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Asymmetrical volumes of the right and left frontal and occipital regions of the human brain.

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Asymmetrical Volumes of
the Right and Left Frontal
and Occipital Regions
of the Human Brain
Daniel R. Weinberger, MD, Daniel J. Luchins, M D ,
John Morihisa, M D , and Richard Jed Wyatt, MD
The volume of a portion of the frontal and occipital
lobes was measured in 40 brains in the Yakovlev Collection. In 32 cases the volume of the right frontal lobe
was larger than that of the left; in the same number of
cases the left occipital lobe was larger than the right ( p
< 0.01). The asymmetries existed in fetal brains as
early as 20 weeks of gestation. The results confirm observations made with computed tomography and indicate that this nonrandom asymmetrical pattern is an
early manifestation of human brain development.
Weinberger DR, Luchins DJ, Morihisa J, Wyatt RJ:
Asymmetrical volumes of t h e right and left frontal
and occipital regions of t h e human brain. Ann
Neurol 1197-100, 1982
Various higher cortical functions in human beings,
such as handedness, language, musical ability, and
spatial perception, appear to be subserved by dominance of one cerebral hemisphere. While these functional asymmetries have been the subject of innumerable studies, the mechanisms underlying them are
unknown. The possibility that neuroanatomical
asymmetries might, at least in part, be responsible
has long been considered, and structural differences
between the hemispheres have been noted by many
neuroanatomists [9, 171. Most neuroanatomical
studies prior to 1968, however, described relatively
minor differences or failed to document quantitatively the magnitude or frequency of the asymmetries. Furthermore, in these early reports, it was
difficult to correlate the findings with either normal
or pathological brain function. Such problems led
Von Bonin in 1962 to imply that neuroanatomical
asymmetries in the brain were of doubtful biological
importance [ 171.
In 1968, Geschwind and Levitsky [3] reported that
the sylvian fissure and planum temporale were larger
From the Adult Psychiatry Branch, Division of Special Mental
Health Research, Intramural Research Program, National Institute
of Mental Health, Saint Elitabeths Hospital, Washington, DC
20032.
Received Mar 17, 1981, and in revised form June 8. Accepted for
publication June 13, 1981.
Address reprint requests to Dr Weinberger.
97
on the left in 65 of 100 brains, and larger on the right
in only 11. This finding, since it involved an area of
the brain fundamental to language, revived the possibility that some lateralized cerebral functions are
linked to neuroanatomical asymmetries. The finding
has been confirmed by others and observed in fetuses
as early as 29 weeks of gestational age [ l , 2, 16, 18,
191.
Other structural asymmetries of potential clinical
importance have been observed recently with computed tomography (CT). In a series of studies, LeMay
reported that in the majority of right-handed individuals, the right frontal lobe is wider than the left
and the left occipital lobe is wider than the right [9111. Reversals of these asymmetries as seen on CT
scans have been associated with left-handedness [ 101,
with recovery from global aphasia [ 141, and with several clinical disorders of high-level brain function including developmental dyslexia [6], verbal intelligence deficits [15], autism [5], and schizophrenia [12,
131.
These CT studies represent a potential advance in
the effort to link asymmetrical structure and function
in the brain. However, they have not been confirmed
in neuroanatomical studies of normal human brain
tissue, raising the possibility that the findings may be
an artifact of the CT scanning or asymmetry measuring process. The only systematic quantitative study of
these regions was done by Inglessis in 1925 [7]. Dividing the brain at the plane of the ear, he compared
the areas of the right and left sides from photographs
of whole-brain coronal sections of 200 pathological
specimens. H e measured only 10 to 12 sections per
brain. Although he failed to observe a consistent
frontal asymmetry, the left occipital region was larger
in 61% of cases compared with 33% on the right.
Another problem with the asymmetries observed
on CT scans is that it is not known whether they represent actual differences in the volume of brain tissue
or simply focal protuberances that appear prominent
on a two-dimensional CT image. The relationship of
the development of the asymmetries to the acquisition of lateralized cerebral functions is also unknown.
In an attempt to resolve some of these uncertainties, we measured the volume of a major portion of
the frontal and occipital lobes of 4 0 serially sectioned
whole brains in the Yakovlev Collection.
collection and of its unique suitability for quantitative morphological research is provided elsewhere [ 8 ] .
Twenty of the 40 cerebra studied were of fetuses and
infants designated in the catalogue of the collection as
“normative,” indicating no evidence of cerebral abnormality. Fifteen cerebra were of fetuses ranging in age from 20
to 42 weeks of gestation. T h e 5 infant brains were from
babies 3.5 to 8 months old. Within this age range, 32
“normative” cerebra sectioned in the coronal plane were
available in the collection. Twelve were excluded before
measurement because either the cerebrum was not intact
or the plane of section was clearly not at 90 degrees to the
anteroposterior axis. T h e other 20 cerebra, 14 of which
also were designated as “normative,” were of 4 children
and 16 adults. The children ranged in age from 3 to 11
years, the adults from 19 to 98. Of the coronally sectioned
normative brains available in this age group, only 1 had to
be excluded because the cerebrum was not intact. Six abnormal adult brains were included that showed evidence of
diffuse metabolic brain diseases not known to produce
asymmetrical structural changes. These included 2 cases of
hepatic coma, 2 of Wernicke’s encephalopathy, and 2 of
anoxic encephalopathy. Handedness was not known for
any of the cases. Only specimens sectioned in the coronal
plane were used, since volume can be more easily determined in brains sectioned in this manner.
To ensure a standardized quantitative method, we selected regions demarcated by unmistakable landmarks.
These regions are slightly more generous than those measured in the C T studies. T h e posterior border of the frontal
lobe region (Figure) was defined by the first section anterior to the anterior margin of the genu of the corpus
callosum. Using a planimeter, an accurate mechanical tool
for measuring the area of an irregular space, we determined
the cross-sectional area of the left and right hemispheres in
this section by tracing along the contours of the cortical
gyri. For the adult and child brains, we also measured the
area of white matter in each hemisphere by tracing along
the internal margin of the cortex. The area of gray matter
for the section was derived by subtracting the white matter
area from the area of the total hemisphere. Each measurement was made twice, and the mean was used. Initial and
repeat measurements were invariably within 3% of the
mean. In similar fashion, we measured consecutive sections
at 2,800 p intervals (600 p intervals for fetal brains) until
we reached the frontal pole of the brain. The volume of the
region was derived by multiplying the mean of all the areas
measured for the region by its length. An analogous
method was used to determine the volume of the occipital
lobe region although the anterior border of this region was
defined by the section closest to the midpoint between the
posterior margin of the splenium of the corpus callosum
and the occipital pole (see the Figure).
Methods
The Yakovlev Collection, housed in the Armed Forces ‘Institute of Pathology in Washington, DC, consists of approximately 800 serially sectioned whole brains prepared
to exacting and uniform standards. The material in the collection is described in a comprehensive catalogue compiled
by D r Paul I. Yakovlev. A published description of the
98 Annals of Neurology Vol 11 No 1 January 1982
Results
In 32 cases, the volume of the right frontal lobe region was greater than that of the left ( p < 0.01,
binomial test), by an average of 13%. As expected,
the volumes varied considerably from one brain to
gray and white matter. Although the differences
tended to be in the same direction as for the whole
lobes, the only difference that reached significance by
paired t test was the volume of the left occipital gray
matter, which was larger than that of the right ( p =
0.01). The ratio of gray to white matter was not
significantly different across hemispheres for either
the frontal or occipital regions, and the hemispheric
gray and white matter volumes were highly correlated (Pearson Y > 0. 77, p < 0.001) for all regions
except the left frontal (Y = 0.38,p = 0.10).
Human brain represented in sagittal section. The volume of the
stippled regions was determined.
another, reflecting differences in age and degree of
shrinkage (range for adults: left, 11.3 to 48.2 cm3;
right, 12.4 to 48.0; range for infants and fetuses: left,
0.6 to 12.3 cm3; right, 0.7 to 19.7). The volume of
the left occipital region was greater than that of the
right in 32 of the 40 cases also, by an average of 20%.
The volume of the occipital regions also showed considerable variation from one brain to another (range
for adults: left, 11.2 to 38.8 cm3; right, 9.9 to 31.1;
infants and fetuses: left, 0.8 to 15.0 cm3; right, 0.8
to 11.2). For the total sample, a paired t test revealed
that the volume of the right frontal lobe was
significantly greater than that of the left ( p = 0.01)
and the left occipital lobe had a significantly greater
volume than the right ( p < 0.001). Twenty-eight
cases had larger right frontal and left occipital lobes.
We sought t o determine whether these asymmetries had developed subsequent to the acquisition of a
lateralized cerebral function such as language or
whether they apparently arose during embryological
development of the brain. If the former hypothesis
were the case, the asymmetries should have been less
apparent in the fetal and infant cerebra. This was not
found. The frontal volume was greater on the right in
17 of the 20 brains of fetuses and infants, and the
occipital volume was greater on the left in 15. A
paired t test for these 20 cerebra showed that the
asymmetries were quantitatively significant for both
the frontal ( p < 0.03) and occipital ( p < 0.02) regions. A significant effect of age could not be demonstrated. For the 2 0 cerebra of adults and children, the
right frontal and left occipital volumes also were
greater in 17 and 15 cases, respectively. This difference in volume approached significance for the
frontal asymmetry ( p = 0.1, paired t test) and was
significant for the occipital asymmetry ( p = 0.01) in
this small sample of 20 older cerebra.
We also investigated lateralized asymmetries of
Discussion
In 32 of 40 cerebra in the Yakovlev Collection, the
volume of the right frontal region was larger than that
of the left and the left occipital region was larger than
that of the right. These results indicate that a major
portion of the frontal and occipital lobes of the
human brain is quantitatively asymmetrical and that
this asymmetry tends to be in a consistent, nonrandom direction. The results further indicate that the
linear asymmetries observed on CT scans correspond
to actual differences in the volume of these frontal
and occipital regions. Since the asymmetries are apparent in utero, they are not secondary to the development of functional asymmetries (e.g., language)
or to antenatal environmental factors. Instead, they
appear to be programmed into the embryological development of the brain and may represent part of the
neuroanatomical substrate for lateralized cerebral
functions.
In this study the magnitude of asymmetry was
greater for the occipital than for the frontal lobes.
This finding may explain the relatively high reliability
of determining occipital asymmetries on CT images
as compared with the less reliable determination of
frontal asymmetries [12, 141. The study failed to
confirm the results of a regional cerebral blood flow
study which suggested that the ratio of white to gray
matter was greater on the right [4].
~~
The authors are grateful to Dr Paul I. Yakovlev for his advice and
for help with the use of his collection. We also thank Mr Mohammed Haleem and the Armed Forces Institute of Pathology, Washington, DC. The Yakovlev Collection is supported by Grant
Y01-NS-7-0032 from the National Institute of Neurological and
Communicative Disorders and Stroke.
References
1. Chi JG, Dooling EC, Gilles FH: Gyral development of the
human brain. Ann Neurol 1:86-93, 1977
2. Chi JG, Dooling EC, Gilles FH: Left-right asymmetries of the
temporal speech areas of the human fetus. Arch Neurol
34:346-348, 1977
3. Geschwind N, Levitsky W: Human brain: left-right asymmetries in temporal speech regions. Science 161:181-187, 1968
Brief Communication: Weinberger e t al: Hemispheric Volumetric Asymmetries 99
4. Gur R, Pacher 1, Hungerbuhler JP, Reivich M, Obrast WD,
Amarnek WS, Sackeim HA Differences in the distribution of
gray and white matter in human cerebral hemispheres. Science 207:1226-1228, 1980
5. Hier DB, LeMay M, Rosenberger PB: Autism associated with
reversed cerebral asymmetry. Neurology 28:348-349, 1978
6. Hier DB, LeMay M, Rosenberger PB, Perlo VP: Developmental dyslexia: evidence for a subgroup with a reversal of
cerebral asymmetry. Arch Neurol 35:90 -92, 1978
7. lnglessis M: Untersuchungen uber Symmetrie und Asymmetrie der menschlichen Grosshirnhemispharen. 2 Gesanite
Neurol Psychiatr 95/96:463-474, 1925
8. Kretchman HJ, Schleicher A, Grortschreiber J-F, Rullinan W:
The Yakoviev Collection. J Neurol Sci 4 3 : l l l - 126, 1979
9. LeMay M: Morphological cerebral asymmetries of modern
man, fossil man, and nonhuman primate. Ann N Y Acad Sci
280:349-369, 1976
10. LeMay M: Asymmetries of the skull and handedness. J Neurol
Sci 32:243-253, 1977
11. LeMay M, Kido DK: Asymmetries of CerKbrdl hemispheres
on computed tomograms. J Comput Assist Tomogr 2:471476, 1978
12. Luchirrs DJ, Weinberger DR, Wyatt RJ: Schizophrenia: evidence for a subgroup with reversed cerebral asymnierry. Arch
Gen Psychiatry 36:1309-1311, 1979
13. Naeser MA, Levine HL, Benson DF: Frontal leucotorny size
and hemispheric asymmetries on computerized romographic
scans of schizophrenics with variable recovery. Arch Neurol
38:30-37, 1981
14. Pieniadz JM, Naeser MA, Koff E, Levine HL: CT scan reversed cerebral hemispheric asymmetries and improved recovery in aphasia. Presented at the 17th Annual Meeting of
the Academy of Aphasia, San Diego, 1979
15. Rosenberger PB, Hier DB: Cerebral asymmetry and verbal
intellectual deficits. Ann Neurol 8:300-304, 1980
16. Teszner D, Tzavaras A, Gruner J, Hacaeii H: Etude
anatomique de I'asymkie droite-gauche d u planum temporale. Rev Neurol (Paris) 126:444-462, 1972
17. Von Bonin G: Anatomical asymmetries of the cerebral heniispheres. In Mountcastle VB (ed). lnterhernispheric Relations
and Cerebral Dominance. Baltimore, The Johns Hopkins
University Press, 1962, pp 6-14
18. Wada J, Clarke J, Hamm A: Cerebral hemispheric asymmetry
in humans. Arch Neurol 32:239-246, 1975
19. Witelson SF, Pallie W: Left hemisphere specialization for language in the newborn: neuroanatomical evidence of asymmetry. Brain 96:641-646, 1973
Abnormal Vertical
Eye Movements in the
Locked-in Syndrome
P. Larmande, MD," D. H h n , MI>,fM . Jdn, MDJ
A. Elie, MD,$ and A. Gouazt, MlIt
As a rule, vertical ocular movements are thought to
depend on niesencephalic structures, horizontal gaze
on pontine structures. The ocular motility examination of a patient with pontine hernorrhage and no lesion of the niesencephalon showed bilateral palsy of
horizontal gaze and a dissociated loss of vertical
movements: saccades were slowed, while pursuit managements were unchanged. The findings suggest that
the pontine reticular formation is necessary in generation of normal vertical ocular saccades.
Larmande P, l-I&iin D, Jan M, Elie A, Gouaze A:
Abnormal vertical eye movements i n the lockrd-in
syndrome. Ann Neurol 11:lOO --102, 1982
The locked-in syndrome, identified by Plum and
Posner [12], is a rare clinical entity consisting of
tetraplegia with facial paralysis and bilateral paresis
of horizontal gaze. The only remaining voluntary
movements are blinks of the eyelids, which allow
contact with the patient, anti vertical eye movements,
which are usually maintained.
No qualitative study of the vertical eye nioveinents
in locked-in syndrome has been published, but these
movements are often described as normal [7,111. In
one of our patients suffering from locked-in syndrome, we could confirm the presence of vertical
ocular movements. The clinical and graphic recorded
abnormalities of these movements a r e described.
Case Report
A 50-year-old woman with longstanding hypertension was
admitted after she suffered a left heiiiiplegia without loss
of consciousness. lrnmediately following admission her
condition deceriorared severely: bilateral hemipfegia developed associated wirh respiratory paralysis that necessitated tracheal inrubation and assisted ventilation. Nevertheless, the patient remained conscious and communicated
From the *Clinique Neurologique and the tService de Neurochirurgie, C.H.R. de Tours, Tours, France, and t h e $Service
d'Anatoinie Pathologique, C.€I.R.Beaujou, Clichy, France.
Received Feb 9, 1981, and in reviseJ form May 1.Accepted for
publicatiori May 1 1 , 1981.
Address reprint requests tu t)r l.drmaide, Clinique Neurdogique,
Centre Hospitalier K6giunal de Tours, 2, Hd Tonntlli, 37044
Tours C d e x , France.
100 0364-5 134/821010100-03$01 2 5 @ 178 1 by the American Neurological Association
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