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Dorsal Forebrain Anomaly in Williams Syndrome
Albert M. Galaburda, MD;
J. Eric Schmitt, BS;
Scott W. Atlas, MD;
Stephan Eliez, MD;
Ursula Bellugi, EdD;
Allan L. Reiss, MD
Arch Neurol. 2001;58:1865-1869.
ABSTRACT
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Background Williams syndrome (WMS) is a rare neurogenetic
condition with a behavioral phenotype that suggests a dorsal and/or
ventral developmental dissociation, with deficits in dorsal but not the
ventral hemispheric visual stream. A shortened extent of the dorsal
central sulcus has been observed in autopsy specimens.
Objective To compare gross anatomical features between the
dorsal and ventral portions of the cerebral hemispheres by examining
the dorsal extent of the central sulcus in brain magnetic resonance
images from a sample of subjects with WMS and age- and sex-matched
control subjects.
Subjects Twenty-one subjects having clinically and
genetically diagnosed WMS (mean ± SD age,
28.9 ± 7.9 years) were compared with 21 age- and sex-matched typically developing controls (mean ± SD
age, 28.8 ± 7.9 years).
Design High-resolution structural magnetic resonance images
were acquired. The extent of the central sulcus was qualitatively
assessed via surface projections of the cerebral cortex.
Results The dorsal central sulcus is less likely to
reach the interhemispheric fissure in subjects with WMS than in
controls for both left (P<.001,
 2 = 15.79) and right (P<.001,
2 = 12.95) hemispheres. No differences
between the groups were found in the ventral extent of the central
sulcus.
Conclusions Anomalies in the dorsal region in patients with
WMS are indicative of early neurodevelopmental problems affecting the
development of the dorsal forebrain and are most likely related to the
deficits in visuospatial ability and behavioral timing often observed
in this condition.
INTRODUCTION
EVEN BEFORE Gall and Spurzheim, Luigi Rolando, professor of anatomy in Sardinia after
whom the central sulcus is named, called attention to the relationship
between cortical folding and function in the human brain.1
In this article we compare the fissure of Rolando in Williams syndrome
(WMS) and control brains with the goal of better understanding the
neural basis of abnormal cognitive function in WMS. Williams syndrome
is a mental retardation syndrome associated with a hemideletion in the
long arm of chromosome 7 (7q11.23), which consists of a unique
constellation of somatic, brain, and cognitive features.2, 3
At least 15 genes are involved in the deletion and partial deletions
with equally partial phenotypic manifestations of WMS. Approximately 1
in 25 000 births exhibit the deletion and accompanying
phenotype.4, 5 Our research has centered in part on the
description of the neuroanatomical phenotype for the purpose of
linking, on the one hand, brain to physiology and behavior, and, on the
other, to the genomic anomaly. The anatomical research in our
laboratories is driven by a general hypothesis derived from the
analysis of behaviors patients with WMS exhibit.3, 6 Namely,
these patients, whose mental retardation is equivalent in range to that
seen in Down syndrome, show an unusual and uneven neuropsychological
profile. This consists of deficits in processing visuospatial tasks,
relative preservation of many aspects of language, a preserved ability
to process human faces, an unusual personality characterized by lack of
fear of strangers, highly affective speech, occasionally inappropriate
friendliness, and a great deal of interest in and often remarkable
ability for things musical.3, 6, 7
The best neuroanatomical fit for the constellation of behavioral
findings seen in WMS appears to be the primary involvement of the
dorsal portions of the hemispheres, which in the caudal half of the
brain are concerned with representation
and processing of visuospatial
information8, 9, 10 and in the frontal lobes with, among other
things, the on-off timing of behavior.11 By contrast,
behaviors associated with the ventral and perisylvian portions of the
hemispheres, concerned with many aspects of language,12, 13, 14
object properties of visual and other stimuli,15, 16, 17 and
programs for the performance of various motor behaviors (eg,
speech18, 19) appear to be at least relatively spared in
WMS. However, individuals with WMS are often gregarious and speak
excessively,6 which, again, could reflect abnormality in
the dorsomedial frontal lobe. The attention disorder often seen in WMS,
with attention-deficit rates reported at 4 times those of the normal
population, also implicates the dorsomedial frontal
cortex.20, 21
Therefore, one part of the research in our laboratories has focused on
comparing gross anatomical features between the dorsal and ventral
portions of the cerebral hemispheres. Herein we report a finding
involving the central sulcus. Specifically, after noticing that the
central sulcus was too short in its dorsal extent in several autopsy
specimens from brains of cases with WMS, by comparison to the
investigators' own experience and published data,2, 9 we
examined the dorsal extent of the central sulcus in brain magnetic
resonance images from a sample of persons with WMS and age- and sex-matched control subjects.
SUBJECTS AND METHODS
SUBJECTS
Twenty-one subjects (12 women and 9 men) diagnosed as having
WMS (mean ± SD age, 28.9 ± 7.9 years; age
range, 19-44 years) were compared with 21 healthy control subjects
individually matched for age and sex (mean ± SD age,
28.8 ± 7.9 years; age range, 19-48 years).
Both groups were recruited by the Laboratory for Cognitive Neuroscience
at the Salk Institute for Biological Studies, La Jolla, Calif.
Diagnoses of WMS were determined genetically by fluorescent in situ
hybridization probes for elastin, a gene consistently found in the
critical deletion region associated with WMS.4, 5 All
diagnoses were confirmed by a medical geneticist. Controls were
typically developing individuals without evidence of psychiatric or
neurologic disorder.
Each subject gave informed consent for their participation in the study
via consent forms that were approved by the institutional review board
at the Salk Institute for Biological Studies. Some of the subjects with
WMS in this study have been described in other neuroimaging
studies.22, 23, 24
RADIOLOGIC IMAGING
Magnetic resonance images of each subject's brain were
acquired with a 1.5-T scanner (GE-Signa; General Electric, Milwaukee,
Wis). Contiguous sagittal images were acquired with a
3-dimensional volumetric radio frequency spoiled gradient echo-pulse
sequence using the following scan parameters: repeat time, 24
milliseconds; echo time, 5 milliseconds; flip angle, 45°; number of
excitations, 2; acquisition matrix size, 256 x 192
pixels; field of view, 240 mm; slice thickness, 1.2 mm; and
124 slices. All scans from the subjects with WMS and 26 of the 28
control scans were acquired at the University of California, San Diego
Medical Center Magnetic Resonance Imaging Institute. Two normal
control subjects were scanned at Stanford University, Stanford, Calif,
using an identical pulse sequence and scanner.
The spoiled gradient echo-pulse sequence image data were imported into
the program BrainImage25 for semiautomated removal of
nonbrain tissue.26 The images were then cut into cubic
voxels using a Catmull-Rom reslice algorithm26 and then
subsequently rotated into Talairach space.27 Each
subject's skull-stripped image was rendered via a ray-tracing
algorithm built into the BrainImage environment. The spatial location
of each view used for rating the dorsal central sulcus was standardized
as a superior view (looking down on the superior cortical surface from
above, Figure 1), while ratings
for the ventral central sulcus were performed on standardized lateral
views made at 90° lateral to the superior view. Oblique surface views
at 45° to the left and right of the superior view also were made.
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Figure 1.
Standardized-rendered surface views demonstrating extent of the central
sulcus. The superior view was used to judge whether the central sulcus
met the interhemispheric fissure, while the lateral views were used to
rate whether the central sulcus met the sylvian fissure. The oblique
views were used only to help identify the central sulcus when the
superior and lateral views were ambiguous.
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Two experts in neuroanatomical imaging (A.M.G. and S.W.A.) were asked
to identify the central sulcus in each image and determine whether it
extended fully to the interhemispheric fissure. All rating for the
dorsal central sulcus occurred on the superior view; the lateral views
were used only to confirm the identity of the central sulcus when the
superior view was ambiguous. Both raters were blinded to the identities
and diagnosis of the subjects. Interrater and intrarater reliability
was determined in 20 data sets via the  statistic. The interrater
value was 0.80, while intrarater reliability (for A.M.G.) was 0.86. As
a contrast to the dorsal measure, one of us (A.M.G.) also determined
whether the ventral central sulcus met the sylvian fissure using the
lateral views provided.
DATA ANALYSIS
Simple 2 tests were performed to understand the effect
of diagnosis on right and left central sulcus morphologic features. The
effects of both diagnosis and sex were also examined. Statistical
significance was set at P = .05.
RESULTS
Subjects with WMS were far less likely to have central sulci that
reached the interhemispheric fissure than the control group
(Figure 2). While 68%
(14/21) of the control subjects' central sulci extended fully to the
interhemispheric fissure, only 11% (2/21) did so in patients with WMS.
This observation was statistically significant both for the right
(P<.001; 2 = 12.95) and left
(P<.001; 2 = 15.79) central
sulci. Table 1 summarizes these results.
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Figure 2.
Characteristic neuroanatomy of Williams syndrome (WMS). The
magnified views demonstrate the extent of the central sulcus (in white)
as it approaches the interhemispheric fissure. Note that the control
subject has central sulci that reach completely to the interhemispheric
fissure and that curve slightly posteriorly, while the central sulci of
the WMS-affected subject are separated by unusual gyral convolutions.
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Shortened Extent of the Dorsal Central Sulcus in Patients With Williams Syndrome (WMS)*
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The dissimilarities between groups in the dorsal extent of the central
sulcus were not observed on its ventral end. Overall, 13% (3/21) of
the central sulci in controls reached the sylvian fissure compared with
14% (3/21) in subjects with WMS. Neither hemisphere was statistically
significantly different between the 2 groups. No differences owing to
sex were found in either group.
COMMENT
Before Vicq D'Azyr, graphic depictions of cortical folding are mostly
chaotic, but even the latter does not endeavor to mark gyri and sulci
on the median surface, other than the parieto-occipital sulcus.
However, one can see in his drawing of the medial hemispheric surface
the classic notch of the central sulcus, curled posteriorly and
concaved upward, just anterior to the upward turn of the cingulate
sulcus.28 Later, Rolando draws the fissure on the lateral
surface of the brain, where it is seen to be particularly short; it
does not reach either the dorsal edge of the convexity or the sylvian
fissure.29 There are distortions in Rolando's drawing that
suggest that the anatomist has taken a fair amount of license for the
purpose of illustration. For instance, he spreads open the sylvian
fossa to show the insula, thus, distorting perisylvian sulci. Also, he
draws a circular gyrus around the medial edge of the hemisphere
(cingulate gyrus), including frontal, parietal, occipital, and temporal
edges, that might be the reason for which the central sulcus fails to
reach all the way to the medial surface. Such gyrus has never been
observed by others.
It is well recognized that there is a great deal of variability in the
gross appearance of the central sulcus.30 This variability
is mostly in the shape of the sulcus at the surface of the brain (as
opposed to the buried aspect of the sulcus), but length and extent also
vary. For instance, Damasio31 finds that only 28% of
brains show a central sulcus that reaches the sylvian fissure.
Critchley32 cites a figure between 10% and 20%, whereas
Cunningham33 cites a figure of 19%. Damasio31
simply states that the sulcus arises from the interhemispheric fissure,
implying that this is the rule. In the detailed description of the
sulcus by Critchley,32 nothing is mentioned about the
dorsal extent. Crosby et al describe the fissure as "beginning in the
medial surface of the hemisphere."34(p344)
Eberstaller35 reports that in nearly all cases the central
sulcus reaches the medial surface, while this figure is placed at only
88% by Lang.36 Additional information is gleaned from
drawings and photographs accompanying the writings on this subject. For
instance, the typical cuneiform head of the sulcus on the medial
surface is seen in the drawings of Eberstaller.35 Where the
sulcus reaches over the dorsal hemispheric margin to continue on the
medial surface, it indents the margin causing a depression that has
been called the "crochet de Rolando" or "crochet Rolandique" by
French authors.30 This is also the case in the 4
hemispheres Damasio illustrates.31
Ono et al30 present the most detailed modern description of
the central sulcus. These authors state that in 20% of cases the
central sulcus does not reach the dorsal margin of the hemisphere and
that in some of these it ends in a bifurcation (a frequent pattern in
WMS). However, when they present their data graphically, they
report extension to the medial surface in 56% of the cases on the
right hemisphere and 72% of the cases on the left hemisphere. Our
figures are 55% (11/21) and 80% (17/21), respectively, in our control
sample, which is consistent with Ono et al.30
According to Ono et al the central sulcus does not usually reach the
sylvian fissure, being separated from it by a gyrus that connects the
inferior ends of the precentral and postcentral gyri. This bridge is
called the "pli de passage frontopariétal inférieur" or
"opercule Rolandique." Ono et al report that the central sulcus
reaches
all the way to the sylvian fissure in 16% of
the cases, right or left hemispheres. Our figures are 13% (3/21) for
controls and 14% (3/21) for patients with WMS, also without
hemispheric differences. Illustrations by the classic authors are
roughly equivalent.33, 37
During development, the central sulcus appears first on the convexity
between the fifth and sixth gestational months and then approaches the
dorsal margin of the hemisphere.37 According to
Retzius,37 only 64% of fetal cases show full extension of
the central sulcus to the medial surface. Chi et al38
report that the sulcus first appears during the 20th week of gestation,
but occasionally the right one is seen as early as the 17th week. No
comment is made about the sulcus's relation to the interhemispheric
fissure, but examination of the drawings presented with the text in Chi
et al shows that the sulcus is still short of the midline at the end of
the 31st week, arriving at the interhemispheric fissure between the
32nd and 35th weeks.
Similarly, there is little information we could gather on the anatomy
of the central sulcus in nonhuman primates. In general, illustrations
of the central sulcus in monkeys show a sulcus that does not reach the
medial edge of the hemisphere or the sylvian fissure, whereas in the
chimpanzee, it appears to reach the medial surface as in the
human.39, 40, 41, 42
In the present study we found that the central sulcus in WMS-affected
subjects usually does not reach the medial surface of the brain.
Overall (left and right hemispheres together), the sulcus reached the
midline in 68% (14/21) of the control brains while this was true in
only 11% (3/21) of WMS-affected brains. In the right hemisphere, the
figures were 55% (11/21) and 0%, respectively, whereas in the left,
they were 80% (17/21) and 24% (5/21). There were no
differences between WMS-affected and control brains in the ventral
extension of the central sulcus.
It might be wrongly said that the pattern of the central sulcus in WMS
is generally ontogenetically immature and comparable to a developmental
stage before 31 weeks' gestation because this judgment would apply
only to the dorsal extent of the central sulcus, thus belying a
regionalized maturational difference. Similarly unjustified would be
the general conclusion that the finding reflects a primitive
phylogenetic development, since the ventral portion of the sulcus does
not differ between WMS-affected and control brains. Foreshortening
dorsally could be the result of decreased development of the cortices
surrounding the central sulcus itself—areas 4, 3, 1, and 2. In this
case, dorsal foreshortening may imply changes in these
functional-architectonic areas, which are involved in lower limb and
trunk representation. More likely, however, or at least the preferred
interpretation of these writers, the lack of opercularization of the
dorsal extent of the central sulcus may reflect changes in overall
dorsomedial opercularization of the hemispheres. Thus, expansion of
dorsal cortices (eg, Broadmann areas 6, 8, 5, and 7) in the normal
condition would have the effect of growth toward the dorsomedial cortex
dorsally and into the frontal and parietal opercula ventrally, thus
carrying the central sulcus with it in both directions. Relative lack
of expansion of the homotypical cortices of the frontal and parietal
lobes would also explain the morphologic features of the central sulcus
in fetal human brains and in nonhuman primates. Therefore, the relative
lack of opercularization of the central sulcus dorsally but not
ventrally would suggest that the problem in the WMS-affected brain is
dorsal and not perisylvian, thus consistent with the behavioral
findings. Ventral cortical functions, including object recognition,
speech, and language, and even the excellent face recognition abilities
seen in patients with WMS all relate to the ventral visual and
cognitive pathways, whereas poor visuospatial function, hyperactivity,
and lack of approach inhibition implicate the dorsal pathways. This
interpretation makes the prediction that the superior parietal lobule
measured directly and the superior frontal gyrus will be found to be
smaller in WMS-affected brains compared with controls. This prediction
is being tested in our laboratories.
AUTHOR INFORMATION
Accepted for publication July 24, 2001.
This research was supported by National Institutes of Health grants
HD33113 at the Salk Institute for Biological Studies (Dr Bellugi) and
MH01142 and HD31715 (Dr Reiss). This work also was partially
supported by a grant from the MIND (Music Intelligence Neural
Development) Institute, University of California, Davis; the David and
Lucille Packard Foundation, Los Altos, Calif, and the Sinclair Fund,
Stanford (Dr Reiss).
We are grateful to the participants in these studies and to the
local, regional, and national WMS associations. Special thanks to Julie
Korenberg and David Feinstein for their advice and work that made the
manuscript possible.
From the Division of Behavioral Neurology,
Department of Neurology, Beth Israel–Deaconess Medical Center and
Harvard Medical School, Boston, Mass
(Dr Galaburda); Stanford Psychiatry Neuroimaging Laboratory, Department of Psychiatry and
Behavioral Sciences (Mr Schmitt and
Drs Eliez and Reiss) and the
Division of Neuroradiology, Department of Radiology
(Dr Atlas), Stanford University School of Medicine, Stanford, Calif; and the
Laboratory for Cognitive Neuroscience, Salk Institute for Biological
Studies, La Jolla, Calif (Dr Bellugi).
Corresponding author and reprints: Albert M. Galaburda, MD, Beth
Israel–Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215
(e-mail: agalabur{at}caregroup.harvard.edu).
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