How early are fetal cerebral sulci visible at prenatal ultrasound and

Ultrasound Obstet Gynecol 2004; 24: 706–715
Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.1802
How early are fetal cerebral sulci visible at prenatal
ultrasound and what is the normal pattern of early fetal
sulcal development?
A. TOI*, W. S. LISTER† and K. W. FONG*
*Department of Medical Imaging, Mount Sinai Hospital, University of Toronto, Toronto and †Department of Medical Imaging, Peach Arch
Hospital, White Rock, British Columbia, Canada
K E Y W O R D S: anatomy; brain; fetus; neurodevelopment; normal; ultrasound
ABSTRACT
Objectives To evaluate the time of appearance and
pattern of development of fetal cerebral sulci at prenatal
ultrasound.
Methods We studied 50 normal fetuses for visibility
of cerebral sulci, especially sulci which appear early in
anatomical studies, namely the parieto-occipital fissure,
calcarine sulcus, cingulate sulcus, convexity sulci and
insula/Sylvian fissure. The gestational ages of the fetuses
studied ranged from 15.6 to 29.6 weeks.
Results Sulci could be seen by transabdominal ultrasound
as early as 18.5 weeks. Medial hemispheric sulci and the
insula were visible earlier and more confidently than
convexity sulci. The earliest gestational ages at which
specific sulci could be seen in any fetus were as follows: parieto-occipital fissure 18.5 weeks, calcarine sulcus
18.5 weeks, cingulate sulcus 23.2 weeks and convexity
sulci 23.2 weeks. In the present series, the gestational
ages at which these sulci were always visible were as
follows: parieto-occipital fissure > 20.5 weeks, calcarine
sulcus > 21.9 weeks, cingulate sulcus > 24.3 weeks and
convexity sulci > 27.9 weeks. The insula and its margin (the circular sulcus) and the overgrowing opercula
undergo characteristic maturation. The circular sulcus at the margin of the insula was initially smooth
but started becoming angular after about 17 weeks
as it started to be overgrown by the parietal and
temporal lobe opercula. Initially the insula/operculum
angle was obtuse. An acute angle was first evident at
23.2 weeks and in all fetuses older than 24.5 weeks.
Our ultrasound data were consistent with anatomical studies and fetal magnetic resonance imaging findings.
Conclusions Some cerebral sulci can be seen at prenatal
ultrasound as early as 18.5 weeks. Familiarity with
the normal pattern of sulcal development and the
discriminating gestational ages for the appearance of
different sulci may allow early suspicion of lissencephaly.
Copyright  2004 ISUOG. Published by John Wiley &
Sons, Ltd.
INTRODUCTION
The ultrasound literature suggests that the prenatal
ultrasound diagnosis of lissencephaly is not possible until
27–28 weeks1 – 3 . However, anatomical and magnetic
resonance imaging (MRI) studies have shown that cerebral
sulci start developing much earlier. Anatomical studies
show that some sulci on the medial apposed surfaces of
the hemispheres, which we collectively call the medial
hemispheric sulci, can be seen by 16–19 weeks4,5 . These
medial hemispheric sulci include the parieto-occipital
fissure, calcarine sulcus and cingulate sulcus. Also, at fetal
MRI examinations, medial hemispheric sulci are reported
to appear as early as 18–20 weeks6,7 . Convexity sulci,
namely those on the outer convex surfaces of the cerebral
hemispheres, appear later and are seen by 20–24 weeks
on anatomical studies4,5 and by about 24–27 weeks at
MRI6 – 10 . We include as convexity sulci the central sulcus,
superior temporal sulcus and any other sulcus on the outer
convex brain surface.
Our objective was to establish the pattern of early
normal fetal cerebral sulcal development by prenatal
ultrasound prior to 30 weeks’ gestation. We felt that
such data could lead to the suspicion of abnormalities of
cortical development such as lissencephaly on ultrasound
performed before 27 weeks.
Correspondence to: Dr A. Toi, Ultrasound Department, Mount Sinai Hospital, 3rd Floor, Ontario Power Generation Building, 700
University Avenue, Toronto, Ontario, Canada M5G 1X7 (e-mail: atoi@mtsinai.on.ca)
Accepted: 28 October 2004
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
ORIGINAL PAPER
Normal fetal sulci
METHODS
We studied patients referred for obstetric ultrasound
between 15 and 30 weeks’ gestation. Ultrasound scans
were performed by a single operator. Patients were
included if the fetal anatomy appeared normal or only
minor ultrasound markers were present. Gestational age
was determined by ultrasound biometry (average of
biparietal diameter, abdominal circumference and femur
length) at time of the study scan and was consistent
with stated menstrual dates or age as established by the
first-trimester scan if menstrual history was uncertain.
Birth and newborn records were reviewed after delivery.
Approval for the study was granted by the institutional
research ethics board.
Detailed views of the fetal head and brain were
obtained transabdominally using Philips/ATL HDI 5000
ultrasound machine with 7 or 5 MHz curved array
(C7–4 or C5–2) transducers (Philips/ATL, Bothell, WA,
USA). Transvaginal scanning was not performed since
the transabdominal scans provided adequate visibility
of the brain and sulci in all the study cases. We
evaluated specifically those sulci and fissures which have
been reported to appear relatively early on anatomical
studies, namely the parieto-occipital fissure, the calcarine,
cingulate and convexity sulci and also the insula/Sylvian
fissure4,5,11 (Figure 1). Axial, coronal, sagittal and oblique
views were used as needed to access sulci. A sulcus was
defined as being present if a distinct notch or indentation
could be seen in the expected area of the sulcus. We defined
‘convexity sulcus’ as any sulcus visible as an indentation
on the outer convex hemispheric surface.
The Sylvian fossa was best assessed in the axial
orientation. The insular margin, the circular sulcus, was
judged to be smooth or angular. When angular, the angle
was further defined to be obtuse if the angle between the
insula and the temporal lobe operculum was greater than
90◦ and acute if the angle was less than 90◦ .
RESULTS
Fifty scans in 46 fetuses were included. Forty-two fetuses
were scanned once and four fetuses twice at different
gestational ages. Gestational ages ranged from 15.6
to 29.6 weeks. Fetal numbers in different age groups
were as follows: < 18 weeks (n = 4), 18–19.9 weeks
(n = 21), 20–21.9 weeks (n = 8), 22–23.9 weeks (n =
6), > 24 weeks (n = 11). The indications for ultrasound
scan were as follows: routine (n = 19), anomaly history
(n = 10), suspected abnormality at ultrasound done
elsewhere (n = 8), maternal disease (n = 4), positive
maternal serum screen (n = 4), increased first-trimester
nuchal translucency (n = 3), biophysical profile (n = 2).
All the fetuses had normal appearing heads and brains.
Extracranial anatomy was completely normal in 44
fetuses. Six fetuses showed markers or minor findings
as follows: isolated echogenic intracardiac focus (n = 4),
isolated choroid plexus cyst (n = 1), both choroid plexus
cyst and echogenic intracardiac focus (n = 1). All of these
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
707
(a)
Cingulate
Parietooccipital
Calcarine
(b)
Convexity
sulci
Figure 1 Medial hemispheric (a) and lateral convexity (b) surfaces
of 26-week fetal brain showing the sulci which appear early and
can be recognized at prenatal ultrasound. On the medial
hemispheric surface note the cingulate sulcus, parieto-occipital
fissure and calcarine sulcus. On the lateral convexity surface note
the convexity sulci above and behind the Sylvian fossa (sf). Figure
modified and reproduced, with permission, from Dorovini-Zis K,
Dolman CL, Gestational development of brain, Arch Pathol Lab
Med 1977; 101: 192. Copyrighted  1977, American Medical
Association. All rights reserved.
fetuses had normal newborn examinations by experienced
pediatricians after delivery.
We found that sulci were easier to detect enface in a
direction perpendicular to their plane of orientation. The
sulci on the hemisphere farther from the transducer were
seen more clearly than those in the near field. In general,
the sulci on the medial surfaces of the hemispheres,
specifically the parieto-occipital fissure, calcarine sulcus
and cingulate sulcus, appeared earlier and were more
confidently seen than convexity sulci.
The earliest appearance of a sulcus was as a small
‘dot’ in the expected site of the sulcus. Later, the sulci
formed an obvious ‘V’ indentation. Finally, the sulci
became deeper and were visible as a surface notch and
an echogenic line extending into the brain matter in a ‘Y’
configuration. Similar appearances and progression are
reported at anatomical and MRI studies4,10,12 .
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Toi et al.
708
In the present study we noted the youngest age at which
a specific sulcus was first visible in any fetus and also the
age after which the sulcus was visible in all fetuses. The
parieto-occipital fissure was best imaged axially in a plane
near the upper margin of the occipital horns of the lateral
ventricles. It first appeared at 18.5 weeks, and was always
visible after 20.5 weeks (Figure 2). The calcarine sulcus
was best imaged in a coronal plane through the occipital
lobes. It could be seen as early as 18.5 weeks and was
always visible after 21.9 weeks (Figure 3). The cingulate
sulcus was generally not as confidently seen. It was best
imaged in a coronal plane above the region of the thalami.
(a)
It became visible by 23.2 weeks in some fetuses and was
always seen after 24.3 weeks (Figure 4).
Convexity sulci were seen with more difficulty and
were the last to be seen with confidence. They were best
imaged semi-axially by exploiting the window offered by
the proximal squamosal bony suture and then angling
the plane of the scan on the farther brain surface
from the approximate level of the insula superiorly.
The late detection of convexity sulci is likely to be due
to their initial development in the high parietal regions
where ultrasound access is obstructed by cranial bones.
Convexity sulci could first be seen in some fetuses by
23.2 weeks in the parietal and temporal regions but were
confidently seen only in fetuses older than 27.9 weeks
(Figure 5). The earliest detected convexity sulci were
on the outer convex peripheral hemispheric surface
posterior or superior to the Sylvian fissure and were
(e)
15
20
25
30
Gestational age (weeks)
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
Figure 2 Parieto-occipital fissure. (a) Optimal axial plane of section
through brain to show parieto-occipital fissure. (b) Ultrasound
image of a 17-week fetus showing smooth medial hemispheric
brain surface (arrow) before formation of the parieto-occipital
fissure. (c) Ultrasound image of an 18.7-week fetus showing earliest
indication of the parieto-occipital fissure as a small dot on the near
and far hemispheric surface (arrow). (d) Ultrasound image of a
24.3-week fetus with more advanced fissure development (arrows)
giving a diamond shape. (e) Graph illustrating the visibility of the
parieto-occipital fissure in individual fetuses at different gestational
ages. , visible; , not visible; , unable to assess.
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Normal fetal sulci
709
(a)
c
Figure 3 Calcarine sulcus. (a) Optimal coronal plane of section
through the occipital lobe of the fetal brain to demonstrate the
calcarine sulcus. (b) Ultrasound image of an 18.9-week fetus
showing smooth medial surface of the occipital lobe before
calcarine sulcus formation (arrow). (c) Ultrasound image of a
21.7-week fetus with minimal calcarine sulcus formation visible as
a small dot on the brain surface (arrow). (d) Ultrasound image of a
23.6-week fetus showing more advanced calcarine sulcus
development (arrow). (e) Graph illustrating the visibility of the
calcarine sulcus in individual fetuses at different gestational ages.
, visible; , not visible; , unable to assess.
(e)
15
20
25
30
Gestational age (weeks)
likely to be the superior temporal, central and postcentral
sulci.
When imaged in a direction parallel to their plane of
orientation, sulci appeared as an echogenic plate that
should not be mistaken for a disorder of the brain
parenchyma. This is especially true of the calcarine sulcus,
which on axial views can be seen as an echogenic band
on the medial surface of the occipital lobe just medial to
the occipital horn (Figure 6).
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
The insula/Sylvian fissure showed a characteristic
pattern of development (Figure 7). In early pregnancy
the Sylvian fossa was a smoothly margined indentation.
After about 17 weeks’ gestation the smooth Sylvian
fossa indentation developed angular margins at the site
of the developing circular sulcus. This resulted in a
plateau-like appearance with angularity at the margins
(the circular sulcus) where the insula meets the frontal,
parietal and temporal opercula anteriorly, superiorly and
posteriorly. These angles were initially obtuse but became
acute as the opercula progressively overgrew the insula
and eventually met to form the closed Sylvian fissure.
Acute insula/operculum angles could be seen as early as
23.2 weeks in some fetuses. After 24.5 weeks the angles
were always acute (Figure 7e).
DISCUSSION
We have demonstrated that some cerebral sulci are
readily visible at transabdominal ultrasound earlier than
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Toi et al.
710
(a)
(d)
15
20
25
30
Gestational age (weeks)
Figure 4 Cingulate sulcus. (a) Optimal coronal plane of section through brain to show cingulate sulcus. (b) Ultrasound image of a 24.8-week
fetus with an almost smooth medial hemispheric surface with only minimal dot-like irregularity, which is the earliest sign of sulcus formation
(arrow). (c) Ultrasound image of a 30.3-week fetus showing appearance of cingulate sulci (arrows). csp, cavum septi pellucidi. (d) Graph
illustrating the visibility of the cingulate sulcus in individual fetuses at different gestational ages. , visible; , not visible; , unable to assess.
previously described. These include the parieto-occipital
fissure and the calcarine, cingulate and some convexity
sulci. It is important to understand how, when and where
to look for early normal cerebral sulcal development.
While sulci can be appreciated on multiple different
views and projections, we have found that the views
perpendicular to the expected course of the sulci are the
most effective in detecting early sulcal development. It is
important to remember that this technique demonstrates
only part of a sulcus and helps establish its initial
development. It does not mean that the entire sulcus
and adjacent cortex are developing normally.
There is correlation between anatomical, ultrasound
and MRI studies of sulcal development (Table 1).
However, the agreement is not perfect which is likely
to be due to different definitions and opinions as to
what constitutes the earliest manifestation of a sulcus.
Further variation in assigning appearance times of sulci
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
could relate to the different techniques that have been
used (for example, variations in thickness of slices in
fetal neuropathological studies, use of photographs with
differing lighting, and variations in orientation of serial
sections of the brains). Also anatomical studies are only
possible when normal pregnancy has been interrupted for
various reasons and it is assumed that this has not affected
cerebral maturation. In imaging studies, case numbers are
generally small, the percentage with visible sulci is not
always mentioned, and the earliest time of appearance
of sulci is often not distinguished from the time of high
percentage of visibility.
Anatomical reports of sulcal appearance times differ by
as much as 4–6 weeks4,5 . Generally, sulcal detection by
imaging studies lags behind their anatomical appearance.
The identification of the parieto-occipital fissure and
calcarine sulcus by imaging lags behind anatomical
identification by about 2 weeks (anatomy 16 weeks vs.
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
507
10–44†
8–10
14
16
16
18
20
23
20–25
26
(22)
(22)
24
24
28
24
24–26
24–26
24–26
25
12–38§
Lan et al.9
(2000)
80
22–41‡
Dorovini-Zis
and Dolman5
(1977)
20
24
27
24
28
24
NA
NA¶
Girard et al.6
(2001)
24.5–32
32–40
30–33
29–38
28–33
24.5–32
51
23–43**
Ruoss et al.10
(2001)
173
22–38††
(22–23)
(22–23)
(22–23)
24–25
24–25
27
27
27
Garel et al.8
(2001)
Magnetic resonance imaging
18–19
18–19
24–25
26–27
26–27
26–27
40
14–38‡‡
14
Levine and
Barnes7
(1999)
25–27
70
10–37§§
12
21
25
25
26
Bernard et al.11
(1988)
(14)
18
18
26
262
14–40¶¶
Monteagudo and
Timor-Tritsch16
(1997)
Ultrasound
23.2–27.9
18.5–20.5
18.5–21.9
23.2–24.3
50
15–29***
Present study
(2004)
The numbers in parentheses indicate the age range at which the sulcus was visible on the youngest brain available, although the sulcus was likely to have been identifiable earlier. *Any sulcus on outer
convex hemispheric surface, generally central, postcentral or superior temporal sulcus. †Gestational age determined from last menstrual period (LMP) given by mother. Ages when named sulci were
seen in 25–50% of brains. ‡Gestational age as given by mother and microscopic evaluation of fetal kidneys. Renal age derived from histology used in 11 cases with unknown or discrepant dates.
§Gestational age estimated from LMP compensated by ultrasound crown–rump length measurement. ¶Gestational age determination technique not described. **Postpartum premature and term
infant magnetic resonance imaging (MRI) study. Neonatal gestational age was calculated from LMP as well as early prenatal ultrasound. ††Age when sulci visible in over 75% of fetuses. Gestational
age determined by 12-week ultrasound scan. ‡‡Gestational age based on LMP. All fetuses underwent an ultrasound scan on the same day as MRI and the ultrasound scan result correlated with
menstrual age within 1 week. §§Gestational age determined from LMP and correlated with postnatal Dubowitz score and dating by ultrasound. ¶¶Patients included if they had known dates in
agreement with ultrasound dates. ***Present study: 50 measurements in 46 fetuses at different gestational ages. Fetal age calculated from ultrasound biometry, which was in agreement with
menstrual dates and/or first-trimester ultrasound scan. NA, not available.
Fetuses (n)
Age range (weeks)
Interhemispheric sulcus
Callosal sulcus
Parieto-occipital fissure
Calcarine sulcus
Cingulate sulcus
Central sulcus
Superior temporal sulcus
Convexity sulci*
Chi et al.4
(1977)
Anatomical
Examination type/study
Table 1 Age (menstrual weeks) when some cerebral sulci appear in normal fetuses at anatomical, magnetic resonance imaging and ultrasound examinations
Normal fetal sulci
711
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Toi et al.
712
(a)
B
A
(e)
15
Figure 5 Convexity sulci. (a) Optimal planes of section through a
fetal brain to demonstrate lower (A) and higher (B) convexity
cerebral sulci. (b) Ultrasound image of a 20.2-week fetus showing
smooth surface of brain (arrow) before development of visible sulci
(c) Ultrasound image of a 23.2-week fetus showing early
appearance of a convexity sulcus (arrow) posterior to the Sylvian
fossa (sf) imaged approximately along Plane A. (d) Ultrasound
image of a 27.9-week fetus showing multiple unmistakable
convexity sulci (arrows) imaged at about Plane B. (e) Graph
illustrating the visibility of the convexity sulci in individual fetuses
at different gestational ages. , definite; , probable; ,
not present.
20
25
30
Gestational age (weeks)
ultrasound and MRI 18 weeks). The cingulate sulcus is
more difficult to see and its appearance on ultrasound
and MRI lags anatomical descriptions by about 7 weeks
(anatomy 16 weeks vs. ultrasound 23 weeks and MRI
24 weeks). We believe that reported variations in
identification of sulci will decrease as familiarity with
the expected appearances increases.
The insula/Sylvian fissure has a characteristic pattern of development. Anatomically, by 14 weeks, the
Sylvian fossa becomes recognizable as a smooth lateral
depression4,5 . By 18–22 weeks its edges become more
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
distinctly demarcated by the circular sulcus4,13,14 . These
margins enclose a triangular plate-like area, which is
the insula or island of Reil. The apex of the triangle
is posterior and it widens and opens anteriorly. As the
temporal and parietal lobes enlarge they overgrow the
insula (operculization). Anatomically, operculization can
be seen by about 22–24 weeks5,10,15 . It starts at the posterior pointed end of the insula and proceeds zip-like
anteriorly5,16 . By 28–35 weeks, most of the insula is
covered4,13,16 , but full closure of the most anterior part
is not achieved until birth to 2 years14 . The insular plate
remains smooth until insular sulci appear anatomically
starting about 32–35 weeks4,14 at which time they can
also be recognized on MRI7 . This pattern of development was also seen in the present study. As temporal and
parietal operculization progressed, the angle between the
insula and overgrowing brain changed from obtuse to
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Normal fetal sulci
713
Figure 6 Echogenic appearance of calcarine sulcus in an older fetus
when imaged by ultrasound in an axial plane parallel to its plane of
orientation. (a) Coronal view at 27.7 weeks shows the calcarine
sulcus (arrows). Note the ‘Y’ appearance characteristic of
well-developed sulci in later pregnancy. The plane of the white
arrows indicates the plane of the scan used in Figure 6b and 6c.
(b) Axial view along the arrowed plane in Figure 6a shows an
echogenic area (arrowheads) between the medial brain surface and
ventricle (v). This is the normal appearance of the calcarine sulcus
when it is imaged exactly along its plane. This should not be
mistaken for brain abnormality. (c) Axial view just caudad to
Figure 6b shows normal homogeneous hypoechoic white matter
between medial brain surface (arrow) and ventricle (v) when
imaging occurs just off the plane of the calcarine sulcus.
acute. An acute angle could be seen in some fetuses by
23.2 weeks and in every fetus older than 24.5 weeks.
The present study did not evaluate the effects of fetal
gender, twinning and intrauterine growth restriction on
sulcal development nor determine left–right symmetry of
development. Fetal gender does not appear to affect sulcal
development, with male and female brains developing
similarly at anatomical, autopsy and neonatal cerebral
ultrasound studies4,17,18 . There are, however, reports of
variation in sulcal appearance time related to the other
factors.
Left–right symmetry of time of appearance of sulci
is the rule in anatomical studies4,5,11,17 but a few
exceptions are reported. Dorovini-Zis and Dolman
evaluated symmetry in 23/80 brain samples and reported
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
that 5/23 showed left–right differences5 . In three cases
the right superior temporal sulcus was evident earlier. In
two cases the central sulcus appeared earlier, once on the
right and once on the left. Chi et al. reported that the right
superior frontal and superior temporal sulci, secondary
sulci and right insular sulci were visible 1–2 weeks earlier
than the left4 .
In twins, Chi et al. found a delay of 2–3 weeks between
19 and 32 weeks but catch-up occurred by 33 weeks4 .
Levine and Barnes studied six pairs of twins by MRI
and found that some developed sulci at a similar rate to
singletons but others lagged up to 3 weeks7 .
Growth-restricted and small-for-gestational-age fetuses,
and chronically stressed fetuses of mothers with chronic
hypertension, can show accelerated functional and
anatomical development. Hadi, in an autopsy study of
23 fetuses from 27 to 34 weeks’ gestation, found gyral
maturation accelerated by 2 to 11 weeks in 19/23 fetuses
in which growth restriction or maternal hypertension
were present17 . Functional maturation also appears to
occur earlier in such fetuses19 .
Other factors should also be considered when evaluating sulcal development. With severe ventriculomegaly
the brain may become so compressed that sulci may
not be adequately visible and cannot be evaluated. Also
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Toi et al.
714
(a)
(e)
15
17
19
21
23
25
27
29
Gestational age (weeks)
delays in sulcal development have been reported in association with other central nervous system abnormalities
including holoprosencephaly, agenesis of corpus callosum, porencephaly, encephaloceles7,19 , microgyria,
ischemia11 , tumors, encephalitis and severe intracranial
hemorrhage14 . Thickening of sulci may be seen with
subdural hematoma, external hydrocephaly, meningitis,
toxoplasmosis and Sturge-Weber syndrome11 .
It is important to remember that in the early second
trimester the normal brain is still quite smooth and abnormal cortical development should not be diagnosed before
20 weeks of gestation. In addition, there is a spectrum of
abnormal cortical development. Minor or focal lesions are
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
Figure 7 Insula and Sylvian fossa/fissure. (a) Optimal axial plane
through brain to show insula and Sylvian fissure development and
operculum formation. (b) Ultrasound image of a 17.8-week fetus
showing smooth Sylvian fossa (arrow) without any angularity
(arrowhead). The white line inferiorly shows the normal shape of
the smooth Sylvian fossa in early pregnancy. (c) Ultrasound image
of an 18.9-week fetus showing a plateau-like Sylvian fossa (arrow)
with obtuse posterior angulation (arrowhead) at the site of the
developing circular sulcus. (d) Ultrasound image of a 29.6-week
fetus showing further development of the Sylvian fissure (arrow).
The temporal operculum is overgrowing the insula and forms an
acute angle posteriorly (arrowhead). (e) Graph illustrating the
visibility of the insular angularity in individual fetuses at different
gestational ages. , acute angle; , obtuse angle; , not angular;
, unable to assess.
likely to elude early prenatal detection by ultrasound at
any age. Major abnormalities may be suspected by prenatal ultrasound. We have reviewed in a separate report our
experience in the prenatal diagnosis of lissencephaly20 .
In summary, we have described the ultrasound pattern
of sulcal development in normal fetuses from 15 to
29 weeks’ gestation. We do not advocate a complete
sulcal evaluation as part of the routine anatomical survey
at 18–20 weeks. However, some cerebral sulci, especially
the parieto-occipital fissure and calcarine sulcus, appear
early and are usually readily visible when evaluating the
occipital horns of the lateral ventricles. Knowledge of the
sulcal development pattern is useful if there is suspicion
Ultrasound Obstet Gynecol 2004; 24: 706–715.
Normal fetal sulci
of brain abnormality such as mild ventriculomegaly and
in pregnancies with prior problems. We urge caution in
the use of the present data as they are derived from
a relatively small number of fetuses. A further study
with a larger number of fetuses would help to confirm
the discriminating gestational ages for the appearance
of different sulci and help determine biological and
interobserver variation.
ACKNOWLEDGMENT
The authors wish to thank Dr Sandeep Ghai for help with
reference material.
REFERENCES
1. Blaas HG, Eik-Nes SH, Kiserud T, van der Hagen CB, Smedvig E. Lissencephaly type I. 1992; http://TheFetus.net/[Accessed
26 May 2004].
2. McGahan JP, Pilu G, Nyberg DA. Cerebral malformations.
In Diagnostic Imaging of Fetal Anomalies, Nyberg DA,
McHahan JP, Pretorius DH, Pilu G (eds). Lippincott Williams
& Wilkins: Philadelphia, PA, 2003; 221–290.
3. Monteagudo A, Timor-Tritsch IE. Fetal neurosonography of
congenital brain anomalies. In Ultrasonography of the
Prenatal and Neonatal Brain, Timor-Tritsch IE, Monteagudo A,
Cohen HL (eds). McGraw-Hill: New York, NY, 2001;
151–258.
4. Chi JG, Dooling EC, Gilles FH. Gyral development of the
human brain. Ann Neurol 1977; 1: 86–93.
5. Dorovini-Zis K, Dolman CL. Gestational development of brain.
Arch Pathol Lab Med 1977; 101: 192–195.
6. Girard N, Raybaud C, Gambarelli D, Figarella-Branger D. Fetal
brain MR imaging. Magn Reson Imaging Clin N Am 2001; 9:
19–56, vii.
7. Levine D, Barnes PD. Cortical maturation in normal and
abnormal fetuses as assessed with prenatal MR imaging.
Radiology 1999; 210: 751–758.
8. Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury JF,
Sebag G, Hassan M. Fetal cerebral cortex: normal gestational
landmarks identified using prenatal MR imaging. AJNR Am J
Neuroradiol 2001; 22: 184–189.
Copyright  2004 ISUOG. Published by John Wiley & Sons, Ltd.
715
9. Lan LM, Yamashita Y, Tang Y, Sugahara T, Takahashi M,
Ohba T, Okamura H. Normal fetal brain development:
MR imaging with a half-Fourier rapid acquisition with
relaxation enhancement sequence. Radiology 2000; 215:
205–210.
10. Ruoss K, Lovblad K, Schroth G, Moessinger AC, Fusch C.
Brain development (sulci and gyri) as assessed by early
postnatal MR imaging in preterm and term newborn infants.
Neuropediatrics 2001; 32: 69–74.
11. Bernard C, Droulle P, Didier F, Gerard H, Larroche JC, Plenat F, Bomsel F, Roland J, Hoeffel JC. Echographic aspects of
cerebral sulci in the ante- and perinatal period [in French]. J
Radiol 1988; 69: 521–532.
12. van der Knaap MS, van Wezel-Meijler G, Barth PG, Barkhof F,
Ader HJ, Valk J. Normal gyration and sulcation in preterm and
term neonates: appearance on MR images. Radiology 1996;
200: 389–396.
13. Chen CY, Zimmerman RA, Faro S, Parrish B, Wang Z, Bilaniuk LT, Chou TY. MR of the cerebral operculum: abnormal
opercular formation in infants and children. AJNR Am J Neuroradiol 1996; 17: 1303–1311.
14. Naidich TP, Grant JL, Altman N, Zimmerman RA, Birchansky SB, Braffman B, Daniel JL. The developing cerebral surface.
Preliminary report on the patterns of sulcal and gyral maturation – anatomy, ultrasound, and magnetic resonance imaging.
Neuroimaging Clin N Am 1994; 4: 201–240.
15. Patriquin H, Fontaine S, Michaud J, Lafortune M, Boisvert J.
Development of the fetal brain in the second trimester: an
anatomic and ultrasonographic demonstration. Can Assoc
Radiol J 1992; 43: 131–137.
16. Monteagudo A, Timor-Tritsch IE. Development of fetal gyri,
sulci and fissures: a transvaginal sonographic study. Ultrasound
Obstet Gynecol 1997; 9: 222–228.
17. Hadi HA. Fetal cerebral maturation in hypertensive disorders
of pregnancy. Obstet Gynecol 1984; 63: 214–219.
18. Worthen NJ, Gilbertson V, Lau C. Cortical sulcal development
seen on sonography: relationship to gestational parameters. J
Ultrasound Med 1986; 5: 153–156.
19. Amiel-Tison C, Pettigrew AG. Adaptive changes in the developing brain during intrauterine stress. Brain Dev 1991; 13:
67–76.
20. Fong KW, Ghai S, Toi A, Blaser S, Winsor EJT, Chitayat D.
Prenatal ultrasound findings of lissencephaly associated with
Miller–Dieker syndrome and comparison with pre- and
postnatal magnetic resonance imaging. Ultrasound Obstet
Gynecol 2004; 24: 716–723.
Ultrasound Obstet Gynecol 2004; 24: 706–715.