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Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Right-hemisphere language dominancein temporal lobe epilepsy: Clinical and neuropsychological correlates Rebecca Rausch a
a b c
c
, Kyle Boone & Catherine M. Ary
a
Reed Neurological Research Center ,
b
Departments of Psychiatry and Biobehavioral Sciences , c
Neurology University of California , Los Angeles Published online: 04 Jan 2008.
To cite this article: Rebecca Rausch , Kyle Boone & Catherine M. Ary (1991) Right-hemisphere language dominancein temporal lobe epilepsy: Clinical and neuropsychological correlates, Journal of Clinical and Experimental Neuropsychology, 13:2, 217-231, DOI: 10.1080/01688639108401039 To link to this article: http://dx.doi.org/10.1080/01688639108401039
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sublicensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Clinical and Experimental Neuropsychology 1991, Vol. 13, NO.2, p ~217-231 .
0168-8634/91/1302-0217$3.O0 0 Swets & Zitlinger
Right-Hemisphere Language Dominance in Temporal Lobe Epilepsy: Clinical and Neuropsychological Correlates*
Downloaded by [University of Strathclyde] at 08:41 10 October 2014
Rebecca R a u s ~ h ' * * -Kyle ~ , Boone', and Catherine M. Ary' 'Reed Neurological Research Center and 2Departmentsof Psychiatry and Biobehavioral Sciences and 3Neurology University of California, Los Angeles
ABSTRACT Prior to and following temporal lobe surgery, patients with right-hemisphere language dominance and focal left temporal lobe epilepsy (RHLD-LTLSz) were compared to right-handed patients with left-hemisphere language dominance and either left temporal lobe epilepsy (LHLD-LTLSz) or right temporal lobe epilepsy (LHLD-RTLSz). The group of RHLD-LTLSz patients had a more consistent history of brain involvement before the age of 5 years and had a higher seizure frequency rating than did either LHLD patient group. Cognitively, RHLD-LTLSz patients did not show significant deficits in psychometric intellectual scores. In addition, they did not demonstrate comparable degrees of verbal memory loss as found either pre- or postoperatively in LHLD-LTLSz patients. The right-handed RHLD-LTLSz and the right-handed LHLD-LTLSz groups both appeared to exhibit bilaterally depressed fine-motor coordination. The left-handed RHLD-LTLSz patients did not show the same motor deficiencies. These latter findings suggest that hemispheric dominance for bilateral motor control may exist independent of language dominance, but not independent of handedness.
The prevalence of language dominance in the right-hemisphere is thought to be rare in the normal population, particularly in right-handed individuals. Based on the occurrence of crossed aphasia, Zangwill (1979) estimated that, at most, only 1-2% of the normal right-handed population has right-hemisphere language dominance (RHLD). The probability of RHLD in the left-handed population is considerably greater and has been estimated to be as high as 20% (Satz, 1979). A substantially higher rate of RI%D occurs in patients with early damage or disruption of functions in the left-hemisphere, regardless of handedness. In epileptic pa-
* We thank the investigators and staff of the UCLA Epilepsy Program for their generous support and contribution. This study was supported in part by Public Health Service Grant # NS 02808. Requests for reprints should be sent to Rebecca Rausch, Ph.D., Reed Neurological Research Center, Department of Neurology, University of California, Los Angeles, CA 90024-1769, USA. Accepted for publication: May 12, 1990.
Downloaded by [University of Strathclyde] at 08:41 10 October 2014
218
REBECCA RAUSCH ET AL.
tients with clinical evidence of left-hemisphere involvement, 13-15% of righthanded patients may demonstrate RHLD with the intracarotid Sodium Amobarbital procedure (IAF’; Rasmussen & Milner, 1975; Rausch & Walsh, 1984). Patients who are left-handed and have a history of significant neurological signs indicative of early left-hemisphere damage (i.e., hemiparesis, aphasia, etc.) have an estimated 53% chance of having RHLD (Rasmussen & Milner, 1977). The functional significance of pathological “shifting” of language dominance to the right-hemisphere in response to early left-hemisphere damage has barely been approached. Few studies have assessed hemispheric language capabilities directly and, thus, have failed to identify those patients with early left-hemisphere damage who remained left-hemisphere language dominant (LHLD) vs. those wherein language dominance was shifted to the right-hemisphere. Frequently used reports of handedness and/or results of dichotic listening and tachistoscopic tasks to estimate language dominance have a high error rate (c.f., Strauss & Wada, 1983; Strauss, Wada, & Kosaka, 1985). Using more definitive methods to assess hemispheric language dominance (e.g., IAP, intracranial stimulation), Lansdell(l969) reported on the intellectual profiles of 18 patients with RHLD, 15 of whom were left-handed. He found that, the earlier the left-hemisphere is damaged, the more likely that the patient would show relative strengths in verbal processes and deficits in nonverbal processes. Specifically, RHLD patients whose neurological symptoms occurred prior to age 5 years had relatively higher verbal Wechsler-Bellevue scores, while RHLD patients, whose symptoms appeared after age 5 years, had relatively higher nonverbal Wechsler-Bellevue scores. The effect of hemispheric reorganization on other neuropsychological functions was not addressed. The present study reports comprehensive medical and neuropsychological findings on eight RHLD patients. These patients were identified from a select group of epileptic patients. All eight RHLD patients had seizures originating from the left temporal lobe. The association of RHLD and focal left temporal lobe seizures has been previously reported (Rausch & Walsh, 1984). Five of the current RHLD patients were right-handed, and three patients were left-handed. Seven RHLD patients underwent an anterior left (nondominant) temporal lobectomy for treatment of their seizure disorders. Pre- and postoperative characteristics of these patients are compared to right-handed epileptic patient groups who are known LHLD.
METHOD Subject Selection Subjects were identified from a group of patients with medically intractable complexpartial seizures who had a unilateral, primary seizure onset in the anterior temporal lobe. Seizure onset was localized by EEG telemetry, utilizing surface and, in some cases, depth recordings of spontaneous seizures. As part of their diagnostic work-up, the patients had undergone the TAP. During the
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RIGHT-HEMISPHERELANGUAGE DOMINANCE
219
IAP, hemispheric dominance was determined by language examination following selective injections of 125 mg of Sodium Amobarbital into the internal carotid arteries (cf., Rausch & Risinger, 1990). Each hemisphere was perfused separately with a minimal 30min delay between injections. Language testing occurred within the first 2 min following the injection and during the period of drug-induced hemisphere EEG slowing and conualateral hemiparesis. Orientation to the examiner and test stimuli was established first. The language protocol included evaluation of verbal sequencing, repetition, naming, reading, and response to simple verbal commands. A hemisphere was classified as dominant for language if, following perfusion of that hemisphere, the patient was unable to perform any of the language tasks administered, and if, following injection of the other hemisphere, the patient could perform these tasks during the same post-injection interval. Patients who had evidence of bilateral language (i.e., speech errors after both injections or no speech errors after either injection) and those whose language dominance could not be determined were excluded from the present study. Eight patients were identified with RHLD and also had comprehensive preoperative neuropsychological data. All eight RHLD patients (5 right-handed and 3 left-handed) had documented left temporal lobe seizures (LTLSz). Fifty-one right-handed patients with LHLD and available preoperative neuropsychological data were identified. Thirty-two patients had focal seizures originating from the right temporal lobe (RTLSz), and 19 patients had focal seizures originating from the left temporal lobe (LTLSz). Seven of the eight RHLD-LTLSz patients and all of the LHLD patients underwent a unilateral anterior temporal lobectomy to remove the seizure focus. The surgery removed the anterior portions of the hippocampus, hippocampal gyms, uncus, lateral temporal neocortex and lateral 2/3’s of the amygdala (cf., Crandall. Engel. & Rausch, 1983; Falconer, 197 l).
Clinical Parameters of Patient Groups As shown in Table 1 , the patient groups differed on the following characteristics. First,
the RHLD-LTLSz patients differed from both LHLD patient groups in age at first clinical event 0,> .05 but < .lo; Exact Probability Test, Fisher, 1934). All RHLD-LTLSz patients experienced a clinically significant cerebral event before the age of 5 years, while only 65% of the LHLD-LTLSz patients and 70%of the LHLD-RTLSz patients had evidence of a clinical event before the age of 5 years. Secondly, the patient groups differed in their seizure frequency. The group of RHLDLTLSz patients had a higher seizure frequency than did either the LHLD-LTLSz or the LHLD-RTLSz patient groups (p < .05;Mann & Whitney, 1947). In addition, the RHLDLTLSz patients had alower age at first seizure than did the LHLD-RTLSz patients ( p < .05), but not the LHLD-LTLSz patients. The two LHLD patient groups did not differ on any of the clinical variables. Table 2 shows the preoperative laboratory findings and pathological analyses of the resected tissue of the RHLD-LTLSz patients. Pathological results were found to be characteristic of patients with focal temporal lobe epilepsy, with hippocampal sclerosis the most frequent diagnosis (Babb & Brown, 1987). Following surgery, all patients experienced a significant reduction in their seizure frequency. Neuropsychological Measures Patients were administered a comprehensive neuropsychological evaluation prior to any surgical intervention and approximately one year postoperatively (M= 1.2 years, SD = 0.40). Psychological measurements used in the present study were as follows:
3 10
M
10 11
2
24 3 12 12
M P
Age at pre-op testing (yrs)
w - o p seizure frequency b
Education (yrs)
Gender C
Family history of Left Handers d N
16
12
M
15
M P -
3
18
11
.5
.5
3
40
11
11
1.5
P
M
12
2
37
12
8
1
P
F
13
3
21
10
.5
.5
P
F
8
3
14
.5
.5
.5
5.8(5.1)
4.4(5.2)
M(SD)
8.2 (4.9) 10.2(5.5)
4.3 (4.7)
1.3 (1.3)
M(kSD)
LTLSz
5P2N
6M 2F
11.8 (2.1)
2.1(0.8)
25.8(7.1)
12.2(7.5)
9.3(8.4)
4.9(6.5)
M(SD)
RTLSz
11P 6N
12M 7F
15P15N
16M16F
12.8 (2.4) 13.3(2.5)
2.8 (0.5) 2.1(0.7)
26.5 (1 1.7) 25.5(6.9)
~~
GROUP M (fSD) OR FREQUENCY DISTRIBUTION RHLD -LTLSZ LHLD
a N’s vary per parameter as function of data available. 3 = more than 1 seizure per day; 2 = 2 seizures per week up to 1 seizure per day; 1 = 1 seizure per week or less. F = female; M = male. P = positive; N = negative.
Note: All RHLD patients had left temporal lobe seizures. Dash indicates data not available.
N
M
43
0
0
Age at consistent seizure disorder (yrs)
4
10
0
Age at first seizure (yrs)
4
2.5
195 925 200
107 114 139 VIII 924
Age at first clinical event (yrs)
Patient #:
Left-Handed
Right-Handed
INDIVIDUAL PARAMETERS RHLD -LTLSZ
Table 1. Clinical Parameters of RHLD -LTLSz and Right-Handed LHLD-LTLSz and LHLD-RTLSz Patients a
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m
$I
2
6
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RIGHT-HEMISPHERELANGUAGE DOMINANCE
221
Psychomerric Intelligence: The Wechsler Adult Intelligence Scale (WAIS, Wechsler, 1955) was used as a measurement of psychometric intelligence, except for Patient #200 who was administered the Wechsler Intelligence Scale for Children - Revised (WSC-R, Wechsler, 1974). Scores analyzed included the Full Scale IQ (FSIQ), and the factor scores of Cohen (1957): Verbal Comprehension (VC) and Perceptual Organization (PO). Attention and concentration: Attentional abilities were represented by the age-corrected Digit Span subtest of the WAIS or WISC-R and the Cohen (1957) factor score, Memory and Freedom from Distractibility (MFD). Language functioning: Word generation ability (Fluency) was evaluated by Thurstones’ Primary Mental Ability Test (Pendleton, Heaton, Lehman, & Hulihan, 1982). Naming skills were assessed by a dysnomia screening test (Rausch & Benson, 1980) that consisted of 12 pictured items of increasing difficulty. Perceptuallmotor organizational skills: Perceptual skills were evaluated by the Street Visual Gestalt Test (Street, 1931), the Trail Making Test, Parts A and B (Davies, 1968; Reitan, 1958), and paper-and-pencil copying of the Rey-Ostenieth Complex Figure (BennettLevy, 1984; Osterrieth, 1944; Rey, 1941). Memory: Immediate verbal and nonverbal memory were assessed by the Associative Learning (AL), Logical Prose Paragraph A (LPA). and Visual Reproduction (VR) subtests of the Wechsler Memory Scale (WMS. Wechsler & Stone, 1945). The WMS LPA was scored by the Schear method (1986). A visually-presented paired-associative task that contained six novel word-pairs was also employed. Delayed memory was assessed by asking for recall of the material from the WMS subtests after a 45-min interruption. In addition, delayed recall of the Rey-Osterrieth Complex Figure was obtained 45 min after the patient had initially copied the design. Motor functioning: Bilateral finger dexterity and grip strength were assessed by the Finger Tapping Test, the Grooved Pegboard Test, and the Grip Strength Test (Bomstein, 1985; Matthews & Klove, 1964; Reitan & Davison, 1974).
RESULTS
Preoperative Neuropsychological Findings As shown in Table 3, performances of the patient groups were not significantly different on tests of psychometric intelligence, attention, and general language functioning. Performances of the two groups of LHLD patients differed significantly on several measures of verbal memory and fine motor coordination; the LHLD-LTLSz patients performed worse than LHLD-RTLSz patients in both domains. The RHLD-LTLSz patients did not show the same consistent pattern of depressed scores as did the LHLD-LTLSz patients. On three measures of verbal memory that were found to be depressed in LHLD-LTLSz patients, the RHLDLTLSz patients performed significantly better than LHLD-LTLSz patients and at levels comparable to the LHLD-RTLSz patients. On tests of fine motor coordination, the mean performances of the group of RHLD-LTLSz patients did not differ from those of either LHLD patient group. However, review of the individual scores of the RHLD-LTLSz patients revealed that the right-handed RHLD-LTLSz patients showed relatively consistent depression in fine motor coordination that was similar to the impaired performance
LTL
#VIII
#195
LTL
LTL
LTL
#I39
febrile illness at 11 months accompanied by cyanosis for 10 min
suspected febrile seizures at age of 6 months
at 1 1/2 yrs, fell out of back of wagon and struck head
LTJ.
#I14
#924
2 hr coma at age 2 ID yrs due to eating castor bean measles at age 4 yrs; as recuperating, fell and hit head with numerous seizures, hospitalized for 2 weeks widespread ecchyomoses 1st seizure when few days old; congenital deformities of hands and feet
LTLa
#lo7
Patient Seizure Possible Etiological No. Focus Event
deficient short-term memory
normal
normal
mentally slow
normal
normal
Neurologic Examination
normal
normal
normal
normal
normal
normal
normal
normal
normal
normal
normal
Angiogram CT
small filling normal defect in floor of 3rd ventricle; possible cerebellar atrophy; cause unknown normal
normal
normal
PEG
Table 2. Laboratory and Pathology Results of RHLD-LTLSz Patients
left temporal hypometabolism left temporal hypometabolism left temporal hypometabolism
metabolism
hypo-
left temporal
symmetric but poor quality symmetric
PET
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gyrus
hamartoma in left middle temporal
WNL
insufficient tissue
WNL
No surgery
left hippocampal sclerosis
-
WNL
left hippocampal WNLb sclerosis
PATHOLOGICAL FINDINGS Mesial Late.ral Structure Neocortex
m
3:
F
3
w
E W
E
h)
seizures at 5 1/2 months
LTL
#200
WNL = Within Normal Limits
Note: Dash indicates data not available a LTL = Left Temporal Lobe
seizures at 6 months
LTL
#925
normal
normal
normal
normal
normal
left posterior temporal calcification normal
insufficient tissue
WNL
left temporal left hippocampal WNL hyposclerosis metabolism
left temporal hypometabolism
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v)
-9
E
107
Psychometric Intelligence FSIQ 124 99 91 Cohen VC 118.2 93.0 95.8 Cohen PO 138.5 88.8 86.5 Cohen VC-PO -20.3 4.2 9.3 Attention 9 10 Digit Span 9 (Age-Corrected S S ) CohenMFD 108.7 108.5 88.4 Language Fluency Total 41 33 37 Dysnomia Exam 11 PerceptuaVMotor Organization Street 7 7 Rey -0stemeth 23.5 22.0 26.0 COPY 58 50 TrailMakingAb 30 Trail Making B 60 76 62 Memory - Verbal Auditory WMSALimmed 10.5 15.0 16.0 delay 5 6 7 8 hard pairs retained 100 100 100
Patient #:
20.5 7 100
31 11 11 18.0 31 92 13.0 5 100
55 7
10 22.5 32 53 13.0 4
100
75 10 7 20.0 21 81 15.5 6 75
28.5 24 42
8
27 10
88.4 102.9
94.2
108.1
10
8
13
8
93 104 113 83 112.6 83.2 86.0 97.2 116.8 78.4 116.8 108.1 4.2 4.8 -30.8 -10.9
100
15.5 7
19.5 16 40
5
96.9(8.8)
14.9(2.9) 5.9( 1.l)
22.5(3.5) 32.8(14.4) 63.3(18.6)
8.q2.0)
42.7(16.9) 9.8(1.6)
-
99.5(8.7)
9.6(1.6)
99.q14.1) 96.5(12.8) 103.6(20.1) -7.1(13.6)
55.0(42.2)
Kl(3.6) 4.8( 1.6)
25.q4.0) 44.1(22.0) 91.9(38.6)
7.q1.3)
41.6(20.4) 8.5(2.4)
103.q12.3)
10.9(2.6)
88.q20.4)
.05
.05
.02
.02
.02
Group Comparisons1 1 2 3 P-Vahea
17.q2.8) 6.1( 1.2)
26.q3.1) 36.3( 18.1) 75.9(31.0)
7.5(1.5)
48.q18.7) lO.l(l.0)
99.9(11.3)
10.2(2.5)
96.7(9.0) 103.3(13.6) 95.5(11.3) 104.q18.2) 98.4(10.0) 104.7(15.4) -2.9(11.9) -0.3( 14.7)
GROUP M (fSD) RHLD-LTLSZ LHLD LTLSZ RTLS~ M(fSD) M(fSD) M(fSD)
97.1
10
86.0 94.6 -8.6
85
INDIVIDUAL SCORES RHLD-LTLSz Right-Handed Left-Handed 114 139 VIII 924 195 925 200
Table 3. Preoperative Neuropsychological Scores of RHLD-LTLSz Patients and Right-Handed LHLD-LTLSz and LHLD-RTLSz Patients
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F
h,
4.5
25.0 26 23 42
18.0 56 53 49 47 70 65 71 64
48
10 2 20
10 13 8 1 3 80 100
51 62 67
48
21 24
-
18
14
5.0 3.0 60
12.0 10.0 83
9.0 6.5 72 10.7(3.2)
8.9(3.2) 4.0(3.7) 39.1(33.0)
40.1(12.4) 37.3(11.4) 44.9(7.0) 43.1(5.4) 83.3(24.5) 75.q 19.0)
El(7.0) 40.2(12.5) 36.4(10.9) 47.0(4.9) 41.7(5.3) 85.0(18.3) 96.1(30.5)
15.7(8.7)
10.6(2.0) 9.8(3.6) 8.9(3.8) 8.q3.5) 81.0(26.6) 79.3( 15.5)
14.3(2.9)
8.5(3.5) 6.6(3.1) 77.6(24.7)
40.6(11.3) 35.3(9.6) 49.9(6.2) 46.8(6.5) 70.9(8.6) 76.2( 11.2)
13.5(8.1)
9.9(3.1) 7.5( 3.4) 72.3(26.5)
14.0(3.2)
lOS(3.4) 7.9(3.9) 72.8(21.6) .02
.05
a P-value of Mann-Whitney (1947) test.
Lower scores indicate better performance.
Note: Bold scores indicate
Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen19
Right-hemisphere language dominancein temporal lobe epilepsy: Clinical and neuropsychological correlates Rebecca Rausch a
a b c
c
, Kyle Boone & Catherine M. Ary
a
Reed Neurological Research Center ,
b
Departments of Psychiatry and Biobehavioral Sciences , c
Neurology University of California , Los Angeles Published online: 04 Jan 2008.
To cite this article: Rebecca Rausch , Kyle Boone & Catherine M. Ary (1991) Right-hemisphere language dominancein temporal lobe epilepsy: Clinical and neuropsychological correlates, Journal of Clinical and Experimental Neuropsychology, 13:2, 217-231, DOI: 10.1080/01688639108401039 To link to this article: http://dx.doi.org/10.1080/01688639108401039
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [University of Strathclyde] at 08:41 10 October 2014
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sublicensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Journal of Clinical and Experimental Neuropsychology 1991, Vol. 13, NO.2, p ~217-231 .
0168-8634/91/1302-0217$3.O0 0 Swets & Zitlinger
Right-Hemisphere Language Dominance in Temporal Lobe Epilepsy: Clinical and Neuropsychological Correlates*
Downloaded by [University of Strathclyde] at 08:41 10 October 2014
Rebecca R a u s ~ h ' * * -Kyle ~ , Boone', and Catherine M. Ary' 'Reed Neurological Research Center and 2Departmentsof Psychiatry and Biobehavioral Sciences and 3Neurology University of California, Los Angeles
ABSTRACT Prior to and following temporal lobe surgery, patients with right-hemisphere language dominance and focal left temporal lobe epilepsy (RHLD-LTLSz) were compared to right-handed patients with left-hemisphere language dominance and either left temporal lobe epilepsy (LHLD-LTLSz) or right temporal lobe epilepsy (LHLD-RTLSz). The group of RHLD-LTLSz patients had a more consistent history of brain involvement before the age of 5 years and had a higher seizure frequency rating than did either LHLD patient group. Cognitively, RHLD-LTLSz patients did not show significant deficits in psychometric intellectual scores. In addition, they did not demonstrate comparable degrees of verbal memory loss as found either pre- or postoperatively in LHLD-LTLSz patients. The right-handed RHLD-LTLSz and the right-handed LHLD-LTLSz groups both appeared to exhibit bilaterally depressed fine-motor coordination. The left-handed RHLD-LTLSz patients did not show the same motor deficiencies. These latter findings suggest that hemispheric dominance for bilateral motor control may exist independent of language dominance, but not independent of handedness.
The prevalence of language dominance in the right-hemisphere is thought to be rare in the normal population, particularly in right-handed individuals. Based on the occurrence of crossed aphasia, Zangwill (1979) estimated that, at most, only 1-2% of the normal right-handed population has right-hemisphere language dominance (RHLD). The probability of RHLD in the left-handed population is considerably greater and has been estimated to be as high as 20% (Satz, 1979). A substantially higher rate of RI%D occurs in patients with early damage or disruption of functions in the left-hemisphere, regardless of handedness. In epileptic pa-
* We thank the investigators and staff of the UCLA Epilepsy Program for their generous support and contribution. This study was supported in part by Public Health Service Grant # NS 02808. Requests for reprints should be sent to Rebecca Rausch, Ph.D., Reed Neurological Research Center, Department of Neurology, University of California, Los Angeles, CA 90024-1769, USA. Accepted for publication: May 12, 1990.
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218
REBECCA RAUSCH ET AL.
tients with clinical evidence of left-hemisphere involvement, 13-15% of righthanded patients may demonstrate RHLD with the intracarotid Sodium Amobarbital procedure (IAF’; Rasmussen & Milner, 1975; Rausch & Walsh, 1984). Patients who are left-handed and have a history of significant neurological signs indicative of early left-hemisphere damage (i.e., hemiparesis, aphasia, etc.) have an estimated 53% chance of having RHLD (Rasmussen & Milner, 1977). The functional significance of pathological “shifting” of language dominance to the right-hemisphere in response to early left-hemisphere damage has barely been approached. Few studies have assessed hemispheric language capabilities directly and, thus, have failed to identify those patients with early left-hemisphere damage who remained left-hemisphere language dominant (LHLD) vs. those wherein language dominance was shifted to the right-hemisphere. Frequently used reports of handedness and/or results of dichotic listening and tachistoscopic tasks to estimate language dominance have a high error rate (c.f., Strauss & Wada, 1983; Strauss, Wada, & Kosaka, 1985). Using more definitive methods to assess hemispheric language dominance (e.g., IAP, intracranial stimulation), Lansdell(l969) reported on the intellectual profiles of 18 patients with RHLD, 15 of whom were left-handed. He found that, the earlier the left-hemisphere is damaged, the more likely that the patient would show relative strengths in verbal processes and deficits in nonverbal processes. Specifically, RHLD patients whose neurological symptoms occurred prior to age 5 years had relatively higher verbal Wechsler-Bellevue scores, while RHLD patients, whose symptoms appeared after age 5 years, had relatively higher nonverbal Wechsler-Bellevue scores. The effect of hemispheric reorganization on other neuropsychological functions was not addressed. The present study reports comprehensive medical and neuropsychological findings on eight RHLD patients. These patients were identified from a select group of epileptic patients. All eight RHLD patients had seizures originating from the left temporal lobe. The association of RHLD and focal left temporal lobe seizures has been previously reported (Rausch & Walsh, 1984). Five of the current RHLD patients were right-handed, and three patients were left-handed. Seven RHLD patients underwent an anterior left (nondominant) temporal lobectomy for treatment of their seizure disorders. Pre- and postoperative characteristics of these patients are compared to right-handed epileptic patient groups who are known LHLD.
METHOD Subject Selection Subjects were identified from a group of patients with medically intractable complexpartial seizures who had a unilateral, primary seizure onset in the anterior temporal lobe. Seizure onset was localized by EEG telemetry, utilizing surface and, in some cases, depth recordings of spontaneous seizures. As part of their diagnostic work-up, the patients had undergone the TAP. During the
Downloaded by [University of Strathclyde] at 08:41 10 October 2014
RIGHT-HEMISPHERELANGUAGE DOMINANCE
219
IAP, hemispheric dominance was determined by language examination following selective injections of 125 mg of Sodium Amobarbital into the internal carotid arteries (cf., Rausch & Risinger, 1990). Each hemisphere was perfused separately with a minimal 30min delay between injections. Language testing occurred within the first 2 min following the injection and during the period of drug-induced hemisphere EEG slowing and conualateral hemiparesis. Orientation to the examiner and test stimuli was established first. The language protocol included evaluation of verbal sequencing, repetition, naming, reading, and response to simple verbal commands. A hemisphere was classified as dominant for language if, following perfusion of that hemisphere, the patient was unable to perform any of the language tasks administered, and if, following injection of the other hemisphere, the patient could perform these tasks during the same post-injection interval. Patients who had evidence of bilateral language (i.e., speech errors after both injections or no speech errors after either injection) and those whose language dominance could not be determined were excluded from the present study. Eight patients were identified with RHLD and also had comprehensive preoperative neuropsychological data. All eight RHLD patients (5 right-handed and 3 left-handed) had documented left temporal lobe seizures (LTLSz). Fifty-one right-handed patients with LHLD and available preoperative neuropsychological data were identified. Thirty-two patients had focal seizures originating from the right temporal lobe (RTLSz), and 19 patients had focal seizures originating from the left temporal lobe (LTLSz). Seven of the eight RHLD-LTLSz patients and all of the LHLD patients underwent a unilateral anterior temporal lobectomy to remove the seizure focus. The surgery removed the anterior portions of the hippocampus, hippocampal gyms, uncus, lateral temporal neocortex and lateral 2/3’s of the amygdala (cf., Crandall. Engel. & Rausch, 1983; Falconer, 197 l).
Clinical Parameters of Patient Groups As shown in Table 1 , the patient groups differed on the following characteristics. First,
the RHLD-LTLSz patients differed from both LHLD patient groups in age at first clinical event 0,> .05 but < .lo; Exact Probability Test, Fisher, 1934). All RHLD-LTLSz patients experienced a clinically significant cerebral event before the age of 5 years, while only 65% of the LHLD-LTLSz patients and 70%of the LHLD-RTLSz patients had evidence of a clinical event before the age of 5 years. Secondly, the patient groups differed in their seizure frequency. The group of RHLDLTLSz patients had a higher seizure frequency than did either the LHLD-LTLSz or the LHLD-RTLSz patient groups (p < .05;Mann & Whitney, 1947). In addition, the RHLDLTLSz patients had alower age at first seizure than did the LHLD-RTLSz patients ( p < .05), but not the LHLD-LTLSz patients. The two LHLD patient groups did not differ on any of the clinical variables. Table 2 shows the preoperative laboratory findings and pathological analyses of the resected tissue of the RHLD-LTLSz patients. Pathological results were found to be characteristic of patients with focal temporal lobe epilepsy, with hippocampal sclerosis the most frequent diagnosis (Babb & Brown, 1987). Following surgery, all patients experienced a significant reduction in their seizure frequency. Neuropsychological Measures Patients were administered a comprehensive neuropsychological evaluation prior to any surgical intervention and approximately one year postoperatively (M= 1.2 years, SD = 0.40). Psychological measurements used in the present study were as follows:
3 10
M
10 11
2
24 3 12 12
M P
Age at pre-op testing (yrs)
w - o p seizure frequency b
Education (yrs)
Gender C
Family history of Left Handers d N
16
12
M
15
M P -
3
18
11
.5
.5
3
40
11
11
1.5
P
M
12
2
37
12
8
1
P
F
13
3
21
10
.5
.5
P
F
8
3
14
.5
.5
.5
5.8(5.1)
4.4(5.2)
M(SD)
8.2 (4.9) 10.2(5.5)
4.3 (4.7)
1.3 (1.3)
M(kSD)
LTLSz
5P2N
6M 2F
11.8 (2.1)
2.1(0.8)
25.8(7.1)
12.2(7.5)
9.3(8.4)
4.9(6.5)
M(SD)
RTLSz
11P 6N
12M 7F
15P15N
16M16F
12.8 (2.4) 13.3(2.5)
2.8 (0.5) 2.1(0.7)
26.5 (1 1.7) 25.5(6.9)
~~
GROUP M (fSD) OR FREQUENCY DISTRIBUTION RHLD -LTLSZ LHLD
a N’s vary per parameter as function of data available. 3 = more than 1 seizure per day; 2 = 2 seizures per week up to 1 seizure per day; 1 = 1 seizure per week or less. F = female; M = male. P = positive; N = negative.
Note: All RHLD patients had left temporal lobe seizures. Dash indicates data not available.
N
M
43
0
0
Age at consistent seizure disorder (yrs)
4
10
0
Age at first seizure (yrs)
4
2.5
195 925 200
107 114 139 VIII 924
Age at first clinical event (yrs)
Patient #:
Left-Handed
Right-Handed
INDIVIDUAL PARAMETERS RHLD -LTLSZ
Table 1. Clinical Parameters of RHLD -LTLSz and Right-Handed LHLD-LTLSz and LHLD-RTLSz Patients a
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m
$I
2
6
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RIGHT-HEMISPHERELANGUAGE DOMINANCE
221
Psychomerric Intelligence: The Wechsler Adult Intelligence Scale (WAIS, Wechsler, 1955) was used as a measurement of psychometric intelligence, except for Patient #200 who was administered the Wechsler Intelligence Scale for Children - Revised (WSC-R, Wechsler, 1974). Scores analyzed included the Full Scale IQ (FSIQ), and the factor scores of Cohen (1957): Verbal Comprehension (VC) and Perceptual Organization (PO). Attention and concentration: Attentional abilities were represented by the age-corrected Digit Span subtest of the WAIS or WISC-R and the Cohen (1957) factor score, Memory and Freedom from Distractibility (MFD). Language functioning: Word generation ability (Fluency) was evaluated by Thurstones’ Primary Mental Ability Test (Pendleton, Heaton, Lehman, & Hulihan, 1982). Naming skills were assessed by a dysnomia screening test (Rausch & Benson, 1980) that consisted of 12 pictured items of increasing difficulty. Perceptuallmotor organizational skills: Perceptual skills were evaluated by the Street Visual Gestalt Test (Street, 1931), the Trail Making Test, Parts A and B (Davies, 1968; Reitan, 1958), and paper-and-pencil copying of the Rey-Ostenieth Complex Figure (BennettLevy, 1984; Osterrieth, 1944; Rey, 1941). Memory: Immediate verbal and nonverbal memory were assessed by the Associative Learning (AL), Logical Prose Paragraph A (LPA). and Visual Reproduction (VR) subtests of the Wechsler Memory Scale (WMS. Wechsler & Stone, 1945). The WMS LPA was scored by the Schear method (1986). A visually-presented paired-associative task that contained six novel word-pairs was also employed. Delayed memory was assessed by asking for recall of the material from the WMS subtests after a 45-min interruption. In addition, delayed recall of the Rey-Osterrieth Complex Figure was obtained 45 min after the patient had initially copied the design. Motor functioning: Bilateral finger dexterity and grip strength were assessed by the Finger Tapping Test, the Grooved Pegboard Test, and the Grip Strength Test (Bomstein, 1985; Matthews & Klove, 1964; Reitan & Davison, 1974).
RESULTS
Preoperative Neuropsychological Findings As shown in Table 3, performances of the patient groups were not significantly different on tests of psychometric intelligence, attention, and general language functioning. Performances of the two groups of LHLD patients differed significantly on several measures of verbal memory and fine motor coordination; the LHLD-LTLSz patients performed worse than LHLD-RTLSz patients in both domains. The RHLD-LTLSz patients did not show the same consistent pattern of depressed scores as did the LHLD-LTLSz patients. On three measures of verbal memory that were found to be depressed in LHLD-LTLSz patients, the RHLDLTLSz patients performed significantly better than LHLD-LTLSz patients and at levels comparable to the LHLD-RTLSz patients. On tests of fine motor coordination, the mean performances of the group of RHLD-LTLSz patients did not differ from those of either LHLD patient group. However, review of the individual scores of the RHLD-LTLSz patients revealed that the right-handed RHLD-LTLSz patients showed relatively consistent depression in fine motor coordination that was similar to the impaired performance
LTL
#VIII
#195
LTL
LTL
LTL
#I39
febrile illness at 11 months accompanied by cyanosis for 10 min
suspected febrile seizures at age of 6 months
at 1 1/2 yrs, fell out of back of wagon and struck head
LTJ.
#I14
#924
2 hr coma at age 2 ID yrs due to eating castor bean measles at age 4 yrs; as recuperating, fell and hit head with numerous seizures, hospitalized for 2 weeks widespread ecchyomoses 1st seizure when few days old; congenital deformities of hands and feet
LTLa
#lo7
Patient Seizure Possible Etiological No. Focus Event
deficient short-term memory
normal
normal
mentally slow
normal
normal
Neurologic Examination
normal
normal
normal
normal
normal
normal
normal
normal
normal
normal
normal
Angiogram CT
small filling normal defect in floor of 3rd ventricle; possible cerebellar atrophy; cause unknown normal
normal
normal
PEG
Table 2. Laboratory and Pathology Results of RHLD-LTLSz Patients
left temporal hypometabolism left temporal hypometabolism left temporal hypometabolism
metabolism
hypo-
left temporal
symmetric but poor quality symmetric
PET
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gyrus
hamartoma in left middle temporal
WNL
insufficient tissue
WNL
No surgery
left hippocampal sclerosis
-
WNL
left hippocampal WNLb sclerosis
PATHOLOGICAL FINDINGS Mesial Late.ral Structure Neocortex
m
3:
F
3
w
E W
E
h)
seizures at 5 1/2 months
LTL
#200
WNL = Within Normal Limits
Note: Dash indicates data not available a LTL = Left Temporal Lobe
seizures at 6 months
LTL
#925
normal
normal
normal
normal
normal
left posterior temporal calcification normal
insufficient tissue
WNL
left temporal left hippocampal WNL hyposclerosis metabolism
left temporal hypometabolism
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v)
-9
E
107
Psychometric Intelligence FSIQ 124 99 91 Cohen VC 118.2 93.0 95.8 Cohen PO 138.5 88.8 86.5 Cohen VC-PO -20.3 4.2 9.3 Attention 9 10 Digit Span 9 (Age-Corrected S S ) CohenMFD 108.7 108.5 88.4 Language Fluency Total 41 33 37 Dysnomia Exam 11 PerceptuaVMotor Organization Street 7 7 Rey -0stemeth 23.5 22.0 26.0 COPY 58 50 TrailMakingAb 30 Trail Making B 60 76 62 Memory - Verbal Auditory WMSALimmed 10.5 15.0 16.0 delay 5 6 7 8 hard pairs retained 100 100 100
Patient #:
20.5 7 100
31 11 11 18.0 31 92 13.0 5 100
55 7
10 22.5 32 53 13.0 4
100
75 10 7 20.0 21 81 15.5 6 75
28.5 24 42
8
27 10
88.4 102.9
94.2
108.1
10
8
13
8
93 104 113 83 112.6 83.2 86.0 97.2 116.8 78.4 116.8 108.1 4.2 4.8 -30.8 -10.9
100
15.5 7
19.5 16 40
5
96.9(8.8)
14.9(2.9) 5.9( 1.l)
22.5(3.5) 32.8(14.4) 63.3(18.6)
8.q2.0)
42.7(16.9) 9.8(1.6)
-
99.5(8.7)
9.6(1.6)
99.q14.1) 96.5(12.8) 103.6(20.1) -7.1(13.6)
55.0(42.2)
Kl(3.6) 4.8( 1.6)
25.q4.0) 44.1(22.0) 91.9(38.6)
7.q1.3)
41.6(20.4) 8.5(2.4)
103.q12.3)
10.9(2.6)
88.q20.4)
.05
.05
.02
.02
.02
Group Comparisons1 1 2 3 P-Vahea
17.q2.8) 6.1( 1.2)
26.q3.1) 36.3( 18.1) 75.9(31.0)
7.5(1.5)
48.q18.7) lO.l(l.0)
99.9(11.3)
10.2(2.5)
96.7(9.0) 103.3(13.6) 95.5(11.3) 104.q18.2) 98.4(10.0) 104.7(15.4) -2.9(11.9) -0.3( 14.7)
GROUP M (fSD) RHLD-LTLSZ LHLD LTLSZ RTLS~ M(fSD) M(fSD) M(fSD)
97.1
10
86.0 94.6 -8.6
85
INDIVIDUAL SCORES RHLD-LTLSz Right-Handed Left-Handed 114 139 VIII 924 195 925 200
Table 3. Preoperative Neuropsychological Scores of RHLD-LTLSz Patients and Right-Handed LHLD-LTLSz and LHLD-RTLSz Patients
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F
h,
4.5
25.0 26 23 42
18.0 56 53 49 47 70 65 71 64
48
10 2 20
10 13 8 1 3 80 100
51 62 67
48
21 24
-
18
14
5.0 3.0 60
12.0 10.0 83
9.0 6.5 72 10.7(3.2)
8.9(3.2) 4.0(3.7) 39.1(33.0)
40.1(12.4) 37.3(11.4) 44.9(7.0) 43.1(5.4) 83.3(24.5) 75.q 19.0)
El(7.0) 40.2(12.5) 36.4(10.9) 47.0(4.9) 41.7(5.3) 85.0(18.3) 96.1(30.5)
15.7(8.7)
10.6(2.0) 9.8(3.6) 8.9(3.8) 8.q3.5) 81.0(26.6) 79.3( 15.5)
14.3(2.9)
8.5(3.5) 6.6(3.1) 77.6(24.7)
40.6(11.3) 35.3(9.6) 49.9(6.2) 46.8(6.5) 70.9(8.6) 76.2( 11.2)
13.5(8.1)
9.9(3.1) 7.5( 3.4) 72.3(26.5)
14.0(3.2)
lOS(3.4) 7.9(3.9) 72.8(21.6) .02
.05
a P-value of Mann-Whitney (1947) test.
Lower scores indicate better performance.
Note: Bold scores indicate
