Visual and auditory naming in patients with left or bilateral temporal lobe epilepsy

Epilepsy Research 55 (2003) 29–37

Visual and auditory naming in patients with left or bilateral temporal lobe epilepsy Brian D. Bell a,∗ , Michael Seidenberg b , Bruce P. Hermann a , Kelli Douville b b

a Department of Neurology, University of Wisconsin, 600 Highland Avenue, Madison, WI 53792, USA Department of Psychology, Finch University of Health Sciences/Chicago Medical School, North Chicago, IL 60064, USA

Received 1 October 2002; received in revised form 24 April 2003; accepted 12 May 2003

Abstract Impairment on visual naming tests is relatively common among temporal lobe epilepsy (TLE) patients. Recent reports suggested that the ability to name objects on the basis of their descriptions is an even more sensitive and perhaps more ecologically valid measure of naming problems among left hemisphere TLE patients. To further explore the nature of dysnomia in TLE, the current study assessed a group of patients with either left or bilateral TLE (n = 16) and a group of healthy controls (n = 11) on computerized measures of naming to description or auditory naming (AN) and visual naming (VN). Both speed and accuracy scores on AN distinguished patients from controls better than VN scores. There was a trend for AN speed, but not other naming test variables, to be associated with self-reported word finding problems. AN speed and accuracy, but not VN scores, correlated significantly with a broad range of other cognitive test scores. In summary, AN speed and accuracy are sensitive indexes of cognitive dysfunction in TLE patients. AN may be an appropriate analogue of the word finding demands of conversational speech because of its multiple neuropsychological demands. These results provide further evidence of the potential value of AN assessment in TLE patients. Further study of the cognitive processes required during AN, its relation to word finding problems in discourse, and the effect of anterior temporal lobectomy on this ability is warranted. © 2003 Elsevier B.V. All rights reserved. Keywords: Temporal lobe epilepsy; Naming; Word finding; Language; Neuropsychology

1. Introduction Tests designed to measure object naming ability typically consist of visual stimuli, which are most often line drawings of objects (Benton et al., 1994; Goodglass and Kaplan, 1983; Lambon Ralph et al., 1998; McKenna and Warrington, 1980; Snodgrass ∗ Corresponding author. Tel.: +1-608-263-5430; fax: +1-608-265-0172. E-mail address: [email protected] (B.D. Bell).

and Vanderwart, 1980). There is a well-documented association between intractable mesial temporal lobe epilepsy (TLE) and impairment on visually-based object naming tests, particularly in groups of patients with TLE lateralized to the language dominant hemisphere (Chelune et al., 1991; Davies et al., 1995, 1998; Hermann et al., 1997, 1999; Hermann and Wyler, 1988; Howell et al., 1994; Langfitt and Rausch, 1996; Mayeux et al., 1980; Sawrie et al., 2000; Saykin et al., 1995; Schwartz et al., 1998). However, it has been suggested that visual naming

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(VN) tests might be insufficiently sensitive to naming difficulties, because clinical evidence indicates that some TLE patients who complain of word finding problems in everyday conversational speech perform within normal limits on these tests (Hamberger et al., 2001; Hamberger and Seidel, 2003; Hamberger and Tamny, 1999). Hamberger and Tamny (1999) assessed TLE patients on both a visual naming test and an auditory naming (AN) test. In the latter, participants named objects on the basis of their verbal definitions rather than their pictorial representations. Impairment was more common on AN (70%) compared to VN (30%) among the 10 left hemisphere TLE patients. Because few (<10%) controls and individuals with right TLE demonstrated impairment on either test, AN was superior to VN at classifying the members of these three groups. The authors concluded that AN “may more accurately characterize and lateralize TLE-associated language dysfunction” (p. 229). A follow-up study (Hamberger and Seidel, 2003) presented similar results, with 76% of the left TLE patients demonstrating impairment on one or more AN variables compared to 36% of the right TLE group. The potential importance of examining naming ability in the auditory modality also was supported by recent studies of intra- or extra-operative cortical stimulation in TLE patients who were candidates for anterior temporal lobectomy due to intractable seizures. Two studies have identified anatomical sites linked distinctly to AN within the language dominant temporal lobe (Hamberger et al., 2001; Malow et al., 1996). In the report by Malow et al., stimulation in the inferotemporal and frontal cortices disrupted naming in each modality equally, but AN was disrupted more often than VN by stimulation in the anterior and posterior lateral temporal cortex. In the second study, posterior temporal lobe stimulation usually disturbed both VN and AN, whereas anterior temporal lobe stimulation disturbed AN almost exclusively (Hamberger et al., 2001). The current study examined the performance of healthy controls and TLE patients on computer-based AN and VN tests in order to acquire additional data about the naming performance of TLE patients when stimuli were presented in the auditory versus visual modality. We recruited patients who had a diagnosis of either left or bilateral TLE, because they would be most likely to demonstrate some degree of dysnomia

and thus allow an examination of the ability of the two tests to discriminate patients from controls. Additional information about AN and VN performance in the TLE patients was acquired by analyzing the relationships among the experimental naming data and clinical neuropsychological and self-report questionnaire data. These analyses tested the hypotheses that AN is a quite sensitive measure of dysnomia, depends on a wider range of cognitive processes compared to VN, and is a useful analogue of the word finding demands of conversational speech (Hamberger et al., 2001; Hamberger and Seidel, 2003; Hamberger and Tamny, 1999). Finally, the association between naming performance and attributes of the object names themselves also was examined for AN and VN. In summary, findings to date suggest that AN assessment could be a valuable addition to the neuropsychological evaluation of TLE patients. However, because AN measures have been applied relatively rarely in cognitive assessments of neurologic patients (e.g. Barton et al., 1969; Coughlan and Warrington, 1978; Goodglass and Stuss, 1979; Graham and Hodges, 1997; Schmidtke and Vollmer, 1997), further examination of performance on such measures in comparison to visual naming tests is needed.

2. Methods 2.1. Participants The 16 epilepsy patients had complex partial seizures of definite or probable temporal lobe origin and no MRI abnormalities other than hippocampal and/or general atrophy evident on clinical reading of their scans. The patients and the majority of the controls (9 of the 11) in this study underwent a cognitive evaluation between 1998 and 2001 prior to participating in the current study in 2001. A board certified neurologist with expertise in epilepsy reviewed the medical records of potential study patients before the initial assessment. This review included information pertaining to seizure semiology, previous EEGs and neuroimaging, and clinical history and course. Based on this review, each patient was classified as having seizures of definite, probable, or possible temporal lobe origin. Definite TLE was defined by continuous video/EEG monitoring demonstrating temporal lobe

B.D. Bell et al. / Epilepsy Research 55 (2003) 29–37

seizure onset. Probable TLE was defined by clinical semiology reported to reliably identify complex partial seizures of temporal lobe origin versus onset in other regions, in conjunction with interictal EEGs, neuroimaging findings, and developmental and clinical history. Only those patients meeting criteria for definite and probable TLE were recruited for study participation. All 16 patients in the current study had a seizure focus in the left temporal lobe (five ictal, six interictal EEG) or in the temporal lobes bilaterally (two ictal, three interictal EEG). None of the patients included in this report had undergone an anterior temporal lobectomy at the time that they were assessed on any of the cognitive measures. Table 1 presents demographic and seizure history information for the participants. All participants were paid $40.00 for taking part in the study. Nine of the 11 controls and all of the 16 patients had IQ data available. Each of the participants with available intelligence test data had a full scale IQ in the non-mentally retarded range on the seven-subtest short form of the Wechsler Adult Intelligence Scale-III (WAIS III; Pilgrim et al., 2000; Ward, 1990; Wechsler, 1997a). Each healthy control was a friend, relative, or spouse of a TLE patient. Controls were recruited for the study if they did not meet any of the WAIS III exclusion criteria (Wechsler, 1997a). There were no significant differences between the controls and the TLE patients on the demographic variables (see Table 1). 2.2. Neuropsychological battery The initial cognitive assessment included tests measuring attention, motor dexterity, language, visualTable 1 Demographic and seizure history data Group

n Age Education FSIQ Female (%) Age of onset (years)

Controls

TLE

11 31.0 (10.3) 13.6 (2.2) 104.8 (15.7)a 55

16 33.4 12.6 95.8 81 20.1

(12.1) (2.4) (13.7) (13.3)

P ≥ 0.14 for all variables. FSIQ: WAIS III full scale IQ based on the Ward (1990) seven-subtest short form. a Control (n = 9).

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perception, executive ability, and episodic memory. Neuropsychological data were not available for two controls, who were recruited specifically for the present study. None of the patients had suffered an episode of status epilepticus between the two assessments. The mean interval in months between the general neuropsychological assessment and the computerized naming testing was 21.7 (S.D. = 9.0) for the patients. There is evidence that naming ability remains quite stable over extended test–retest intervals among TLE subjects (Hermann et al., 1996; Sawrie et al., 1996). These data are consistent with other reports of stability in semantic memory in TLE groups (Helmstaedter, 2002; Holmes et al., 1998). 2.3. Experimental visual naming and naming to description tests In previous studies of AN in TLE patients, different items were used for the AN and VN measures. Although these items were matched on word length and frequency, the possibility remains that item selection, in addition to test modality, had a significant impact on performance. For the present research, two lists of 63 object names were matched, on the basis of data available from other studies (Baayen et al., 1993; Morrison et al., 1997), on a wide range of word attribute variables: percentage of living versus non-living items, objective age of acquisition (based on the age at which 75% of a sample children who were from 2.5 to 10.9 years old named an item correctly (total sample = 280)), familiarity, visual complexity, imageability (how easily a word aroused a mental image), number of phonemes, name agreement, word frequency, and number of words per definition. For each of the two lists, a AN and a VN test were created. The AN and VN tests presented and the order of test presentation were counterbalanced across the participants. Whereas speed of response on AN and VN tasks has been measured manually in previous research, naming speed was measured with a voice-activated timer in this study. The AN and VN measures designed for this study were presented by means of E-Prime software (Psychology Software Tools Inc., 2000). They consisted mainly of objects from a standardized set of drawings (Snodgrass and Vanderwart, 1980; Snodgrass and Yuditsky, 1996), with 21 items from

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Morrison et al. (1997) also included. For each list, line drawings were used as the stimuli in the VN test. The AN test was created for each of the two lists of objects by developing a definition for each of the 126 items. Each definition consisted of 5–17 words (M = 13.1, S.D. = 2.6). An attempt was made to keep the vocabulary of the definitions as basic as possible, to insure that all participants would be likely to understand all components of the definitions. Each definition included a brief physical description and either a functional attribute or an encyclopedic fact about the object (e.g. a glass container used to hold flowers and water = vase). The participants were informed that there were two naming tests, each consisting of 63 items, and that their goal was to name each object as quickly as possible. They were asked to say each name loudly into a hand-held microphone. The instructions also indicated that many of the objects probably would be familiar to them, but that some would be harder to name than others and some they might be unable to name. They were told that they could make a guess, if they were not certain of the correct name, but that they should remain silent if they had no idea as to what the name of an object might be. For AN, participants were told that they would hear a tape recording of a woman’s voice presenting definitions of objects one at a time from the computer’s speakers, that it was permissible to name the object being described before the end of the definition, if they were sure they knew what was being described, and that a bell briefly would sound just before the onset of each definition to serve as an alert to focus attention. For the VN test, participants were informed that they would be asked to name black and white drawings of objects and that the appearance of a black cross in the middle of the computer screen would alert them that the next item was about to be presented. After each response, the screen went blank for a brief interval, and then the cross appeared, followed by the next drawing. If no response was made, a new drawing appeared after the previous stimulus had been shown for 10 s. Twelve practice items were administered before each test. These items allowed the participants to become familiar with the test procedure and with use of the microphone. The participants were asked if they had any questions about the task before and after the practice items were administered.

Occasionally, a correct naming response was too low in volume to set off the timer or was preceded by an error or a non-speech sound. These items were excluded from the response speed analyses, but were included as correct in the accuracy analyses. The data of one control were excluded from the analyses because of excessive movement of the microphone, which caused a consistent delay in responding.

3. Results Thirteen of the 126 stimulus items were excluded from the analyses for both tests because less than 60% of the controls responded accurately to them on either VN (beetle, leopard, syringe) or AN (barrel, bottle, cannon, desk, fox, microscope, peacock, raccoon, whistle, windmill). The poor naming accuracy within the control group for the three excluded VN items is consistent with the fact that these objects have shown relatively poor name agreement among controls in previous studies (Morrison et al., 1997; Snodgrass and Vanderwart, 1980). 3.1. Group comparisons Non-parametric statistical analyses were used because of the non-normal distribution of naming variables. The mean response speed of the control group was faster than the mean response speed of the TLE group on both AN, U = 37.0, P = 0.01, and VN, U = 40.0, P = 0.02 (see Table 2). The control group was more accurate compared to the TLE group at AN, U = 34.0, P = 0.01. The control group was not significantly more accurate at VN, U = 65.5, P = 0.27.

Table 2 Means and standard deviations by naming test and group Naming test

Group

speeda

Auditory naming Visual naming speed Auditory naming accuracy Visual naming accuracy Boston Naming Test a ∗

Speed in milliseconds. P < 0.01.

Controls

TLE

6169 (483) 1047 (276) 0.92 (0.07) 0.96 (0.05) 55.9 (4.3)

6980 (892)∗ 1323 (278)∗ 0.82 (0.09)∗ 0.94 (0.06) 50.7 (3.5)∗

B.D. Bell et al. / Epilepsy Research 55 (2003) 29–37 Table 3 Percentage of each group with impairment on auditory naming and visual naming speed and accuracy and Boston Naming Test accuracy Group

Test AN

Control TLE a

BNTa

VN

Accuracy

Speed

Accuracy

Speed

Accuracy

9 69

9 69

9 44

9 38

11 38

Control (n = 9).

3.2. Classification of patients and controls Similar to the approach of Hamberger and Seidel (2003), who operationally defined AN impairment as a score at or below the fifth percentile of the control group, we chose the score of the control who performed worst on each measure as the cut-off score for impairment in order to compare AN versus VN performance at the individual level. For AN, the cut-off scores were 6700 ms for response speed and 87% correct for accuracy. For the VN, the cut-off scores were 1499 ms for speed and 93% for accuracy. Thus, one (9%) of the controls was impaired on each of the four experimental naming variables. Using these cut-off scores, a much larger subset of the patients was impaired on each of the four naming test variables: AN speed = 69%, AN accuracy = 69%, VN speed = 38%, and VN accuracy = 44% (Table 3). By chi-square analyses, both AN speed and accuracy impairment status differentiated patients from controls at a significant level (P < 0.01). There was a trend for VN speed impairment status to differentiate patients from controls (P = 0.10), but there was no such trend for VN accuracy status (P = 0.49). AN distinguished patients from controls better than any other cognitive measure in our battery of tests, including the BNT. When the 11 patients with left TLE were compared to the 11 controls, the results were similar: AN speed impairment status differentiated the groups at a significant level (P < 0.05) and there was a trend for AN accuracy status to differentiate the groups (P = 0.13), whereas frequency of VN speed and accuracy impairment did not distinguish the patients from controls (P > 0.26).

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Considering only the patient group, the percentage of patients who were impaired at AN speed was significantly higher than the percentage of patients who were impaired at VN speed (one-tailed, z = 1.75, P < 0.05). There was a trend for the percentage of patients impaired at AN accuracy to be higher than the percentage impaired at VN accuracy (one-tailed, z = 1.47, P = 0.07). 3.3. Correlations between naming and QOLIE-89 language items There are five items in the language index of the Quality of Life in Epilepsy inventory (QOLIE-89; Devinsky et al., 1995). For each item, patients rate their ability on a six-point scale on the basis of the following instructions: “The following questions are about language problems you may have. Circle one number for how often you have trouble speaking or how often these problems have interfered with your normal work or living.” The items are: (1) finding the correct word, (2) understanding what others are saying in conversation, (3) understanding directions, (4) understanding what you read, and (5) writing. QOLIE-89 data were not available for one patient. For the remainder of the TLE participants (n = 15), the QOLIE-89 language index did not correlate significantly with any of the naming variables. AN speed (rs = −0.43, P = 0.11) was the only naming test variable for which the correlation with the QOLIE-89 language index approached significance. Of the correlations among the naming variables and the five individual QOLIE-89 language index items, only the correlation between “finding the correct word” and AN speed approached significance (rs = −0.49, P = 0.07). Considering other cognitive test variables, the QOLIE-89 “finding the correct word” item also correlated significantly with number of WCST-64 perseverations and pegboard test speed. 3.4. Correlations between naming and demographic and epilepsy variables Among the patients, none of the computerized naming test variables correlated significantly with any demographic variable or epilepsy variable, including age, gender, years of education, age at seizure onset, duration of epilepsy, current frequency of all seizures,

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Table 4 Significant (P < 0.05) Spearman correlations between AN scores and other cognitive variables for the TLE patients Test

AN

Table 5 Partial correlations significant at the <0.01 level between naming speed and accuracy and object name attribute variables by naming test Variable

FSIQ VIQ BNT WRAT-3 Reading WMS III Immediate WMS III General Trail Making Test A WCST Perseverations

Speed

Accuracy

−0.53 −0.72 −0.56 −0.61 −0.51 −0.54 0.59 0.52

0.58 0.63 0.68 0.58 −0.53 −0.54

Note: The VN scores did not correlate significantly with any cognitive variables. BNT: Boston Naming Test (Goodglass and Kaplan, 1983). WRAT-3: Wide Range Achievement Test—3rd edition (Wilkinson, 1993). WCST: Wisconsin Card Sorting Test— 64 Card version (Kongs et al., 2000). Trail Making Test A (Reitan, 1979). WMS III: Wechsler Memory Scale—3rd edition, Immediate and General Memory Indexes (Wechsler, 1997b).

estimated lifetime number of secondarily generalized seizures, and number of anti-epilepsy medications.

Age of acquisition Celex log frequency Imageability Syllables

Naming speed

Accuracy

AN

VN

AN

0.37 −0.35

0.29

0.30 −0.33

VN −0.30 0.30

0.27

Note: Covariates in the analyses were number of words per auditory definition for AN and drawing-name agreement for VN.

to which the drawings were rated as good depictions of what they were supposed to represent (all were concrete objects) correlated significantly with VN speed. Therefore, picture-name agreement was used as a covariate in the correlation analyses involving VN performance. Table 5 shows the attributes of the object names (Morrison et al., 1997) that correlated at the P < 0.01 level with the AN and VN variables. Age of acquisition was the most consistent correlate of the naming measures.

3.5. Correlations between naming and neuropsychological variables 4. Discussion The patients’ AN speed and accuracy correlated significantly with multiple cognitive measures (see Table 4). On the other hand, their VN scores did not correlate significantly with any other cognitive test. Even with IQ as a covariate, one-tailed correlations between the AN scores and group membership were significant (P < 0.05), whereas the correlation between VN scores and group were not (P > 0.10). 3.6. Correlations between naming and attributes of the target objects Because the correlations between naming test results and object name attribute variables were quite similar for patients and controls, data from all participants were included in the following correlation analyses. AN speed and accuracy correlated significantly with the length of the auditory definitions. Therefore the latter variable was used as a covariate when examining the relationship between AN and the attribute variables. Picture-name agreement (Morrison et al., 1997; Snodgrass and Vanderwart, 1980) or the degree

It is well-established that many individuals with TLE, especially those with left hemisphere (language dominant) TLE, show impairment on tests measuring VN ability. However, AN ability has received little attention in this group. Hamberger and colleagues reported that there are important differences between AN and VN performance in TLE patients in the context of both traditional clinical assessment (Hamberger and Seidel, 2003; Hamberger and Tamny, 1999) and presurgical stimulation studies (Hamberger et al., 2001). We assessed controls and TLE patients, who had left or bilateral temporal lobe seizure onset, on AN and VN measures. Although we used different auditory definitions and there were some differences in the objects used as stimuli, our findings are consistent overall with those of Hamberger and colleagues. When the individual participants in the present study were classified on the basis of cut-off scores, both AN speed and accuracy discriminated patients versus controls better than VN speed and accuracy. The AN variables

B.D. Bell et al. / Epilepsy Research 55 (2003) 29–37

also distinguished patients from controls better than any other measure in our battery, including BNT accuracy, a traditional test of visual naming. In addition, we found that there was a trend for severity of word finding complaint to correlate with AN speed, but not with other naming scores. This finding is consistent with the idea that AN is an ecologically valid measure of dysnomia. That is, AN appears to be related to word finding difficulty in everyday conversation, as suggested by Hamberger and colleagues. Consistent with the hypothesis (Hamberger and Tamny, 1999, pp. 238–239) that AN performance is related to a broad range of abilities, AN speed and accuracy correlated significantly with numerous neuropsychological test scores. In light of this correlational data, it could be argued that AN is measuring more than naming ability. However, it may be the complex cognitive demands of AN that make it an appropriate analogue of the word finding process in everyday conversational discourse. The finding of a consistent relationship between the age at which object names typically are acquired and the experimental naming variables parallels our previous report of a strong relationship between this attribute variable and BNT performance in a different group of TLE patients (Bell et al., 2000). Both age of acquisition of object names and word frequency, which showed a relationship with two of the four naming variables, should be taken into account in the design of object naming measures (Barry et al., 1997; Ellis and Morrison, 1998; Lambon Ralph et al., 1998; Nickels and Howard, 1995; Snodgrass and Yuditsky, 1996). Object imageability (how easily a word generates a mental image of an object) and number of syllables also were significant correlates of specific naming variables. The finding that AN and VN speed and accuracy were sometimes affected by different word attribute variables perhaps offers further support for the contention that AN and VN make different cognitive demands. The seemingly slow mean AN response speed in this study can be explained by the fact that the timer was triggered when the description of an object began, rather than when the description was completed. The fact that participants could respond on the AN items before the auditory definition was completed raises the possibility that motivational factors could have influenced test performance. In future investigations, it

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might be preferable to prevent responding until the definition is completed. Because we did not include a right TLE group for comparison, it is possible that the slow response speed in our patients compared to controls is associated with general mental slowing as opposed to language dysfunction specifically. However, previous reports have suggested that the slow AN response speed is specific to left temporal dysfunction (Hamberger and Seidel, 2003; Hamberger and Tamny, 1999), and our AN accuracy findings would not be affected directly by general mental slowing. Our finding of (non-significantly) reduced IQ in the TLE group compared to the control group is consistent with the vast majority of studies of TLE. Previous researchers have pointed out the inadvisability of matching such groups for intelligence when reduced IQ is a common characteristic of the disease process itself. In addition, controlling for IQ statistically did not change the findings appreciably. With IQ as a covariate, correlations between AN scores and group membership remained statistically significant (P < 0.05), whereas the correlation between VN scores and group were not significant. Other limitations of this study include the relatively small sample size, the interval between the administration of the BNT and the other naming measures, and the fact that not all patients had undergone ictal EEG monitoring to determine lateralization of seizure onset. Its strengths include the use of relatives and friends of the patients to form the control group, computerized response speed timing, well-matched naming stimuli for the naming tests, analysis of the relationship between naming test performance and attributes of the object names, and the analysis of the association between naming speed and accuracy and neuropsychological and language self-report data. In summary, the results demonstrate that AN accuracy and speed are sensitive measures of cognitive impairment in TLE patients. Performance on these measures distinguished the majority of the TLE patients from controls and AN response speed correlated better than other naming variables with self-reported word finding complaints. Future studies should investigate whether AN consistently distinguishes left and right TLE patients better than VN, and whether presurgical AN ability is consistently linked to self-reported word finding ability, discourse performance, and post-ATL

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language outcome. Future research also could determine whether computerized tests of naming speed offer more information than traditional clinical tests.

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