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Anatomical left-right asymmetry of language-related temporal cortex is different in left- and right-handers.

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Anatomical Left-Rght Asymmetry of
Language-related 1emporal cortex Is
Dfierent in Left- and fight-HandeIrs
~
T
1
1 -
1
Helmuth Steinmetz, MD," Jens Volkmann," Lutz Jancke, PhD,t and Hans-Joachim Freund, MD"
Asymmetry of the planum temporale, a language-related intrasylvian area on the superior temporal gyrus, is the most
remarkable anatomical left-right asymmetry of the human brain. The in vivo application of magnetic resonance
morphometry in 52 healthy volunteers (26 dextrals and 26 sinistrals) revealed that planum temporale asymmetry is
correlated with hand dominance. Left-handers had a significantly lesser degree of leftward planum temporale asymmetry than right-handers. Thus, a structural-functional relation exists in cerebral asymmetry. The correlation is likely to
reflect language representation. Because familial sinistrality influenced the anatomical pattern in left-handers and
planum temporale asymmetry is already present in the newborn, prenatal factors must play an important role in the
development of functional laterality.
Steinmetz H, Volkmann J, Jhcke L, Freund H-J. Anatomical left-right asymmetry of language-related temporal
cortex is different in left- and right-handers. Ann Neurol 1991;29:315-319
Until now, inferior parietal arteriographic asymmetry
has been the only proven anatomical correlate of functional laterality [l, 2). O n the opposite bank of the
sylvian fissure lies the planum temporale (F'T), which
is located on the upper surface of the temporal lobe
and posterior to the anterior transverse gyrus of Heschl
13, 41. On the language-dominant left hemisphere, the
PT thus coincides with the core of the classic posterior
speech region of Wernicke [5}. Taking together several postmortem studies [3, 6-17), the area of the left
PT was larger than its right counterpart in 73.5% of
532 adult brains. Mainly based on these findings, F T
asymmetry has been assumed to be a substrate of language Literalization { S , 18-21). No direct evidence for
this hypothesis has been obtained because morphometry of the PT has only been possible postmortem. We
have recently shown the validity and reliability of highresolution magnetic resonance (MR) morphometry of
the I
T 1173, a noninvasive, in vivo technique used
in this study to correlate anatomical with behavioral
measures.
According to the incidence of aphasia after unilateral
cerebral lesions [22, 231, sodium amobarbital injection
into the carotid arteries 1241, or unilateral electroconvulsive therapy [ 2 5 ] , 25 to 85% of the sinistral population have an anomalous, that is, bilateral or right functional representation of language. This figure is at least
10-fold higher than in dextrals [22, 26-28). Familial
From the Departments of 'Neurology, and ?Psychobiology and Psychocybernetics, Heinrich-Heine University, Diisseldarf, Germany.
Received Jul 12, 1990. Accepted for publication Sep 13, 1990.
sinistrality increases the incidence of bilateral o r right
language dominance, especially in left-handers 1271.
Therefore, different patterns of PT asymmetry were to
be expected in 2 handedness groups if PT asymmetry
was related to language lateralization.
Materials and Methods
Pvobands and Handedness Measurements
Fifty-two healthy volunteers were examined. Twenty-six volunteers were self-described sinistrals (mean age, 26.4 years),
and 26 were self-described dextrals (mean age, 24.9 years),
with a maleifemale ratio of 1 in both groups. All subjects
gave informed consent and were questioned on sinistral relatives. Handedness was assessed by each subject's motor
performance with the right (R) and left (L) hand. The tests
included (1) a measurement of the maximal index fingertapping rate over 20 seconds, and (2) a paper-and-pencil
hand-dominance test (HDT)(301 with 3 dexterity tasks (tracing lines, dotting circles, and tapping on squares),each to be
performed with maximal speed and precision over 15 seconds. Larerality coefficients (R - L)/(R + L) were determined for each test and rounded off to one decimal point.
Negative values indicated left-handedness and positive values, right-handedness.
In Vivo M R Morphomety
MR imaging was performed using a 1.5 T superconductive
magnet and a circularly polarized head coil. After parallel
alignment of the interhemispheric plane of the brain with the
Address correspondence to Dr Steinmetz, Department of Neurology, University Clinic, Heinrich-Heine University, Moorenstr 5 ,
D-4000 Dusseldorf I, Germany.
Copyright 0 1991 by the American Neurological Association
3 15
Fig 1. (A-D) Magnetic resonance (MR) morphometv ofthe entire
convolutional sayface of the human planum temporale vast, lowangle shot iMR sequence). A-D are noncontigu0u.r sagittal dices
of 1.17 mm thickness photographed from the monitor o f a total of
128 c0ntiguou.r .rections obtainedfor each brain; order from medial
to lateral, anterior is on the left. On A-D, the lejit arrows mark
the bottom of Hescbl’s sulcus, that is, the anterior border of the
planum temporale. The o r a l elevation immediateh anterior t o
this sulcus is Heschls- orus, which is usually prominent on medial
sections (A, B) and flattens lateral& (D).Right arrows mark the
pnrterior border G f the planum {see text for the anatomical dejnition). Note the excellent gray matter-uhite matter contrasts,
which allow a cursor to be traced within the supratemporal cortex
for length detemzination of the cuwed gyral outlines ofthe planum
temporale between the arrou2s.
316 Annals of Neurology Vol 2‘) No 3 March 1991
sagittal plane of imaging, a strongly T1-weighted gradient
echo pulse sequence (fast, low-angle shot; Fig 1) was applied.
For all MR examinations, the technical factors were 40-msec
repetition time, 5-msec echo time, 40-degree flip angle, 1
excitation, 25-cm field of view, 15-cm thickness of the excited volume, 128 partitions, and 256 x 256-image matrix.
This resulted in 128 contiguous slices with a thickness of
1.17 mm and a pixel size of 1 x 1 mm. Morphometric
evaluation of the PT was performed on an image-processing
workstation by a “blinded” observer (H.S.). The following
method was used (see Fig 1):The sagittal slice containing the
retroinsular origin of the anterior transverse gyrus of Heschl
was identified {17, 31). Progressing laterally, the length of
DiJferent Patterns of Planum Temporale Asymmetry in 2 Hanu'tdness Group5
Handedness criteriona
Self description
n
RH
LH
RHRH+
LHTapping
LH+
RH
LH
RHRH+
LHLH
RH
LH
RHRH +
LH LH +
+
HDT
p (two-sided)'
Mean 6pT (SD)b
26
26
18
8
15
11
27
22
18
9
12
10
29
20
18
11
12
8
-0.347
-0.223
-0.357
-0.325
-0.266
-0.164
-0.374
-0.193
-0.388
-0.345
-0.246
-0.130
- 0.359
-0.174
-0.357
-0.363
-0.252
-0.029
(0.330)}
(0.274)
(0.314)
(0.386)
(0.283)}
(0.263)
(0.291)
(0.287)
(0.257)]
(0.366)
(0.315ij
(0.251)
(0.315 ) ]
(0.276)
(0.314)}
(0.332)
(0.281)]
(0.214)
NS
I
NS
NS
0.023
NS
NS
0.012
NS
0.045
"Differentmethods were used to assess handedness: self description, index finger-tapping rate, and hand-dominance test (HDT).Note that the
different handedness criteria produced different numbers (n) of RII and LH in the same population of 52 probands. Three subjects showed
no hand-motor lateralization o n tapping or HDT.
bAnatomical asymmetry coefficient 6PT 1161. A negative 6FT indicates leftward PT asymmetry.
'Mann-Whitney U test comparing 6pT between handedness groups and between subgroups of RII and LH with or without familial sinistrality.
p values less than 0.05 were considered significant.
RH = right-handers;LH = left-handers;RH +, LH + = subgroups of R H or LH with at least cine left-handed first-degree relative; R H - ,
LH - = subgroups of RH or LH without a left-handed first-degree relative; SD = standard deviation; NS
not significant.
~
the PT was determined on each subsequent scan by tracing
a cursor manually within the gray matter of the posterior
supratemporal plane from the anterior to the posterior borT.Length measurements on single slices were
der of the I
automatically summed with those from the previous sections
and multiplied with the slice thickness (equals total surface
area). With this method, the entire convoluted cortical surface of the PT was measured, because the cursor followed
all gyral and sulcal contours, thereby correcting for individual
variability of cortical folding [31}.The anterior border of the
PT was defined as the bottom of Heschl's sulcus, that is, the
sulcus lying behind the anterior transverse gyrus as identified
by Pfeifer's criterion of retroinsular commencement [4, 17,
3 11. The posterior border of the PTwas defined as the posterior end of the supratemporal plane, that is, the point of
transition of the posterior descending ramus of the sylvian
fissure into the posterior ascending ramus of the sylvian fissure. Thus, all cortex buried in the posterior descending
ramus was included with the PT.Cortex buried in the posterior ascending ramus was excluded from the PT.The lateral
border of the F T was defined as the lateral rim of the supratemporal plane. The medial border was defined as the retroinsular point where the anterior and posterior borders of the
PT coincide. In subjects in whom the anterior border of the
PT (Heschl's sulcus) did not continue up to the lateral border, a straight subsidiary line was used to complcte the anterior border laterally. This subsidiary line started from the
lateral end point of Heschl's sulcus and ran perpendicularly
to the midsagittal plane {31). Left-right asymmetry of the PT
surface area was expressed as the asymmetry coefficient 6pT
= (R - LVC0.5 (R + L)] with R and L being the surface
areas of the right and left planum temporale [16]. Negative
values indicate leftward asymmetry, and positive values indicate rightward asymmetry.
Statistical Analysis
Because it was unknown whether the data fulfilled thc assumptions for parametric statistical procedures, distributionfree statistical methods were applied [32).For the anatomical
comparison of left- and right-handers, the Mann-Whitney U
test was used. A level of 5% was accepted as the level of
significance.
Results
The mean degree of leftward anatomical lateralitation
was less in left-handers compared with right-handers.
The anatomical difference was significant only for
hand-motor lateralization, not for stated handedness
(Table). Familial sinistrality was a factor in left-handers,
in whom those with at least 1 left-handed first-degree
relative explained most of the overall anatomical difference between handedness groups (see Table; Figs 2,
3). No correlations were found between the strength
of hand-motor lateralization (tapping or HDT scores)
and the degree of anatomical left-right asymmetry
(SPT).
Discussion
Reduced functional asymmetry for language is well
known in left-handers 122-25, 291. The present study
demonstrates reduced anatomical asymmetry of language-related temporal cortex in left-handers as well.
Steinmctz et al: Left-Right Asymmetries
317
m Rn+
0RH2
0
.-0
s*
.
I
-
0
6
2
m LH+
0LH-
8 1
7 -
- 6
I
1
(D
c
0
0
6 5 4 -
5 -
.-n
3
*
4 -
0
2 -
z6
1 -
3 -
-
v-
3 2 -
1-n I
-1
-0.8
n n m
-0.6 -0.4
-0.2
0
0.2
0.4
-1
Asymmetry coefficient
F i g 2. Uistribiition of anatomical asymmetry coe/ficients 6PT in
Tight-banders without (RH -) and with (RH +) sinistrality
among $nt-degree relatiz?es.Almost nowml distributions are seen
in both subgroups. A manual dexterity task was used to de&
handedness ( H D T , see text).
It is likely that the anatomical difference between the
handedness groups is related to their different patterns
of language organization.
Until now, the assumption that left-right asymmetry
of the F'T underlies language lateralization was based
on the following findings: (1) O n average, 73.S% of
randomly selected adult cadaver brains showed leftward asymmetry of the PT {3, 6-17}, (2) the left PT
is centered in the classic posterior speech region of
Wernicke [ j } , (3) gross asymmetry of the l
T correlated with cytoarchitectonic asymmetry of auditory association areas thought to play a role in language processing {3, 201, ( 4 ) positron emission tomography
demonstrated a left-lateralized increase in glucose metabolism or cerebral blood flow of the region of the
left PT on verbal auditory stimulation 133, 341, ( 5 )
phylogenetically, PT asymmetry first appears in the
higher primates, suggesting a relation with the evolution of language {35]. The present demonstration of
a correlation between PT asymmetry and handedness
provides the first experimental support for this biological theory of human laterality.
That familial sinistrality inff uenced the anatomical
pattern in left-handers also agrees with this theory. Familid sinistrality has been shown to produce a right
hemisphere shift of language representation, especially
in left-handers {29}.
Of course, the 73.5973 incidence of leftward PT
asymmetry observed in unselected samples is far below
the expected frequency of left hemisphere language
dominance in the normal population (> 95%). All
quantitative data on language organization in left- and
right-handers {22-291, however, were derived from
studies on the incidence of aphasia emphasizing disturbances of speech output 1367. Other aphasiologic data
[37), as well as split-brain 138-40) and hemispherectomy studies [41-431, suggest that speech perception
318 Annals of Neurology Vol 29 No 3 March 1991
-0.8 -0.6 -0.4
-0.2
0.2
0
0.4
Asymmetry coefficient
Fig 3. Distvibution of anatomical asymmetry coefficients6PT in
left-handers .without (LH -1 and with ILH 1 sinistrulity
among .first-degreerelatives. Compared with the right-handers of
Figure 2, the distribution in LH - is sh$ed slightly toward
is narrower
anatomical symmetry. The distribution in LH
and cepltered around SPT = 0. A manual dexterity task was
used to define handedness (HD?', see text).
+
+
is much less lateralized than speech production, even in
right-handers. Because the PT is covered by secondary
auditory and auditory association cortex {20, 441, F T
asymmetry is likely to reflect a perceptive dimension
of language dominance. This also helps to explain why
there was no subgroup of left-handers, in the present
study, showing reverse anatomical asymmetry, as
would have been expected from classic functional data
~41.
Gross left-right asymmetry of the PT has been
shown to correlate with cytoarchitectonic asymmetry
of auditory association area Tpt of Galaburda and colleagues {20), which is mainly located on the posterolateral portion of the FT. This suggests that in vivo MR
morphometry detects a true asymmetry of languagerelated cortex. The noninvasive MR method might
therefore contribute to the presurgical evaluation of
language dominance.
Asymmetry of the PT appears in the human fetus
between the 29th and 32st gestational week [S, 451,
that is, it precedes language learning. Thus, the present
demonstration of a relation between anatomical and
functional latetaliration emphasizes the importance of
prenatal factors for the development of hemisphere
specialization. Apart from its clinical implications, in
vivo MR morphometry constitutes a new method of
studying the influence of genetic or humoral factors in
the determination of human brain laterality.
This study was supported by grants from the Deutsche Forschungsgemeinschaft (SFB 200/22).
We thank Prof Dr Armin Thron, Head of the Department of Neuroradiology, Rheinisch-Westfahsche Technische Hochschule Aachm,
for providing us rime in their magnetic resonance facility.
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319
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