534 |
|Logical memory II||6.93 (2.97)||7.80 (2.90)||2.361||0.127||0.286|
|Verbal paired associates II||6.67 (3.07)||8.47 (3.14)|| 8.871 || 0.004 || 0.580 |
|Word list II||7.05 (2.29)||8.25 (2.80)|| 5.879 || 0.017 || 0.469 |
|WMS-III auditory recognition delayed index||88.27 (15.91)||92.35 (14.43)||1.903||0.171||0.269|
|Nonverbal measures|| || || || || |
|WAIS-III perceptual organization index||94.51 (13.01)||99.29 (14.93)||3.106||0.081||0.341|
|Picture completion||8.49 (2.79)||9.24 (2.75)||1.914||0.170||0.271|
|Block design||8.95 (2.57)||9.69 (2.79)||2.025||0.158||0.276|
|Matrix reasoning||10.04 (2.58)||10.92 (3.19)||2.486||0.118||0.303|
|Ruff figural fluency – unique designs||40.83 (8.59)||42.91 (10.98)||1.168||0.282||0.211|
|Ruff figural fluency – error ratio||57.43 (10.79)||54.66 (9.24)||1.965||0.164||0.276|
|WMS-III visual immediate memory index||85.55 (15.33)||90.61 (15.05)||2.937||0.090||0.333|
|Faces I||8.55 (2.88)||9.24 (2.93)||1.494||0.224||0.238|
|Family pictures I||7.02 (3.34)||7.84 (3.21)||1.676||0.198||0.250|
|WMS-III visual delayed memory index||84.82 (15.81)||89.98 (15.82)||2.821||0.096||0.326|
|Faces II||8.35 (2.66)||9.04 (2.77)||1.728||0.192||0.254|
|Family pictures II||6.85 (3.39)||7.75 (3.52)||1.762||0.187||0.260|
|WMS-III spatial span||8.33 (3.15)||9.45 (3.24)||3.282||0.073||0.351|
Chi-square analyses indicated that low average to impaired verbal memory performance (standard score <90) occurred at a significantly higher rate for patients with greater WFDs (42% and 46%) as compared to patients with fewer WFDs (18% and 24%; = 7.34, p = 0.007 on an immediate verbal recall index and = 5.60, p = 0.018 on a delayed verbal recall index).
Results suggest that WFDs confound performance on verbal cognitive measures, but not nonverbal cognitive measures, in adult patients with left TLE. These findings provide further support for a role of language in verbal memory performance in patients with left TLE and extend the current literature by demonstrating that retrieval-based WFDs are associated with poorer performance on measures of word-pair learning and delayed word-list recall.
The lack of a significant effect of WFDs on immediate memory (word-list learning and story recall) and delayed verbal recognition measures may be due to the fact that the verbal stimuli were presented to the patient immediately prior to their response, thereby placing little demand for retrieval of previously stored information. Performance on such tasks may be significantly related to attention/working memory abilities, and post hoc analyses supported this hypothesis (Pearson r correlations ranged from 0.274 to 0.352). Given the contextual nature of the story recall task, which may place relatively low demand for lexical retrieval of a specific word for successful completion of the task, we did not find the lack of a relationship between WFDs and story recall surprising. As Mayeux et al. (1980) suggested in their original manuscript, circumlocution and circumstantiality may help compensate for naming difficulties. Of the verbal memory measures used in this study, these strategies would aid performance most on the story recall task.
Overall, our findings support the hypothesis originally proposed by Mayeux et al. (1980) and Hermann et al. (1988) that language difficulties underlie impaired performance on learning and memory measures in patients with left TLE and extend their findings to suggest that retrieval-based naming difficulties contribute to this relationship. This study also demonstrates that WFDs have a significant impact on other verbal measures besides memory, including verbal intelligence, fluency, and reading. Although extent of temporal lobe damage may have influenced both WFDs and verbal cognitive performance, the homogenous patient group with left MTS used in the current study was selected to reduce the influence of this potential confound. Therefore, current results suggest that performance on verbal cognitive tasks, including memory measures, likely underestimates true cognitive ability in patients with WFDs. Because preoperative memory performance is one of the best predictors of memory outcome following temporal lobectomy (Busch & Naugle, 2008), any underestimate of preoperative memory ability may lead to inaccurate assessment of cognitive risk following surgery. Therefore, the nature and extent of WFDs in patients with TLE should be thoroughly assessed, particularly in epilepsy surgery candidates, and verbal cognitive results in such patients should be interpreted with caution.
Portions of this article were presented at the 2008 American Epilepsy Society Meeting in Seattle, Washington.
None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.