Seizure: European Journal of Epilepsy
Volume 17, Issue 7 , Pages 604-610, October 2008

The lateralizing value of IQ in mesiotemporal epilepsy: Differences between patients with unitemporal and bitemporal epileptiform discharges

  • Sang-Ahm Lee

      Affiliations

    • Department of Neurology and Neurosurgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea
    • Corresponding Author InformationCorresponding author. Tel.: +82 2 3010 3445; fax: +82 2 474 4691.
    • ,
  • Chul-Ho Kim

      Affiliations

    • Department of Neurology and Neurosurgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea
    • ,
  • Suk-Yoon Kang

      Affiliations

    • Department of Neurology, Kangnam Sacred Heart Hospital, Hallym University Medical Center, Seoul, Republic of Korea
    • ,
  • Young-Joo No

      Affiliations

    • Department of Neurology and Neurosurgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea
    • ,
  • Joong-Koo Kang

      Affiliations

    • Department of Neurology and Neurosurgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea
    • ,
  • Jung-Kyo Lee

      Affiliations

    • Department of Neurology and Neurosurgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Republic of Korea

Received 10 November 2007; received in revised form 15 February 2008; accepted 29 February 2008. published online 07 April 2008.

Article Outline

Summary 

Purpose

We investigated the lateralizing ability of intelligence scores in mesial temporal lobe epilepsy (MTLE) patients according to the distribution of interictal epileptiform discharges (IEDs).

Methods

This study enrolled 82 MTLE patients. All patients had preoperative neuropsychological evaluations, including Korean Wechsler Adult Intelligence Scale. Patients were categorized as having uni- or bitemporal IEDs based on IEDs distribution (cutoff point, 90%).

Results

In patients with unitemporal IEDs, performance IQ (PIQ) was significantly lower in the right than in the left subgroup (89.6 vs. 99.4, p<0.05). Verbal IQ (VIQ)–PIQ discrepancy scores differed significantly between the left and right subgroups, being negative in the left and positive in the right subgroup. Based on multivariate analyses, two variables, right MTLE (p=0.042) and the unitemporal distribution of IEDs (p=0.030), were independently related to the VIQ–PIQ discrepancy of more than 10 points. About 47.4% of those with unitemporal IEDs had VIQ–PIQ discrepancies of greater than 10 points and the rate for correct lateralization was 77.8%. In patients with bitemporal IEDs, however, none of the intelligence scores showed evidence of correct lateralization. In patients with bitemporal IEDs, Full-scale IQ and PIQ were significantly lower in the left subgroup, and there was a significant difference in VIQ–PIQ discrepancy scores with the wrong direction.

Conclusions

We found that intelligence scores had some lateralizing ability, but only in MTLE patients with unitemporal IEDs.

Keywords: Temporal lobe epilepsy, Wechsler Adult Intelligence Scale, Laterality, Electroencephalography

 

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Introduction 

Material-specific memory deficit is considered a primary neuropsychological marker of mesial temporal lobe epilepsy (MTLE).1, 2, 3 Neuropsychological deficits in MTLE are, however, not limited to the learning-memory domain but extend into more generalized impairment of higher cognitive-intellectual functioning.4, 5, 6, 7 A growing body of neuroimaging evidence has shown that brain dysfunction in MTLE is not limited to the mesiotemporal area but extends into widespread extratemporal regions.8, 9, 10, 11, 12, 13

With regard to the potential lateralizing ability of intelligence deficits in patients with MTLE, some studies showed significantly lower verbal intelligence quotient (VIQ) in left than in right MTLE patients but no significant difference in performance intelligence quotient (PIQ) between the two groups.14, 15 Others, however, found that PIQ as well as VIQ were significantly lower in left than in right MTLE patients.16, 17 However, the great majority of studies failed to find supporting evidence for significant lateralized intelligence deficits.3, 18, 19, 20, 21 The inconsistency of the results of previous studies may be due, at least in part, to intelligence scores such as VIQ and PIQ being of relatively low sensitivity in measuring verbal and nonverbal intelligence. The inconsistency may also be due to methodological inadequacies, such as differences between studies in the types of patients recruited or heterogeneous patient populations within a particular study, rather than to a true absence of the lateralizing ability of intelligence in MTLE.

We have hypothesized that the lateralizing effect of intelligence in MTLE patients may be evident in those with unilateral, but not bilateral, temporal lobe dysfunction, primarily because bilateral temporal lobe dysfunction may make the potential laterality effect of intelligence less clear. Bitemporal interictal epileptiform discharges (IEDs) have been shown to be very sensitive markers of bitemporal dysfunction.22 Serles et al.23 suggested that false lateralization based on seizure semiology was more frequent in patients with bitemporal spikes. Steinhoff et al.24 also found that false ictal EEGs lateralization was more frequent in patients with bitemporal IEDs than those with unitemporal IEDs. This study evaluated only patients with MTLE due to hippocampal sclerosis, as confirmed by pathological analysis and seizure outcome after surgery. After categorizing MTLE patients into two subgroups depending on the distribution of interictal spikes, we investigated the differences in the lateralizing ability of intelligence scores between MTLE patients with unitemporal and bitemporal IEDs.

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Methods 

Patients 

We evaluated a consecutive series of patients who received preoperative examinations for treatment of intractable seizures from 1996 to 2002 at Asan Medical Center. Patients were included if they had mesial temporal sclerosis, as confirmed by postoperative pathological analysis; were seizure free for at least 1 year after anterior temporal lobectomy; had preoperative neuropsychological evaluations, including Korean Wechsler Adult Intelligence Scale (K-WAIS)25; and had left language dominant hemisphere, as determined by the intracarotid sodium amytal procedure. Because patients were only included when postoperative pathology revealed mesiotemporal sclerosis, only after operation it was decided whether the presurgical neuropsychological data would be used in this study. Subjects were excluded if their full-scale intelligence quotient (FSIQ) score was less than 70, if they had anomalous language representation, or if they had focal neurological deficits, progressive neurological disorders, or active psychiatric or medical disorders.

Scalp/sphenoidal EEG 

Data were obtained through continuous video-EEG monitoring. The length of monitoring averaged 3.7 days (range, 1.5–7.3 days). Antiepileptic medication was usually reduced or completely withdrawn to facilitate the recording of seizures. In all cases, EEGs were recorded using an international 10–20 system plus bilateral sphenoidal and inferior temporal electrodes. For EEG recording and analysis, we used a digital system that allowed for reformatting the data in any desired montage.

IEDs were assessed by visual analysis of interictal EEG samples of 2min duration every hour stored on optical disks. About 2.8h (range, 1.3–5.8h) of interictal data were reviewed. IEDs were defined as spikes, sharp waves, spike wave complexes, or multiple spike discharges. A continuous run of epileptiform waveforms would be considered as one discharge if not interrupted by normal activity of more than 1s. If 90% or more of all discharges occurred over one temporal lobe, which always corresponded to the side of resection, patients were defined as having unitemporal IEDs. Patients with less than 90% of IEDs over one temporal lobe were classified as having bitemporal IEDs. The scoring of IED and the assignments to the groups with either unitemporal or bitemporal IED was performed by one author (S.Y. Kang), who was blinded to the results of K-WAIS. The evaluation of IEDs was supervised by the other author (S.A. Lee).

Korean Wechsler Adult Intelligence Scale (K-WAIS) 

The K-WAIS25 was preoperatively administered to each patient in the context of a comprehensive neuropsychological evaluation. The structure and pattern of the K-WAIS are the same as those of the WAIS-R.26 In this study, we used four measures: FSIQ, VIQ, PIQ, and VIQ–PIQ discrepancy.

Data analysis 

Patients with clear and exclusively unilateral seizure foci were assigned to the left or right MTLE groups depending on the location of pathology. Patients in each group were further subdivided into unitemporal and bitemporal subgroups based on interictal spike distribution. Student's t-tests were used to compare each of the intelligence scores in these groups and subgroups. Using logistic regression analysis, we determined which clinical variables were independently related to the VIQ–PIQ discrepancy of more than 10 points. Clinical variables included were age, sex, age at seizure onset, duration of epilepsy, laterality of MTLE, the distribution of interictal spikes (unitemporal or bitemporal), and preoperative use of topiramate. If the discrepancy scores between VIQ and PIQ were greater than 10, which was unlikely to occur as a result of measurement error (statistically reliable splits),27 further analysis was conducted to determine the ability of the intelligence scores to lateralize. All statistical analyses were performed using SPSS version 12.0 for Windows.

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Results 

General characteristics 

This study included 82 patients (44 men, 38 women); their demographic characteristics are shown in Table 1. All patients had drug-resistant complex partial seizures sometimes with secondary generalization. Their seizure frequencies were 0.5–4 seizures per month. They were treated with 1–4 antiepileptic drugs, with most patients (90.2%) taking 2–3 drugs. Of the 82 patients, 12 (14.6%) were taking topiramate and 8 (9.8%) were taking phenobarbital.

Table 1. Patient characteristics
Total (n=82)UnitemporalaBitemporalb
LMTLE (n=18)RMTLE (n=20)LMTLE (n=18)RMTLE (n=26)
Sex ratio, M:F44:3810:814:65:1315:11
Age at seizure onset (year)11.912.110.711.812.6
Duration of epilepsy (year)18.517.319.421.416.5
Age at operation (year)30.329.530.133.329.0
Years of education11.812.512.110.811.8
Number of antiepileptic drugs2.542.442.652.672.42

LMTLE=left mesial temporal lobe epilepsy; RMTLE=right mesial temporal lobe epilepsy.

aPatients with unitemporal interictal spikes.

bPatients with bitemporal interictal spikes.

Among the 82 patients, 36 patients had left MTLE and 46 had right MTLE; there were no statistically significant between-group differences in gender, age at operation, age at onset, duration of epilepsy, duration of education, and number of antiepileptic drugs. Of the 82 patients, 38 had unilateral IEDs (18 left, 20 right) and 44 had bitemporal IEDs (18 left, 26 right); there were also no significant differences in patient characteristics between the left and right MTLE subgroups according to the IED distribution.

Differences between left and right MTLE groups regardless of IED distribution 

There were no significant differences in summary IQ scores and VIQ–PIQ discrepancy scores between the left and right MTLE groups (Table 2).

Table 2. Intelligence scores in left and right MTLE patient groups
LMTLE (n=36)RMTLE (n=46)p-Value
FSIQ93.5 (13.8)95.4 (14.2)0.532
VIQ93.7 (13.7)96.4 (14.1)0.384
PIQ93.6 (13.8)94.6 (14.7)0.761
VIQ–PIQ0.1 (8.3)1.8 (11.5)0.457

Data are reported as mean (standard deviation). FSIQ=full-scale IQ; VIQ=verbal IQ; PIQ=performance IQ; VIQ–PIQ=verbal-performance IQ discrepancy.

Differences between left and right subgroups in patients with unitemporal IEDs 

PIQ was significantly lower in the right subgroup than in the left subgroup (89.6 vs. 99.4, p<0.05) (Table 3). Mean VIQ–PIQ discrepancy scores were negative in the left MTLE subgroup and positive in the right subgroup, and the difference was statistically significant (−4.2 vs. 5.5, p<0.01). FSIQ and VIQ did not differ between the left and right subgroups.

Table 3. Intelligence in patients with left or right mesial temporal lobe epilepsy depending on uni- or bitemporal interictal spikes
Patients with unitemporal IEDsPatients with bitemporal IEDs
LMTLE (n=18)RMTLE (n=20)p-ValueLMTLE (n=18)RMTLE (n=26)p-Value
FSIQ97.2 (16.2)92.2 (14.0)0.32189.8 (9.9)97.8 (14.1)0.041
VIQ95.3 (16.2)95.1 (14.9)0.97292.2 (10.9)97.5 (13.6)0.177
PIQ99.4 (15.7)89.6 (13.6)0.04587.8 (8.8)98.5 (14.6)0.008
VIQ–PIQ−4.2 (7.1)5.5 (13.3)0.0094.4 (7.3)−1.0 (9.3)0.045

Abbreviations same as in Table 2. Data are given as mean (S.D.) values.

Differences between left and right subgroups in patients with bitemporal IEDs 

FSIQ was significantly lower in the left subgroup than in the right subgroup (89.8 vs. 97.8, p<0.05) (Table 3). PIQ score was also lower in the left than in the right subgroup (87.8 vs. 98.5, p<0.01). The VIQ–PIQ discrepancy scores also differed significantly (p<0.05), but their direction was not consistent with the laterality of temporal lobe seizure onset. VIQ did not differ between the left and right subgroups.

Factors contributing to the VIQ–PIQ discrepancy of more than 10 points 

Among the 82 patients, 29 patients (35.4%) showed the VIQ–PIQ discrepancy of more than 10 points. Univariate analyses showed that three variables were significantly correlated with VIQ–PIQ discrepancy of greater than 10 points: sex, laterality of MTLE, and the distribution pattern of IEDs. Based on multivariate analyses, two variables, right MTLE (p=0.042) and the unitemporal distribution of IEDs (p=0.030), were independently related to the VIQ–PIQ discrepancy of more than 10 points.

Lateralizing values of VIQ–PIQ discrepancy of more than 10 points in either unitemporal or bitemporal MTLE patients 

In the unitemporal group, 27.8% of patients with left MTLE and 65.0% of patients with right MTLE showed statistically reliable splits (i.e., greater than 10 points), and the rates for correct lateralization were as high as 100% and 69.2%, respectively (Table 4). In the bitemporal group, however, the frequency of VIQ–PIQ discrepancy was as low as 25% and the correct lateralization rate was also low (27.3%).

Table 4. Lateralizing values relative to verbal-performance IQ discrepancy
Patients with VIQ–PIQ discrepancy of >10 pointsPatients with correct lateralization
Unitemporala
LMTLE (n=18)5 (27.8%)5 (100%)
RMTLE (n=20)13 (65%)9 (69.2%)
Both (n=38)18 (47.4%)14 (77.8%)

Bitemporalb
LMTLE (n=18)3 (16.7%)0 (0%)
RMTLE (n=26)8 (30.7%)3 (37.5%)
Both (n=44)11 (25%)3 (27.3%)

LMTLE=left mesial temporal lobe epilepsy; RMTLE=right mesial temporal lobe epilepsy; VIQ=verbal IQ; PIQ=performance IQ.

aPatients with unitemporal interictal spikes.

bPatients with bitemporal interictal spikes.

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Discussion 

In agreement with many previous studies, we observed no lateralized intelligence deficits in patients with MTLE regardless of the distribution of IEDs.3, 18, 19, 20, 21, 28 In patients with unitemporal IEDs, however, PIQ was significantly lower in right than in left MTLE, whereas VIQ and FSIQ did not differ. As a result, VIQ–PIQ discrepancy scores showed the expected direction. That is, VIQ was lower than PIQ in the left MTLE subgroup, whereas PIQ was lower than VIQ in the right MTLE subgroup. Also the VIQ–PIQ discrepancy of more than 10 points was independently related to the unitemporal IEDs and right MTLE subgroup. These findings are indicative of the lateralizing ability of intelligence deficits in MTLE patients with unitemporal IEDs.

The lateralized intelligence deficits observed in MTLE may be due to an asymmetric disease process associated with unilateral MTLE, involving widespread extratemporal and neocortical temporal dysfunction. Results obtained using quantitative MRI and functional brain imaging have suggested these potential lateralized intelligence deficits in MTLE.8, 9, 10, 11 For example, in an examination of the temporal neocortex and the underlying white matter in patients with unilateral temporal lobe epilepsy, the total volume of the temporal lobe was found to be more reduced in the temporal lobe ipsilateral to the seizure focus (15%) than in the contralateral lobe (7%).10 Moreover, relative reductions in glucose metabolism of the left hemisphere and left lateral temporal lobe in MTLE patients were found to correlate with lower VIQ scores.8

In patients with bitemporal IEDs, both FSIQ and PIQ were significantly lower in left than in right MTLE, whereas there was no difference in VIQ. Consequently, the direction of VIQ–PIQ discrepancy was not consistent with the laterality of temporal lobe seizure onset. Thus, we found an association between the presence of seizure focus in the left side and significant reductions in PIQ and FSIQ in MTLE patients with bitemporal IEDs.

We found that PIQ was more susceptible to epileptogenic lesion, regardless of the laterality of seizure focus. Right MTLE patients with unilateral IEDs tended to have lower PIQ without a reduction of FSIQ, whereas left MTLE patients with bitemporal IEDs tended to have reductions in both PIQ and FSIQ. These findings are somewhat inconsistent with early research in this area,29 but support data obtained more recently.30, 31

Intelligence has been conceptualized as having two dimensions, fluid and crystallized intelligence.32 Crystallized intelligence is related to retained information, as measured by vocabulary subtests, whereas fluid intelligence is related to the ability to manipulate information, as measured by subtests such as digit-symbol substitution. VIQ is thought to represent a measure of crystallized intelligence, whereas PIQ is thought to represent fluid intelligence.33 Fluid intelligence has been reported to be more susceptible to aging or acquired brain injury than crystallized intelligence.27, 33 Left brain injury may be accompanied by various differences in IQ profiles (PIQ>VIQ, VIQ=PIQ, or VIQ<PIQ), whereas right brain injury is associated with a PIQ lower than VIQ.26, 31 These findings are, in part, supported by our results, in that VIQ–PIQ discrepancy of more than 10 points was significantly related to right MTLE. Consequently, the VIQ–PIQ discrepancy has no diagnostic predictive validity in individuals with left hemispheric lesions.31 In patients with diffuse bilateral brain injury, PIQ was found to be lower than VIQ.27 Taken together, these findings indicate that acquired brain damage often has greater adverse impact on PIQ than on VIQ.

Lower PIQ in patients with left hemispheric lesions may be reflective of the neurological reorganization of cognitive functions that occur in these patients.34 Lateralized reorganization of language functions in patients with early left hemisphere brain injuries may ‘crowd’ out nonlinguistic abilities ordinarily mediated by the nondominant right hemisphere.35 Our finding of lower PIQ in left MTLE patients, however, is less likely to be due to ‘crowding’ because we included only patients with clear left hemisphere language dominance.

The evidence for an association between laterality of seizure focus and overall intellectual ability has been inconsistent.4, 16, 36, 37 We observed an association between left MTLE and significantly lower FSIQ, but only in patients with bitemporal IEDs. Glosser et al.37 also found that the presence of an epileptic focus in the left hemisphere was associated with lower IQ in patients with intractable temporal lobe epilepsy. The psychometric definition of intelligence relies heavily on measures of linguistic and analytic capacities, which are cognitive functions most often mediated by the left cerebral hemisphere.38 Consequently patients with primary neurological dysfunction in the left hemisphere might be expected to score lower on standardized intelligence tests than patients with damaged right hemisphere. Bitemporal interictal spikes generally reflect more severe and generalized brain dysfunction, which may explain our finding that MTLE patients with bitemporal, but not unitemporal IEDs had lower IQ scores.

The VIQ–PIQ discrepancies have limited their diagnostic predictive validity as markers of lateralized brain damage.31 This study also showed that the low percentage of patients with bitemporal IEDs exhibited a statistically reliable VIQ–PIQ split. However, the base rate of a reliable VIQ–PIQ split in the patient subgroup with unitemporal IEDs was nearly 50%, and the sensitivity of the split in right MTLE was higher (65%) than left MTLE. The rate for correct lateralization was as high as 77.8% in patients with unitemporal IEDs, whereas this rate was as low as 27.3% in patients with bitemporal IEDs. These findings indicate that the VIQ–PIQ discrepancy has, at least in part, some diagnostic predictive validity in MTLE patients with unitemporal IEDs.

This study has some limitations. First, the scoring of IEDs using an algorithm of 2min/h was limited, and raised the question of dependency of the findings on chance, since the state of the patient was not considered. Second, the classification of patients into uni- or bitemporal cases were based on the 90% cutoff point of spikes being distributed over one temporal lobe. This way was arbitrary. Epileptiform activity, however, has often been considered “lateralized” in temporal lobe epilepsy by many investigators if >80–90% of the epileptiform discharges originated from one temporal lobe.22, 39, 40, 41, 42 Third, multivariate analysis was applied limitedly. So influences of the potential variables such as age and education level on intelligence were not completely excluded although there were no significant differences between patient subgroups in sex, age at seizure onset, age at operation, duration of epilepsy, and years of education. Finally, we could not completely exclude the possibility that medication such as topiramate or phenobarbital affected their intellectual ability.

In conclusion, we found that intelligence scores had some lateralizing ability, but only in MTLE patients with unitemporal interictal spikes occurring over one temporal lobe; this finding may reflect brain dysfunction more obviously lateralized to the epileptogenic region. In addition, we found that PIQ was more susceptible to epileptogenic lesions, regardless of the laterality of seizure focus.

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PII: S1059-1311(08)00059-9

doi:10.1016/j.seizure.2008.02.008

Seizure: European Journal of Epilepsy
Volume 17, Issue 7 , Pages 604-610, October 2008

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