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Stimulus type affects Wada memory performance
Epilepsy & Behavior 13 (2008) 458–462
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Stimulus type affects Wada memory performance S. Marc Testa a,*, Julianna Ward a, Nathan E. Crone b, Jason Brandt a,b a
Department of Psychiatry and Behavioral Sciences, Division of Medical Psychology, The Johns Hopkins University School of Medicine, 600 N. Wolfe Street, Meyer 218, Baltimore, MD 21287, USA Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA
b
a r t i c l e
i n f o
Article history: Received 14 February 2008 Revised 30 June 2008 Accepted 30 June 2008 Available online 3 August 2008 Keywords: Wada Intracarotid amobarbital procedure Temporal lobe epilepsy Material-specific memory Functional laterality Language dominance
a b s t r a c t The effects of amytal injection side, seizure focus laterality, and stimulus type (real and line-drawn objects, printed words, and faces) on recognition memory were studied during the Wada procedure. To-be-remembered stimuli were presented during cerebral anesthesia to 35 patients with left temporal lobe epilepsy (LTLE) and 28 patients with right temporal lobe epilepsy (RTLE), all with left hemisphere language dominance. In both groups, recognition of real and line-drawn objects was best after anesthetization of the lesional hemisphere. Recognition of faces was poor after either injection in patients with RTLE, but only after right injection in patients with LTLE. Conversely, recognition of words by patients with LTLE was impaired equally after either injection, but more so after left than right injection in patients with RTLE. The findings suggest that (1) real and line-drawn objects are ‘‘dually encoded” and memory accuracy depends on seizure focus laterality, and (2) accuracy in recognition of words and faces is related to seizure focus laterality, but may also depend on the language dominance of the hemisphere being assessed. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction The Wada test (or intracarotid amobarbital procedure) is used to predict whether neurosurgical patients are at risk for postoperative memory decline. It is performed most often in patients who are candidates for anterior temporal lobectomy (ATL) for the treatment of medically refractory epilepsy [1–3]. During the Wada test, the memory capacity of one cerebral hemisphere is evaluated while the opposite hemisphere is deactivated with a short-acting barbiturate. Traditionally, the Wada test has been employed to predict risk of global postoperative amnesia [4]. Candidates for ATL are at increased risk for severe memory impairment when the memory functions of the ‘‘healthy” (i.e., nonlesional) hemisphere are poor. However, the Wada procedure may be useful in predicting risk of more subtle, perhaps material-specific, postoperative memory deficits [2]. Patients appear to be at risk for postoperative material-specific memory decline when the memory functions of each cerebral hemisphere, especially those of the hemisphere containing the seizure focus, are intact [5,6]. Although the relationship between Wada test memory performance and verbal memory decline after left ATL is regarded as fairly robust [7–11], findings of nonverbal memory decline after right ATL have been less consistent [2,6]. There is some evidence that the nature of the to-be-remembered stimuli influences Wada * Corresponding author. Fax: +1 410 955 0504. E-mail address: [email protected] (S.M. Testa). 1525-5050/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2008.06.020
test memory performance [12–15]. Thus, it would be clinically relevant to assess patients during the Wada procedure with material that could help predict an individual’s risk of decline after right ATL [15]. It has been demonstrated repeatedly that memory of ‘‘dually encodable” stimuli (such as real objects and line-drawn pictures that can be processed verbally or nonverbally) is poorest after anesthetization of the hemisphere contralateral to the seizure focus, regardless of the hemisphere’s language dominance [12–15]. It is also the case that memory for words during the Wada test depends on the integrity of the language-dominant hemisphere; right-handed patients with left temporal lobe epilepsy may have difficulty remembering words after both injections, even though the nonlesional right hemisphere may encode other stimuli successfully [12–14]. A few studies report the use of facial stimuli during the Wada test. Perrine et al. [14] exposed 24 patients with right temporal lobe epilepsy (RTLE) and 21 patients with left temporal lobe epilepsy (LTLE) to various stimuli (two line-drawn objects, two printed words, one colored shape, one abstract shape, one math expression, and one face) during the Wada procedure. They found that memory for the facial stimulus was equivalently poor for both groups after right injection, but worse in RTLE than LTLE (although not significantly so) after left injection. However, a similar pattern emerged for object drawings, words, and the colored shape. In 12 patients with LTLE and 8 with RTLE, Christiansen et al. [16] found faces (as well as common objects and abstract figures, but not
S.M. Testa et al. / Epilepsy & Behavior 13 (2008) 458–462
words) were best recognized when presented to the right, nonlesional hemisphere of the LTLE group. In a more recent study, Kelley et al. [17] demonstrated better memory of faces after left than right hemisphere injection (as well as better memory of words after right than left injection) in a group of 18 patients with TLE [17]. Use of nonverbal stimuli in the Wada test, such as unfamiliar figures, line drawings, and scenes, has generally been unsuccessful in predicting memory decline after right temporal lobectomy [15]. Although it is accepted widely that successful facial memory depends on the functional integrity of the right temporal lobe [18–20], this has not been demonstrated clearly using Wada test methodology. The few studies that have used faces as stimuli had either a limited number of items [14] or too few subjects [16,17]. Although Kelly et al. [17] demonstrated a double dissociation between injection side and memory for words and faces, they did not consider the effect of seizure focus laterality in their analyses. Thus, we sought to address these issues and determine how recognition memory of faces (and other stimuli) is affected by side of amytal injection and seizure focus laterality. If facial recognition depends on right hemisphere functioning, performance will be poor in the RTLE group after injection of either hemisphere, but more impaired after right than left injection in the LTLE. 2. Methods 2.1. Participants Participants were 63 adults with medically refractory epilepsy who were being evaluated for temporal lobe resection. Seizure laterality was determined by 24-hour video/EEG monitoring of at least three ictal events. Thirty-five had left temporal foci and 28 had right temporal foci. All patients were left hemisphere dominant for language (details described below). LTLE and RTLE groups were equivalent on relevant demographic and disease-related variables (see Table 1). Most patients were right-handed and in their midthirties, with average estimated IQs and some college education. In general, recurrent seizures began in the late teenage years, and patients were taking an average of two antiepileptic drugs at the time of the Wada test. Sixty percent (21 patients) of those with LTLE had MRI findings supportive of mesial temporal sclerosis (MTS), 23 (65.7%) underwent standard left anterior temporal lobectomy, 7 (20%) did not have surgery at the time these data were analyzed, 3 (8.5%) had a left temporal lobectomy with amygdalectomy sparing the hippocampus, and 2 (5.7%) underwent resection of parahippocampal tumors. In the RTLE group, 16 (57%) had MRI findings indicative of MTS, 26 pa-
Table 1 Demographic and disease-related variables for LTLE and RTLE groups LTLE (N = 35)
RTLE (N = 28)
M
SD
M
34.97 14.23 18.74 19.08 1.86 97.38
15.14 2.41 14.06 15.17 0.55 14.17 LTLE
36.39 13.25 18.69 17.64 1.79 96.38
Sex (% women) Racial background (%) Caucasian African-American Asian Handedness (% right-handed)
Age Education Age at onset Duration of Illness Number of AEDs Estimated IQa
a
SD
F
P
11.21 2.27 14.49 16.94 0.74 12.63 RTLE
0.17 2.69 0.0002 0.13 0.19 0.08 X2
0.68 0.11 0.99 0.73 0.66 0.78 P
60.0
46.4
1.15 1.41
0.28 0.50
85.7 14.3 0.0 82.9
85.7 10.7 3.6 96.4
2.90
0.09
IQ was estimated using the Shipley Institute of Living Scale in some subjects and the Wechsler Adult Intelligence Scale III in others.
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tients (92.9%) underwent standard right temporal lobectomy, 1 patient (3.6%) did not have surgery at the time these data were analyzed, and 1 patient (3.6%) had resection of lateral posterior temporal neocortex. 2.2. Procedure On the day prior to the Wada test, all patients received a complete neuropsychological assessment. In addition, to establish a baseline level of performance for the Wada test and to familiarize patients with the general testing procedure, we assessed each patient’s memory (without drug) using stimuli similar to those used during the actual Wada test. The next day, immediately following cerebral angiography, approximately 125 mg of sodium amobarbital was administered transfemorally to the hemisphere containing the seizure focus. Additional amobarbital was administered if hemiparesis was not induced within 5 seconds. Following injection, patients attempted to name six real objects (e.g., ruler, apple, flashlight, watch) and four line drawings of objects (e.g., lamp, bird, ear of corn, nail), to read six printed words (e.g., sink, deaf, swamp), and to judge the affect expressed in four photographs of faces (e.g., happy, sad, angry, or surprised). Each of these 20 items was presented for 4 to 8 seconds during which the patient’s eye movements were continually monitored to assess visual attention. Before each item was removed from the patient’s visual field, the examiner stated ‘‘Remember this”. The patient’s ability to name the six objects and read the six words contributed to his or her language score. The language score also included the patient’s ability to follow basic verbal instructions in a Token Test and repeat sentences. Strength was assessed to gauge the amytal affect at predetermined times during stimulus presentation. On full reversal of EEG slowing and at least 10 minutes after amobarbital injection, each of the 20 previously presented items and an equal number of novel distractor items were presented one at a time for assessment of yes/no recognition. A minimum of 30 minutes after the first injection, another angiography was performed, sodium amobarbital was administered to the hemisphere contralateral to the seizure focus, and a new set of stimuli were presented for language and memory testing. For baseline and each injection, memory accuracy was assessed for each stimulus type using a measure of discrimination (true positives minus false positives). The memory scores reported here were computed by subtracting the baseline discrimination score from each injection’s discrimination score and dividing the difference by the total number of possible targets (i.e., six possible targets for words and objects, and four possible targets for line-drawn pictures and faces). For example, a patient with a baseline discrimination score of 5 for objects (e.g., with 6 of 6 true positives and 1 of 6 false positives) and a left injection discrimination score of 2 for objects (3 true positives and 1 false positive) would have a score of 0.50 (i.e., (2–5)/6). This scoring method was selected because it accounts for each patient’s baseline performance and the derived score depicts a relative decline from baseline for each injection. To our knowledge, only the study of Kelly et al. [17] incorporated baseline performance into their statistical analyses. A language score was tallied after each injection to reflect the total number of correct responses while naming objects, reading words, following instructions, and repeating sentences. To calculate language dominance, the difference between language scores after right (Rinj) and left (Linj) injection was divided by the sum of both scores ([LInj – RInj]/[RInj + LInj]), with –1 reflecting strong left hemisphere language dominance and +1 reflecting strong right hemisphere language dominance. A language laterality score < 0.20 was used to indicate left hemisphere language dominance [21,22]. Only subjects with scores lower than this value were included in the current study.
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2.3. Data analyses A 2 (seizure focus group) 2 (injection side) 4 (material type) mixed-model repeated-measures ANOVA was performed. Withingroup analyses across injections were computed with paired sample t tests.
Table 2 Wada test memory performance by side of injection and material type for left and right TLE groups Injection side
Proportional Decline from Baseline
Words
Linedrawn Objects
RTLE SD
M
SD
Left
Real objects Words Line-drawn objects Faces
0.42 0.37 0.19 0.34
0.37 0.32 0.39 0.44
0.69 0.64 0.54 0.55
0.29 0.30 0.28 0.46
Right
Real objects Words Line-drawn objects Faces
0.60 0.38 0.30 0.62
0.39 0.35 0.35 0.35
0.18 0.24 0.11 0.52
0.25 0.28 0.33 0.37
poral lobe seizure focus or amytal, results in impaired facial memory. Comparison of the ipsilateral injection memory scores (i.e., when testing the memory functions of the ‘‘healthy” hemisphere) reveals that memory for real objects was better after right injection for patients with RTLE than after left injection for patients with LTLE (F(1, 61) = 8.61, P < 0.01, gp2 = 0.124). This suggests that the ‘‘healthy” left hemisphere of patients with RTLE is relatively better at processing real objects than the ‘‘healthy” right hemisphere of patients with LTLE. Although the pattern of memory for words (F(1, 61) = 2.79, P = 0.10, gp2 = 0.044) and line-drawn objects (F(1, 61) = 0.864, P = 0.36, gp2 = 0.014) is similar to that for real objects, these contrasts failed to meet statistical significance. Although the pattern for facial memory is opposite that for real objects (i.e., memory was better after left injection for patients with LTLE than after right injection for those with RTLE), the difference was not statistically significant (F(1, 61) = 2.870, P = 0.10, gp2 = 0.045). Comparison of the contralateral injection memory scores (i.e., testing the memory functions of the ‘‘epileptic” hemisphere) reveals that memory for words (F(1, 61) = 9.354, P < 0.01, gp2 = 0.133) and line-drawn objects (F(1, 61) = 8.518, P < 0.01, gp2 = 0.123) was worse in the epileptic right than left hemisphere. Memory for real objects (F(1, 61) = 1.021, P = 0.32, gp2 = 0.016) and faces (F(1, 61) = 0.438, P = 0.51, gp2 = 0.007) was impaired equally after contralateral injection.
LTLE Real Objects
LTLE M
3. Results The data are depicted graphically in Fig. 1 and numerically in Table 2. Overall, the effect of seizure focus laterality was not significant (F(1, 61) = 0.457, P = 0.50, gp2 = 0.007). Patients with LTLE performed as well as those with RTLE, pooled over injection side and stimulus type. There was a main effect for injection side: memory performance was worse after left than right injection (F(1, 61) = 9.96, P < 0.01, gp2 = 0.140). There was also a main effect of material type (F(3, 59) = 8.70, P < 0.001, gp2 = 0.307); recognition memory was worst for faces and best for line-drawn objects. As expected, memory was much less accurate after anesthetization of the hemisphere contralateral to the seizure focus (group injection side interaction: F(1, 61) = 59.97, P < 0.001, gp2 = 0.496). A material injection side interaction (F(3, 59) = 5.81, P = 0.01, gp2 = 0.228) revealed that memory was worse for faces after right than left injection and poorer after left injection for all other stimulus types. Most importantly, the three-way interaction was significant (F(3, 59) = 3.27, P < 0.05, gp2 = 0.142). Recognition of real objects and line-drawn objects was worse after injection of the ‘‘healthy” hemisphere than it was after injection of the hemisphere containing the seizures focus. This suggests that these stimuli are processed by both hemispheres and memory can be disrupted by dysfunction of either hemisphere. However, recognition of words was better after right than left injection for RTLE (t(27) = –5.19, P < 0.001, d = 1.37), and equally impaired for both injections for LTLE (t(34) = 0.24, P < 0.90, d = 0.04). This suggests that the left hemisphere is critical for recognition of words. Conversely, memory for faces was better after left than right injection for LTLE (t(34) = 3.43, P = 0.002, d = 0.70), but impaired after both injections for RTLE (t(27) = –0.42, P = 0.68, d = 0.09). This suggests that impairing the functioning of the right hemisphere, either by a tem-
Material type
RTLE
Faces
Real Objects
Left Inj.
Right Inj.
Words
Linedrawn Objects
Faces
0.00 -0.10 -0.20 -0.30 -0.40 -0.50 -0.60 -0.70 -0.80 -0.90 -1.00
Fig. 1. Pattern of memory performance for patients with LTLE and RTLE after left or right cerebral intracarotid amobarbital anesthetization represented as a proportional decline from baseline memory accuracy. Means ± SE.
S.M. Testa et al. / Epilepsy & Behavior 13 (2008) 458–462
4. Discussion The findings demonstrate that memory accuracy is poorest for real objects and line-drawn objects after anesthetization of the hemisphere contralateral to the seizure focus. This is consistent with numerous studies [12,13,15,16,23]. However, the pattern of memory performance is much different for words and faces. In patients with LTLE, the memory capability of the ‘‘healthy” right hemisphere was good for objects, line-drawn objects, and faces, but relatively poor for words. This particular pattern suggests that memory of printed words cannot be subserved by the right hemisphere in isolation, and is consistent with previous studies [12–16]. However, memory for stimuli presented to the left hemisphere of the RTLE group was good for objects, words, and line-drawn objects, but not for faces. This finding is new, and suggests that memory for faces is most vulnerable when right hemispheric processes are interrupted, either by a seizure focus or by deactivation. The pattern of findings from this study is consistent with several studies [12–14] in which accuracy of memory for words was equivalent after each injection in LTLE, but poorer after left than right injection in RTLE. One study did not show this effect with abstract words [16], but found that concrete words were remembered better after right hemisphere injection, regardless of lesion side. Better recognition of words after right than left injection, regardless of seizure focus laterality, was also reported by Vingerhoets and colleagues [15]. All these studies find that recognition of words is superior in the healthy left hemisphere. However, recognition of words for patients with LTLE after right hemisphere anesthesia is variable across studies. The results of Perrine et al. [14] suggest that memory of faces is worst following injection of the hemisphere contralateral to the seizure focus. However, only one face stimulus was used. Like our findings, the data of Christiansen et al. [16] suggest that facial stimuli are remembered best after left hemisphere deactivation in patients with LTLE. An alternative explanation of our findings is that the left hemisphere is dominant for real objects, line-drawn objects, and words. A seizure focus in the left hemisphere diminishes this pattern, but a seizure focus in the right hemisphere makes it more apparent. An opposite pattern is observed for memory of faces and right hemisphere dominance. For faces, a right hemisphere seizure focus diminishes the asymmetry, but a left hemisphere seizure focus makes the asymmetry more apparent. However, our findings that objects (either real or line-drawn) can be represented by either hemisphere, but that faces and words are preferentially represented by the right and left hemispheres, respectively, are consistent with those using various methodologies [14,24,25]. In neurologically normal adult volunteers, Kelley et al. [24] found bilaterally increased dorsal frontal and mesial temporal activation during picture encoding, but greater left than right activation during word encoding, and greater right than left activation during facial encoding. In another study of patients being monitored for seizure localization with bilateral hippocampal depth electrodes, electrical stimulation was delivered to either the right or left hippocampus during memory encoding of pictured objects, words, and faces [25]. Recognition of objects was no different than baseline after stimulation of either the left or right hippocampus. However, stimulation of the left hippocampus during encoding of words interfered with later word memory, and stimulation of the right hippocampus during facial encoding interfered with delayed facial memory. Future studies should consider the several methodological factors that may have influenced the current pattern of findings. First, it is quite possible that the current results reflect the nature of our encoding procedures rather than stimulus type. For instance, pa-
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tients were asked to read words and name pictures during item encoding, but asked to label the emotional expression of each facial stimulus. Thus, the right hemisphere preference for faces might be explained, in part, by the encoding strategy employed. Second, we did not counterbalance injection order within each seizure focus group and this may have confounded our results [26]. Finally, all of our patients were left hemisphere language dominant. Thus, firm conclusions about the relationship between material-specific memory processing and hemispheric language dominance would require a study design that includes patients with right hemisphere dominant, or bilaterally represented, language functions. The apparent vulnerability of words and faces to left and right hemisphere disruption, respectively, (rather than to a contralesional injection) suggests that words and faces may provide useful information about material-specific memory decline. Thus, it may be the case that patients with LTLE with accurate memory of words after left injection may have more favorable outcomes than patients with LTLE whose memory of words is poor after each injection. Alternatively, one can imagine a patient with RTLE who performs as expected for real objects, line-drawn objects, and words (i.e., worse memory after left than right injection), but whose memory for faces declines after either injection. Most clinicians would probably agree that such a patient would not be at high risk for global amnesia, but may be at higher risk for nonverbal memory decline after right ATL than another patient with RTLE with intact recognition of faces after right injection. However, these specific, case-level scenarios have not been addressed in the literature. Because the Wada test is an invasive procedure with some morbidity [10,27,28], noninvasive methods of assessing the functional integrity of each temporal lobe would be desirable. Indeed, detection of preoperative nonverbal memory deficits in RTLE and prediction of postoperative decline of nonverbal memory after right ATL may not depend on the Wada test results. First, studies in presurgical patients with TLE have shown that facial memory is worse in patients with RTLE than in those with LTLE [18,29]. Second, fMRI has been shown to correlate with neuropsychological functioning after ATL [30,31] and, more specifically, with nonverbal memory after nondominant ATL [32]. Although data appear to be mounting in this direction, to date, very few studies have compared these various methodologies directly [28,30,33]. Acknowledgments This study was made possible by the Gertrude A. Sergievsky Research Endowment supported by the Epilepsy Foundation Behavioral Sciences Postdoctoral Fellowship (S.M.T.). This study was presented at the 35th Annual Meeting of the International Neuropsychological Society, Portland, Oregon, USA, 2007. We thank Robin Sue Miller, M.S., for her valuable assistance recording data during the Wada procedures, as well as the faculty and staff of the Johns Hopkins University Epilepsy Center. We also acknowledge the very helpful comments and suggestions made by the reviewers. References [1] Chelune GJ. Hippocampal adequacy versus functional reserve: predicting memory functions following temporal lobectomy. Arch Clin Neuropsychol 1995;10:413–32. [2] Kneebone AC, Chelune GJ, Dinner DS, Naugle RI, Awad IA. Intracarotid amobarbital procedure as a predictor of material-specific memory change after anterior temporal lobectomy. Epilepsia 1995;36:857–65. [3] Loring DW, Lee GP, Meador KJ, et al. The intracarotid amobarbital procedure as a predictor of memory failure following unilateral temporal lobectomy. Neurology 1990;40:605–10. [4] Kubu CS, Girvin JP, McLachlan RS, Pavol M, Harnadek MCS. Does the intracarotid amobarbital procedure predict global amnesia after temporal lobectomy? Epilepsia 2000;41:1321–9.
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Stimulus type affects Wada memory performance S. Marc Testa a,*, Julianna Ward a, Nathan E. Crone b, Jason Brandt a,b a
Department of Psychiatry and Behavioral Sciences, Division of Medical Psychology, The Johns Hopkins University School of Medicine, 600 N. Wolfe Street, Meyer 218, Baltimore, MD 21287, USA Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA
b
a r t i c l e
i n f o
Article history: Received 14 February 2008 Revised 30 June 2008 Accepted 30 June 2008 Available online 3 August 2008 Keywords: Wada Intracarotid amobarbital procedure Temporal lobe epilepsy Material-specific memory Functional laterality Language dominance
a b s t r a c t The effects of amytal injection side, seizure focus laterality, and stimulus type (real and line-drawn objects, printed words, and faces) on recognition memory were studied during the Wada procedure. To-be-remembered stimuli were presented during cerebral anesthesia to 35 patients with left temporal lobe epilepsy (LTLE) and 28 patients with right temporal lobe epilepsy (RTLE), all with left hemisphere language dominance. In both groups, recognition of real and line-drawn objects was best after anesthetization of the lesional hemisphere. Recognition of faces was poor after either injection in patients with RTLE, but only after right injection in patients with LTLE. Conversely, recognition of words by patients with LTLE was impaired equally after either injection, but more so after left than right injection in patients with RTLE. The findings suggest that (1) real and line-drawn objects are ‘‘dually encoded” and memory accuracy depends on seizure focus laterality, and (2) accuracy in recognition of words and faces is related to seizure focus laterality, but may also depend on the language dominance of the hemisphere being assessed. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction The Wada test (or intracarotid amobarbital procedure) is used to predict whether neurosurgical patients are at risk for postoperative memory decline. It is performed most often in patients who are candidates for anterior temporal lobectomy (ATL) for the treatment of medically refractory epilepsy [1–3]. During the Wada test, the memory capacity of one cerebral hemisphere is evaluated while the opposite hemisphere is deactivated with a short-acting barbiturate. Traditionally, the Wada test has been employed to predict risk of global postoperative amnesia [4]. Candidates for ATL are at increased risk for severe memory impairment when the memory functions of the ‘‘healthy” (i.e., nonlesional) hemisphere are poor. However, the Wada procedure may be useful in predicting risk of more subtle, perhaps material-specific, postoperative memory deficits [2]. Patients appear to be at risk for postoperative material-specific memory decline when the memory functions of each cerebral hemisphere, especially those of the hemisphere containing the seizure focus, are intact [5,6]. Although the relationship between Wada test memory performance and verbal memory decline after left ATL is regarded as fairly robust [7–11], findings of nonverbal memory decline after right ATL have been less consistent [2,6]. There is some evidence that the nature of the to-be-remembered stimuli influences Wada * Corresponding author. Fax: +1 410 955 0504. E-mail address: [email protected] (S.M. Testa). 1525-5050/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2008.06.020
test memory performance [12–15]. Thus, it would be clinically relevant to assess patients during the Wada procedure with material that could help predict an individual’s risk of decline after right ATL [15]. It has been demonstrated repeatedly that memory of ‘‘dually encodable” stimuli (such as real objects and line-drawn pictures that can be processed verbally or nonverbally) is poorest after anesthetization of the hemisphere contralateral to the seizure focus, regardless of the hemisphere’s language dominance [12–15]. It is also the case that memory for words during the Wada test depends on the integrity of the language-dominant hemisphere; right-handed patients with left temporal lobe epilepsy may have difficulty remembering words after both injections, even though the nonlesional right hemisphere may encode other stimuli successfully [12–14]. A few studies report the use of facial stimuli during the Wada test. Perrine et al. [14] exposed 24 patients with right temporal lobe epilepsy (RTLE) and 21 patients with left temporal lobe epilepsy (LTLE) to various stimuli (two line-drawn objects, two printed words, one colored shape, one abstract shape, one math expression, and one face) during the Wada procedure. They found that memory for the facial stimulus was equivalently poor for both groups after right injection, but worse in RTLE than LTLE (although not significantly so) after left injection. However, a similar pattern emerged for object drawings, words, and the colored shape. In 12 patients with LTLE and 8 with RTLE, Christiansen et al. [16] found faces (as well as common objects and abstract figures, but not
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words) were best recognized when presented to the right, nonlesional hemisphere of the LTLE group. In a more recent study, Kelley et al. [17] demonstrated better memory of faces after left than right hemisphere injection (as well as better memory of words after right than left injection) in a group of 18 patients with TLE [17]. Use of nonverbal stimuli in the Wada test, such as unfamiliar figures, line drawings, and scenes, has generally been unsuccessful in predicting memory decline after right temporal lobectomy [15]. Although it is accepted widely that successful facial memory depends on the functional integrity of the right temporal lobe [18–20], this has not been demonstrated clearly using Wada test methodology. The few studies that have used faces as stimuli had either a limited number of items [14] or too few subjects [16,17]. Although Kelly et al. [17] demonstrated a double dissociation between injection side and memory for words and faces, they did not consider the effect of seizure focus laterality in their analyses. Thus, we sought to address these issues and determine how recognition memory of faces (and other stimuli) is affected by side of amytal injection and seizure focus laterality. If facial recognition depends on right hemisphere functioning, performance will be poor in the RTLE group after injection of either hemisphere, but more impaired after right than left injection in the LTLE. 2. Methods 2.1. Participants Participants were 63 adults with medically refractory epilepsy who were being evaluated for temporal lobe resection. Seizure laterality was determined by 24-hour video/EEG monitoring of at least three ictal events. Thirty-five had left temporal foci and 28 had right temporal foci. All patients were left hemisphere dominant for language (details described below). LTLE and RTLE groups were equivalent on relevant demographic and disease-related variables (see Table 1). Most patients were right-handed and in their midthirties, with average estimated IQs and some college education. In general, recurrent seizures began in the late teenage years, and patients were taking an average of two antiepileptic drugs at the time of the Wada test. Sixty percent (21 patients) of those with LTLE had MRI findings supportive of mesial temporal sclerosis (MTS), 23 (65.7%) underwent standard left anterior temporal lobectomy, 7 (20%) did not have surgery at the time these data were analyzed, 3 (8.5%) had a left temporal lobectomy with amygdalectomy sparing the hippocampus, and 2 (5.7%) underwent resection of parahippocampal tumors. In the RTLE group, 16 (57%) had MRI findings indicative of MTS, 26 pa-
Table 1 Demographic and disease-related variables for LTLE and RTLE groups LTLE (N = 35)
RTLE (N = 28)
M
SD
M
34.97 14.23 18.74 19.08 1.86 97.38
15.14 2.41 14.06 15.17 0.55 14.17 LTLE
36.39 13.25 18.69 17.64 1.79 96.38
Sex (% women) Racial background (%) Caucasian African-American Asian Handedness (% right-handed)
Age Education Age at onset Duration of Illness Number of AEDs Estimated IQa
a
SD
F
P
11.21 2.27 14.49 16.94 0.74 12.63 RTLE
0.17 2.69 0.0002 0.13 0.19 0.08 X2
0.68 0.11 0.99 0.73 0.66 0.78 P
60.0
46.4
1.15 1.41
0.28 0.50
85.7 14.3 0.0 82.9
85.7 10.7 3.6 96.4
2.90
0.09
IQ was estimated using the Shipley Institute of Living Scale in some subjects and the Wechsler Adult Intelligence Scale III in others.
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tients (92.9%) underwent standard right temporal lobectomy, 1 patient (3.6%) did not have surgery at the time these data were analyzed, and 1 patient (3.6%) had resection of lateral posterior temporal neocortex. 2.2. Procedure On the day prior to the Wada test, all patients received a complete neuropsychological assessment. In addition, to establish a baseline level of performance for the Wada test and to familiarize patients with the general testing procedure, we assessed each patient’s memory (without drug) using stimuli similar to those used during the actual Wada test. The next day, immediately following cerebral angiography, approximately 125 mg of sodium amobarbital was administered transfemorally to the hemisphere containing the seizure focus. Additional amobarbital was administered if hemiparesis was not induced within 5 seconds. Following injection, patients attempted to name six real objects (e.g., ruler, apple, flashlight, watch) and four line drawings of objects (e.g., lamp, bird, ear of corn, nail), to read six printed words (e.g., sink, deaf, swamp), and to judge the affect expressed in four photographs of faces (e.g., happy, sad, angry, or surprised). Each of these 20 items was presented for 4 to 8 seconds during which the patient’s eye movements were continually monitored to assess visual attention. Before each item was removed from the patient’s visual field, the examiner stated ‘‘Remember this”. The patient’s ability to name the six objects and read the six words contributed to his or her language score. The language score also included the patient’s ability to follow basic verbal instructions in a Token Test and repeat sentences. Strength was assessed to gauge the amytal affect at predetermined times during stimulus presentation. On full reversal of EEG slowing and at least 10 minutes after amobarbital injection, each of the 20 previously presented items and an equal number of novel distractor items were presented one at a time for assessment of yes/no recognition. A minimum of 30 minutes after the first injection, another angiography was performed, sodium amobarbital was administered to the hemisphere contralateral to the seizure focus, and a new set of stimuli were presented for language and memory testing. For baseline and each injection, memory accuracy was assessed for each stimulus type using a measure of discrimination (true positives minus false positives). The memory scores reported here were computed by subtracting the baseline discrimination score from each injection’s discrimination score and dividing the difference by the total number of possible targets (i.e., six possible targets for words and objects, and four possible targets for line-drawn pictures and faces). For example, a patient with a baseline discrimination score of 5 for objects (e.g., with 6 of 6 true positives and 1 of 6 false positives) and a left injection discrimination score of 2 for objects (3 true positives and 1 false positive) would have a score of 0.50 (i.e., (2–5)/6). This scoring method was selected because it accounts for each patient’s baseline performance and the derived score depicts a relative decline from baseline for each injection. To our knowledge, only the study of Kelly et al. [17] incorporated baseline performance into their statistical analyses. A language score was tallied after each injection to reflect the total number of correct responses while naming objects, reading words, following instructions, and repeating sentences. To calculate language dominance, the difference between language scores after right (Rinj) and left (Linj) injection was divided by the sum of both scores ([LInj – RInj]/[RInj + LInj]), with –1 reflecting strong left hemisphere language dominance and +1 reflecting strong right hemisphere language dominance. A language laterality score < 0.20 was used to indicate left hemisphere language dominance [21,22]. Only subjects with scores lower than this value were included in the current study.
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2.3. Data analyses A 2 (seizure focus group) 2 (injection side) 4 (material type) mixed-model repeated-measures ANOVA was performed. Withingroup analyses across injections were computed with paired sample t tests.
Table 2 Wada test memory performance by side of injection and material type for left and right TLE groups Injection side
Proportional Decline from Baseline
Words
Linedrawn Objects
RTLE SD
M
SD
Left
Real objects Words Line-drawn objects Faces
0.42 0.37 0.19 0.34
0.37 0.32 0.39 0.44
0.69 0.64 0.54 0.55
0.29 0.30 0.28 0.46
Right
Real objects Words Line-drawn objects Faces
0.60 0.38 0.30 0.62
0.39 0.35 0.35 0.35
0.18 0.24 0.11 0.52
0.25 0.28 0.33 0.37
poral lobe seizure focus or amytal, results in impaired facial memory. Comparison of the ipsilateral injection memory scores (i.e., when testing the memory functions of the ‘‘healthy” hemisphere) reveals that memory for real objects was better after right injection for patients with RTLE than after left injection for patients with LTLE (F(1, 61) = 8.61, P < 0.01, gp2 = 0.124). This suggests that the ‘‘healthy” left hemisphere of patients with RTLE is relatively better at processing real objects than the ‘‘healthy” right hemisphere of patients with LTLE. Although the pattern of memory for words (F(1, 61) = 2.79, P = 0.10, gp2 = 0.044) and line-drawn objects (F(1, 61) = 0.864, P = 0.36, gp2 = 0.014) is similar to that for real objects, these contrasts failed to meet statistical significance. Although the pattern for facial memory is opposite that for real objects (i.e., memory was better after left injection for patients with LTLE than after right injection for those with RTLE), the difference was not statistically significant (F(1, 61) = 2.870, P = 0.10, gp2 = 0.045). Comparison of the contralateral injection memory scores (i.e., testing the memory functions of the ‘‘epileptic” hemisphere) reveals that memory for words (F(1, 61) = 9.354, P < 0.01, gp2 = 0.133) and line-drawn objects (F(1, 61) = 8.518, P < 0.01, gp2 = 0.123) was worse in the epileptic right than left hemisphere. Memory for real objects (F(1, 61) = 1.021, P = 0.32, gp2 = 0.016) and faces (F(1, 61) = 0.438, P = 0.51, gp2 = 0.007) was impaired equally after contralateral injection.
LTLE Real Objects
LTLE M
3. Results The data are depicted graphically in Fig. 1 and numerically in Table 2. Overall, the effect of seizure focus laterality was not significant (F(1, 61) = 0.457, P = 0.50, gp2 = 0.007). Patients with LTLE performed as well as those with RTLE, pooled over injection side and stimulus type. There was a main effect for injection side: memory performance was worse after left than right injection (F(1, 61) = 9.96, P < 0.01, gp2 = 0.140). There was also a main effect of material type (F(3, 59) = 8.70, P < 0.001, gp2 = 0.307); recognition memory was worst for faces and best for line-drawn objects. As expected, memory was much less accurate after anesthetization of the hemisphere contralateral to the seizure focus (group injection side interaction: F(1, 61) = 59.97, P < 0.001, gp2 = 0.496). A material injection side interaction (F(3, 59) = 5.81, P = 0.01, gp2 = 0.228) revealed that memory was worse for faces after right than left injection and poorer after left injection for all other stimulus types. Most importantly, the three-way interaction was significant (F(3, 59) = 3.27, P < 0.05, gp2 = 0.142). Recognition of real objects and line-drawn objects was worse after injection of the ‘‘healthy” hemisphere than it was after injection of the hemisphere containing the seizures focus. This suggests that these stimuli are processed by both hemispheres and memory can be disrupted by dysfunction of either hemisphere. However, recognition of words was better after right than left injection for RTLE (t(27) = –5.19, P < 0.001, d = 1.37), and equally impaired for both injections for LTLE (t(34) = 0.24, P < 0.90, d = 0.04). This suggests that the left hemisphere is critical for recognition of words. Conversely, memory for faces was better after left than right injection for LTLE (t(34) = 3.43, P = 0.002, d = 0.70), but impaired after both injections for RTLE (t(27) = –0.42, P = 0.68, d = 0.09). This suggests that impairing the functioning of the right hemisphere, either by a tem-
Material type
RTLE
Faces
Real Objects
Left Inj.
Right Inj.
Words
Linedrawn Objects
Faces
0.00 -0.10 -0.20 -0.30 -0.40 -0.50 -0.60 -0.70 -0.80 -0.90 -1.00
Fig. 1. Pattern of memory performance for patients with LTLE and RTLE after left or right cerebral intracarotid amobarbital anesthetization represented as a proportional decline from baseline memory accuracy. Means ± SE.
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4. Discussion The findings demonstrate that memory accuracy is poorest for real objects and line-drawn objects after anesthetization of the hemisphere contralateral to the seizure focus. This is consistent with numerous studies [12,13,15,16,23]. However, the pattern of memory performance is much different for words and faces. In patients with LTLE, the memory capability of the ‘‘healthy” right hemisphere was good for objects, line-drawn objects, and faces, but relatively poor for words. This particular pattern suggests that memory of printed words cannot be subserved by the right hemisphere in isolation, and is consistent with previous studies [12–16]. However, memory for stimuli presented to the left hemisphere of the RTLE group was good for objects, words, and line-drawn objects, but not for faces. This finding is new, and suggests that memory for faces is most vulnerable when right hemispheric processes are interrupted, either by a seizure focus or by deactivation. The pattern of findings from this study is consistent with several studies [12–14] in which accuracy of memory for words was equivalent after each injection in LTLE, but poorer after left than right injection in RTLE. One study did not show this effect with abstract words [16], but found that concrete words were remembered better after right hemisphere injection, regardless of lesion side. Better recognition of words after right than left injection, regardless of seizure focus laterality, was also reported by Vingerhoets and colleagues [15]. All these studies find that recognition of words is superior in the healthy left hemisphere. However, recognition of words for patients with LTLE after right hemisphere anesthesia is variable across studies. The results of Perrine et al. [14] suggest that memory of faces is worst following injection of the hemisphere contralateral to the seizure focus. However, only one face stimulus was used. Like our findings, the data of Christiansen et al. [16] suggest that facial stimuli are remembered best after left hemisphere deactivation in patients with LTLE. An alternative explanation of our findings is that the left hemisphere is dominant for real objects, line-drawn objects, and words. A seizure focus in the left hemisphere diminishes this pattern, but a seizure focus in the right hemisphere makes it more apparent. An opposite pattern is observed for memory of faces and right hemisphere dominance. For faces, a right hemisphere seizure focus diminishes the asymmetry, but a left hemisphere seizure focus makes the asymmetry more apparent. However, our findings that objects (either real or line-drawn) can be represented by either hemisphere, but that faces and words are preferentially represented by the right and left hemispheres, respectively, are consistent with those using various methodologies [14,24,25]. In neurologically normal adult volunteers, Kelley et al. [24] found bilaterally increased dorsal frontal and mesial temporal activation during picture encoding, but greater left than right activation during word encoding, and greater right than left activation during facial encoding. In another study of patients being monitored for seizure localization with bilateral hippocampal depth electrodes, electrical stimulation was delivered to either the right or left hippocampus during memory encoding of pictured objects, words, and faces [25]. Recognition of objects was no different than baseline after stimulation of either the left or right hippocampus. However, stimulation of the left hippocampus during encoding of words interfered with later word memory, and stimulation of the right hippocampus during facial encoding interfered with delayed facial memory. Future studies should consider the several methodological factors that may have influenced the current pattern of findings. First, it is quite possible that the current results reflect the nature of our encoding procedures rather than stimulus type. For instance, pa-
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tients were asked to read words and name pictures during item encoding, but asked to label the emotional expression of each facial stimulus. Thus, the right hemisphere preference for faces might be explained, in part, by the encoding strategy employed. Second, we did not counterbalance injection order within each seizure focus group and this may have confounded our results [26]. Finally, all of our patients were left hemisphere language dominant. Thus, firm conclusions about the relationship between material-specific memory processing and hemispheric language dominance would require a study design that includes patients with right hemisphere dominant, or bilaterally represented, language functions. The apparent vulnerability of words and faces to left and right hemisphere disruption, respectively, (rather than to a contralesional injection) suggests that words and faces may provide useful information about material-specific memory decline. Thus, it may be the case that patients with LTLE with accurate memory of words after left injection may have more favorable outcomes than patients with LTLE whose memory of words is poor after each injection. Alternatively, one can imagine a patient with RTLE who performs as expected for real objects, line-drawn objects, and words (i.e., worse memory after left than right injection), but whose memory for faces declines after either injection. Most clinicians would probably agree that such a patient would not be at high risk for global amnesia, but may be at higher risk for nonverbal memory decline after right ATL than another patient with RTLE with intact recognition of faces after right injection. However, these specific, case-level scenarios have not been addressed in the literature. Because the Wada test is an invasive procedure with some morbidity [10,27,28], noninvasive methods of assessing the functional integrity of each temporal lobe would be desirable. Indeed, detection of preoperative nonverbal memory deficits in RTLE and prediction of postoperative decline of nonverbal memory after right ATL may not depend on the Wada test results. First, studies in presurgical patients with TLE have shown that facial memory is worse in patients with RTLE than in those with LTLE [18,29]. Second, fMRI has been shown to correlate with neuropsychological functioning after ATL [30,31] and, more specifically, with nonverbal memory after nondominant ATL [32]. Although data appear to be mounting in this direction, to date, very few studies have compared these various methodologies directly [28,30,33]. Acknowledgments This study was made possible by the Gertrude A. Sergievsky Research Endowment supported by the Epilepsy Foundation Behavioral Sciences Postdoctoral Fellowship (S.M.T.). This study was presented at the 35th Annual Meeting of the International Neuropsychological Society, Portland, Oregon, USA, 2007. We thank Robin Sue Miller, M.S., for her valuable assistance recording data during the Wada procedures, as well as the faculty and staff of the Johns Hopkins University Epilepsy Center. We also acknowledge the very helpful comments and suggestions made by the reviewers. References [1] Chelune GJ. Hippocampal adequacy versus functional reserve: predicting memory functions following temporal lobectomy. Arch Clin Neuropsychol 1995;10:413–32. [2] Kneebone AC, Chelune GJ, Dinner DS, Naugle RI, Awad IA. Intracarotid amobarbital procedure as a predictor of material-specific memory change after anterior temporal lobectomy. Epilepsia 1995;36:857–65. [3] Loring DW, Lee GP, Meador KJ, et al. The intracarotid amobarbital procedure as a predictor of memory failure following unilateral temporal lobectomy. Neurology 1990;40:605–10. [4] Kubu CS, Girvin JP, McLachlan RS, Pavol M, Harnadek MCS. Does the intracarotid amobarbital procedure predict global amnesia after temporal lobectomy? Epilepsia 2000;41:1321–9.
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