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70
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
A
2
B
1
2
1
4
3
3
4
C
Figure 2–61. ( A, B) Median sections through the posterior fossa and the upper portion of the spinal cord. The open arrow indicates the cisterna
magna; the small arrow, the medulla oblongata; and the arrowhead, the fourth ventricle (at 17 postmenstrual weeks). B is similar to A, the arrows and
the numbers showing the levels at which the cross-sections shown in C were taken. (1, 2) These sections were taken at the cervical level. The arrow
indicates the spinal cord. (3, 4) These sections were obtained at the level of the medulla oblongata.
c
CP
A
B
Figure 2–62. Imaging the upper spinal cord and the posterior fossa at 18 postmenstrual weeks. (A) Median section. The small arrow indicates the
medulla oblongata; the arrowhead, the cisterna magna; the double arrow, the spinal cord. (B) Paramedian section through the cerebellar hemisphere (C)
and the posterior horn of the lateral ventricle with the choroid plexus (CP).
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
4
71
C
B
A
B
C
Figure 2–63. Anatomy of the cerebellum and the vermis in the posterior fossa at 15 to 16 postmenstrual weeks. (A) A low almost-axial section reveals
the open communication (Magendie) between the cerebello medullary cistern (cisterna magna) and the fourth ventricle (arrow). (B) A somewhat higher
section still shows the communication. (C) The highest of the three sections demonstrates that the vermis at this level is already present.
cm
a
a
cm
A
cm
a
a
B
C
Figure 2–64. Anatomy of the posterior fossa at 19 postmenstrual weeks and 4 days. A, B. Two parallel axial sections demonstrating the still partially
open connection between the cisterna magna (cm) and the median aperture of the fourth ventricle (small arrows). The slightly more echogenic lowermost portions of the two cerebellar hemispheres are evident. The arrowhead indicates the fourth ventricle. a, Amygdala. C. Median section. The white
line is the plane along which the two axial sections in A and B were taken. p, pons; c, cerebellum. The arrowhead marks the fourth ventricle.
72
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
FH
BPD level
Temporal
horn
Figure 2–65. Schematic representation of a sagittal view of the fetal ventricular system at a level slightly above that normally used for obtaining the
biparietal diameter. FH, Frontal horn; At, atrium; OH, occipital horn; CSP, cavum septi pellucidi; HW, hemispheric width; CAD, cerebroatrial distance;
VGC, cerebral vein of Galen; AW, atrial width. (From Pilu and colleagues, 1989, 59 with permission.)
Studying the infratentorial region reveals the following
structures: the cisterna magna, with fine, linear echoes of
Body
VGC
At
CAD
OH
AW
At
83 , 84
At
FH
CSP
HW
FH
(lateral edge-to-lateral edge) measurement has been plot-
ted and published by several centers.
the arachnoid; the hemispheres, with their hyperechoic
cortex; the extremely hyperechoic vermis; the pons; the
fourth ventricle; and, on a median section, the connection
between the fourth ventricle and the cisterna magna, that
is, the median aperture (Magendie).
The late closure of the cerebellar vermis, toward the 18th
postmenstrual week, was documented by Bromley et al
using transabdominal scanning. Using the transfontanelle
approach, we have noted several fetuses with even later “closure” of the vermis, with normal neonatal outcome.
For easier orientation the posterior fossa is depicted in
the following figures: horizontal (axial) sections— Figures
2–52 ; 2–59 ; 2–61 ; and 2–64A and B ; coronal sections—
Figures 2–38-5 , and 2–59 ; and median and sagittal sections—
Figures 2–43A , 2–45 , 2–59A and B , 2–60A and B, and
2–64C .
Figures 2–61A, B and 2–62A , depict the upper spinal
cord. To achieve a good view of the posterior fossa and the
upper spinal cord, the transducer should ideally be over
the nuchal area of the fetus. It is obvious that such views
are not always possible. Gentle manipulation of the fetal
position using the abdominally placed second hand of
the scanning person, in combination with equally gentle
touching with the tip of the vaginal probe, may ease the
fetus into the desired position.
By knowing the normal anatomy of the posterior fossa,
early detection of pathology (eg, Dandy-Walker malformation, atrophy of the vermis, and posterior cephalocele) is
feasible as early as 10 to 11 postmenstrual weeks.
Because the size of the cerebellum is easy to image on
axial as well as coronal sections, this structure has been
discussed in detail by various authors. The bicerebellar
Sulci, Fissures, and Gyri
Examination of the sulci, fissures, and gyri is one of
the many instances when fetal neuroimaging is fashioned after that of the neonatal brain scanning by
82
ultrasonography.
Neuropathologists and pediatric neurologists use
sequential sulcal and gyral developments as a clinical estimate of fetal age, particularly between 22 and 34 postmenstrual weeks.
the cingulate gyrus may predict disease in the immediate
neighborhood of this structure.
In spite of the fact that rather crude timing of the fetal
age is possible, based on the developmental stages of the
gyri and the sulci, it seems that perinatologists may never
have to rely on these markers to determine age. However,
it may at times be important to assess cortical maturation
and development, as well as diseases that affect formation
of the cerebral cortex.
Performing antenatal neurosonography enables us to
evaluate some of the sulci, fissures, and gyri of the developing fetal brain. Before these structures are shown as
they progressively appear on the US screen, a list of the
major sulci, fissures, and gyri of the mature human brain is
shown in Figures 2–66 through 2–70 . These images depict
the mature brain in normal neonates. The next step is to
examine the sequential appearance of the sulci, fissures,
and gyri as a function of increasing fetal age, expressed in
weeks from the LMP. Tables 2–6 and 2–7 were compiled
using data from Chi and associates.
photographs of 507 brains and serial sections of 209 brains
85 – 90
Deformities or delayed development of
91
92
This group examined
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Postcentral gyrus
73
Callosal sulcus
Precentral
Cingulate gyrus
Cingulate sulcus
Corpus callosum:
Splenium
Body
Genu
Rostrum
Anterior commissure
Subcallosal area
Parolfactory sulcus
Paraterminal gyrus
Optic nerve and chiasm (II)
Pituitary gland
(anterior and posterior lobes)
Figure 2–66. Medial surface of the cerebral hemisphere and median section through the diencephalon, brain stem, cerebellum, and rostral spinal cord
of a mature brain. The sulci, the gyri, and other major structures of the medial cerebral surface are shown. (From Martin, 2003,
*
Mammillary
body
Oculomotor nerve (III)
gyrus
Central sulcus
Medulla
Cingulate sulcus (marginal ramus)
Superior parietal lobule
Precuneus
Parieto-occipital sulcus
Cuneus
Calcarine fissure
Cingulate gyrus (isthmus)
*
Septum pellucidum
Fornix
Thalamic adhesion
Superior and
inferior colliculi
Cerebral aqueduct
Midbrain
IV ventricle
Vermis of cerebellum
Cerebellar hemisphere
Pons
Central canal
61
with permission.)
from pathologic specimens of fetuses 10 to 44 weeks from
the LMP. They concluded that many gyri become well
defined within a short period (between 26 and 28 postmenstrual weeks). Thereafter, only a few gyri develop.
During the last trimester, the gyri and the sulci become
more prominent and deep, giving rise to secondary and
tertiary gyri.
In 1977 a study examining 80 brains ranging in age
from 22 postmenstrual weeks to 1 month of postnatal life
was published by Dorovini-Zis and Dolman.
93
They concluded that at 22 postmenstrual weeks, the cerebral hemispheres are smooth, and the lateral sulci on both sides are
wide open. The parieto-occipital and calcarine fissures are
present on the medial surface. By 24 postmenstrual weeks,
the central sulcus begins to form, and the cingulate sulcus
is seen. By 26 postmenstrual weeks, deepening of these
fissures and sulci occurs. A great growth spurt takes place
between 28 and 30 postmenstrual weeks. The sulci and
the gyri deepen and become more branched. Figure 2–66
depicts the development of the sulci and the gyri as
described in the work of Dorovini-Zis and Dolman.
Slagle’s group
91
studied the development of the cin-
93
gulate sulcus in preterm infants by performing cranial
ultrasonographic scans. Two hundred eleven infants from
24 to 40 postmenstrual weeks were studied on their third
prenatal day of life. These investigators identified five patterns: (1) a discontinuous line of the sulcus appears; (2) a
continuous line appears; (3) first branches of the primary
sulcus appear (marginal ramus); (4) multiple branches
of the primary sulcus appear; and (5) multiple branches
appear and merge with other sulci, giving the surface a
“cobblestone” appearance.
Figure 2–71 depicts the sequential appearance
of these five patterns. The first pattern appeared at
74
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Figure 2–67. Lateral surface of the
cerebral hemisphere, emphasizing
the gyri and the sulci of a mature
brain. (From Martin, 2003,
permission.)
61
with
Superior frontal gyrus
Middle frontal gyrus
Inferior frontal gyrus:
Triangular par t
Opercular part
Orbital part
Orbital gyri
Superior temporal gyrus
Superior temporal sulcus
Middle temporal gyrus
Inferior temporal sulcus
Inferior temporal gyrus
Precentral sulcus
Precentral gyrus
Lateral sulcus
Central sulcus
Postcentral gyrus
Postcentral sulcus
Superior parietal lobule
Intraparietal sulcus
Inferior parietal
lobule
Supramarginal
gyrus
Angular gyrus
Occipital gyri
Preoccipital notch
Cerebellar hemisphere
Flocculus
Pons
Medulla
Figure 2–68. Inferior surface of the
cerebral hemispheres and the diencephalon. The gyri and the sulci are
marked. The brain stem is transected
at the rostral midbrain. (From Martin,
61
with permission.)
2003,
Lateral olfactory stria
Anterior perforated
substance
Rhinal sulcus
Uncus
Parahippocampal
gyrus
Collateral sulcus
Occipitotemporal
gyrus
Inferior temporal
gyrus
Substantia
nigra
Olfactory bulb
Olfactory tract
Occipital gyri
Gyrus rectus
Olfactory sulcus
Orbital gyri
Pineal gland
Corpus callosum (splenium)
Optic nerve (II)
Optic chiasm(II)
Optic tract(II)
Infundibulum
Mammillary body
Posterior perforated
substance
Oculomotor
nerve(III)
Basis pedunculi
Red nucleus
Periaqueductal gray
matter
Cerebral aqueduct
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Suprior frontal gyrus
Middle frontal gyrus
Inferior frontal gyrus:
Orbital part
Triangular part
Opercular part
Inferior parietal
lobule
Intrapariental sulcus
Superior parietal
lobule
Supramarginal gyrus
Angular gyrus
Precentral sulcus
Precentral gyrus
Central sulcus
Postcentral gyrus
Postcentral sulcus
75
Occipital gyri
Figure 2–69. Gyri and sulci of the superior surface of the cerebral hemisphere. (From Martin, 2003,
24 postmenstrual weeks, the first line was seen at 26 ± 2
postmenstrual weeks, first branching appeared at 32 ± 3
postmenstrual weeks, multiple branches occurred at 34
± 3 postmenstrual weeks, and the cobblestone pattern
appeared after 38 postmenstrual weeks. This study suggested that cingulate sulcus maturation occurs in a predictable pattern ( Figure 2–72 ). Slagle and colleagues
91
also
studied 30 infants with evidence of brain damage. These
infants showed significant delay in the postnatal development of the cingulate sulcus.
Our observations of the developing cortex using
transvaginal ultrasonography focused on three readily
available planes. The first is the median plane, which
touches the medial aspect of the cerebral hemisphere and
scans along the longitudinal fissure. The second available
plane is a midcoronal plane at the level of the anterior
horns. The third is an extreme lateral right or left oblique
plane “touching” almost tangentially the upper surface of
the cerebral hemispheres, emphasizing the lateral sulcus
and the insula.
94
We focused on the following sulci and fissures: on the
median plane the cingulate sulcus with its marginal ramus,
the posterior occipital sulcus, and the calcarine sulcus; and
on the coronal plane the longitudinal fissure, with its progressive branching of the cingulate sulcus. Finally, on the
lateral sagittal section we examined the shape of the lateral
sulcus and the underlying insula. Figures 2–73 , 2–74 , and
2–75 clearly show progressive deepening and branching as
well as curving of the different fissures and sulci and the
appearance of the insula, respectively. Relative flatness of
the cortex is present until 24 to 25 postmenstrual weeks,
with widely gaping longitudinal fissures, calcarine, posterior occipital fissures, and lateral sulcus (insula). At 28 to
30 postmenstrual weeks, significant depth and branching
of the sulci and fissures occur. Between 30 and 60 postmenstrual weeks, more secondary branching develops,
and at 38 postmenstrual weeks, the tertiary branching is
94
seen.
The clinical significance of these observations is still
not clear. It may be possible to establish whether the cortex progresses along a well-defined and age-dependent
pattern. It may also be feasible to detect diseases of the
fetal brain that are expressed by a delayed or nonexistent
maturational process.
The sonographic appearance of the sulci and the
fissures is dependent on the higher-echogenicity pia
mater (pachymeninx) and the pia-arachnoid complex,
also called the “soft brain covering,” or the leptomeninx.
Note that the high echogenicity of the choroid plexus
is due to the highly vascular and abundant presence of
the pia mater. The highly echogenic leptomeninx or the
choroid plexus in close proximity to the CSF generates a
61
with permission.)
76
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
25 semanas 31 semanas27 semanas
35 semanas Final
Figure 2–70. The surface of the fetal brain is relatively smooth in the first 20 weeks after which the sulci, gyri, and fissures develop. This image
demonstrates the concept of the gradual changes in the surface of the fetal brain throughout the pregnancy. (Reproduced, with permission, from
Dr P. Jeanty, Editor www.Thefetus.net. Magnetic Resonance in the Fetus, Part 1. H. Werner, et al. Thefetusnet.net, 2005.)
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Table 2–6. TEMPORAL DEVELOPMENT OF THE CEREBRAL HEMISPHERES
Gestational Age *
(No. Examined) Sulci and Fissures Gyri
77
10–15 weeks (n = 6) Interhemispheric fissure, sylvian fissure,
transverse cerebral fissure, callosal sulcus
16–19 weeks (n = 13) Parieto-occipital fissure, olfactory sulcus,
circular sulcus, cingulate sulcus, calcarine
fissure
20–23 weeks (n = 41) Rolandic sulcus, collateral sulcus,
superior temporal sulcus
24–27 weeks (n = 46) Prerolandic sulcus, middle temporal
sulcus, postrolandic sulcus, interparietal
sulcus, superior frontal sulcus, lateral
occipital sulcus
28–31 weeks (n = 36) Inferior temporal sulcus, inferior
frontal sulcus
32–35 weeks (n = 29) Marginal sulcus
Secondary superior, middle, and inferior
frontal; superior and middle temporal;
superior and inferior parietal; prerolandic
and postrolandic, superior and inferior
occipital sulci and gyri; insular gyri
36–39 weeks (n = 31) Secondary transverse and inferior temporal
and cingulate sulci and gyri; tertiary
superior, middle, and inferior frontal and
superior and inferior parietal sulci and gyri
—
Gyrus rectus, insula, cingulate gyrus
Parahippocampal gyrus, superior temporal gyrus
Prerolandic gyrus, middle temporal gyrus, postrolandic gyrus, superior and inferior parietal lobules,
superior and middle frontal gyri, superior and
inferior occipital gyrus, cuneus and lingual gyrus,
fusiform gyrus
Inferior temporal gyrus, triangular gyrus, medial
and lateral orbital gyrus, callosomarginal gyrus,
transverse temporal gyrus, angular and supramarginal gyrus, external occipitotemporal gyrus
Paracentral gyrus
Anterior and posterior orbital gyri
40–44 weeks (n = 29) Secondary orbital, callosomarginal, and
insular sulci and gyri; tertiary inferior
temporal and superior and inferior
occipital gyri and sulci
From Chi and colleagues, 1977,92 with permission.
*Postmenstrual weeks.
highly visible interface, which appears as bright echoes.
The dura is prominent in those places where it protrudes
into the brain to separate structures. These two duracontaining places are the falx ( Figures 2–21 , 2–38 , 2–39 ,
2–41 , 2–53 , and 2–59 ) and the tentorium ( Figures 2–31 ,
2–38 , 2–40 , and 2–41 ). The pia closely follows the surface
of the cortex. Wherever a fissure or a sulcus is present,
the pia (and, at times, the arachnoid) closely follows,
making this a sonographically easily recognized structure. In the case of the cerebellar cortex, and even more
so the vermis of the cerebellum, which have extremely
abundant and tightly folded gyri and sulci, the sonographic image shows extremely bright echoes. The sonographic hallmark of the vermis is its easily recognizable
high echogenicity, due to the repeatedly infolded double
layers of leptomeninges ( Figures , 2–44 , 2–45 , 2–51 , 2–57 ,
2–63 , and 2–64 ).
It is hard to image sonographically the convexity of
the cerebral hemisphere. Thus, it is rare to see a small
area of the tangential picture of the gyri and the sulci.
However, the medial surface of the cerebral hemisphere
along the longitudinal fissure is easily imaged by the ultrasonographic techniques. It is this flat surface where good
images of the cortex are obtained.
Fetal and neonatal sulcal examination by ultrasonography is a noninvasive and convenient method to assess
cerebral maturation. This cerebral maturation has so far
been proven only in neonates. However, if the proper
methodology is developed for use in fetal neurosonology,
it may prove to be useful.
78
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Table 2–7. REGIONAL DEVELOPMENT OF THE CEREBRAL HEMISPHERES
Lobe Fissures and Sulci Weeks* Gyri Weeks
Frontal Interhemispheric fissure 10 Gyrus rectus 16
Transverse cerebral fissure 10 Insula 18
Callosal sulcus 14 Cingulate gyrus 18
Sylvian fissure 14 Prerolandic gyrus 24
Olfactory sulcus 16 Superior frontal gyrus 25
Circular sulcus 18 Middle frontal gyrus 27
Cingulate sulcus 18 Triangular gyrus 28
Rolandic sulcus 20 Medial and lateral orbital gyrus 28
Prerolandic sulcus 24 Callosomarginal gyrus 28
Superior frontal sulcus 25 Anterior and posterior orbital gyrus 36
Inferior frontal sulcus 28
Parietal Interhemispheric fissure 10 Cingulate gyrus 18
Transverse cerebral fissure 10 Postrolandic gyrus 25
Sylvian fissure 14 Superior parietal lobule 26
Parieto-occipital fissure 16 Inferior parietal lobule 26
Rolandic sulcus 20 Angular gyrus 28
Postrolandic sulcus 25 Supramarginal gyrus 28
Interparietal sulcus 26 Paracentral gyri 35
Temporal Sylvian fissure 14 Superior temporal gyrus 23
Superior temporal sulcus 23 Parahippocampal gyrus 23
Collateral sulcus 23 Middle temporal gyrus 26
Middle temporal sulcus 26 Fusiform gyrus 27
Inferior temporal sulcus 30 Inferior temporal gyrus 30
External occipitotemporal gyrus 30
Transverse temporal gyrus 31
Occipital Interhemispheric fissure 10 Superior occipital gyri 27
Calcarine fissure 16 Inferior occipital gyri 27
Parieto-occipital sulcus 16 Cuneus 27
Collateral sulcus 23 Lingual gyrus 27
Lateral occipital sulcus 27 External occipitotemporal gyrus 30
After Chi and colleagues, 1977,92 with permission.
*Postmenstrual weeks.
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
A B
79
CD
E
Figure 2–71.
or more discontinuous linear echoes (arrow); (B) Continuity—a single continuous linear echo (arrows); (C) First branch—perpendicular echo of the
primary sulcus (arrowhead); (D) Multiple branches—additional branches off the primary sulcus (arrowheads); and (E) “Cobblestone” pattern branches
from the cingulate sulcus, merging with other cortical sulci. (From Slagle and colleagues, 1989,
Developmental stages of the cingulate sulcus. Paramedian sonograms demonstrating five developmental stages: (A) The presence of one
91
with permission.)