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Brain injury handedness and speech lateralization in a series of amobarbital studies.

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Brain Injury, Handedness, and
Speech Laterahation in a Series
of Amobarbital Studies
A
Roger P. Woods, MD,” Carl B. Dodrill, PhD,t and George A. Ojemann, MDt
Data on handedness and speech lateralization in patients selected for amobarbital studies have frequently been extrapolated to the normal population, despite the high frequency of brain injuries which might alter lateralization in
these patients. To achieve a better definition of the relationships between brain injury, handedness, and speech
lateralization, we reviewed the records of 237 consecutivepatients who underwent amobarbital testing. Brain injuries
sufficient to cause right hemiparesis were strongly associated with left handedness and atypical (right hemisphere or
bilateral) speech representation. Among nonhemiparetic patients, abnormal extratemporal radiological findings were
associated with an increased incidence of left handedness and atypical speech lateralization. It was not possible to
demonstrate any alteration in handedness or speech representation resulting from abnormalities restricted to the
temporal lobes, although such alterations could not be excluded. Handedness and speech lateralization established
using amobarbital studies in neurosurgical patients may not be representative of the normal population.
Woods RP, Dodrill CB, Ojemann GA. Brain injury, handedness, and speech lateralization in a series
of amobarbital studies. Ann Neurol 1988;23:510-518
Brain asymmetries have been of considerable interest
in neurology for more than a century. The relationship
between handedness and speech lateralization has received a great deal of attention because it has both
practical and theoretical implications. For many years,
the only data available for analysis of this relationship
came from series of patients with unilateral brain injuries [l-41. Based on these data, it was possible to
show that speech lateralization in left handers is not
uniformly the mirror image of speech lateralization in
right handers, as some had originally assumed. Nonetheless, left handers do show a higher proportion of
atypical speech representation than right handers. Furthermore, some studies have found a difference in the
incidence of aphasia and recovery from aphasia among
left handers and their relatives as compared to right
handers, suggesting a qualitative difference in the degree of speech lateralization in left handers, independent of the direction of latedzation {5- 111.
Since the 1960s, these studies have been supplemented by data from patients undergoing neurosurgical procedures in whom speech representation has
been determined preoperatively by unilateral injection
of sodium amobarbital using the Wada technique 112151. Data from the largest of these amobarbital studies, summarized by Rasmussen and Milner in 1978
[12), has been cited without reservation in numerous
texts as being representative of the distribution of
handedness and speech lateralization in the general
population.
Unfortunately, extrapolation of the data of Rasmussen and Milner to the normal population poses problems-their subjects all had had prior brain injuries,
often at an early age 1121. From their data, it is clear
that early injury to the left brain leads to a decrease in
left hemisphere speech and an increase in atypical (i.e.,
right or bilateral) speech representation. Rasmussen
and Milner did not address the question of whether
early injury to the right hemisphere might also alter
speech lateralization. Since the data that are generally
cited exclude only patients with early left hemisphere
injury and not those with early right hemisphere injury, extrapolation of these data to the normal population assumes that early right hemisphere injury cannot
alter speech representation even though early left
hemisphere injury clearly does. The data cited show
that among right handers without early left hemisphere
injury, 4% have right hemisphere speech and 96%
have left hemisphere speech and that among such left
handers, 15% have right hemisphere speech, 15%
have bilateral speech, and 70% have left hemisphere
speech.
From the Departments of *Medicine and tNeurological Surgery,
University of Washington, Seattle, WA 98195.
Address correspondence to Dr Dodrill, Epilepsy Center, Harborview Medical Center (ZA-50), 325 Ninth Ave, Seattle, WA 98104.
Received Aug 3, 1987, and in revised form Nov 17. Accepted for
publication Nov 30, 1987.
510 Copyright 0 1988 by the American Neurological Association
Another issue not addressed in the study of Rasmussen and Milner is the question of whether brain
injury might alter handedness as well as speech representation. Data from other sources suggest that this is
indeed the case [2, 161. Finally, the right-handed subjects studied by Rasmussen and Milner were selected
because they had some factor suggesting the possibility
of atypical lateralization; therefore, their right handers
may not be representative of right handers in general.
To address some of these issues further, we have
retrospectively reviewed the results of amobarbital
testing in 237 consecutive patients undergoing neurosurgical procedures at the University of Washington
from 1973 to 1986. This report summarizes our findings.
Methods and Patients
The clinical history and results of neuropsychological testing
and radiological studies of 237 consecutive patients who
underwent amobarbital testing at the University of Washington were reviewed. Eleven of these patients were excluded
because amobarbital testing was incomplete or inconclusive. Fifteen additional patients were excluded because they
had undergone cortical resection, which might have altered
speech representation at some time before amobarbital testing. Three patients were excluded because they had a history
of aphasia or cerebrovascular accident as adults without associated hemiparesis. Of the remaining 208 patients, 10 had a
clinical history of right hemiparesis, 6 had a clinical history of
left hemiparesis, and 192 had no history of hemiparesis.
Of the 208 patients not excluded, 189 were age 16 or
older, 13wereage 1 2 t o 15,and5wereage9to 11.Theage
of one patient was not available.
One hundred ninety-seven of the 208 patients underwent
amobarbital testing as part of preoperative evaluation for
resection of epileptic foci. Amobarbital testing is performed
on all such patients at the Regional Epilepsy Center of the
University of-Washington. Evaluation of these patients also
included extensive neuropsychological testing, electroencephalography, and neuroradiological studies. During the
course of neuropsychological testing, handedness was established for each of 7 different activities, a family history
of handedness was obtained, and intelligence testing was
performed using the Wechsler Adult Intelhgence Scale,
Wechsler Adult Intelligence Scale-Revised, or Wechsler Intelligence Scale for Children-Revised. Of the remaining 11
patients, 3 had left aneriovenous malformations without seizures and underwent neuropsychological testing as outlined
above. Five patients had seizures but did not undergo
neuropsychological testing. One patient had a right parietal
hematoma without seizures, and no clinical history was available for 2 patients.
The procedure used for amobarbital testing has been described previously [17]: 100 to 125 mg of sodium amobarb i d was injected into either the right or left internal carotid
artery, resulting in a transient contralateral hemiparesis. After the injection, language was tested by asking the patient to
name objects and to read sentences aloud. Testing was continued until performance returned to a baseline established
before amobarbital injection. The hemisphere that was being
considered for operation was routinely perfused first, and the
other hemisphere was perfused at least 30 minutes later.
Studies in which both carotids were not injected were considered incomplete for the purposes of this study. Based on
the results of amobarbital testing, speech lateralization was
classified as left, right, or bilateral.
Lesion side was defined as the side on which operation was
performed. If patients did not undergo operation, lesion side
was defined on the basis of electroencephalographic results,
radiological abnormalities, and the clinical assessment of lesion side. If no consistent lesion side could be established
using these criteria, lesion side was classified as unknown.
Writing hand was established by observing the patient
writing. Handedness was defined as right if the patient preferred the right hand for a majority of the 7 handedness
inventory criteria (writing, throwing a ball, hammering a nail,
using an eraser, turning a doorknob, cutting with a knife, and
using scissors), and left if the patient preferred the left hand
for a majority of the criteria. Handedness of patients who did
not undergo neuropsychological testing was classified as unknown.
Radiological studies reviewed included pneumoencephalograms, computed tomographic scans of the head, metritamide-enhanced computed tomographic scans, and magnetic resonance imaging scans of the head. Studies were
classified as abnormal if they showed any abnormality outside
the temporal lobe. Lesions confined to the temporal lobe
were fairly common, since many of these patients suffer from
temporal lobe epilepsy, and radiological studies other than
angiograms showing such abnormalities were classified as
normal. Radiological studies were classified as unknown if no
radiological reports were available.
Family histories of handedness were obtained from the
patient andor relatives at the time of neuropsychological
testing. Family history of handedness was classified as sinistral if any first-degree relative (excluding the patient) was left
handed. Families with at least one right-handed first-degree
relative and no known left-handed first-degree relatives were
classified as dextral. If handedness information was not available for any first-degree relative, family history of handedness was classified as unknown.
Because many of the sample sizes are small, all significance
values reported here were calculated using Fisher’s exact
method C183, and all are two-tailed. To convey more accurately the meaning of these significance values, 95%
confidence intervals for the odds ratio were also calculated
using an exact method [19J For a contingency table in the
form:
a b
c d
the odds ratio is defined as d b c . The odds ratio can range
from zero to infinity. An odds ratio of 1 indicates that the
two properties represented in the 2 x 2 table are independent of one another. An odds ratio greater than 1 indicates a
positive association between the two properties of interest,
so the values of a and d are increased relative to b and c. An
odds ratio less than 1 indicates a negative association, so the
values of a and d are decreased relative to b and c. For
Woods et al: Brain Injury and Laterality 511
Table 1 . Handedness, Speech, Lesion Si&, Extratemporal Radiological Findings, and lntelligence a~ a Function of Hemiparesis
Handedness
Hemiparesis
Leftb
Right
None
Significance, right hemiparesis
versus no hemiparesis'
Odds ratio (95% confidence)
Left
Right
0
5
10
26
0
Speech
Atypical"
Lesion Side
Left
p < 0.001
5
1(1)
9(3)
1
24(14)
168
p < 0.001
12.31-m
7.86-2,717
157
Extratemporal
Radiological
Findings
Left
Right
3
10
96
3
0
89
p = 0.002
Abnormal
4
9
48
1.99-m
Intelligence
(FSIQ)
< 85
Normal
2
85
3
9
51
2
1
132
p < 0.001
1
1
135
p < 0.001
3.30-1,118
3.04-1,029
"Atypical includes right and bilateral speech. Values in parentheses show bilateral speech only.
bValuesfor left hemiparesis are not significantly different from those for no hemiparesis except for radiological findings in whichp = 0.02. See
text for odds ratio confidence intervals.
'Calculated using Fisher's exact method.
FSIQ = Full Scale IQ.
Table 2. Handedness, Speech, Lesion Side, and Intelligence as a Function of Extratemporal
Radiological Findings in Patients without Hemiparesis
~
~~
~
~~
~
~
Handedness
Extratemporal
Radiological Findings
Left
Abnormal
Normal
Significanceb
Odds ratio (95% confidence)
Right
12
12
33
118
p < 0.001
1.32-9.55
Speech
Lesion
Intelligence
(FSIQ)
Atypical"
Left
Left
wht
<85
2
1~7)
W7)
37
123
29
64
18
66
15
34
30
96
p
= 0.02
1.11-8.20
NS
0.79-3.5 1
85
NS
0.62-3.10
*Atypical includes right and bilateral speech. Values in parentheses show bilateral speech only.
bCalculated using Fisher's exact method.
FSIQ = Full Scale IQ; NS = not significant.
example, an odds ratio of 10 in favor of an association between atypical speech and left handedness would indicate
that the ratio of left handers to right handers among patients
with atypical speech is 10 times the ratio of left handers to
right handers among patients with left hemisphere speech.
Similarly, an odds ratio of 0.10 in favor of an association
between atypical speech and left handedness would imply
that the ratio of left handers to right handers among patients
with atypical speech is only one-tenth of the corresponding
ratio among patients with left hemisphere speech. An odds
ratio of 1 would imply identical ratios of left handers to right
handers in both subgroups of patients, indicating that handedness and speech representation are unrelated. Ninety-five
percent confidence intervals for simple proportions were calculated exactly on the basis of a binomial distribution f20J
Results
Bmin Injury and Bruin Laterulizutzon
Four indices of brain injury were used in this study:
hemiparesis, radiological abnormality, lesion side, and
intelligence.
HEMIPARESIS. As shown in Table 1, right hemiparesis was associated with marked increases in both
left handedness and atypical speech representation.
512 Annals of Neurology
Vol 23 N o 5 May 1988
Right hemiparesis was also associated with a significant
increase in radiological abnormalities and with an increased number of patients with Full Scale I Q (FSIQ)
scores less than 85 on intelligence testing. Although
left hemiparesis was associated with an increase in extratemporal radiological abnormalities ( p = 0.02, odds
ratio confidence interval 1.06-558), it was not associated with any significant increase or decrease in right
handedness (odds ratio confidence interval 0.14-~),
left hemisphere speech (odds ratio confidence interval
0.07-35.18), or FSIQ less than 85 (odds ratio confidence interval 0.42-47.35). As demonstrated by the
very wide confidence intervals for the odds ratios, this
lack of significance should be attributed to the small
number of patients with left hemiparesis and not to the
absence of any m e association between these factors.
RADIOLOGICAL ABNORMALITIES AND LESION SIDE.
Table 2 compares nonhemiparetit patients who had
abnormal extratemporal radiologicd studies with nonhemiparetic patients who had normal extratemporal
radiological studies. Abnormal extratemporal radiological studies were associated with a significant increase
in left handedness and in atypical speech represen-
Table 3. Relationship Between Lesion Side and Handedness
and Speech in Nonhemiparetic Patientj
Results of Extratemporal
Radiological Studies
Abnormal
Left lesion
Right lesion
Significanceb
Odds ratio
Normal
Left lesion
Right lesion
Significanceb
Odds ratio
Handedness
Speech
Left
Right
Atypicala
8
3
19
lO(7)
14
19
17
p = 0.03
1.03-41 1
1(0)
NS
0.37- 13.39
8
4
Left
52
7(4)
62
5(3)
57
61
NS
NS
0.59-11.38
0.38-6.33
"Atypical includes right and bilateral speech. Values in parentheses
show bilateral speech only.
bCalculated using Fisher's exact method.
NS = not significant.
tation. No significant relationship was found between
radiological study results and lesion side or intelligence, and relationships strong enough to generate
odds ratios of more than 3.51 and 3.10, respectively,
can be excluded on the basis of these data.
Table 3 further subdivides the data shown in Table 2
to compare the correlates of right- and left-sided lesions. Among patients with abnormal extratemporal
radiological studies, those with left-sided lesions had a
significant increase in atypical speech compared to patients with right-sided lesions. Although left-sided lesions did not produce a significant increase in left
handedness among patients who had abnormal extratemporal radiological studies, odds ratios as high as
13.39 in favor of such a relationship cannot be excluded. Similarly, among patients who had normal extratemporal radiological studies, the odds ratio favoring a relationship between left-sided lesions and left
handedness may be as high as 11.38 and the ratio
favoring a relationship between Ieft-sided lesions and
atypical speech may be as high as 6.33, although no
significant relationship was found in either case.
Tables 4 and 5 list the radiological abnormalities
associated with left- and right-sided lesions as a function of speech representation and handedness. Lesions
limited to the temporal lobe are not included. In general, abnormalities associated with atypical speech or
left handedness were more destructive andor extensive than abnormalities associated with right handedness and unilateral left hemisphere speech. Lesions
associated with unilateral right hemisphere speech
were particularly extensive and invariably associated
with left handedness.
The percentage of patients showing definite evidence of right or left brain injury (either hemiparesis
or radiological abnormalities outside the temporal
lobes) is shown in Table 6. Left-handed patients who
Table 4. Extratemporal Radiological Abnormalities as a Function of Speecb and Handedness in Patients with Left-Sided Lesions
~~
Atypical Speech
and Right Hemiparesis
(All Left Handed)
Left cerebral atrophy
Left cerebral atrophy"
Left cerebral porencephaly
Left frontal porencephaly"
Left atrophy and
frontoparietal
porencephalya
Left atrophy and frontal porencephaly"
Left atrophy and cyst"
Left temporoparietal
contusion"
~~
Atypical Speech
and Left Handed
Atypical Speech
and Right Handed
Left Speech
and Left Handed
Left Speech
and Right Handed
Left porencephaly
Left parietooccipital
atrophy"
Left parietooccipital
AVM"
Left parietooccipitotemporal AVM"
Diffuse atrophy
Left multilobe AVM
Callosal agenesis
Left parietal atrophy
and ulogyria
Left angioma
Left vascular mass
Left atrophy'
Left cerebral atrophy
(2 patients)
Left frontotemporal
atrophy
Left frontal tumor
Left parietal density
Left parietooccipital
defect
Left temporoparietal
density
Left ventricular enlargement (2 patients)
Bioccipitd calcification
Intracranial calcification
Hydrocephalus
Pineal lesion
Abnormal
Rght frontoparietd
infarctb
Bilateral atrophy
Lateral ventricle
asymmetry
Ventriculomegaly
Left atrophyb
"Speechlimited to the right hemisphere.
bPatient had left hemiparesis.
'Patient had right hemiparesis.
AVM = arteriovenous malformation.
Woods et ak Brain Injury and Laterality
513
Table 5 . Extratemporal Radiological Abnormalities as a Function of Speech and Handedness in Patients with Right-SaAd Lesions
Atypical Speech
and Left Handed
Left Speech
and Left Handed
Left Speech
and Right Handed
Left Speech
and Left Hemiparesis
Right sylvian fissure enlargement"
Right temporooccipital
lesion
Cortical atrophy
Right frontal atrophy (2 patients)
Right occipitoparietal low density
Right occipitoparietal
calcification
Right atrophy
Right parietal decreased density
Right hemiatrophy
Right ventricle dilation (2 patients)
Right occipital calcification
Atrophy of frontal gyms
Atrophy
Left atrophy
Abnormal
U h t hemiatrophy
Frontal hypervascularity
"Speech limited to the right hemisphere.
Table 6. Percentage of Patients Showing Evidence of Significant Extratemporal Injury
~~~
~
~
~
~
~
t o the Right or
Ldt Hemisphere
FQht Hemisphere
Injurya ("5)
Left Hemisphere
Injuryb (%)
13
13
13
13
7
10
12
13
27
33
55
58
78
20
~
Right-handed patients with left hemisphere speech (n = 137)
Patients with left hemisphere speech (n = 152)
Right-handed patients (n = 152)
Left-handed patients with left hemisphere speech (n = 15)
kght-handed patients with atypical speech (n = 15)
Left-handed patients (n = 33)
Patients with atypical speech (n = 33)
Left-handed patients with atypical speech (n = 18)
All patients (n = 185)'
9
6
6
12
"Left hemiparesis or abnormal radiological findings with a right-sided lesion.
bIbght hemiparesis or abnormal radiological findings with a left-sided lesion
'22 nonhemiparetic patients were excluded because radiological results, handedness, or lesion side was unavailable. One patient with left
hemiparesis was excluded because complete handedness information was unavailable.
had atypical speech had definite left-brain injuries
significantly more often than left-handed patients with
left hemisphere speech or those who were right
handed with atypical speech ( p = 0.002). Furthermore, patients in these last two groups had left brain
injuries significantly more often than right-handed patients with left hemisphere speech ( p = 0.008). These
results indicate that both left handedness and atypical
speech are markers for brain injury and that the combination of left handedness and atypical speech is a
stronger marker than either of these alone.
Among nonhemiparetic patients with no radiological abnormalities outside the temporal lobes, the combination of left handedness and atypical speech was
seen in 3 patients, all of whom had left-sided lesions.
The sample size is too small for this finding to be
significant.
514 Annals of Neurology Vol 23 N o 5 May 1988
RADIOLQGICAL
TEMPORAL LOBE ABNORMALITIES.
In these data, radiological abnormalities limited to the
temporal lobes were excluded in classifying radiological findings because such abnormalities were very
common in these subjects, many of whom suffer from
temporal lobe epilepsy. To determine whether leftsided radiological lesions limited to the temporal lobe
might also lead to an increase in left handedness or
atypical speech representation, patients with n o
radiological abnormalities outside the temporal lobe
were reanalyzed. Among such patients, 31 of 108
rat-handed patients with left hemisphere speech
dominance had left temporal radiological abnormalities. One of 12 left-handed patients had a left temporal radiological abnormality (not significant, odds
ratio 0.00-1.70), and 3 of 12 patients with atypical
speech representation had left temporal radiological
abnormalities (not significant, odds ratio 0.13-3.62).
Similar results were obtained when these patients were
divided into subgroups of those whose FSIQ was 85 or
above versus those whose score was less than 85.
These findings are consistent with the impression that
abnormalities restricted to the temporal lobe do not
alter handedness or speech lateralization.
INTELLIGENCE. Although FSIQ scores less than 85
were more frequent in conjunction with left handedness and atypical speech representation in the group
of patients with right hemiparesis (Table l), similar
levels of intelligence were not associated with any
significant variation in handedness, speech representation, or lesion side among nonhemiparetic patients,
even when patients were subdivided on the basis of
radiological results andor lesion side (data not shown).
Among nonhemiparetic patients, the 95% confidence
interval for the odds ratio favoring an association between left handedness and an FSIQ less than 85 was
0.31 to 2.54, and the confidence interval for the odds
ratio favoring an association between atypical speech
and an FSIQ less than 85 was 0.46 to 3.63.
Handedness and Speech Laterulization
Table 7 shows the relationship between handedness
and speech among patients with normal and abnormal
extratemporal radiological studies. Among the group
of patients with abnormal results, left handedness was
associated with a significant increase in atypical speech
lateralization. Furthermore, if the patients with normal
and abnormal radiological studies are combined, the
relationship between left handedness and atypical
speech is highly significant ( p < 0.001, odds ratio
confidence interval 1.87-17.45). This apparent association may be due to a true association between handedness and speech representation, or it may result at
least in part from an association of left handedness with
brain lesions that are more likely to result in atypical
speech representation.
To evaluate this latter possibility, left-handed patients with left-sided lesions and radiological abnormalities outside the temporal lobes were compared to
left-handed patients without extratemporal radiological
abnormalities with regard to speech representation.
Five of 8 patients with left-sided lesions and extratemporal radiological abnormalities had atypical speech,
whereas 3 of 12 patients without extratemporal abnormalities had atypical speech. Although this finding was
not significant, even very high odds ratios in favor of a
relationship between left-sided extratemporal radiological abnormalities and atypical speech among left
handers could not be excluded (odds ratio 0.5152.53). The lack of significance may therefore be due
to the small number of left-handed patients, and it is
possible that the type or degree of brain injury may be
Table 7. Relationship Between Handedness and Speech
in Nonhemiparetic Patients
Results of Extratemporal
Radiological Studies
Abnormal
Left handed
Right handed
Significanceb
Odds ratio (95%
confidence)
Normal
Left handed
Right handed
Significanceb
Odds ratio (95%
confidence)
Speech
Atypical"
6(2)
Left
6
28
5(5)
p = 0.04
0.99-3 1.37
9
3(2)
9(5)
109
NS
0.58-20.23
"Atypical includes right and bilateral speech. Values in parentheses
show bilateral speech only.
bCalculated using Fisher's exact method.
NS = not significant.
a confounding variable in the relationship between
handedness and speech laterahation.
Among patients with normal extratemporal radiological studies, left handedness was not associated with
a significant increase in atypical speech representation,
although odds ratios as high as 20.23 in favor of
such an association cannot be excluded. Table 8 shows
95 % confidence intervals for various handedness and
speech lateralization subgroups among patients with
normal extratemporal radiological studies. Here again,
the possibility that brain injury may act as a confounding variable altering handedness andor speech representation should be kept in mind.
Right Hemisphere Speech Versus Bilateral Speech
Patients with right hemisphere speech were compared
to patients with bilateral speech to determine whether
they differed from one another in terms of hemiparesis, radiological abnormality, intelligence, lesion
side, handedness, or family handedness history. Only
one such relationship was found: among patients with
hemiparesis or abnormal extratemporal radiological
studies, all 10 patients with right hemisphere speech
were left handed, whereas 5 of 11 patients with bilateral speech were left handed ( p = 0.01). No significant differences could be found between patients with
right hemisphere speech and those with bilateral speech
among nonhemiparetic patients with normal extratemp o d radiological studies, regardless of FSIQ andor
lesion side. In all of these cases, the sample sizes were
small, so the lack of a significant association should not
be interpreted as the absence of any association.
To ensure that combining patients with right hemisphere speech and bilateral speech into the single category (atypical speech) did not obscure any significant
Woods et al: Brain Injury and Laterality 515
Table 8. 95% ConfidenceInteruals for the Percentage of
Patients with Normal Extratemporal Radiological Studies Who
Are Left-handed or Who Have Atypical Speech Lateralization
Handedness or
Speech Lateralization
95 % Confidence
Interval
Left handedness
Left handedness in those with
left hemisphere speech
Left handedness in those with
atypical speech
Atypical (bilateral or right)
speech
Atypical speech in right handers
Atypical speech in left handers
5-16
4- 14
5-57
5-16
4-14
5-57
relationships, all of the significance values reported
here were recalculated twice. In the first recalculation,
patients with bilateral speech were excluded, and in
the second recalculation patients with right hemisphere speech were excluded. Although some relationships lost significance in one or both recalculations,
no new significant relationships were identified.
Definition of Left Handedness
To confirm that the lack of association between handedness and speech lateralization among patients with
normal extratemporal radiological studies was not a
result of the definition of left handedness used in this
study (left hand preference for a majority of the 7
handedness inventory criteria), the data for these patients were reanalyzed defining handedness on the
basis of writing hand only. There was no significant
relationship between left handedness and atypical
speech among patients with normal extratemporal
radiological studies (odds ratio 0.4 1- 12.63, regardless
of FSIQ andor lesion side (data not shown). However,
there was a significant relationship between lesion side
and handedness among patients with normal extratemporal radiological studies and FSIQ less than 85: 5
of 17 patients with left-sided lesions were left handed
for writing, whereas 0 of 17 with right-sided lesions
were left handed for writing ( p = 0.04).
Family Hanakdness History
No significant relationship between family handedness
history and handedness or speech lateralitation was
found, regardless of radiological results, intelligence,
andor lesion side. Fifty-five patients had sinistral family histories, 133 had dextral histories, and 20 had unknown family histories. Among patients with normal
extratemporal radiological studies, the 9596 confidence interval for the odds ratio favoring an association between left handedness and a family history of
left handedness was 0.12 to 3.19. The 95% confidence
516 Annals of Neurology Vol 23 No 5 May 1988
interval for the odds ratio favoring an association between atypical speech and a family history of left handedness was 0.40 to 6.84. Of interest, left handers with
a family history of left handedness were more likely to
have atypical speech lateralization than other patients.
Among patients with normal extratemporal radiological studies, 2 of 3 left handers with a family history of
left handedness had atypical speech (both bilateral); 10
of the remaining 121 patients had atypical speech (5
bilateral, 5 right;p = 0.02).
Discussion
The hypothesis that injury to the left brain can result
in pathological left handedness dates back to the early
1900s, when it was proposed to explain the increase in
left handedness found in epileptic patients {2}. More
direct evidence for this hypothesis became available in
the 1950s when Roberts [21} published data showing
that 69% of 7 1 neurosurgical patients with early injury
to the left hemisphere were left handed, while only
11% of 65 patients with early injury to the right hemisphere were left handed (p < 0.001). In the present
study, the patients with left brain lesions associated
with right hemiparesis were all classified as left handed.
Among patients without hemiparesis, those with abnormal extratemporal radiological studies were left
handed significantly more often than patients with normal extratemporal radiological studies, suggesting that
brain abnormality contributes to left handedness in this
population as well.
The possibility that left hemisphere injury associated
with epilepsy might alter speech representation was
first suggested by Broca C22). This hypothesis is supported by the study of Rasmussen and Milner 112)
in epileptic patients selected for amobarbital testing.
They found atypical speech representation in 5596 of
134 patients with early left hemisphere injury, but in
only 16% of 262 patients without evidence of early
left hemisphere injury ( p < 0.001). More recent
amobarbital studies have verified their observations.
Strauss and Wada {14} reported that 7 of 11 patients
with early injuries to the left hemisphere had right
hemisphere speech (those with bilateral speech were
excluded), and none of the 17 patients with early right
or bilateral injuries had right hemisphere speech ( p <
0.001). Ajersch and Milner [l5} reported atypical
speech representation in 13 of 13 patients with right
hemiparesis.
In the current study, 9 of 10 patients with left hemisphere injury sufficient to cause right hemiparesis had
atypical speech representation. Among nonhemiparetic patients with abnormal extratemporal radiological findings, left-sided lesions were associated with
atypical speech representation significantly more often
(10 of 29) than right-sided lesions (1 of 18)( p = 0.03).
Most of the radiological left hemisphere injuries as-
sociated with left handedness or atypical speech representation were fairly extensive. Left hemisphere atrophy or porencephaly were frequent findings. Large
left arteriovenous malformations were also associated
with a shift in handedness or speech, an association
that has been noted previously 1231. Among the patients studied, left hemisphere radiological abnormalities sufficient to exclude speech completely from the
left hemisphere were always associated with left handedness and often with right hemiparesis.
There is less agreement as to whether lesions limited
to the temporal lobes can alter speech lateralization.
Rasmussen and Milner 112) found that lesions sparing
the primary speech zones in the frontal and parietal
regions rarely altered speech lateralization. However,
Rausch and Walsh 1131 suggested that lesions limited
to the temporal lobe may be sufficient to alter speech
representation. They found that 6 of 26 right handers
with left hemisphere epileptic foci had atypical speech
representation, while none of 30 right handers with
right hemisphere foci had atypical speech representation ( p = 0.007). In the present study, no definite
evidence of a relationship between lesion side and
handedness or speech lateralization was found among
patients with normal extratemporal radiological studies, but even moderately hgh odds ratios in favor of
such relationships could not be excluded.
A relationship between left handedness and atypical
speech representation among epileptic patients undergoing neurosurgical evaluation has been demonstrated
in several studies 112-14, 21). In the present study,
nonhemiparetic left-handed patients were significantly
more likely to have atypical speech lateralization than
nonhemiparetic right-handed patients. Within 95%
confidence intervals, the odds of a nonhemiparetic lefthanded patient having atypical speech representation
were somewhere between 1.8 and 17.5 times the odds
of a nonhemiparetic right-handed patient.
There is evidence to suggest that the type of brain
injury may be a confounding variable altering the apparent relationship between handedness and speech
representation. Thus left handedness may be associated with brain injuries that are more likely to result in
atypical speech representation. We found that lefthanded patients with atypical speech were significantly
more likely than left-handed patients with left hemisphere speech to have definite evidence of left hemisphere injury (rght hemiparesis or extratemporal
radiological abnormality with left-sided seizure focus).
Similarly, Rasmussen and Milner 112) found early left
hemisphere injury in 66 of 102 left-handed patients
with atypical speech representation but in only 26 of
112 left-handed patients with left hemisphere speech
representation ( p < 0.001). Although we could not
prove that brain injury contributes to the relationship
between handedness and speech lateralization among
nonhemiparetic patients, we were also unable to exclude a strong contribution from brain injury.
The finding of bilateral speech representation in a
patient with agenesis of the corpus callosum deserves
special comment. It has been suggested that the corpus
callosum mght be involved in the development of
brain lateralization. A major argument against this hypothesis has been the observation that left handedness
is not increased in patients with agenesis of the corpus
cdosum 1247. This is the third reported patient with
callosal agenesis in whom amobarbital speech testing
has been reported. The first patient had unilateral
speech representation, but it was not specified whether
speech was unilateral on the left or on the right 1251.
The second patient, reported by Gott and Saul 1261,
had bilateral speech representation. Given that two of
three patients with agenesis of the corpus callosum
have bilateral speech representation, the hypothesis
that the corpus callosum plays a role in the development of speech lateralization may warrant further consideration.
Extrapohtion to Normal Subjects
Unfortunately, amobarbital testing is so invasive that it
is performed only in patients who have lateralized
brain abnormalities amenable to surgical intervention.
The data discussed above indicate that it is clearly important to exclude patients with lateralized brain injuries that might alter speech or handedness before
extrapolating results from amobarbital testing to the
normal population. This is particularly important when
considering the relationship between handedness and
speech lateralization because the magnitude of this relationship can be distorted if some brain injuries are
more likely to alter handedness and speech than
others. We were unable to demonstrate a relationship
between handedness and speech lateralization after excluding patients with hemiparesis or radiological evidence of brain injury outside the temporal lobes.
However, it is clear from the 95% confidence intervals
in Tables 7 and 8 that it is not possible to rule out such
a relationship. We did find that left-handed patients
with a family history of left handedness demonstrated a
significantly increased incidence of atypical speech lateralization.
Supported in part by NIH grant NS 171 1 1 awarded by the National
Institute of Neurological and Communicative Disorders and Stroke.
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