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Interictal and postictal performances on dichotic listening test in children with focal epilepsy
Brain and Cognition 76 (2011) 310–315
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Interictal and postictal performances on dichotic listening test in children with focal epilepsy G. Carlsson ⇑, G. Wiegand, U. Stephani Dept. Neuropediatrics, Medical Center of Schleswig-Holstein, Campus Kiel, Germany
a r t i c l e
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Article history: Available online 14 April 2011 Keywords: Dichotic listening Children Drug resistant Epilepsy Focal seizures
a b s t r a c t Dichotic listening test (DL) is an important tool to disclose speech dominance in healthy subjects and in clinical cases. The aim of this study was to probe if focal epilepsy in children reveals a corresponding suppression of the ear reports contralateral to seizure onset site. Thus, 15 children and adolescents with clinically and electroencephalographically diagnosed focal epilepsy selected for left-hemisphere speech dominance without mental retardation were compared to matched controls according to age, gender, IQ and handedness. All children were assessed with DL for three times: Interictally (t0), postictally 5’ (t1) and 1 h (t2). At t0, all groups revealed a right ear advantage (REA), indicating a left-hemisphere speech dominance. There was a continuous increase in right correct score (REC) over the trials for normal controls. Five minutes postictally, there was an abrupt decrease in REC with a sustained left ear correct score (LEC) for children with epilepsy, independent of which side suffered from seizures. This effect was maintained even after 1 h. Thus, in children with left-hemisphere speech dominance the epileptic discharges caused a suppression of REC regardless of origin. The seizures may have a prolonged impact on attention and auditory perception for a considerable time after consciousness has been regained. Ó 2011 Elsevier Inc. All rights reserved.
1. Background The pioneering work by Kimura (1961a, 1961b) showed that the dichotic listening (DL) test has the ability to study hemispheric function and speech dominance in adult patients with focal epilepsy. Kimura (1961b) found that the right ear was more efficient to perceive dichotically presented verbal material than the left ear regardless of the site of focal seizure onset. This was especially true for the group of patients with left hemisphere dominance for speech, assessed by Wada test (Loring et al., 1990; Wada, 1949; Wada & Rasmussen, 1969). In patients with right-hemisphere speech dominance the left ear was more efficient to perceive the verbal material. The DL has been shown to be valid for assessing speech dominance in children and adults with drug resistant focal epilepsies. The validity as compared to gold standard, the Wada procedure, was considered to be about 0.8 to 0.95 for adults (Strauss, Gaddes, & Wada, 1987; Zatorre, 1989) and to about 0.9 for children and adolescents (Hugdahl, Carlsson, Uvebrant, & Lundervold, 1997).
⇑ Corresponding author. Address: University Medical Center Schleswig-Holstein, Dept. Neuropediatrics, Campus Kiel, Arnold-Heller-Str. 3, Bld 9, DE-24105 Kiel, Germany. Fax: +49 431 597 1769. E-mail address: [email protected] (G. Carlsson). 0278-2626/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2011.03.014
Recently, excellent correlations between DL tests and speech fMRI have been found also in children with temporal lobe epilepsy (e.g. da Fontoura, de Moraes Branco, Anés, Costa da Costa, & Wetters Portuguez, 2008; Fernandes, Smith, Logan, Crawley, & McAndrews, 2006). Thus, individuals with left hemisphere dominance for speech generally show a REA, whereas those with right hemisphere dominance for speech typically reveal a LEA, which is consistent with Kimuras findings (1961a). In children and adolescents with an early structural brain abnormality in the right hemisphere a clearly stated REA was revealed indicating left-hemisphere speech dominance. A reverse picture, i.e. a clear LEA, was found in children and adolescents with early left-sided brain impairment indicating right hemisphere dominance (Carlsson, Hugdahl, Uvebrant, Wiklund, von Wendt, 1992; Hugdahl & Carlsson, 1996; Isaacs, Christie, Vargha-Khadem, & Mishkin, 1996; Korkman, Granström, & Berg, 2004; Korkman & von Wendt, 1995). The dichotic listening (DL) technique is probably the most frequently used experimental method to assess lateralization of language function (Bryden, 1988; Hugdahl, 1995). Previous studies have been performed with either dichotic presentation of digits, words or fused words. However, the majority has been performed with consonant–vowel or consonant–vowel-consonant materials. The consonant vowel (CV) syllables are consistently found to produce the most robust right ear advantages (REA, Hugdahl, 1995) in
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right-handed individuals (Hugdahl & Andersson, 1984; Schankweiler & Studdert-Kennedy, 1967; Studdert-Kennedy & Schankweiler, 1970). The right ear advantage (REA) may be explained by a structural model (Kimura, 1967; Sparks & Geschwind, 1968). According to this, the contralateral auditory projections dominate and the ipsilateral auditory projections are suppressed or inhibited, i.e. given left-hemisphere speech dominance, the left ear inputs will be transformed first to the right hemisphere via corpus callosum, and then be perceived in the left hemisphere. Since Kimura (1961a, 1961b) several other studies have reported on the relationship between focal epilepsy and speech representation in patients with temporal lobe epilepsy (Berlin, LoweBell, Jannetta, & Kline, 1972; Mazzucchi & Parma, 1978; Mazzucchi, Visintini, Magnani, Cattelani, & Parma 1985; McIntyre, Pritchard, and Lombrose, 1976; Oxbury & Oxbury, 1969; Lee et al., 1994; Gramstad, Engelbretsen, & Hugdahl, 2006; Gramstad, Engelsen & Hugdahl, 2003; Grote, Pierre-Louise, Smith, Roberts, and Varney, 1995). Although several studies have found significant ‘‘lesion effects’’ to the ear contralateral to the lesion or side of focal epilepsy onset, other studies have failed to report this effect, particularly when it comes to the prediction of individual performance (Grote et al., 1995; Lee et al., 1994). In patients with left-sided focal epilepsy without structural abnormality, without documented speech dominance, there was an increase in REA (Mazzucchi & Parma, 1978; Mazzucchi et al., 1985) according to a facilitatory effect of focal epilepsy. However, in adult patients with left-hemisphere speech dominance and left focal epilepsy without evidence of structural lesions usually are a significant decrease in REA and concomitantly in the right ear correct scores (Lee et al., 1994). Gramstad et al. (2003, 2006) found that a left hemisphere cognitive dysfunction rather leads to a lack of REA in patients with TLE with left-hemisphere speech dominance, and not the focal epilepsy per se. Epileptic seizures are followed by dynamic alternations in neurological and cognitive function in the postictal period (Holmes, 1986). Postictal signs are accordingly considered to provide reliable information for the localization of the seizure onset region in patients with focal epilepsy (Leutmezer & Baumgartner, 2002). Thus, postictal memory impairments in patients with focal epilepsies correlated highly with cerebral localization and lateralization of seizure onset (Andrewes, Puce, & Bladin, 1990; Helmstaedter, Elger, & Lendt, 1994). Epileptic seizures may likewise alter DL performance. Roberts, Varney, Paulsen, and Richardson (1990) showed that patients with focal epilepsy changed their DL pattern in a normalized direction after successful antiepileptic drug treatment. Similarly, Helmstaedter, Fritz, Gonzáles Pérez, Elger, and Weber (2006) found in a patient with left-sided focal epilepsy a seizure driven right-hemispheric speech dominance according to fMRI, which reversed from the right to the left hemisphere when seizures were successfully controlled for. In the same way, others have found that the left ear advantage in DL test before a resection of a left-sided brain cyst can be normalized and change to a right ear advantage after surgery (Wester & Hugdahl, 2003). Thus, a left ear advantage may be demonstrated without evidence of right-hemisphere speech dominance, but may rather indicate a left-hemisphere suppression or impairment. Similarly, Carlsson, Hufnagel, Jansen, Claviez, and Navabi (2010) found in a child with a right-frontal meningeoma an extreme REA, which normalized after resection. The aim of the present study was to investigate the effects of left- and right-hemispheric focal seizures on dichotic listening performances in children with left hemisphere dominance for speech. According to Kimuras structural model (1967) it is expected that epileptic activity may in the first place alter the right ear correct scores and concomitantly REA independent of whether the leftor right hemisphere is triggered by seizures. Continuous compari-
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sons between interictal and postictal registrations were considered to facilitate this purpose. This is a new attempt to achieve an optimal connection between active focal seizures and lateralized cognitive functions. Accordingly, DL performances were collected repeatedly up to an hour postictally in patients with documented seizure onset in the left or right hemisphere. 2. Methods 2.1. Participants Fifteen children with drug resistant focal epilepsy (8 females and 7 males; mean age 14.3 yrs, SD 3.2) were admitted to the comprehensive epilepsy center (UK-SH, campus Kiel) for long-term video EEG monitoring and neuropsychological assessment. Inclusion criteria were focal epilepsy with documented left hemisphere dominance for speech according to fMRI (10/15) or according to the comprehensive neuropsychological assessments. All subjects with mental retardation (IQ < 70), hearing impairment, incomplete DL records, or those suspected for right hemisphere dominance were excluded. The control group was recruited from an inpatient ward (Departments of Pediatrics and Neuropediatrics at the University clinic Schleswig–Holstein, Campus Kiel) matched to the study group on gender, age, IQ and handedness. The control group comprised 15 children (8 females and 7 males, mean age 12.6, SD 1.9) without central nervous system affections. Intelligence was determined by the German standardization of Culture Fair Test of intelligence (CFT1 or CFT20-R, ad modum Cattell) or Wechsler Intelligence Scales for Children (WISC-IV). The focal epilepsy group achieved a mean IQ of 89 (SD 13.3). Ten of the children with focal seizures (Left/Right: 7/3) showed an average intelligence (IQ > 84), five children (L/R = 4/1) a low average intelligence (IQ 70–84). The control group achieved a mean IQ of 94 (SD 16.2). Nine children revealed an average intelligence (IQ > 84), and six showed a low average intelligence (IQ 70–84). Handedness was determined by Edinburgh’s handedness questionnaire containing 10 items according to hand preference for manual items (Oldfield, 1971). Fourteen children in the seizure group were right-handed (93.3%) and one left-handed (6.7%). All children in the control group were right-handed. There were no statistically significant differences between the seizure groups and normal controls with regard to gender, age, IQ or handedness (Table 1). 2.2. The dichotic listening (DL) test The dichotic stimulus materials consisted of the six stop-consonants /b/, /d/, /g/, /p/, /t/, /k/ which were paired with the vowel /a/ to form six consonant–vowel (CV) syllables (/ba/, /da/, /ga/ etc.). The syllables was paired with each other for all possible combinations, thus yielding 36 dichotic pairs including 6 homonymic pairs (/ba/-/ba/, / da/-/da/, etc.). The homonymic trials were excluded in the statistical analyses. A male German speaking voice (baritone) from Northern German Radio (NDR) recorded the syllables with constant intonation and intensity on a tape, which was subsequently digitalized and copied on a CD at Hugdahl’s laboratory in Bergen, Norway, considered for use on conventional CD-player. The mean duration of the stimulus was approximately 350 ms, and the interval between stimuli was about 4 s. The children were presented the stimulus material over headphones and instructed to report the syllable they heard first, or best. Thus, reporting only one item on each trial irrespective of whether they perceived one or both items.
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Table 1 Patient characteristics: age, gender, IQ, group (L = left focal, R = right focal, C = control), and distribution of speech dominance according to fMRI, hand preference (R/L), and Laterality-index (Li) according to the labels Right Ear Advantage (REA), Left Ear Advantage (LEA) and No Ear Advantage (NEA) for interictal (t0), postictal 50 (t1) and postictal 1 h (t2) trials. The criterion for a REA, LEA or NEA was set to better recall from the right or left ear, or equal reports from both ears. Case
Age (yrs)
Gender (M/F)
IQ
Group (L/R/C)
Handpref(R/L)
Li. (t0)
Li (t1)
Li (t2)
Affected lobes
fMRI (L/R)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
7.9 9.9 10.7 11.0 13.9 15.3 15.5 17.3 17.6 17.9 18.2 13.9 14.2 15.1 16.8 9.1 9.5 9.8 11.3 12.5 12.5 12.7 13.2 13.2 13.4 13.5 13.6 14.5 14.7 15.8
M M F M F M M F F M F F M F F M M M F F F M F F F F M F M M
70 71 118 89 107 97 102 84 94 85 73 89 87 80 87 106 90 132 78 70 96 101 84 82 99 90 80 111 83 111
L L L L L L L L L L L R R R R C C C C C C C C C C C C C C C
R R R R R R R R R L R R L R R R R R R R R R R R R R R R R R
REA REA REA REA LEA REA REA REA REA REA REA REA LEA REA NEA LEA REA REA REA REA NEA REA REA NEA LEA REA REA REA REA REA
REA LEA REA LEA REA LEA REA LEA REA LEA LEA LEA REA LEA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA
REA REA LEA REA REA LEA NEA NEA REA REA LEA LEA LEA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA
T T T T P T O T T T T F T T F
L L L
2.3. Procedure The children with epilepsy were tested by medical personnel in connection with the Video-EEG-monitoring. Interictal testing (t0) was performed when no seizure activity was present, confirmed by the Video-EEG. The DL test was repeated 5 min after the children had regained awareness after a clinically and through the EEGrecordings confirmed ictal event (t1), i.e. early postictal recordings. Subsequently, after about another 55 min (t2), the procedure was repeated. The video-EEG recordings were continuously inspected to confirm that no focal seizure was present during the DL testing. The control group was correspondingly assessed with dichotic listening test at three occasions, at 1 day (t0) and the next day tested twice (t1 and t2) with 1 h in between. Intelligence and lateral preferences were assessed in the intermediate period. 2.4. Scoring of data and statistical analyses Data were scored for each subject as the frequency of correctly recalled syllables for the right and left ear input. The raw scores were transformed into percent scores (x/30100). The laterality-index (%) was calculated according to the formula: [(right ear left ear)/(right ear + left ear) 100], where right ear and left ear represent the number of correct right ear and left ear scores, respectively. The data were subjected to two different kinds of analysis of variance (ANOVA). The first analysis was based on the design 3 groups (left- and right focal seizure group and controls) 2 ear inputs (right/left) for each event (t0, t1 and t2) to evaluate whether there were any differences in DL performance for the left and right ear among groups and test-trials. The laterality-index was accordingly analyzed. Significant effects were followed-up with the Tukey HSD test. ANOVA for repeated measures was performed for DL measures, based on the design 3 groups (left- and right focal seizure group and controls) 2 Ear inputs (left/right) 3 Test-trials (t0, t1 and
L L L L L L L
t2). This analysis would answer the question of whether the DLT can differentiate between the groups over the course of events. The laterality-index was accordingly analyzed. Follow-up test were performed with pairwise contrast-analyses, or pairwise t-tests.
3. Results All children with left- and right-sided focal epilepsy and normal controls were considered left hemisphere dominant for speech as determined by fMRI, handedness and DL performance (Table 1). According to descriptive data, interictally (t0) ten of the 11 children with left-sided foci showed a REA (91%). Immediately after the seizure ceased and consciousness was regained (t1) five children still showed REA (45%) and six a LEA (55%). One hour postictally (t2) six children showed a REA (55%), whereas three a LEA (27%) and two NEA (18%). Interictally two of the four children with right-sided foci revealed a REA (t0), one child a LEA and another one a NEA. In the immediate (t1) as well as in the late postictal trial (t2) two children showed a REA and two a LEA. On the group level, there was a decrease in laterality-index (Li) and right ear correct (REC) reports for both focal seizure groups from the interictal (t0) to the early postictal trial (t1). At the late postictal event (t2) the REC reports recovered slightly for left seizure group, but slightly decreased for the right seizure group. The control group showed at the same time throughout an increase in the Li and REC reports. The LEC reports were, however, stable for all groups over the three trials (Table 2). In the first ANOVA there were no differences between the focal seizure groups for age, IQ or any of the dependent variables. Additionally, there were no differences between the focal seizure groups and normal controls for age and IQ. Statistically significant group differences were found with regard to REC reports at t1 [F(2, 27) = 6.58, p = .005] and at t2
G. Carlsson et al. / Brain and Cognition 76 (2011) 310–315 Table 2 Dichotic listening performance according to percent correct reports to the right and left ear (mean and range) for 15 children with left- versus right focal seizures and 15 normal controls over the three occasions (t0, t1 and t2). Group
Li (range)
REC
REC (range)
LEC
LEC (range)
Left-sided foci t0 11 19.7 11 1.9 t1 t2 11 8.7
N
Li
02.6–48.1 33.3–36.4 30.4–33.3
45.8 33.9 37.9
30.0–66.7 10.0–53.3 16.7–63.3
30.8 31.2 31.2
23.3–46.7 20.0–40.0 10.0–50.0
Right-sided foci t0 4 4.1 t1 4 1.7 t2 4 -1.6
06.7–13.0 14.3–20.0 26.3–16.7
35.0 34.2 28.3
23.3–43.3 30.0–40.0 23.3–43.3
31.7 33.3 30.0
26.7–36.7 26.7–40.0 16.7–40.0
Controls t0 15 t1 15 t2 15
12.5–61.5 3.7–55.6 4.0–58.3
44.8 48.9 53.1
23.3–70.0 33.3–70.0 40.0–66.6
29.5 27.5 27.3
16.6–40.0 20.0–43.3 16.6–40.0
19.4 27.1 32.0
[F(2, 27) = 9.74, p = .0007], and to laterality-index at t1 [F(2, 27) = 8.40, p = .001] and at t2 [F(2, 27) = 7.19, p = .003]. In the follow-up tests, Tukey HSD revealed significant differences for REC between normal controls (NC) and the left focal seizure group (LFG) at t1 (p < .01) and at t2 (p < .01), and between NC and the right focal seizure group (RFG) at t2 (p < .01). Moreover, there were significant differences for laterality-index between NC and LFG at t1 (p < .01) and at t2 (p < .05), and between NC and the right focal seizure group (RFG) at t1 (p < .05) and at t2 (p < .05). The ANOVA for repeated measures revealed a main group effect for REar and Lear correct reports over the three events [F(4, 52) = 3.09, p < .05]. Furthermore, there was a significant interaction effect between groups and correct reports for left-ear (LEar) and right-ear (REar) inputs over the events [Wilks lambda = .42338, F(8, 48) = 3.2211, p < .01]. Planned comparisons showed significant differences for exclusively REC reports between the LFG and NC at t1 [F(2, 54) = 8.65, p < .001] and at t2 [F(2, 54) = 7.29, p < .01], as well as differences between the RFG and NC at t1 [F(2, 54) = 4.54, p < .05] and at t2 [F(2, 54) = 9.13, p < .001]. Furthermore, there was a significant decrease in REC reports for LFG between t0 and t1 [F(2, 54) = 11.43, p < .0001] and between t0 and t2 (T = 2.47, p < .05). The RFG did not show statistically significant changes in REC reports from interictal and over the postictal events. However, the NC revealed a significant increase in REC reports between t0 and t2 [F(2, 54) = 4.77, p = .01]. Moreover, there were no significant differences between groups for LEC reports. The laterality-index (Li) showed a main group effect [F(2, 27) = 7.36, p < .01], and a significant interaction effect [F(2, 54) = 3.30, p < .05]. In the planned comparison there was a significant difference between the LFG and NC at t1 [F(1, 27) = 14.15, p < .001] and at t2 [F(2, 27) = 9.17, p < .01], which coincided with a significant decrease in laterality-index from t0 to t1 [F(1, 27) = 11.16, p < .01] for LFG and a continuous and significant increase of Li from t0 to t2 [F(2, 27) = 9.49, p = .005] for normal controls. Additionally, there was significant differences for Li between RFG and NC at t1 [F(2, 27) = 7.17, p = .01] and at t2 [F(2, 27)=9.49, p < .01], which imply that Li tended to decrease for the RFG at the late postictal event. 4. Discussion To sum up the main findings, postictally there was a significant decrease in laterality-index 5 min and up to 1 h after consciousness was regained for the LFG as well as for the RFG. A corresponding
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impact on the REC reports was found for the LFG and qualitatively for RFG compared to NC. Moreover, neither right- nor left-sided focal seizure showed an impact on the left ear correct reports in these children. Interictally, there was a right ear advantage in the group with left- and right-sided focal seizures as well as in normal controls. This is in agreement with the presumed left hemisphere dominance for speech, which was supported by right-handedness in all control children and in a clear majority of the children with focal epilepsy. The speech fMRI confirmed the left hemisphere dominance in two-thirds of the children with epilepsy. As one left-handed child showed a LEA in DL suspicious for right hemisphere dominance, but revealed left hemisphere dominance according to fMRI, the left hemisphere was considered dominant. For another left-handed child in the epilepsy group the fMRI was not yet performed, though considered as left hemisphere dominant according to a REA according to DL. However, in the interictal condition there were no differences between the three groups for any DL measure. Interestingly, the LFG showed a comparably high level for REC reports as normal controls, whereas the RFG tended to displayed inferior REC scores compared to the LFG and normal controls (cf. Fig. 1 and Table 2). This result is in line with previous findings (e.g. Kimura, 1961b), that verbal material from the right ear is more reliable transmitted to the left speech dominant hemisphere. Considering the DL performance for children with left-sided focal seizures from the interictal over the two postictal assessments, there was a striking decrease in laterality-index immediately after a seizure, implying a ‘‘lesion effect’’. One hour after the ictal event the laterality-index recovered, however, not reaching the level attained interictally (cf. Fig. 2). Likewise, the REC reports decreased in the early postictal and recovered slightly in the late postictal registration. The present results seem to corroborate with previous findings, that the REC is suppressed according to the left hemisphere impairment (e.g. Kimura, 1961b; Loring et al., 1990; Grote et al., 1995). However, this effect could not be shown in the interictal but solely in the postictal conditions for right ear inputs. Similarly, the children with right-sided focal seizures showed a decline for Li and for REC reports over postictal events, in the absence of a simultaneous impact on LEC reports. Thus, this contradicts the assumed contralateral ‘‘lesion effect’’ for RFG. Moreover, there were no differences between the left- and right-sided focal groups for any DL measure over the interictal and postictal events, and the LEC reports remained substantially unchanged in the groups. Although, this small group with rightsided foci (N = 4) revealed corresponding results as the group with left-sided foci, so it may be unlikely that a larger sample produce a different result, especially as the RFG tended to show slight improved LEC 5 min and a decrease on hour postictally (Fig. 1). The small increase of LEC in the RFG may give some support for a facilitatory effect of the epileptogenic focus (cf. Mazzucchi & Parma, 1978; Mazzucchi et al., 1985). After all, the present study support the assumption that the right hemisphere functions seem less important than left hemisphere functions in explaining the impact of focal seizures (e.g. Gramstad et al., 2003, 2006; Kimura, 1961b). Present findings appear to be consistent with the structural model of DL, where the right hemisphere primarily is regarded as a relay station for left ear stimuli, which need to be transferred to the left hemisphere for cognitive processing (Kimura, 1967; Sparks & Geschwind, 1968). Since no differences between the focal epilepsy groups were found, and both groups showed a decrease in REC reports in the postictal events without affection of the LEC reports, this may indicate a generally reduced attention or vigilance caused by the distribution of seizure activity to different parts of the brain regardless
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65 60 55
% correct reports
50 45 40 35 30 25 20 15 10 t0
t1
t2
t0
t1
t2
t0
t1
RFG
LFG
NC
t2
REar LEar
Fig. 1. Percent correct reports for the right-ear (REar) and left-ear (LEar) input over the three test-occasions (interictal = t0, 5 min postictally = t1, 1 h postictally = t2) for the left focal group (LFG), right focal group (RFG) and normal controls (NC).
50
40
Laaterality-index (%)
30
20
10
0
-10
-20
-30 t0
t1
t2
LFG RFG NC
Fig. 2. Laterality-index (%) over the three test-occasions (interictal = t0, 5 min postictally = t1, 1 h postictally = t2) for the left focal group (LFG), right focal group (RFG) and normal controls (NC).
of seizure origin. However, for left hemisphere dominant cases the left hemisphere functions were particularly impaired irrespective which side trigger a seizure. In conclusion, the present findings could not support a ‘‘lesion effect’’ or suppression of the ear contralateral to the focal site in all children, which may most likely be due to the fact that focal seizures are a network disease involving brain regions distant from the seizure focus (Grant, 2005; Spencer, 2002). The time to recover full consciousness after epileptic seizures is also variable. Children
with complex partial seizures regain consciousness within a few minutes. Generally, most children regain consciousness within 30–40 min after seizure, although some need many hours to recover (Allen, Ferrie, Livingstone, & Feltbower, 2007). This may depend on existing seizure type and involvement of the contralateral hemisphere. Generally, in some cases with focal epilepsy, there is generally more than one epileptogenic network and occasionally more than one seizure type involved, but each individual seizure type has a consistent site of onset (ILEA, 2010). Thus, there are
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many unpredictable factors involved, which can distort the view of solely unilateral impairment in focal epilepsy. However, in the present study the children were exclusively assessed with DL test after consciousness was achieved and no subclinical discharges were observed according to video-EEG monitoring. The present study have shown that the DL performance on the basis of group-data showed a suppression of REC in cases with lefthemisphere speech dominance regardless side of seizure onset. However, the results may be confounded by an impaired attention shortly after consciousness regained after seizure regardless of focal site. This was not considered as an expression of altered speech dominance (e.g. Helmstaedter et al., 2006), but regarded rather as a general and temporary suppression of auditory perception, i.e. in the speech dominant hemisphere. Thus, the present findings agree well with Kimuras (1961b) statement, that the right ear has an advantage in transferring verbal material to left dominant hemisphere. Taken together, epileptic focal discharges, regardless of origin, have an impact on right ear correct reports in children with left hemisphere dominance for speech. Children with seizures origination from the right hemisphere did not differ in any respect from those with left-sided focal seizures. However, focal seizures may have a prolonged impact on perception of verbal material and attention, also after consciousness has been regained. Finally, as not all children may be fully recovered 1-h postictally according to DL, implicating a continuing impact of seizures on auditory perception, a prolonged dichotic assessment together with the forced attention paradigm and visual attention measures are proposed to reveal the impact of seizure on attention and at the same time document when full cognitive recovery is attained. This information may have theoretical as well as pragmatic consequences. References Allen, J. E., Ferrie, C. D., Livingstone, J. H., & Feltbower, R. G. (2007). Recovery of consciousness after epileptic seizure in children. Archives of Disease in Childhood, 92, 39–42. Andrewes, D. G., Puce, A., & Bladin, P. F. (1990). Post-ictal recognition memory predicts laterality of temporal lobe seizure focus: comparison with postoperative data. Neuropsychologia, 28, 957–967. Berlin, C. I., Lowe-Bell, S. S., Jannetta, P. J., & Kline, D. G. (1972). Central auditory deficits after temporal lobectomy. Archives of Otolaryngology, 96, 4–10. Bryden, M. P. (1988). An overview of the dichotic listening procedure and its relation to cerebral organization. In K. Hugdahl (Ed.), Handbook of dichotic listening: Theory, methods and research (pp. 1–44). New York: John Wiley & Sons Inc. Carlsson, G., Hufnagel, M., Jansen, O., Claviez, A., & Navabi, A. (2010). Rapid recovery of motor and cognitive functions after resection of a right frontal lobe meningeoma in a child. Child’s Nervous System, 26, 105–111. Carlsson, G., Hugdahl, K., Uvebrant, P., Wiklund, L.-M., & von Wendt, L. (1992). Pathological left-handedness revisited: Dichotic listening in children with left versus right congenital hemiplegia. Neuropsychologia, 30, 471–481. da Fontoura, D. R., de Moraes Branco, D., Anés, M., Costa da Costa, J., & Wetters Portuguez, M. (2008). Language brain dominance in patients with refractory temporal lobe epilepsy. Arquivos de Neuropsiquatria, 66(1), 34–39. EA, I. L. (2010). Revised terminology and concepts for organization of the epilepsies: Report of the commission on classification and terminology. Epilepsia, 51(4), 676–685. Fernandes, M. A., Smith, M. L., Logan, W., Crawley, A., & McAndrews, M. P. (2006). Comparing language lateralization determined by dichotic listening and fMRI activation in frontal and temporal loes in children with epilepsy. Brain and Language, 96(1), 106–114. Gramstad, A., Engelbretsen, B. A., & Hugdahl, K. (2003). Left hemisphere dysfunction affects dichotic listening in patients with temporal lobe epilepsy. International Journal of Neuroscience, 113(9), 177–196. Gramstad, A., Engelbretsen, B. A., & Hugdahl, K. (2006). Dichotic listening with forced attention in patients with temporal lobe epilepsy: Significance of left hemisphere cognitive dysfunction. Scandinavian Journal of Psychology, 47(3), 163–170. Grant, A. C. (2005). Interictal perceptual function in epilepsy. Epilepsy & Behavior, 6, 511–519.
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F., et al. (1990). Cerebral language lateralization: Evidence from intracarotid amobarbital testing. Neuropsychologia, 28, 831–838. Mazzucchi, A., & Parma, M. (1978). Responses to dichotic listening tasks in temporal epileptics with and without clinically evident lesions. Cortex, 14, 381–390. Mazzucchi, A., Visintini, D., Magnani, G., Cattelani, R., & Parma, M. (1985). Hemispheric prevalence changes in partial epileptic patients on perceptual and attentional tasks. Epilepsia, 26, 379–390. McIntyre, M., Pritchard, P. B., & Lombroso, C. T. (1976). Left and right temporal lobe epileptics: A controlled investigation of some psychological differences. Epilepsia, 17, 377–386. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113. Oxbury, J. M., & Oxbury, S. M. (1969). Effects of temporal lobectomy on the report of dichotically presented digits. Cortex, 5, 3–14. Roberts, R. J., Varney, N. R., Paulsen, J. S., & Richardson, E. 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Interictal and postictal performances on dichotic listening test in children with focal epilepsy G. Carlsson ⇑, G. Wiegand, U. Stephani Dept. Neuropediatrics, Medical Center of Schleswig-Holstein, Campus Kiel, Germany
a r t i c l e
i n f o
Article history: Available online 14 April 2011 Keywords: Dichotic listening Children Drug resistant Epilepsy Focal seizures
a b s t r a c t Dichotic listening test (DL) is an important tool to disclose speech dominance in healthy subjects and in clinical cases. The aim of this study was to probe if focal epilepsy in children reveals a corresponding suppression of the ear reports contralateral to seizure onset site. Thus, 15 children and adolescents with clinically and electroencephalographically diagnosed focal epilepsy selected for left-hemisphere speech dominance without mental retardation were compared to matched controls according to age, gender, IQ and handedness. All children were assessed with DL for three times: Interictally (t0), postictally 5’ (t1) and 1 h (t2). At t0, all groups revealed a right ear advantage (REA), indicating a left-hemisphere speech dominance. There was a continuous increase in right correct score (REC) over the trials for normal controls. Five minutes postictally, there was an abrupt decrease in REC with a sustained left ear correct score (LEC) for children with epilepsy, independent of which side suffered from seizures. This effect was maintained even after 1 h. Thus, in children with left-hemisphere speech dominance the epileptic discharges caused a suppression of REC regardless of origin. The seizures may have a prolonged impact on attention and auditory perception for a considerable time after consciousness has been regained. Ó 2011 Elsevier Inc. All rights reserved.
1. Background The pioneering work by Kimura (1961a, 1961b) showed that the dichotic listening (DL) test has the ability to study hemispheric function and speech dominance in adult patients with focal epilepsy. Kimura (1961b) found that the right ear was more efficient to perceive dichotically presented verbal material than the left ear regardless of the site of focal seizure onset. This was especially true for the group of patients with left hemisphere dominance for speech, assessed by Wada test (Loring et al., 1990; Wada, 1949; Wada & Rasmussen, 1969). In patients with right-hemisphere speech dominance the left ear was more efficient to perceive the verbal material. The DL has been shown to be valid for assessing speech dominance in children and adults with drug resistant focal epilepsies. The validity as compared to gold standard, the Wada procedure, was considered to be about 0.8 to 0.95 for adults (Strauss, Gaddes, & Wada, 1987; Zatorre, 1989) and to about 0.9 for children and adolescents (Hugdahl, Carlsson, Uvebrant, & Lundervold, 1997).
⇑ Corresponding author. Address: University Medical Center Schleswig-Holstein, Dept. Neuropediatrics, Campus Kiel, Arnold-Heller-Str. 3, Bld 9, DE-24105 Kiel, Germany. Fax: +49 431 597 1769. E-mail address: [email protected] (G. Carlsson). 0278-2626/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bandc.2011.03.014
Recently, excellent correlations between DL tests and speech fMRI have been found also in children with temporal lobe epilepsy (e.g. da Fontoura, de Moraes Branco, Anés, Costa da Costa, & Wetters Portuguez, 2008; Fernandes, Smith, Logan, Crawley, & McAndrews, 2006). Thus, individuals with left hemisphere dominance for speech generally show a REA, whereas those with right hemisphere dominance for speech typically reveal a LEA, which is consistent with Kimuras findings (1961a). In children and adolescents with an early structural brain abnormality in the right hemisphere a clearly stated REA was revealed indicating left-hemisphere speech dominance. A reverse picture, i.e. a clear LEA, was found in children and adolescents with early left-sided brain impairment indicating right hemisphere dominance (Carlsson, Hugdahl, Uvebrant, Wiklund, von Wendt, 1992; Hugdahl & Carlsson, 1996; Isaacs, Christie, Vargha-Khadem, & Mishkin, 1996; Korkman, Granström, & Berg, 2004; Korkman & von Wendt, 1995). The dichotic listening (DL) technique is probably the most frequently used experimental method to assess lateralization of language function (Bryden, 1988; Hugdahl, 1995). Previous studies have been performed with either dichotic presentation of digits, words or fused words. However, the majority has been performed with consonant–vowel or consonant–vowel-consonant materials. The consonant vowel (CV) syllables are consistently found to produce the most robust right ear advantages (REA, Hugdahl, 1995) in
G. Carlsson et al. / Brain and Cognition 76 (2011) 310–315
right-handed individuals (Hugdahl & Andersson, 1984; Schankweiler & Studdert-Kennedy, 1967; Studdert-Kennedy & Schankweiler, 1970). The right ear advantage (REA) may be explained by a structural model (Kimura, 1967; Sparks & Geschwind, 1968). According to this, the contralateral auditory projections dominate and the ipsilateral auditory projections are suppressed or inhibited, i.e. given left-hemisphere speech dominance, the left ear inputs will be transformed first to the right hemisphere via corpus callosum, and then be perceived in the left hemisphere. Since Kimura (1961a, 1961b) several other studies have reported on the relationship between focal epilepsy and speech representation in patients with temporal lobe epilepsy (Berlin, LoweBell, Jannetta, & Kline, 1972; Mazzucchi & Parma, 1978; Mazzucchi, Visintini, Magnani, Cattelani, & Parma 1985; McIntyre, Pritchard, and Lombrose, 1976; Oxbury & Oxbury, 1969; Lee et al., 1994; Gramstad, Engelbretsen, & Hugdahl, 2006; Gramstad, Engelsen & Hugdahl, 2003; Grote, Pierre-Louise, Smith, Roberts, and Varney, 1995). Although several studies have found significant ‘‘lesion effects’’ to the ear contralateral to the lesion or side of focal epilepsy onset, other studies have failed to report this effect, particularly when it comes to the prediction of individual performance (Grote et al., 1995; Lee et al., 1994). In patients with left-sided focal epilepsy without structural abnormality, without documented speech dominance, there was an increase in REA (Mazzucchi & Parma, 1978; Mazzucchi et al., 1985) according to a facilitatory effect of focal epilepsy. However, in adult patients with left-hemisphere speech dominance and left focal epilepsy without evidence of structural lesions usually are a significant decrease in REA and concomitantly in the right ear correct scores (Lee et al., 1994). Gramstad et al. (2003, 2006) found that a left hemisphere cognitive dysfunction rather leads to a lack of REA in patients with TLE with left-hemisphere speech dominance, and not the focal epilepsy per se. Epileptic seizures are followed by dynamic alternations in neurological and cognitive function in the postictal period (Holmes, 1986). Postictal signs are accordingly considered to provide reliable information for the localization of the seizure onset region in patients with focal epilepsy (Leutmezer & Baumgartner, 2002). Thus, postictal memory impairments in patients with focal epilepsies correlated highly with cerebral localization and lateralization of seizure onset (Andrewes, Puce, & Bladin, 1990; Helmstaedter, Elger, & Lendt, 1994). Epileptic seizures may likewise alter DL performance. Roberts, Varney, Paulsen, and Richardson (1990) showed that patients with focal epilepsy changed their DL pattern in a normalized direction after successful antiepileptic drug treatment. Similarly, Helmstaedter, Fritz, Gonzáles Pérez, Elger, and Weber (2006) found in a patient with left-sided focal epilepsy a seizure driven right-hemispheric speech dominance according to fMRI, which reversed from the right to the left hemisphere when seizures were successfully controlled for. In the same way, others have found that the left ear advantage in DL test before a resection of a left-sided brain cyst can be normalized and change to a right ear advantage after surgery (Wester & Hugdahl, 2003). Thus, a left ear advantage may be demonstrated without evidence of right-hemisphere speech dominance, but may rather indicate a left-hemisphere suppression or impairment. Similarly, Carlsson, Hufnagel, Jansen, Claviez, and Navabi (2010) found in a child with a right-frontal meningeoma an extreme REA, which normalized after resection. The aim of the present study was to investigate the effects of left- and right-hemispheric focal seizures on dichotic listening performances in children with left hemisphere dominance for speech. According to Kimuras structural model (1967) it is expected that epileptic activity may in the first place alter the right ear correct scores and concomitantly REA independent of whether the leftor right hemisphere is triggered by seizures. Continuous compari-
311
sons between interictal and postictal registrations were considered to facilitate this purpose. This is a new attempt to achieve an optimal connection between active focal seizures and lateralized cognitive functions. Accordingly, DL performances were collected repeatedly up to an hour postictally in patients with documented seizure onset in the left or right hemisphere. 2. Methods 2.1. Participants Fifteen children with drug resistant focal epilepsy (8 females and 7 males; mean age 14.3 yrs, SD 3.2) were admitted to the comprehensive epilepsy center (UK-SH, campus Kiel) for long-term video EEG monitoring and neuropsychological assessment. Inclusion criteria were focal epilepsy with documented left hemisphere dominance for speech according to fMRI (10/15) or according to the comprehensive neuropsychological assessments. All subjects with mental retardation (IQ < 70), hearing impairment, incomplete DL records, or those suspected for right hemisphere dominance were excluded. The control group was recruited from an inpatient ward (Departments of Pediatrics and Neuropediatrics at the University clinic Schleswig–Holstein, Campus Kiel) matched to the study group on gender, age, IQ and handedness. The control group comprised 15 children (8 females and 7 males, mean age 12.6, SD 1.9) without central nervous system affections. Intelligence was determined by the German standardization of Culture Fair Test of intelligence (CFT1 or CFT20-R, ad modum Cattell) or Wechsler Intelligence Scales for Children (WISC-IV). The focal epilepsy group achieved a mean IQ of 89 (SD 13.3). Ten of the children with focal seizures (Left/Right: 7/3) showed an average intelligence (IQ > 84), five children (L/R = 4/1) a low average intelligence (IQ 70–84). The control group achieved a mean IQ of 94 (SD 16.2). Nine children revealed an average intelligence (IQ > 84), and six showed a low average intelligence (IQ 70–84). Handedness was determined by Edinburgh’s handedness questionnaire containing 10 items according to hand preference for manual items (Oldfield, 1971). Fourteen children in the seizure group were right-handed (93.3%) and one left-handed (6.7%). All children in the control group were right-handed. There were no statistically significant differences between the seizure groups and normal controls with regard to gender, age, IQ or handedness (Table 1). 2.2. The dichotic listening (DL) test The dichotic stimulus materials consisted of the six stop-consonants /b/, /d/, /g/, /p/, /t/, /k/ which were paired with the vowel /a/ to form six consonant–vowel (CV) syllables (/ba/, /da/, /ga/ etc.). The syllables was paired with each other for all possible combinations, thus yielding 36 dichotic pairs including 6 homonymic pairs (/ba/-/ba/, / da/-/da/, etc.). The homonymic trials were excluded in the statistical analyses. A male German speaking voice (baritone) from Northern German Radio (NDR) recorded the syllables with constant intonation and intensity on a tape, which was subsequently digitalized and copied on a CD at Hugdahl’s laboratory in Bergen, Norway, considered for use on conventional CD-player. The mean duration of the stimulus was approximately 350 ms, and the interval between stimuli was about 4 s. The children were presented the stimulus material over headphones and instructed to report the syllable they heard first, or best. Thus, reporting only one item on each trial irrespective of whether they perceived one or both items.
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Table 1 Patient characteristics: age, gender, IQ, group (L = left focal, R = right focal, C = control), and distribution of speech dominance according to fMRI, hand preference (R/L), and Laterality-index (Li) according to the labels Right Ear Advantage (REA), Left Ear Advantage (LEA) and No Ear Advantage (NEA) for interictal (t0), postictal 50 (t1) and postictal 1 h (t2) trials. The criterion for a REA, LEA or NEA was set to better recall from the right or left ear, or equal reports from both ears. Case
Age (yrs)
Gender (M/F)
IQ
Group (L/R/C)
Handpref(R/L)
Li. (t0)
Li (t1)
Li (t2)
Affected lobes
fMRI (L/R)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
7.9 9.9 10.7 11.0 13.9 15.3 15.5 17.3 17.6 17.9 18.2 13.9 14.2 15.1 16.8 9.1 9.5 9.8 11.3 12.5 12.5 12.7 13.2 13.2 13.4 13.5 13.6 14.5 14.7 15.8
M M F M F M M F F M F F M F F M M M F F F M F F F F M F M M
70 71 118 89 107 97 102 84 94 85 73 89 87 80 87 106 90 132 78 70 96 101 84 82 99 90 80 111 83 111
L L L L L L L L L L L R R R R C C C C C C C C C C C C C C C
R R R R R R R R R L R R L R R R R R R R R R R R R R R R R R
REA REA REA REA LEA REA REA REA REA REA REA REA LEA REA NEA LEA REA REA REA REA NEA REA REA NEA LEA REA REA REA REA REA
REA LEA REA LEA REA LEA REA LEA REA LEA LEA LEA REA LEA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA
REA REA LEA REA REA LEA NEA NEA REA REA LEA LEA LEA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA REA
T T T T P T O T T T T F T T F
L L L
2.3. Procedure The children with epilepsy were tested by medical personnel in connection with the Video-EEG-monitoring. Interictal testing (t0) was performed when no seizure activity was present, confirmed by the Video-EEG. The DL test was repeated 5 min after the children had regained awareness after a clinically and through the EEGrecordings confirmed ictal event (t1), i.e. early postictal recordings. Subsequently, after about another 55 min (t2), the procedure was repeated. The video-EEG recordings were continuously inspected to confirm that no focal seizure was present during the DL testing. The control group was correspondingly assessed with dichotic listening test at three occasions, at 1 day (t0) and the next day tested twice (t1 and t2) with 1 h in between. Intelligence and lateral preferences were assessed in the intermediate period. 2.4. Scoring of data and statistical analyses Data were scored for each subject as the frequency of correctly recalled syllables for the right and left ear input. The raw scores were transformed into percent scores (x/30100). The laterality-index (%) was calculated according to the formula: [(right ear left ear)/(right ear + left ear) 100], where right ear and left ear represent the number of correct right ear and left ear scores, respectively. The data were subjected to two different kinds of analysis of variance (ANOVA). The first analysis was based on the design 3 groups (left- and right focal seizure group and controls) 2 ear inputs (right/left) for each event (t0, t1 and t2) to evaluate whether there were any differences in DL performance for the left and right ear among groups and test-trials. The laterality-index was accordingly analyzed. Significant effects were followed-up with the Tukey HSD test. ANOVA for repeated measures was performed for DL measures, based on the design 3 groups (left- and right focal seizure group and controls) 2 Ear inputs (left/right) 3 Test-trials (t0, t1 and
L L L L L L L
t2). This analysis would answer the question of whether the DLT can differentiate between the groups over the course of events. The laterality-index was accordingly analyzed. Follow-up test were performed with pairwise contrast-analyses, or pairwise t-tests.
3. Results All children with left- and right-sided focal epilepsy and normal controls were considered left hemisphere dominant for speech as determined by fMRI, handedness and DL performance (Table 1). According to descriptive data, interictally (t0) ten of the 11 children with left-sided foci showed a REA (91%). Immediately after the seizure ceased and consciousness was regained (t1) five children still showed REA (45%) and six a LEA (55%). One hour postictally (t2) six children showed a REA (55%), whereas three a LEA (27%) and two NEA (18%). Interictally two of the four children with right-sided foci revealed a REA (t0), one child a LEA and another one a NEA. In the immediate (t1) as well as in the late postictal trial (t2) two children showed a REA and two a LEA. On the group level, there was a decrease in laterality-index (Li) and right ear correct (REC) reports for both focal seizure groups from the interictal (t0) to the early postictal trial (t1). At the late postictal event (t2) the REC reports recovered slightly for left seizure group, but slightly decreased for the right seizure group. The control group showed at the same time throughout an increase in the Li and REC reports. The LEC reports were, however, stable for all groups over the three trials (Table 2). In the first ANOVA there were no differences between the focal seizure groups for age, IQ or any of the dependent variables. Additionally, there were no differences between the focal seizure groups and normal controls for age and IQ. Statistically significant group differences were found with regard to REC reports at t1 [F(2, 27) = 6.58, p = .005] and at t2
G. Carlsson et al. / Brain and Cognition 76 (2011) 310–315 Table 2 Dichotic listening performance according to percent correct reports to the right and left ear (mean and range) for 15 children with left- versus right focal seizures and 15 normal controls over the three occasions (t0, t1 and t2). Group
Li (range)
REC
REC (range)
LEC
LEC (range)
Left-sided foci t0 11 19.7 11 1.9 t1 t2 11 8.7
N
Li
02.6–48.1 33.3–36.4 30.4–33.3
45.8 33.9 37.9
30.0–66.7 10.0–53.3 16.7–63.3
30.8 31.2 31.2
23.3–46.7 20.0–40.0 10.0–50.0
Right-sided foci t0 4 4.1 t1 4 1.7 t2 4 -1.6
06.7–13.0 14.3–20.0 26.3–16.7
35.0 34.2 28.3
23.3–43.3 30.0–40.0 23.3–43.3
31.7 33.3 30.0
26.7–36.7 26.7–40.0 16.7–40.0
Controls t0 15 t1 15 t2 15
12.5–61.5 3.7–55.6 4.0–58.3
44.8 48.9 53.1
23.3–70.0 33.3–70.0 40.0–66.6
29.5 27.5 27.3
16.6–40.0 20.0–43.3 16.6–40.0
19.4 27.1 32.0
[F(2, 27) = 9.74, p = .0007], and to laterality-index at t1 [F(2, 27) = 8.40, p = .001] and at t2 [F(2, 27) = 7.19, p = .003]. In the follow-up tests, Tukey HSD revealed significant differences for REC between normal controls (NC) and the left focal seizure group (LFG) at t1 (p < .01) and at t2 (p < .01), and between NC and the right focal seizure group (RFG) at t2 (p < .01). Moreover, there were significant differences for laterality-index between NC and LFG at t1 (p < .01) and at t2 (p < .05), and between NC and the right focal seizure group (RFG) at t1 (p < .05) and at t2 (p < .05). The ANOVA for repeated measures revealed a main group effect for REar and Lear correct reports over the three events [F(4, 52) = 3.09, p < .05]. Furthermore, there was a significant interaction effect between groups and correct reports for left-ear (LEar) and right-ear (REar) inputs over the events [Wilks lambda = .42338, F(8, 48) = 3.2211, p < .01]. Planned comparisons showed significant differences for exclusively REC reports between the LFG and NC at t1 [F(2, 54) = 8.65, p < .001] and at t2 [F(2, 54) = 7.29, p < .01], as well as differences between the RFG and NC at t1 [F(2, 54) = 4.54, p < .05] and at t2 [F(2, 54) = 9.13, p < .001]. Furthermore, there was a significant decrease in REC reports for LFG between t0 and t1 [F(2, 54) = 11.43, p < .0001] and between t0 and t2 (T = 2.47, p < .05). The RFG did not show statistically significant changes in REC reports from interictal and over the postictal events. However, the NC revealed a significant increase in REC reports between t0 and t2 [F(2, 54) = 4.77, p = .01]. Moreover, there were no significant differences between groups for LEC reports. The laterality-index (Li) showed a main group effect [F(2, 27) = 7.36, p < .01], and a significant interaction effect [F(2, 54) = 3.30, p < .05]. In the planned comparison there was a significant difference between the LFG and NC at t1 [F(1, 27) = 14.15, p < .001] and at t2 [F(2, 27) = 9.17, p < .01], which coincided with a significant decrease in laterality-index from t0 to t1 [F(1, 27) = 11.16, p < .01] for LFG and a continuous and significant increase of Li from t0 to t2 [F(2, 27) = 9.49, p = .005] for normal controls. Additionally, there was significant differences for Li between RFG and NC at t1 [F(2, 27) = 7.17, p = .01] and at t2 [F(2, 27)=9.49, p < .01], which imply that Li tended to decrease for the RFG at the late postictal event. 4. Discussion To sum up the main findings, postictally there was a significant decrease in laterality-index 5 min and up to 1 h after consciousness was regained for the LFG as well as for the RFG. A corresponding
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impact on the REC reports was found for the LFG and qualitatively for RFG compared to NC. Moreover, neither right- nor left-sided focal seizure showed an impact on the left ear correct reports in these children. Interictally, there was a right ear advantage in the group with left- and right-sided focal seizures as well as in normal controls. This is in agreement with the presumed left hemisphere dominance for speech, which was supported by right-handedness in all control children and in a clear majority of the children with focal epilepsy. The speech fMRI confirmed the left hemisphere dominance in two-thirds of the children with epilepsy. As one left-handed child showed a LEA in DL suspicious for right hemisphere dominance, but revealed left hemisphere dominance according to fMRI, the left hemisphere was considered dominant. For another left-handed child in the epilepsy group the fMRI was not yet performed, though considered as left hemisphere dominant according to a REA according to DL. However, in the interictal condition there were no differences between the three groups for any DL measure. Interestingly, the LFG showed a comparably high level for REC reports as normal controls, whereas the RFG tended to displayed inferior REC scores compared to the LFG and normal controls (cf. Fig. 1 and Table 2). This result is in line with previous findings (e.g. Kimura, 1961b), that verbal material from the right ear is more reliable transmitted to the left speech dominant hemisphere. Considering the DL performance for children with left-sided focal seizures from the interictal over the two postictal assessments, there was a striking decrease in laterality-index immediately after a seizure, implying a ‘‘lesion effect’’. One hour after the ictal event the laterality-index recovered, however, not reaching the level attained interictally (cf. Fig. 2). Likewise, the REC reports decreased in the early postictal and recovered slightly in the late postictal registration. The present results seem to corroborate with previous findings, that the REC is suppressed according to the left hemisphere impairment (e.g. Kimura, 1961b; Loring et al., 1990; Grote et al., 1995). However, this effect could not be shown in the interictal but solely in the postictal conditions for right ear inputs. Similarly, the children with right-sided focal seizures showed a decline for Li and for REC reports over postictal events, in the absence of a simultaneous impact on LEC reports. Thus, this contradicts the assumed contralateral ‘‘lesion effect’’ for RFG. Moreover, there were no differences between the left- and right-sided focal groups for any DL measure over the interictal and postictal events, and the LEC reports remained substantially unchanged in the groups. Although, this small group with rightsided foci (N = 4) revealed corresponding results as the group with left-sided foci, so it may be unlikely that a larger sample produce a different result, especially as the RFG tended to show slight improved LEC 5 min and a decrease on hour postictally (Fig. 1). The small increase of LEC in the RFG may give some support for a facilitatory effect of the epileptogenic focus (cf. Mazzucchi & Parma, 1978; Mazzucchi et al., 1985). After all, the present study support the assumption that the right hemisphere functions seem less important than left hemisphere functions in explaining the impact of focal seizures (e.g. Gramstad et al., 2003, 2006; Kimura, 1961b). Present findings appear to be consistent with the structural model of DL, where the right hemisphere primarily is regarded as a relay station for left ear stimuli, which need to be transferred to the left hemisphere for cognitive processing (Kimura, 1967; Sparks & Geschwind, 1968). Since no differences between the focal epilepsy groups were found, and both groups showed a decrease in REC reports in the postictal events without affection of the LEC reports, this may indicate a generally reduced attention or vigilance caused by the distribution of seizure activity to different parts of the brain regardless
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65 60 55
% correct reports
50 45 40 35 30 25 20 15 10 t0
t1
t2
t0
t1
t2
t0
t1
RFG
LFG
NC
t2
REar LEar
Fig. 1. Percent correct reports for the right-ear (REar) and left-ear (LEar) input over the three test-occasions (interictal = t0, 5 min postictally = t1, 1 h postictally = t2) for the left focal group (LFG), right focal group (RFG) and normal controls (NC).
50
40
Laaterality-index (%)
30
20
10
0
-10
-20
-30 t0
t1
t2
LFG RFG NC
Fig. 2. Laterality-index (%) over the three test-occasions (interictal = t0, 5 min postictally = t1, 1 h postictally = t2) for the left focal group (LFG), right focal group (RFG) and normal controls (NC).
of seizure origin. However, for left hemisphere dominant cases the left hemisphere functions were particularly impaired irrespective which side trigger a seizure. In conclusion, the present findings could not support a ‘‘lesion effect’’ or suppression of the ear contralateral to the focal site in all children, which may most likely be due to the fact that focal seizures are a network disease involving brain regions distant from the seizure focus (Grant, 2005; Spencer, 2002). The time to recover full consciousness after epileptic seizures is also variable. Children
with complex partial seizures regain consciousness within a few minutes. Generally, most children regain consciousness within 30–40 min after seizure, although some need many hours to recover (Allen, Ferrie, Livingstone, & Feltbower, 2007). This may depend on existing seizure type and involvement of the contralateral hemisphere. Generally, in some cases with focal epilepsy, there is generally more than one epileptogenic network and occasionally more than one seizure type involved, but each individual seizure type has a consistent site of onset (ILEA, 2010). Thus, there are
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many unpredictable factors involved, which can distort the view of solely unilateral impairment in focal epilepsy. However, in the present study the children were exclusively assessed with DL test after consciousness was achieved and no subclinical discharges were observed according to video-EEG monitoring. The present study have shown that the DL performance on the basis of group-data showed a suppression of REC in cases with lefthemisphere speech dominance regardless side of seizure onset. However, the results may be confounded by an impaired attention shortly after consciousness regained after seizure regardless of focal site. This was not considered as an expression of altered speech dominance (e.g. Helmstaedter et al., 2006), but regarded rather as a general and temporary suppression of auditory perception, i.e. in the speech dominant hemisphere. Thus, the present findings agree well with Kimuras (1961b) statement, that the right ear has an advantage in transferring verbal material to left dominant hemisphere. Taken together, epileptic focal discharges, regardless of origin, have an impact on right ear correct reports in children with left hemisphere dominance for speech. Children with seizures origination from the right hemisphere did not differ in any respect from those with left-sided focal seizures. However, focal seizures may have a prolonged impact on perception of verbal material and attention, also after consciousness has been regained. Finally, as not all children may be fully recovered 1-h postictally according to DL, implicating a continuing impact of seizures on auditory perception, a prolonged dichotic assessment together with the forced attention paradigm and visual attention measures are proposed to reveal the impact of seizure on attention and at the same time document when full cognitive recovery is attained. This information may have theoretical as well as pragmatic consequences. References Allen, J. E., Ferrie, C. D., Livingstone, J. H., & Feltbower, R. G. (2007). Recovery of consciousness after epileptic seizure in children. Archives of Disease in Childhood, 92, 39–42. Andrewes, D. G., Puce, A., & Bladin, P. F. (1990). Post-ictal recognition memory predicts laterality of temporal lobe seizure focus: comparison with postoperative data. Neuropsychologia, 28, 957–967. Berlin, C. I., Lowe-Bell, S. S., Jannetta, P. J., & Kline, D. G. (1972). Central auditory deficits after temporal lobectomy. Archives of Otolaryngology, 96, 4–10. Bryden, M. P. (1988). An overview of the dichotic listening procedure and its relation to cerebral organization. In K. Hugdahl (Ed.), Handbook of dichotic listening: Theory, methods and research (pp. 1–44). New York: John Wiley & Sons Inc. Carlsson, G., Hufnagel, M., Jansen, O., Claviez, A., & Navabi, A. (2010). Rapid recovery of motor and cognitive functions after resection of a right frontal lobe meningeoma in a child. Child’s Nervous System, 26, 105–111. Carlsson, G., Hugdahl, K., Uvebrant, P., Wiklund, L.-M., & von Wendt, L. (1992). Pathological left-handedness revisited: Dichotic listening in children with left versus right congenital hemiplegia. Neuropsychologia, 30, 471–481. da Fontoura, D. R., de Moraes Branco, D., Anés, M., Costa da Costa, J., & Wetters Portuguez, M. (2008). Language brain dominance in patients with refractory temporal lobe epilepsy. Arquivos de Neuropsiquatria, 66(1), 34–39. EA, I. L. (2010). Revised terminology and concepts for organization of the epilepsies: Report of the commission on classification and terminology. Epilepsia, 51(4), 676–685. Fernandes, M. A., Smith, M. L., Logan, W., Crawley, A., & McAndrews, M. P. (2006). Comparing language lateralization determined by dichotic listening and fMRI activation in frontal and temporal loes in children with epilepsy. Brain and Language, 96(1), 106–114. Gramstad, A., Engelbretsen, B. A., & Hugdahl, K. (2003). Left hemisphere dysfunction affects dichotic listening in patients with temporal lobe epilepsy. International Journal of Neuroscience, 113(9), 177–196. Gramstad, A., Engelbretsen, B. A., & Hugdahl, K. (2006). Dichotic listening with forced attention in patients with temporal lobe epilepsy: Significance of left hemisphere cognitive dysfunction. Scandinavian Journal of Psychology, 47(3), 163–170. Grant, A. C. (2005). Interictal perceptual function in epilepsy. Epilepsy & Behavior, 6, 511–519.
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