Handedness Language

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Brain (2000), 123, 2512–2518

Handedness and hemispheric language dominance


in healthy humans
S. Knecht, B. Dräger, M. Deppe, L. Bobe, H. Lohmann, A. Flöel, E.-B. Ringelstein and
H. Henningsen

Department of Neurology, University of Münster, Germany Correspondence to: Stefan Knecht, MD, Department of
Neurology, University of Münster, Albert-Schweitzer-Strasse
33, D-48129 Münster, Germany
E-mail: knecht@uni-muenster.de

Summary
In most people the left hemisphere of the brain is was found to increase linearly with the degree of left-
dominant for language. Because of the increased incidence handedness, from 4% in strong right-handers (handedness
of atypical right-hemispheric language in left-handed ⍧ 100) to 15% in ambidextrous individuals and 27% in
neurological patients, a systematic association between strong left-handers (handedness ⍧ –100). The relation-
handedness and dominance has long been suspected. To ship could be approximated by the formula: likelihood
clarify the relationship between handedness and language of right-hemisphere language dominance (%) ⍧ 15% –
dominance in healthy subjects, we measured lateralization handedness (%)/10. These results clearly demonstrate
directly by functional transcranial Doppler sonography that the relationship between handedness and language
in 326 healthy individuals using a word-generation task. dominance is not an artefact of cerebral pathology but a
The incidence of right-hemisphere language dominance natural phenomenon.

Keywords: language lateralization; hemispheric dominance; handedness; functional Doppler ultrasonography

Abbreviations: ANOVA ⫽ analysis of variance; fMRI ⫽ functional MRI ; fTCD ⫽ functional transcranial Doppler
ultrasonography

Introduction
Language is lateralized to the left hemisphere of the brain rests almost exclusively on studies of neurological patients.
but can occasionally also be found in the right hemisphere In this population, however, there is an increased incidence
(Knecht et al., 2000). This variability indicates the high of pathological left-handedness and right language
degree of freedom with which the brain can instantiate dominance, as the control of both dexterity and language
language. Factors associated with lateralization inform us can shift to the right hemisphere after long-standing left-
about limitation to this freedom and may also be important hemisphere lesions (Rasmussen and Milner, 1977; Vargha-
limitations in the recovery from aphasia after stroke by Khadem et al., 1985; Woods et al., 1988; Loring et al.,
recruitment of the intact hemisphere. One factor which has 1990). Evidence from patients with brain lesions of sudden
been associated with language dominance is handedness. onset, such as stroke, provide some indirect evidence about
Since the description of left-hemisphere language regions the status of right-hemisphere language dominance in healthy
in right-handed patients by Paul Broca in the 19th century, subjects. These studies are based on relatively small numbers
it has been speculated that the reverse, i.e. right-hemisphere of atypical aphasias, as in left-handers with right-hemisphere
language dominance, should be true of left-handers. This stroke. Furthermore, patients who present with language
claim has been widely accepted as the ‘Broca rule’, although disturbances after right-sided cerebral infarction have not
Broca never explicitly postulated such a rule (Harris, 1993). infrequently had strokes in the other hemisphere, rendering
Luria was among the first to point out that such an association conjectures on the original hemisphere of language dominance
could not be universally true because even in left-handers unreliable (Pedersen et al., 1995). As a consequence, studies
aphasia usually occurs after a lesion to the left hemisphere of the incidence of aphasia after stroke in relation to
(Luria, 1976). Even now, our knowledge about the suspected handedness have provided widely diverging results. Two
association between handedness and language dominance groups reported an increased incidence of language deficits
© Oxford University Press 2000
Handedness and language dominance 2513

Table 1 Rate of right-hemisphere dominance in relation to parental left-handedness


Handedness of subject

–75 or lower Between 75 or higher


(strong left-handers) –76 and 75 (strong right-handers)

⫹ ⫺ ⫹ ⫺ ⫹ ⫺

Parental left-handedness
n 14 43 13 88 10 145

Degree of handedness, –100 –100 –60 –10 100 100


median (quartiles) (–100, –90) (–100, –90) (–60, 50) (–52, 42) (100, 100) (89, 100)

Right-hemisphere language 29 23 15 17 10 4
dominance (%)

in left- or non-right-handers after right-hemisphere stroke not offered any financial reimbursement. Subjects were
(Gloning, 1977; Basso et al., 1990). Another group found no interviewed about the handedness of their parents. Possible
such increase and suggested a negligible role of the right answers were ‘right’, ‘left’ and ‘unknown’. Subjects were
hemisphere in speech function in most left-handers who do excluded if information from a standardized questionnaire
not have early left-hemisphere damage (Kimura, 1983). suggested the possibility of any neurological disorder,
A new, very efficient perfusion-sensitive technique has particularly perinatal asphyxia or kernicterus, head trauma,
made it possible to clarify the association between handedness loss of consciousness, epileptic seizures, meningitis or
and language dominance in healthy subjects in a encephalitis, or delayed or disturbed language development.
representative and quantitative way. This technique is Subjects were also excluded if they had failed to complete
functional transcranial Doppler ultrasonography (fTCD), and the equivalent of high school (Realschule or Gymnasium).
is based on the same physiological principles as functional Additionally, ~3% of subjects had to be excluded because
MRI (fMRI) (Deppe et al., 2000). It has allowed us to fTCD could not be performed, due to inadequate sonographic
measure the lateralization of language in a validated and penetration of the skull. A total of 326 subjects were thus
highly reproducible way in a total of 188 healthy subjects included in the study: 198 females (age range 15–49 years,
and to control adequate cooperation in every case (Knecht mean 26, SD 5.1) and 128 males (age range 19–46 years,
et al., 1998a, b). We have also employed this technique to mean 26, SD 4.6). All subjects gave informed consent to
assess the variability of language lateralization with respect participation in the study, which was approved by the ethics
to gender in healthy subjects (Knecht et al., 2000). Like committee of the University of Münster. Handedness was
other researchers in the field, we had to confine our study to assessed by the Edinburgh Inventory (Oldfield, 1971), which
moderate and strong right-handers because we lacked ranges from –100 for strong left-handedness to ⫹100 for
sufficient left handers for a representative analysis (Frost strong right-handedness. Individuals were assigned to one of
et al., 1999; Springer et al., 1999). Thus, we had not seven categories of handedness, which are shown in Fig. 3.
been able to evaluate the role of handedness in language Hemispheric language dominance was determined, as in
lateralization (as had been suggested by an anonymous previous studies, by fTCD using a word generation task
reviewer). For the present study, we recruited more than 100 validated by direct comparison with intracarotid amobarbital
left-handed healthy subjects in addition to those reported in injection and fMRI and tested for reproducibility (Knecht
the previous study in order to answer the following questions: et al., 1996, 1997, 1998a, b; Deppe et al., 1997, 1998).
(i) can we confirm an association of language lateralization Details of the procedure are shown in Fig. 1.
and handedness in healthy subjects? (ii) Can we quantify
this relationship? (iii) Can we make predictions about the
basis of language lateralization? Results
The distribution of hemispheric language dominance varied
with the degree of handedness [P ⬍ 0.0001 by analysis of
Methods variance (ANOVA)] (Fig. 2).The more right-handed the
The work was part of the Münster functional imaging study subjects were, the lower was the relative incidence of right-
on the variability of hemispheric specialization in health and hemisphere language dominance, and vice versa (Fig. 3).
disease (Deppe et al., 1997, 2000; Knecht et al., 1998a, b, Overall, strong left-handers demonstrated a nearly sevenfold
2000). Healthy volunteers were recruited by newspaper higher incidence of right-hemisphere language dominance
advertisement. The advertisement was intended to address than strong right-handers. In extreme left-handers the
especially subjects with non-right-handedness. They were incidence of right-hemisphere language dominance was 27%,
2514 S. Knecht et al.

Fig. 1 Schematic illustration of the fTCD procedure in a single subject. For comparison, an fMRI of the
same subject during an identical language task is shown (upper left). The fMRI analysis was performed
by statistical parametric mapping, using software from the Wellcome Department of Cognitive
Neurology, London, UK. fTCD measures the modulation of the cerebral blood flow velocity (CBFV) in
the middle cerebral arteries (MCAs) at a depth of 50 mm during word generation. This allows the
assessment of activity-related perfusion changes in the vascular territories of the left (red) and right
(green) MCAs. These territories comprise potential language areas (van der Zwan et al., 1993). After a
cueing tone (Cue), a letter (Letter) is presented on a computer screen and the subject has to find silently
as many words as possible that start with the displayed letter. Task performance is controlled by having
the subject report the words (Speaking) after a second auditory signal, presented 15 s after presentation
of the letter. The averaging procedure used for fTCD is depicted schematically below. CBFV changes in
both MCAs during single runs (1 to n) of the language task are collected and averaged (usually a total
of 20 runs). Subtraction of averaged CBFV changes in the right and the left MCA provides a measure
of the mean interhemispheric difference in CBFV. The mean interhemispheric CBFV difference curve is
time-locked to fixed events during the task. Calculation of the laterality index during word generation
(LI) is based on the maximal left–right difference during word generation. The LI is highly reproducible
and is proportional to lateralization, as assessed by fMRI and the Wada test (Deppe et al., 1997, 1998,
2000; Knecht et al., 1998a, b). Positive indices represent left-hemisphere language dominance; negative
indices represent right-hemisphere language dominance. In this subject, a positive value indicates left-
hemisphere lateralization for word generation.
Handedness and language dominance 2515

whereas in extreme right-handers it was 4%. The incidences Degree of language lateralization
in the five intermediate groups were 27, 22, 11, 10 and 6%, In addition to the correlation between language lateralization
respectively (Fig. 3). The rate of right-hemisphere language and handedness, a two-way interaction between the absolute
dominance can be approximated on the lowest order by the degree of language lateralization and the direction of
formula: likelihood of right-hemisphere language dominance handedness was found, i.e. subjects in whom the side of
(%) ⫽ 15% – handedness by the Edinburgh Inventory (%)/10. language dominance was the same as the side of dominance
in the control of dexterity had stronger lateralization than
those in whom these factors were dissociated: right-handers
Gender analysis with left language dominance and non-right-handers with
ANOVA on the single and combined influences of gender right language dominance displayed stronger overall
and handedness on language dominance showed no significant lateralization than right-handers with right language
effect of gender (P ⫽ 0.42 and P ⫽ 0.29, respectively). dominance and non-right-handers with left language
dominance (ANOVA, P ⫽ 0.04) (Fig. 4). Use of the
Kolmogorov–Smirnov test did not detect significant
differences in the absolute degree of language lateralization
Analysis of familial handedness between right-handers with right language dominance and
As Table 1 shows, there was a trend for subjects with a
non-right-handers (handedness ⬍30) with left language
family history of left-handedness to have a higher incidence
dominance (P ⬎ 0.1). Also, no significant difference was
of right-hemisphere language dominance. ANOVA on the
detected between right-handers with left language dominance
single and combined influences of familial handedness and
and non-right-handers (handedness ⬍30) with right language
handedness on language dominance was limited by the small
dominance (P ⬎ 0.1).
subgroups and the skewed distribution of handedness (U-
shaped) and language dominance (bimodal). The single
influence of familial handedness and the combined influence
of familial handedness and handedness on language Discussion
dominance did not reach significance (P ⫽ 0.7 and P ⫽ 0.9, This is the first study to show that in healthy subjects there
respectively). Familial handedness only showed a significant is a consistent and almost linear relationship between the
effect on handedness (P ⫽ 0.006). degree of handedness and the direction of language
dominance.
The relationship between handedness and language
dominance has been addressed by Pujol and colleagues (Pujol
et al., 1999). Using a word generation task similar to ours,
they performed a two-slice fMRI examination focusing on
Broca’s speech area in 100 healthy volunteers. They found
frequent participation of the right Broca’s homologue in left-
handers. Our results confirm this finding. Additionally, they
show that the incidence of right language dominance depends
not only on the direction but also on the degree of handedness.
This relationship is consistent and linear. The present findings
also extend our own previous results on the variability of
language lateralization in moderate and strong right-handers
(Knecht et al., 2000). In this group, we had found a 7%
incidence of right-hemisphere language dominance. From the
present sample, almost twice the size of the earlier sample,
it is apparent that in strong right handers, i.e. those with a
handedness index of 100 according to the Edinburgh
Inventory, the incidence of right-hemisphere language
dominance drops to ~4%. In their series of patients with
Fig. 2 Three-dimensional frequency histogram demonstrating the
number of subjects (z-axis) with a given degree of handedness medically intractable seizures, Rasmussen and Milner
(y-axis) and language lateralization, as determined by fTCD categorized handedness as either (i) right or (ii) left or mixed.
(x-axis), in a total of 326 healthy subjects, comprising 198 Among patients without clinical evidence of early damage
females (age range 15–49 years, mean 26, SD 5.5) and 128 to the left hemisphere, they reported right speech lateralization
males (age range 19–46 years, mean 26, SD 4.6). These subjects by the amobarbital procedure in 4% of right-handers and in
include those reported in a preceding paper (Knecht et al., 2000).
Handedness was assessed by the Edinburgh Inventory 15% of left- or mixed-handers (Rasmussen and Milner, 1977).
(Oldfield, 1971) (positive values indicate relative right- Because these data were drawn from a pathological cohort,
handedness and negative values indicate relative left-handedness). it remained unclear from this series whether the relationship
2516 S. Knecht et al.

Handedness –99 or less more than –99; more than –75; more than –25; more than 25; more than 75; more than 99
–75 or less –25 or less 25 or less 75 or less 99 or less

n 37 26 50 18 40 48 107
Right dominance (%) 27 27 22 11 10 6 4

Fig. 3 Relationship between the degree of handedness by the Edinburgh Inventory (x-axis) and the incidence of right-hemisphere
language dominance (y-axis). Bin width for each subgroup is represented by dotted horizontal lines. Error bars, represented by vertical
lines, are based on the formula:


(100 – P) P
σ⫽
n
The relationship between the rate of right-hemisphere dominance and handedness can be approximated by the formula: likelihood of
right language dominance (%) ⫽ 15% – handedness (%)/10. Specific information on the subgroups [width of handedness categories by
the Edinburgh Inventory; number of subjects per category (n) and percent right dominance] is given in the table below the graph.

Table 1 Rate of right-hemisphere dominance in relation to parental left-handedness


Handedness of subject

–75 or lower Between 75 or higher


(strong left-handers) –76 and 75 (strong right-handers)

⫹ ⫺ ⫹ ⫺ ⫹ ⫺

Parental left-handedness
n 14 43 13 88 10 145

Degree of handedness, –100 –100 –60 –10 100 100


median (quartiles) (–100, –90) (–100, –90) (–60, 50) (–52, 42) (100, 100) (89, 100)

Right-hemisphere language 29 23 15 17 10 4
dominance (%)

between handedness and dominance was a natural a linear relationship between the degree of handedness and
phenomenon. Furthermore, because handedness had been the incidence of right-hemisphere dominance for language.
collapsed into only two categories, the data do not indicate Although fTCD has a low spatial resolution, it constitutes
whether the observed relationship between handedness and a very practical tool to determine functional lateralization in
language dominance was categorical or linear. Overall, the a large number of subjects. We used a strictly mathematical
tendency reported by Rasmussen and Milner is in accord distinction between right- and left-hemisphere language
with our data. However, the incidence of right-hemisphere dominance. This approach constitutes a gross simplification
dominance for language was considerably higher in our of the neural basis of language, but allowed us to focus on
strongly left-handed healthy subjects (27%) than in the the relationship of handedness with language lateralization.
group of left- or mixed-handed epilepsy patients from the A left-hemisphere fTCD lateralization index does not exclude
Rasmussen and Milner series (15%). This agrees well with involvement of the right hemisphere; it only demonstrates a
Handedness and language dominance 2517

relationship to each other, such that individuals classified as


left- or right-handers by one method are classified in the
same way by other methods (Corballis, 1997). Differences
in the grading system for handedness may bear on the shape
of the correlation with language dominance, but there is
little to suggest that this relationship would change in
a fundamental way if a different measure of handedness
were used.
The present study demonstrates that left-handedness is
neither a precondition nor a necessary consequence of right-
hemisphere language dominance. However, left-handedness
increases the likelihood of right-hemisphere language
dominance. Furthermore, left-handedness in either parent
may have an additional effect on the likelihood of right-
hemisphere language dominance (Table 2). The degree of
handedness is linearly and highly significantly related to the
side of language dominance. Mathematically, this relationship
Fig. 4 Two-way interaction between the absolute degree of
language lateralization for left and right language dominance (and involves two variables and can be approximated by the
standard deviations) in right-handers (handedness ⬎30 by the following formula: likelihood of right language dominance
Edinburgh Inventory, circles) and non-right-handers (handedness (%) ⫽ 15% – handedness (%)/10. In biological terms, such
艋30 by the Edinburgh handedness inventory, asterisks). a relationship is difficult to explain by a single causative
factor. A more plausible explanation would be that handedness
relatively large increase in perfusion during word generation and language dominance are each determined by multiple
by the left hemisphere. This mathematical distinction was factors, some of which have a role in both phenomena. Such
chosen to exclude the bias which is always involved when multiple and partly overlapping factors could produce (i) a
defining ‘bilateral’ language lateralization (Risse et al., 1997). threshold effect accounting for the 4% incidence of right-
A more ‘bilateral’ lateralization, i.e. a lower degree of hemisphere language dominance in extreme right-handers,
lateralization, was found in subjects in whom dominance of and (ii) a modifier effect accounting for the increase in
manual control (handedness) and dominance of language did incidence of right dominance along with the increase in left-
not fall into the same hemisphere (Fig. 4). This finding may handedness. The present study provides a framework for the
explain why in a large series of patients those with atypical investigation of these factors. For example, assessment of
lateralization for handedness seemed to have slightly less the inheritance of language dominance by functional imaging
severe aphasia than patients with typical handedness (Basso may shed more light on the genetic underpinnings of
et al., 1990). functional asymmetry in the human brain.
Although word generation is a frequently used activation
task and constitutes an essential feature in the production of
language, it is only one of the multiple dimensions of
language (Cuenod et al., 1995; Hertz-Pannier et al., 1997; Acknowledgements
Benson et al., 1999). Other aspects of language, such as We wish to thank Drs F. Stögbauer and I. Jacobi for their
prosody, were not tested in our study, and could therefore comments and helpful discussions. We also wish to thank
show a different relationship with handedness. Professor Dr W. L. Heindel and Dr K. Papke of the
For handedness, a genetic basis is established but does not Department of Radiology at Münster for their cooperation in
fit a simple Mendelian model (Carter-Saltzman, 1980). This performing fMRI. One of these scans was used to illustrate
suggests a role for complex genetic or non-genetic factors in fTCD. This work was supported by the Nachwuchsgruppen-
the formation of the phenotype (McManus, 1991; Annett, Förderung (S.K.: 2000-2005) and the Bennigsen-Foerder-
1996). We assessed handedness with the Edinburgh Inventory. Preis of Nordrhein-Westfalen (IVA 6-400 302 97), the
This is a preference-based measure and shows a J-shaped Innovative Medizinische Forschung of the Medical Faculty
distribution of handedness in the general population. It differs at Münster (Kn-1-1-II/96-34 and KN 3 2 98 01) and the
from the more bell-shaped distribution found by skill-based Deutsche Forschungsgemeinschaft (Kn 285/4-1 and Kn 285/
measures, and it is susceptible to a cultural bias (Corballis, 6-1). Preliminary results of this study were presented at the
1997). Because of its good test–retest reliability, the conference ‘The Science of Aphasia’, September 8–13, 2000.
Edinburgh Inventory has been used in many studies and,
unlike other measures, allows good comparison between
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