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Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Figure 2–72. Developmental sequence of the cingulate sulcus. Shown is
a comparison of the 10%, 50%, and 90% levels of prenatal (stippled bars) and postnatal (open bars) development of the cingulate sulcus. There was no difference in cingulate sulcus landmark timing between prenatal (deter­mined on initial sonograms of 211 infants of 24 to 40 postmenstrual weeks’ gestational age) and postnatal development (determined on serial ultra­sound examinations from week 1 of age to 40 weeks’ postconceptual age in the 144 infants born at less than 32 weeks’ postmenstrual age). (From Slagle and colleagues, 1989, 91 with permission.)
17w 21w 25w
Presence
Continuity
1st branch
Multiple
Branches
Cobblestone
Prenatal
10% 50% 90%
24 26 28 30 32 34 36 40
Postnatal
38
Postconceptional age (weeks)
29w
32w
35w
36w 38w 39w
Figure 2–73. Development of the sulci and the gyri. Coronal sections (usually midcoronal–2) from 17 to 39 postmenstrual weeks are depicted. Note
that at first the straight line of the longitudinal fissure (arrowhead shown at 25 postmenstrual weeks). At 25 to 28 postmenstrual weeks (not shown), the first indentation of the cingulate sulcus (small single arrow) appears and remains evident up to 36 weeks. At 37 to 38 postmenstrual weeks, secondary and, finally, tertiary branches appear (small double arrows). CC, corpus callosum; CG, cingulate gyrus. (From Monteagudo et al, 1997,
94
with permission.)
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
C
CSP
G
G
C
C
C
G
C
81
G
C
G
C
Figure 2–74. Development of the fissures, sulci, and gyri. The median sections from 15 to 39 postmenstrual weeks show the first appearance of the cin-
gulate gyrus (CG), the cingulate sulcus (small double arrow) at 22 postmenstrual weeks, and the calcarine fissure and the parieto-occipital sulcus (arrow) at 21 postmenstrual weeks. Note the progressive appearance of the “cobblestone” gyral pattern, fully recognizable at 38 to 39 postmenstrual weeks. The long arrow points to the callosomarginal sulcus. CC, corpus callosum; CG, cingulate gyrus. (From Monteagudo et al, 1997,
94
with permission.)
82
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
sas
A
Insula
Figure 2–75. The insula, lateral sulcus, and subarachnoid space at 25 postmenstrual weeks. (A) On the left Oblique–2 extremely lateral sagittal section
of the subarachnoid space (sas), the operculum (arrows), and the insula are shown. (B) On the Midcoronal–1 plane, the subarachnoid space surrounding the superior sagittal sinus (sss) and the insula (arrows) are depicted.
B
sss
THREE-DIMENSIONAL FETAL NEUROSCAN
A thorough description of 3D US equipment and its func­tioning, including the explanation of the physics behind the different types of display modalities, is beyond the scope of this chapter. However, for those readers who are interested, we refer them to several texts and articles avail­able in the literature.
We will focus on the three basic steps in performing a 3D US study: acquisition, storage, and display. This section will review these three main components of 3D US and explain how to “manipulate” the acquired volumes. In this volume, this manipulation is also referred as “navigating” or “scrolling.”
Before performing volume imaging of the fetal brain, a dedicated fetal neurosonography should be performed using the transabdominal and/or the transvaginal 2D scan­ning approach. Normal 2D US appearance of the fetal CNS has been described in depth in this chapter.
Volume Acquisition
A well-planned and well-executed volume acquisition is the most important first step in the process of creating good-quality 3D US images. The volume can be obtained using a manual sweep with the probe, across the volume of interest, or automatically, with mechanical transducers enabling fast acquisition of data without movement of the probe itself. The US industry is slowly phasing out manual
95 , 96
acquisition, favoring automated acquisition for many valid reasons. At present, volume US (3D sonography) can be performed using transabdominal or transvaginal scan heads.
Initiating a 3D US examination is similar to that of a 2D US. Once the targeted brain structures of interest are clearly seen on the monitor, the region of interest is selected by using the volume box on the 2D image. Then the special transabdominal or transvaginal 3D transducer is activated. To obtain the volume, the 3D probe creates an extremely rapid sequence of images that are automatically stored into a single volume. Every subsequent activation of the transducer creates a new and separate volume that can be accessed later as needed. The volume acquisition results in a single 3D static data set that consists of numer­ous successive 2D sectional images. As a result, it becomes possible to re-create any desired image by slicing through the volume in any of the three classical planes (coronal, sagittal, and axial), as well as any other plane referred to as “anyplane.” We recommend capturing several volumes of the same structure in different planes.
The first display of images, usually the multiplanar orthogonal planes, appears automatically on the screen. At this point the quality of the picture is examined. If the quality of the displayed images, hence the acquired vol­ume, seems acceptable, the volume can be stored.
Acquisition of good-quality 3D volume is the basis of any 3D analysis. Most factors that determine the acquisi­tion quality can be controlled and varied by the operator,
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
83
such as grayscale settings, acquisition speed, frame rate, and acoustic shadowing. However, fetal position, fetal movement, maternal obesity, and fluid–tissue interface may challenge 3D assessment, just as in 2D US. When volume acquisition takes place, the following factors need to be considered.
1. GRAYSCALE SETTINGS: Because poor-quality 2D images will create poor-quality 3D images, it is mandatory to optimize the grayscale 2D image prior to volume acquisition. The machine settings applied to a good 2D US image should be those applied to a diagnostic-quality 3D US image. We should therefore pay special attention to use the best settings, as the quality of the acquired volume will determine the success in effectively “reading” the 3D images.
2. ACQUISITION TIME AND ANGLE OF ROTATION: These are two of the main features defining volume quality. Angle of rotation determines the number of sections obtained during acquisition. The wider the angle of rotation, the bigger the volume that is acquired and the longer the acquisition time that is required. The longer the acquisition time, the clearer the image will be. However, the probability of move­ment artifacts increases. Thus, because acquisition
should be taken to adjust acquisition time as well as the size of the volume containing the structure to be evaluated. When acquiring a volume of the fetal brain in the sagittal or coronal plane, an angle of rotation of 60 to 80° is suggested, whereas when an axial approach is used, a 45 to 60° angle should be used.
3. ACOUSTIC SHADOWING: As discussed earlier, after 15 to 16 weeks’ gestation, mounting bone thick­ness may preclude an adequate evaluation of 3D images, as any shadowing on the 2D image will be embedded in the 3D volume. Therefore, an attempt to acquire the volume through an acoustic window, just as with 2D US, is highly recommended.
When the volumes are acquired transvaginally, two
volumes should be taken. One should be acquired on the sagittal plane obtained by aligning the US plane with the longitudinal axis of the fetal brain using any of the fontanelles or sagittal suture as an acoustic window. The bregmatic fontanelle offers the larg­est acoustic window in the anterior portion of the brain. The second volume should be acquired on the coronal plane, which is achieved by rotating the probe 90° from the previous scanning plane. Most of the time both approaches are possible. The examiner can always help obtain the desired plane by applying gentle external manipulation of the fetal head with a free hand.
In scanning transabdominally, the 3D volume is
generally obtained using an axial approach. We rec­ommend using two perpendicular planes: an axial plane that can be obtained through the squamosal suture and a sagittal plane through the metopic suture; the latter is sometimes hard to obtain, but
it yields excellent quality volumes. However, acqui­sition in any plane may be feasible; in that case, on-screen or off-line rotation of the brain into the customary classic planes is possible.
The advantages of the 2D transvaginal trans-
fontanelle approach compared with conventional transabdominal scanning of the fetal brain have been described previously in this chapter, as well as in the literature.
41
However, two distinct advantages are added to 2D transvaginal imaging when using 3D transvaginal US.
First, the axial section, which is rarely seen with
2D transvaginal transfontanelle imaging, can be reconstructed on the orthogonal sections, although this reconstructed image will be of lesser qual­ity compared with that of the sagittal and coro­nal planes. Second, the 2D sections obtained from “slicing” the 3D volume are parallel to each other, whereas, when using 2D transvaginal transfontanelle neurosongraphy, the planes obtained radiate from a single point, usually from the anterior fontanelle, and are oblique to one another ( Figure 2–76 ). This may present a real advantage when pictures are presented to neurology or neurosurgeon consultants because they are generally more familiar with the parallel tomographic images of MRI or CT scans.
The most commonly used scanning approach
is clearly the transabdominal 2D scan. It is there­fore natural that most will use 3D scanning of the fetal brain by transabdominal volume acquisition. It should be remembered, however, that when using the transabdominal route, good-quality images may not be feasible at all times. We strongly recommend performing a transvaginal acquisition whenever pos­sible. Furthermore, in those fetuses with suspicion of brain anomaly or when it is impossible to obtain a view in order to correctly assess normal brain anat­omy, an external version of the fetus into the vertex presentation is warranted. This procedure should be tried before one decides to obtain an MRI of the fetal brain, as a good-quality transvaginally obtained volume is superior to most MRI images.
4. FETAL MOVEMENT: Fetal movements during the volume acquisition are the main cause of motion artifacts and are demonstrated by the presence of wavelike stripes on images on almost all planes ( Figure 2–77 ). In order to minimize movement artifacts, if possible, the acquisition should be per­formed during fetal rest or between periods of fetal movements. The choice of longer acquisition times is best for a quiet fetus, whereas faster speeds should be applied for an active fetus. In addition, the patient can be asked to hold her breath during the acquisi­tion time (this will not influence artifacts created by the fetus).
5. FETAL POSITION: Other factors that can compro­mise image quality are position of the fetal head, a fetal hand above the face or if the face is targeted, a fetal face too close to the uterine wall or an anterior placenta. As mentioned before, sometimes the fetal head may need to be manipulated by the nonscanning
84
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
A
Figure 2–76.
ultrasound. The sections recreated from the 3D volume are parallel to each other, similar to those obtained when using a CT or an MRI (A). When scan­ning with conventional 2D ultrasound through the anterior fontanelle, the planes arise from a single point (fontanelle) and fan-out laterally (B).
The diagrams demonstrate the different angles in which the coronal and sagittal views are obtained with 3D (A) and 2D (B) transvaginal
hand to allow access to fontanelles, which serve as an acoustic window.
6. FLUID–TISSUE INTERFACE: Among the factors that may interfere with good-quality surface-rendering imaging is oligohydramnios, the absence of or low amount of amniotic fluid around the region of interest.
Luckily, if the fetus is in the vertex presentation,
many of the above hindrances are avoided, enabling the examiner to concentrate only on positioning the fontanelles and/or sutures vis-à-vis the footprint of the probe.
We should bear in mind that the acquisition plane
provides the best image, thus the best information, whereas images on the reconstructed planes are of lesser quality. This limitation of 3D US is important
B
Data Storage
Once the volume has been acquired, it can be processed directly on the US system at the time of acquisition, or the stored digital volumes can be saved to the computer’s hard disk. Transferring the data onto a CD or a smaller storage device allows the volume to be analyzed off-line using manipulation and postprocessing proprietary and brand­specific software. Different manufacturers have their own software to analyze 3D US volumes, including 4DView (GE Healthcare www.volusonclub.net/emea/4DView), QLAB (Koninklijke Philips Electronics www.healthcare. philips.com), SonoView Pro (Samsung Medison America, Cypress, CA www.samsungmedisonusa.com.), and Inspace interactive 3D viewer (Siemens). Unfortunately, they are not interchangable.
when evaluating targeted structures that are bet­ter evaluated in a specific plane. Thus, spending the time necessary to obtain the adequate acquisi­tion plane is warranted. As the technology (ie, the number of acquired slices) increases and resolution improves, the quality of the reconstructed planes is expected to improve, too.
Display Modalities
Multiple displays are available for the analysis of 3D volumes. These have been extensively described in the literature. modes most used for the purposes of a fetal neuroscan
97 – 100
Of all the available displays, the primary
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
85
A
C
Figure 2–77. Multiplanar display mode of the fetal brain. After a brain volume has been acquired, the three orthogonal planes are displayed on the
screen and volume quality can be assessed. Box A shows a coronal plane through the anterior horns of the lateral ventricles, box B a sagittal view, and box C an axial plane. No alignment of the different planes has been performed; therefore, the views shown in the three planes are asymmetrical. Note in this case how motion during volume acquisition has led to the presence of artifacts, which are demonstrated as wave-like stripes in all three orthogonal planes (arrows).
are the multiplanar mode, the tomographic display, and the inversion mode. However, the other less used modes will be described here, as they have shown poten­tial in improving visualization of different fetal CNS structures.
B
orthogonal planes, as at this very point the three planes meet ( Figures 2–78 and 2–79 ). Thus, the relationships between different anatomical structures can readily and easily be assessed by moving this dot in one of the planes and evaluating the corresponding structure on the other two planes. Once we realize this, we are in possession of a
Multiplanar Imaging (Orthogonal Planes)
This image modality is the first type of display that we use and the one that in our experience is the mainstay of 3D US evaluation of the fetal brain. It allows simultaneous display of an image in the three classical anatomical planes (coronal, sagittal, and axial). The three boxes containing the orthogonal displays are called box A (upper left), which contains the plane parallel to the acquisition plane or start­ing plane, and box B (upper right) and box C (lower left), which contain the reconstructed planes. This allows simul­taneous visualization of all three mutually perpendicular sectional planes. A fourth box may appear on the display screen if the rendering mode is activated; this is called box D (lower right), which contains the rendered image. This screen display corresponds to that seen when using the GE 4DView (www.volusoncub.net/emea/4DView) soft­ware ( Figures 2–78 and 2–79 ).
An important tool available in the orthogonal dis­play mode is the marker dot. The place of the marker dot indicates the same anatomical location on all three
powerful tool to localize anatomy and pathology.
A major advantage of using the multiplanar mode is that views that are not easily accessible by customary 2D transabdominal or even transvaginal US such, as the sagit­tal plane, can be obtained by scrolling or navigating in the volume in a continuous fashion at will.
101
Because one can move freely in the saved brain volume in all three planes, virtually any desired diagnostic plane can be achieved.
Because spatial orientation when scrolling in the vol­ume may appear difficult for inexperienced sonographers, a standardization of transabdominal and transvaginal 3D images is strongly recommended. This will in turn avoid erroneous topographical interpretations. We refer the reader to the literature
102
for a thorough description of standardization of 3D images. Still, different operators and centers may have their preferred way to display the “starting” orthogonal display. However, our group usually displays the orthogonal planes on the screen as follows: in box A, regardless of the acquisition plane, the coronal section of the head; in box B, the median section with the fetal face facing box A (this allows the right and left sides to
86
Figure 2–78. Multiplanar display of the fetal brain at 22 weeks’ gestation in the three orthogonal planes: the coronal plane in box A, the median plane
in box B, and the axial plane in box C. Note the “marker dot” representing the intersection of the three orthogonal planes (arrows), which is placed in this image in the cavum septi pellucidi.
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
AB
C
be displayed as in traditional imaging); in box C, the axial section with the forehead facing inferior on the screen ( Figure 2–80 ). Other groups using different US equipment might display the three planes of the volume in a different manner, with box C demonstrating the sagittal section of the fetal head. There is one advantage to leaving the display unaltered without any rotation: one can realize in which plane the volume was acquired.
Once the volume is orientated as desired, one can start navigating or scrolling in the volume. Each box can be “activated” so that all the functions selected will pertain to that box only. A systematic scrolling protocol is suggested to perform a complete sweep in each of the three orthogo­nal planes in order to include all the recommended planes
AB
for dedicated neurosonography. Using five to seven con­tinuous coronal, three sagittal, and three axial sections will allow a detailed evaluation of the fetal brain anatomy. In addition, other sections and planes can be generated at will.
Multiplanar Mode and Evaluation of Midline Structures
Although 3D US has not been proven to be superior to 2D US in the evaluation of the intracranial anatomy, the use of 3D reconstruction of sagittal planes has been proposed in the literature as an adjunct to traditional 2D neurosonography for evaluating midline structures.
103 – 106
CD
Figure 2–79. Multiplanar display of a fetal face at 32 weeks’ gestation in the three orthogonal planes: the coronal plane in box A, the median plane in
box B, the axial plane in box C, and a rendered image showing the fetal face in box D are presented. Note how both imaging modalities, the multiplanar display and the surface rendering mode, can be used to complement each other. The “marker dot” is placed in this image on the tip of the nose and one can evaluate the integrity of the upper lip on the coronal plane of the multiplanar display and on the rendered image.
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
Anterior
87
1
3
Before manipulation
A
Figure 2–80. Multiplanar image of the fetal brain before and after manipulation of the volume in order to display the three orthogonal planes as
desired. (A) Before manipulation the following steps were performed: 1) the marker dot in box B was placed in the cavum septi pelucidi; 2) 90° Z axis rotation of the axial image in box C was performed so that the front of the fetal head faces downwards; 3) “fine-tune” into the perfect orientation of the three orthogonal planes in order to achieve a perfect alignment in all planes was performed. (B) After manipulation, the orthogonal planes are displayed as follows: in box A, the coronal section of the head, in box B, the sagittal section with the fetus facing the left side of the screen, and in box C, the axial section with the forehead facing inferior on the screen.
2
This is especially useful when a median plane is difficult to obtain due to unfavorable fetal position or when exam­iners do not use a transvaginal approach. In such cases, 3D US imaging enables a rapid and easy mode to obtain the median plane by scrolling in the volume, as described previously.
A good correlation has been demonstrated between the median plane obtained directly by 2D US and those reconstructed with 3D US.
103
Recent studies, including our experience, have shown improved visualization of midline structures, such as the corpus callosum, the brainstem, and the vermis, with 3D US.
104 – 106
Because direct visualiza­tion of the corpus callosum using standard axial planes is not feasible due to its arched shape, coronal and median planes have to be obtained using a 2D transvaginal or transabdominal approach. However, a 3D reconstructed sagittal plane may be obtained from an axial or coro­nal approach, allowing rapid and easy evaluation of the midline structures. Most authors demonstrated that this technique enables adequate evaluation of the corpus cal­losum through the transabdominal scanning route.
100 – 103
However, the following aspects specific to visualization of the corpus callosum and structures of the posterior fossa have to be considered.
The appearance of the reconstructed image will depend on the plane of the volume acquisition. When a 3D transabdominal scanning is performed, and a median plane approach is used, the corpus callosum appears as a thin sonolucent stripe with well-defined echogenic contours ( Figure 2–81A ) On a reconstructed image from an axial plane, some authors suggest that the cor­pus callosum is depicted as a comma-shaped echogenic structure overlying the cavum septi pellucidi (CSP); others that the corpus callosum may not be differentiated clearly from the CSP,
106 – 108
and a single anechoic comma-
104 – 105
shaped image on top of the third ventricle is seen instead
Right Left
Posterior
Right Left
B
Anterior
After manipulation
Posterior
( Figure 2–81B ). Interestingly, other authors believe that this echogenic structure overlying the CSP corresponds instead to the interface of the cingulate gyrus, the cin­gulate sulcus, the CSF, and the blood flow of the callosal arteries.
109
Therefore, because these may be only indirect signs of callosal integrity, when brain pathology is sus­pected, a median plane approach is highly recommended in order to visualize directly the corpus callosum.
Multiplanar Mode and Evaluation of the Posterior Fossa
One of the main advantages of using the multiplanar mode to evaluate the posterior fossa is that it enables simulta­neous visualization of the three orthogonal planes of the cerebellum ( Figure 2–82 ). This allows an easier and more rapid assessment of the integrity of the vermis, along with its size and position. However, at times, when evaluat­ing the posterior fossa with 3D US, a suboptimal quality image is obtained, and the infratentorial structures, such as the cerebellum, the vermis, the fourth ventricle, and the cistern magna, are blurred. This is due to acoustic shadowing of the petrous ridges of the bony base of the skull. When an axial approach is used, this shadowing can be minimized by keeping an angle of ∼45° between the incident US beam and the midline, as suggested by Pilu et al.
108
When the sagittal or coronal plane of acquisi­tion is used in scanning through the posterior fontanelle, image quality can be improved. Other experts suggest the use of a transabdominal transfontanellar approach to improve visualization of the cerebellar structures, as well as the corpus callosum.
Multiplanar Mode and the Three-Horn View
108
Evaluation of the lateral ventricles is part of fetal neu­rosonography. This includes the measurement of the
88
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
A
B
Figure 2–81. Multiplanar analysis of an ultrasound volume of the fetal head obtained by transabdominal scanning: (A) volume acquired using a sagit-
tal plane and (B) volume acquired using an axial plane. Note the difference of resolution of the CC. When a sagittal plane is used, the CC appears as a thin sonolucent stripe with well-defined echogenic contours (arrows). When an axial plane is used, the CC is not easily differentiated from the cavum septi pellucidi. Sometimes a thin echogenic contour that separates it from the underlying CSP (thin arrow) and a comma-shaped echogenic structure overlying both the CC and CSP (arrow head) are seen, as demonstrated in this case.
atrium of the lateral ventricle in the axial plane.
110 , 111
Other measurements of the ventricular system using transab­dominal and transvaginal transfontanelle US have been previously published.
32,112,113
However, our observations led us to believe that the “classical” measurement of the lateral ventricles in the axial plane does not truly represent
proper volume of the fetal brain, it takes only few minutes to manipulate the volume in order to accomplish the three­horn view, as described elsewhere ( Figure 2–83 ). This view can be used to compare the appearance of the ventricular horns and their sizes, providing diagnostic and clinically
useful information. the dynamic and progressive change in shape and size that takes place in all three horns. We therefore looked for a single scanning plane that reveals all three horns (anterior, posterior, and inferior) simultaneously. We termed this plane the “three-horn view.”
114
This scanning plane can be visualized with 2D transvaginal transfontanelle sonography when an oblique section of the brain is obtained; this sec­tion is lateral to the median section of the brain. However, using 3D US is an easier way to obtain the three-horn view, regardless of the acquisition plane. After obtaining the
Tomographic Display
This mode allows a successive and sequential display in which multiple images parallel to each other are displayed at the same time. It is one of the most useful static display modalities used during fetal neuroscan because it enables the visualization of serial sections similar to those used by CT and MRI. One can alternate and create tomographic series using all three orthogonal planes ( Figures 2–84 ,
Chapter 2 Normal Two- and Three-Dimensional Neurosonography of the Prenatal Brain
89
Vermis
ch ch
A
B
bs
4v
T
v
cm
v
Cerebellar hemispheres
C
Figure 2–82. Multiplanar analysis of an ultrasound volume depicting the posterior fossa of a normal fetal brain at 22 weeks acquired by transabdomi-
nal ultrasound using the sagittal fontanelle as an acoustic window . This mode allows simultaneous visualization of the three orthogonal planes of the cerebellum and the main landmarks in order to assess the integrity of the vermis. In the coronal (A) and the axial plane (C) the cerebellar vermis (v) is shown as an echogenic structure in between the two cerebellar hemispheres (ch), which are less echogenic. In the median plane (B), the vermis together with other structures seen on that view such as the tentorium (T), the fourth ventricle (4v), the cistern magna (cm), and the brainstem (bs) are presented. Note that the “marker dot” is placed on the vermis.
Right
Left
Right Left
A
AH
CP
T
IH
PH
C
AH
PH
CP
T
IH
Right 3 horn view Left 3 horn view
BD
Figure 2–83. The “three-horn views” of a normal fetal brain at 22 weeks. In order to generate the right 3HV, first the desired coronal plane is selected
and aligned with the other two orthogonal planes. Then the marker dot (arrowhead) is placed in the right lateral ventricle and the mid-coronal plane is rotated to the right as shown in image a. The result is the 3HV shown in a parasagittal view (highlighted in a box) as presented in image b. To obtain the left 3HV, the first step is identical to that of obtaining the right 3HV. The only difference is that the mid-coronal plane is rotated to the left as shown in image c. The result is the 3HV shown in a parasagittal view (highlighted in a box) presented in image d. Note in both lateral ventricles the thin anterior horn (AH), the posterior horn (PH) of normal size, and the closed inferior horn (IH). Other structures seen on that view are the choroid plexus (CP) and the thalamus (T).