Radiology
Special Report
Setsu Wakana, MD
Hangyi Jiang, PhD
Lidia M. Nagae-Poetscher,
MD
Peter C. M. van Zijl, PhD
Susumu Mori, PhD
Index terms:
Brain, anatomy, 10.92
Brain, MR, 10.121412, 10.121416,
10.121417
Brain, white matter, 10.92
Diffusion tensor, 10.121416
Special Reports
Published online before print
10.1148/radiol.2301021640
Radiology 2004; 230:77– 87
Fiber Tract– based Atlas of
Human White Matter
Anatomy1
Two- and three-dimensional (3D) white matter atlases were created on the basis of
high-spatial-resolution diffusion tensor magnetic resonance (MR) imaging and 3D
tract reconstruction. The 3D trajectories of 17 prominent white matter tracts could
be reconstructed and depicted. Tracts were superimposed on coregistered anatomic
MR images to parcel the white matter. These parcellation maps were then compared with coregistered diffusion tensor imaging color maps to assign visible structures. The results showed (a) which anatomic structures can be identified on
diffusion tensor images and (b) where these anatomic units are located at each
section level and orientation. The atlas may prove useful for educational and clinical
purposes.
©
Abbreviations:
DT ⫽ diffusion tensor
MPRAGE ⫽ magnetization-prepared
rapid gradient echo
ROI ⫽ region of interest
3D ⫽ three-dimensional
2D ⫽ two-dimensional
1
From the Department of Radiology
and Radiological Science, Johns Hopkins University School of Medicine,
217 Traylor Bldg, 720 Rutland Ave,
Baltimore, MD 21205; and F. M. Kirby
Research Center for Functional Brain
Imaging, Kennedy Krieger Institute,
Baltimore, Md. From the 2002 RSNA
scientific assembly. Supported by National Institutes of Health grants RO1
AG20012– 01 and P41 RR15241– 01.
Received December 12, 2002; revision
requested February 25, 2003; revision
received May 8; accepted August 21.
Address correspondence to S.M.
(e-mail: susumu@mri.jhu.edu).
Author contributions:
Guarantor of integrity of entire study,
S.M.; study concepts and design,
S.M.; literature research, S.M., S.W.;
clinical studies, S.W., S.M.; experimental studies, S.W., L.M.N.P.; data
acquisition, S.W., H.J.; data analysis/
interpretation, S.W., H.J., L.M.N.P.;
manuscript preparation, S.M., S.W.;
manuscript definition of intellectual
content, S.M., P.C.M.v.Z.; manuscript
editing, S.M., S.W.; manuscript revision/review, S.M., S.W., P.C.M.v.Z.;
manuscript final version approval, all
authors
©
RSNA, 2003
RSNA, 2003
Diffusion tensor (DT) imaging is a magnetic resonance (MR) imaging technique that can
be used to characterize the orientational properties of the diffusion process of water
molecules (1,2). Usually, the information is contracted to two types of parameters: diffusion anisotropy, which represents the amount of directionality, and orientation of the axis
along which water molecules move preferentially. Application of this technique to the
brain has been demonstrated to provide exceptional information on white matter architecture (3–7). Because at present there are no other imaging modalities that can provide
equivalent information, DT imaging is expected to become an important tool for the study
of brain anatomy and the diagnosis of various white matter abnormalities. Recent developments in postprocessing algorithms for DT imaging also allow study of the threedimensional (3D) configuration of major white matter tracts, for which good agreement
with postmortem anatomic studies has been reported (8 –12).
Various types of DT imaging visualization schemes have been postulated. Orientationbased color coding (or, simply, color mapping) is a visualization approach in which the
image brightness represents diffusion anisotropy, while a red-green-blue color scheme
indicates tract orientation, assuming that the preferential diffusion axis coincides with the
fiber orientation (5,13). This color map presentation has already proved to be useful for
several brain diseases (5,14 –19), and, owing to the increased availability of MR units
equipped with DT imaging capabilities, it is expected to become an important routine
diagnostic method in the near future. This color map may pose some challenges to
neuroradiologists, however, because the contrast and anatomic information it provides is
complex and requires detailed knowledge of the 3D architecture of white matter. In
addition, various intra–white matter structures that can be visualized on DT imaging color
maps have not yet been clearly assigned. The purpose of our study was to create twodimensional (2D) and 3D white matter anatomic atlases based on high-spatial-resolution
DT imaging data.
IMAGING
Subjects
Data were acquired in four healthy volunteers (three men, one woman; age range, 21–29
years). The subjects did not have any history of neurologic abnormality. Institutional
review board approval was obtained for the study, and informed consent was obtained
from all subjects.
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Data Acquisition
A 1.5-T MR unit (Gyroscan NT; Philips
Medical Systems, Best, the Netherlands)
was used. DT imaging data were acquired
by using a single-shot echo-planar imaging sequence with the sensitivity-encoding, or SENSE, parallel-imaging scheme
(reduction factor, 2.5) (20,21). The imaging matrix was 112 ⫻ 112, with a field of
view of 246 ⫻ 246 mm (nominal resolution, 2.2 mm) zero filled to 256 ⫻ 256
pixels. Transverse sections of 2.2-mm
thickness were acquired parallel to the
anterior commissure–posterior commissure line. A total of 55 sections covered
the entire hemisphere and brainstem
without gaps. Diffusion weighting was
encoded along 30 independent orientations (22), and the b value was 700 mm2/
sec. Five additional images with minimal
diffusion weighting (b ⫽ 33 mm2/sec)
were also acquired. The acquisition time
per dataset was approximately 6 minutes.
To enhance the signal-to-noise ratio, imaging was repeated six times. Coregistered magnetization-prepared rapid gradient-echo (MPRAGE) images of the same
resolution were recorded for anatomic
guidance.
Data Processing
The DT imaging datasets were transferred to a workstation and processed by
using DtiMap (H. Jiang, S. Mori; Johns
Hopkins University, mri.kennedykrieger
.org). All diffusion-weighted images were
visually inspected by two authors (S.W.,
S.M.) for apparent artifacts due to subject
motion and instrument malfunction.
Subsequently, the six independent elements of the 3 ⫻ 3 diffusion tensor were
calculated by two authors (S.W., L.M.N.P.)
for each pixel by using multivariate linear fitting method. After diagonalization,
three eigenvalues and three eigenvectors
were obtained (1). For the anisotropy
map, fractional anisotropy was used. The
eigenvector associated with the largest
eigenvalue was used as an indicator of
fiber orientation. On the DT imaging
color maps, red, green, and blue colors
were assigned to right-left, anterior-posterior, and superior-inferior orientations,
respectively (13).
Three-dimensional Tract
Reconstruction
For the 3D tract reconstruction, the fiber assignment by means of continuous
tracking, or FACT, method (8,23,24) was
used, with a fractional anisotropy threshold of 0.15 and an inner product thresh78
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Figure 1. Diagram shows the three operations used in this study. A, AND and NOT operations.
Two ROIs (green) are placed on anatomic landmarks. When the AND operation is used, tracts that
penetrate both ROIs are selected. In this example, black and red tracts are selected, while blue
tracts are removed. NOT operation is used to remove specific tracts that penetrate one or multiple
ROIs (orange). In this example, red tracts are removed. B, OR operation. Multiple tracking results
when multiple ROIs are combined. AND operation poses a strong constraint in tracking results by
selecting only tracts with known trajectories. This is a conservative approach for which results are
potentially more accurate, with the disadvantage that it does not allow visualization of branching
patterns between ROIs. The OR approach may be more susceptible to noise and partial volume
effects.
old of 0.75, which prohibited angles
larger than 41° during tracking. To reconstruct tracts of interest, we used a multiple–region-of-interest (ROI) approach
(9,25–27), which exploits existing anatomic knowledge of tract trajectories.
Tracking was performed from all pixels
inside the brain (“brute force” approach),
and results that penetrated the manually
defined ROIs were assigned to the specific
tracts associated with the ROIs. When
multiple ROIs were used for a tract of
interest, we used three types of operations, AND, OR, and NOT (Fig 1), the
choice of which depended on the characteristic trajectory of each tract.
ROIs were placed by two authors (S.M.,
S.W.), who followed previously described
protocols for brainstem fibers and association fibers (25,26). Fibers connecting
the cortex and the brainstem (corticobulbar tract and corticospinal tract) were reconstructed by placing a first ROI at the
cerebral peduncle and another at the internal capsule. Among these tracts, the
corticospinal tract was identified by placing two ROIs at the pre- and postcentral
gyri and the pyramidal tract in caudal
portion of the pons.
To reconstruct thalamocortical connections, the entire 3D volume of the
thalamus was defined as the first ROI.
The second ROIs for the anterior and posterior thalamic radiations were defined
by using coronal sections, as described
previously (26). For the superior thalamic
radiation, the second ROI occupied the
entire hemisphere within a transverse
section above the corpus callosum. Fibers
in the limbic system tend to be narrow
and tubular, and a single tracking result
sometimes failed to delineate the entire
length. These tracts could be delineated
by combining multiple two-ROI results.
Specifically, the trajectories were divided
into anterior, middle, and temporal regions and were reconstructed separately
by using the two-ROI and AND operations. These results were subsequently
combined with the OR operation to depict the entire length.
Corticocortical connections through
the corpus callosum were reconstructed
by placing the first ROI in the corpus
callosum at a midsagittal level. The second ROI was placed in the corona radiata, which was defined on two coronal
sections (one anterior to the genu of and
the other posterior to the splenium of the
corpus callosum) and on one transverse
section superior to the body of the corpus
callosum. These three reconstruction results (obtained by using the two ROIs with
the AND operation) were then combined
by using the OR operation to depict the
entire corpus callosum. Additional reconstruction for temporotemporal lobe connections (tapetum) was achieved by placing the second ROI in the temporal lobe.
The NOT operation was also used to
remove a subset of projections from a
reconstruction result. An example is separation of the inferior longitudinal and
fronto-occipital fasciculi (26). The NOT
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Figure 2. Four viewing angles of 3D depictions of brainstem fibers.
A, Anterior view; B, left lateral view; C, superior view, D, oblique view
from right posterior angle. Reconstructed fibers are corticospinal tract
(cst, white), superior cerebellar peduncle (scp, purple), middle cerebellar peduncle (mcp, red), inferior cerebellar peduncle (icp, orange),
and medial lemniscus (ml, light green). For anatomic guidance, ventricles (gray), substantia nigra (sn, blue), deep cerebellar nuclei (dcn,
dark green), and thalamus (yellow) are also shown.
operation was also used to remove “relayed” projections often observed in the
thalamus. For example, if the anterior
thalamic radiation is reconstructed by using one ROI at the thalamus and the another at the frontal lobe, a small number
of projections that connect the frontal
lobe and thalamus penetrate the thalamus and proceed to various brain regions
such as the cortex, brainstem, and cerebellum. Some of these trajectories have
been reproducibly observed and may be
real connections, but they were removed
because they apparently do not comply
with the classical definition of the anterior thalamic radiation.
One of the most important limitations
of the tracking technique is that specificity may be lost for tracts that run parallel
to (or are merged with) one another. In
this situation, the tracking tends to retain
the topology: Tracts coming from the
right side to a merging point stay at the
right side, and tracts from the left side
stay at the left side (10). Because of this
limitation and the somewhat ad hoc
nature of ROI placement and the three
operations for individual tracts, the 3D
reconstruction results shown in this report should be treated as an approximation of tract configurations and locations that belong to the same tract
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Figure 3. Four viewing angles of 3D depictions of projection and
thalamic fibers. A, Anterior view; B, left lateral views; C, superior view;
D, oblique view from right anterior angle. Reconstructed fibers are
corticobulbar tracts (cbt, light blue), corticospinal tract (cst, white),
anterior thalamic radiation (atr, bright purple), superior thalamic
radiation (str, purple), and posterior thalamic radiation (ptr, dark
blue). For anatomic guidance, fibers are depicted with putamen and
globus pallidus (light green); caudate nucleus (dark green); thalamus
(yellow); and the hippocampus, amygdala, and ventricles (gray).
E, F, For better visualization of thalamic fibers, two additional lateral
views, one without putamen and globus pallidus (E) and one without
corticospinal and corticobulbar tracts (F) are also given.
systems rather than precise connectivity maps. The reconstruction protocol
described here was applied to the DT
imaging data from the four subjects,
and tracts shown in this report could be
identified in all subjects.
Three-dimensional Volume
Definition of Various Anatomic
Units
By using the coregistered MPRAGE images, the ventricles, caudate nucleus, putamen (including globus pallidus), thalamus,
hippocampus (including amygdala), substantia nigra, and deep cerebellar nuclei
were manually defined to demonstrate the
spatial relationship with various white
matter tracts in three dimensions.
Three-dimensional Demonstration
The 3D depictions of trajectories of
white matter tracts and volumes of gray
matter nuclei were generated by using software (Amira; TGS, San Diego, Calif), with
tube-type tract representation adopted
from Zhang and Laidlaw (28) and Catani et
al (27).
DEMONSTRATION OF WHITE
MATTER TRACTS: 3D
PRESENTATION
White matter tracts were classified into
five functional categories: (a) tracts in the
brainstem, (b) projection fibers (cortex–spinal cord, cortex-brainstem, and cortexthalamus connections), (c) association fibers (cortex-cortex connections), (d) limbic
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Figure 5. Four viewing angles of 3D depictions of limbic system
fibers. A, Anterior view; B, left lateral view; C, superior view;
D, oblique view from right anterior angle. Reconstructed fibers are
cingulum (cg, dark green), fornix (fx, light green), and stria terminalis
(st, yellow). For anatomic guidance, hippocampus and amygdala
(purple) and ventricles (gray) are also shown.
Figure 4. Four viewing angles of 3D depictions of association fibers.
A, Anterior view; B, left lateral view; C, superior view; D, oblique view
from right anterior angle. Reconstructed fibers are superior longitudinal fasciculus (slf, yellow), inferior longitudinal fasciculus (ilf,
brown), superior fronto-occipital fasciculus (sfo, beige), inferior frontooccipital fasciculus (ifo, orange), and uncinate fasciculus (unc, red). E,
F, Left lateral views without superior longitudinal fasciculus (E) and
inferior longitudinal fasciculus (F).
system tracts, and (e) commissural fibers
(right-left hemispheric connections).
Tracts in the Brainstem
The superior, middle, and inferior cerebellar peduncles; corticospinal tract;
and medial lemniscus were reconstructed
as shown in Figure 2 (25). For anatomic
guidance, the ventricles, deep cerebellar
nuclei, substantia nigra, and thalamus
are also shown. (Note that colors assigned here are not related to tract orientation, unlike in color maps.) One end of
the superior cerebellar peduncle terminates at the deep cerebellar nuclei; the
other, at the thalamus. Although majority of the superior cerebellar peduncle
was supposed to cross the midline at the
decussation of the superior cerebellar peduncle, the reconstructed trajectory remained in the same hemisphere. This is
due to the limitation of the fiber-tracking
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technique, which tends to provide a
“kissing” (⬎⬍) solution when two fibers
have a crossing (⫻) trajectory (10). The
trajectory of the inferior cerebellar peduncle approached the superior cerebellar peduncle from the inferolateral side
and passed through the superior side toward the medial direction. The medial
lemniscus traveled along the dorsal side
of the midbrain and pons and turned
sharply toward the ventral side of the
brainstem at the level of the medulla.
These trajectories agree well with postmortem anatomic descriptions of these
tracts (29,30).
Projection Fibers
Trajectories of the main projection fibers are shown in Figure 3. It can be seen
that the corticobulbar tract collects projections from many areas of the cortex to
the brainstem. The projection from pre-
and postcentral gyri (corticospinal tract)
reaches the pyramidal tract at the pons.
The thalamic projections and relationships with the thalamus can be seen
clearly in Figure 3, E and F, where the
putamen (Fig 3, E) and corticobulbar and
corticospinal tracts (Fig 3, F) were removed. All thalamic radiations converged into the internal capsule, located
between the putamen and the thalamus–
caudate nucleus regions. Among other
types of sensory connections between
the thalamus and cortex, the posterior
thalamic radiation includes the optic radiation. The corticobulbar and corticospinal tracts and the thalamic fibers all
penetrate the internal capsule, where the
cortex-brainstem connection occupies
the more lateral regions. This type of
preservation of topology seen in the internal capsule (ie, anterior part projecting
to frontal lobe; posterior part, to occipital
lobe; lateral part, to cortex; and medial
part, to thalamus) may be due in part to
the limitation of the tract-tracking technique, which generally does not allow
tracing of crossing (⫻) configurations.
Therefore, although the 3D reconstruction results can provide macroscopic
views of the tracts, they cannot be directly interpreted in terms of detailed
connectivity information. It is noteworWakana et al
Radiology
Figure 6. Four viewing angles show 3D depictions of callosal fibers.
A, Anterior view; B, left lateral view; C, superior view; D, oblique view
from right anterior angle. Corticocortical connections through corpus callosum (cc) are magenta. Subset of the tracts that project to
temporal lobe (tapetum) are pink.
thy, however, that the topologic preservation seen in the internal capsule actually agrees well with what has been postulated by neuroanatomists on the basis
of postmortem results (30).
Association Fibers
There are numerous types of association fibers, according to reports of postmortem anatomic studies (29 –31). These
include long-range, as well as shortrange, cortical U fibers. In this study, we
focused on four well-documented association tracts, including the superior longitudinal fasciculus, inferior longitudinal
fasciculus, inferior fronto-occipital fasciculus, and uncinate fasciculus (Fig 4). In a
previous study (26), we reported that a
white matter tract called the superior
fronto-occipital fasciculus could not be
identified with certainty by using the
tract-reconstruction approach, although
a tract of substantial size can be recognized at the location where this fascicle
should be found. Catani et al (27) showed
that this tract actually projects to the frontal and parietal lobes, and our present results confirm that finding.
Figure 4 clearly shows the 3D relationship of these association fibers. The superior longitudinal fasciculus projects to
most lateral regions of the temporal lobe
with a characteristic C-shaped trajectory.
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Figure 7. Three-dimensional presentation of projection (green), association (red), and callosal (blue) fibers. A, Anterior view; B, left
lateral view; C, superior view; D, left anterosuperior view. To demonstrate relative locations of these three families of tracts, projection
(Fig 3), association (Fig 4), and callosal (Fig 6) fibers are depicted
simultaneously. E–G, Representative transverse sections. Pixels that
share more than one family of tracts can be identified in terms of
color: Magenta is formed by red (association) plus blue (callosal);
yellow, by green (projection) plus red; and cyan, by green plus blue.
Note dominant presence of projection fibers in cortical areas around
the central sulcus (cs). acr ⫽ anterior region of corona radiata, ec ⫽
external capsule, ic ⫽ internal capsule, pcr ⫽ posterior region of
corona radiata, scr ⫽ superior region of corona radiata.
Trajectories of the inferior longitudinal
and inferior fronto-occipital fasciculi can
be more easily appreciated in Figure 4, E
and F, in which the superior and inferior
longitudinal fasciculi were removed. It can
be seen the inferior longitudinal and inferior fronto-occipital fasciculi share most of
the projections at the posterior temporal
and occipital lobes, while the uncinate and
inferior fronto-occipital fasciculi share the
projections at the frontal lobe. The superior fronto-occipital fasciculus is unique in
that it is the only association fiber tract
that projects medially to the thalamus and
along the ventricle.
Limbic System Fibers
It was possible to reconstruct the cingulum, fornix, and stria terminalis trajectories, which, together with the hippocampus and amygdala and the ventricles, are
shown in Figure 5. The cingulum extensively collected projections from the
nearby cingulate gyrus and extended into
the temporal lobe. The fornix could be easily reconstructed at its body, which projected into the hypothalamus, while the
differentiation of fornix from stria terminalis in the temporal lobe was not clear
with the current imaging resolution (2.2
mm). The cingulum travels along the venAtlas of Human White Matter Anatomy
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Figure 8. Transverse DT imaging color maps (first and third columns) and white matter parcellation maps (second and fourth columns). On
parcellation maps, locations of intercepts of various tract trajectories are shown in the same colors used in Figures 2– 6. On color maps, red, green,
and blue represent fibers running along right-left, anterior-posterior, and superior-inferior axes, respectively. Locations of white matter tracts are
assigned on color maps. Several anatomic landmarks visible on color maps are also annotated on the basis of existing anatomic knowledge. Note
that corona radiata consists of a mixture of various tracts (Fig 8 continues).
tral surface of the hippocampus, while the
fornix and stria terminalis project along
the dorsal surface.
Callosal Fibers
Results of callosal fiber reconstruction
are shown in Figure 6. The massive array of
projections forms the so-called callosal radiation, which connects the corresponding
areas of opposite hemisphere. The projections from the genu of the corpus callosum
form the forceps minor; those from the
splenium form the forceps major. There
are also strong projections from the splenium that sweep inferiorly along the lateral margin of the posterior horn of the
lateral ventricle and project into the temporal lobes; these projections are known
collectively as the tapetum.
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Topologic Relationships among
Projection, Association, and
Callosal Fibers
Unlike the fibers in the limbic system,
which all travel along the ventricles and
hippocampus, the spatial relationships
between projection, association, and callosal fibers may be difficult to appreciate.
In Figure 7, tracts that belong to projection, association, and callosal fibers are
assigned the colors green, red, and blue,
respectively, and are depicted simultaneously. It can be seen that the association fibers tend to occupy most lateral
regions; and the callosal fibers, the medial regions. On 2D images, brain areas
where these fibers overlap can be identified by means of mixed colors such as
yellow (green plus red), magenta (red
plus blue), and cyan (green plus blue).
Note that the same pixel can be shared by
different tracts if vectors in two different
pixels point to the same pixel. Figure 7,
E–G, indicates that the temporal lobe and
external capsule are occupied by association fibers; the internal capsule, by projection fibers; and the corona radiata, by
all three families of fibers.
DEMONSTRATION OF WHITE
MATTER TRACTS: 2D
PRESENTATION
Figures 8 –10 show a series of DT imaging
color maps in transverse, coronal, and
sagittal planes, respectively. Coregistered
MPRAGE images with color-coded white
matter tracts (hereafter, white matter parWakana et al
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Figure 8 (continued). ac ⫽ anterior commissure, acr ⫽ anterior region of corona radiata, alic ⫽ anterior limb of internal capsule, cbt ⫽ corticobulbar
tract, cg ⫽ cingulum, cp ⫽ cerebral peduncle, cst ⫽ corticospinal tract, dscp ⫽ decussation of superior cerebellar peduncle (scp), fx ⫽ fornix, icp ⫽
inferior cerebellar peduncle, ifo ⫽ inferior fronto-occipital fasciculus, ilf ⫽ inferior longitudinal fasciculus, mcp ⫽ middle cerebellar peduncle, ml ⫽
medial lemniscus, ot ⫽ optic tract, pcr ⫽ posterior region of corona radiata, plic ⫽ posterior limb of internal capsule, py ⫽ pyramidal tract, scr ⫽
superior region of internal capsule, sfo ⫽ superior fronto-occipital fasciculus, slf ⫽ superior longitudinal fasciculus, sn ⫽ substantia nigra, st ⫽ stria
terminalis, unc ⫽ uncinate fasciculus, ⴱ ⫽ short-range association fibers, ⴱⴱ ⫽ vertical occipital fasciculus.
cellation maps) are also shown for anatomic guidance. On the parcellation
map, the tract trajectories (identified by
using the 3D reconstruction) are superimposed on the MPRAGE images, with
the same colors used in Figures 2– 6. By
comparing the two types of images, various structures visible on the DT imaging
color maps can be assigned.
Brainstem
Identification of the corticospinal tract
and medial lemniscus on the color maps
was straightforward at the pons levels
(Fig 8, C–F). At the caudal pons-medulla
level, the medial lemniscus became narrower and almost invisible at the decussation (lower level than that in Fig 8,
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A and B). The relative locations of the
superior and inferior cerebellar peduncles
were difficult to distinguish at certain
levels of the pons (eg, Fig 8, E and F), but
side-by-side comparison with the 3Dbased parcellation information helped
identification at those section levels. At
the midbrain level, a structure with rightleft orientation could be always found at
the midline (red tracts on Fig 8, I and J).
On the basis of information regarding
the trajectory of the superior cerebellar
peduncle, which leads to this midline
structure, we determined that the structure
is the decussation of the superior cerebellar
peduncle. In addition to the white matter
tracts, the substantia nigra (Fig 8, I and J)
and deep cerebellar nuclei (Fig 8, C and D)
could be identified. The superior cerebellar
peduncle terminated at the deep cerebellar
nuclei, which agrees with the fact that neurons in the latter are the major sources of
axons of the former.
Projection and Callosal Fibers
These fibers project along the superiorinferior axis for most of their courses, and
transverse sections are the best 2D depictions for investigation of their assignment (Fig 8). At the midbrain level (Fig 8,
I–L), the corticobulbar and corticospinal
tracts could be identified in the cerebral
peduncle; the corticospinal tract occupied the center portion of the cerebral
peduncle, as has been previously reported (25). At the transverse level of the
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Figure 9. Coronal DT imaging color maps (first and third columns) and parcellation maps (second and fourth columns). See caption for Figure 8
for color coding and abbreviations.
internal capsule (Fig 8, M–P), the thalamic fibers (anterior, superior, and posterior thalamic radiations) joined the corticobulbar and corticospinal tracts. The
anterior and posterior limbs of the internal capsule contained the anterior and
superior thalamic radiations, respectively, and the retrolenticular part contained a mixture of the posterior thalamic radiation and association tracts
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(see Fig 11 for nomenclature of internal
capsule). The projection fibers extended
to the corona radiata (anterior and posterior regions of corona radiata could be
identified in Fig 8, M–R; superior region,
in Fig 8, S–X), which consisted of a mixture of various association, projection,
and callosal fibers, as also shown in Figure 7. Three colors were assigned to different regions of the thalamocortical
connections (see also Fig 3). Distributions
of these colors in the thalamus showed
that the anterior thalamic radiation is associated with dorsomedial nuclei; the superior thalamic radiation, with ventrolateral nuclei; and the posterior thalamic
radiation, with posterior nuclei (pulvinar) (Fig 11, A), which agrees well with
postmortem histologic findings (see Fig
11, B) (30).
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Figure 10. Sagittal DT imaging color maps (first and third columns)
and parcellation maps (second and fourth columns). See caption for
Figure 8 for color coding and abbreviations.
Figure 11. Comparison between 2D tracking-based parcellation of thalamus (A) and histologic
study results (B). Anterior thalamic radiation (atr) projects from anterior and medial regions of the
thalamus; superior thalamic radiation (str), from the lateral region; and posterior thalamic
radiation (ptr), from the posterior region (pulvinar). (B adapted and reprinted, with permission,
from reference 32.)
Association Fibers
These fibers travel along the anteriorposterior axis, and coronal sections (Fig
9) are most suitable for the study of their
2D locations. In the frontal lobe (Fig 9, G
and H), it can be clearly seen that many
association fibers (inferior fronto-occipital, uncinate, and superior longitudinal
fasciculi) project through the external
capsule, while the projection fibers (corticobulbar and thalamic fibers) penetrate
the anterior limb of the internal capsule.
In more anterior regions (eg, Fig 9, E and
F, and more anterior sections), the assoVolume 230
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ciation fibers merge with the projection
and thalamic fibers and further with callosal fibers in Figure 9, A and B, and more
anterior sections. The inferior fronto-occipital and uncinate fasciculi have prominent projections to fronto-orbital cortical areas, which agrees with histologic
findings (29). Throughout the levels in
Figure 9, G–L, the inferior fronto-occipital fasciculus occupies the ventral area of
the external capsule. The superior longitudinal fasciculus has a prominent projection into the frontal cortex around the
sylvian fissure (Fig 9, K–P), while the tem-
poral lobe is dominated by the inferior
longitudinal fasciculus projection. It can
be seen in Figure 9, O and P, and more
posterior sections that the inferior
fronto-occipital and inferior longitudinal
fasciculi start to merge and that projection and thalamic fibers also join to form
the retrolenticular part of the internal
capsule and the posterior region of the
corona radiata, which can be identified
on the color maps (green in Fig 9, Q–T) at
the area lateral to the ventricle. In Figure
9, S and T, the superior longitudinal fasciculus makes a sharp turn toward the
temporal lobe. On the color map, this
can be recognized as a change in color
(from green to blue), which is located
lateral to the posterior region of the corona radiata. In Figure 9, S and T, and
Figure 8, O–R, it can be seen that the
white matter lateral to the posterior horn
of the lateral ventricle consists of three
layers of tracts: The superior longitudinal
fasciculus is the most lateral, with a superior-inferior orientation; the posterior
region of the corona radiata (posterior
thalamic radiation, corticobulbar tract,
and inferior fronto-occipital and inferior
longitudinal fasciculi), with an anteriorposterior orientation is in the middle;
and the callosal projection to the temporal lobe (tapetum) is the most medial.
Limbic Fibers
Because of the complex trajectories of
the cingulum, fornix, and stria terminalis, the 3D-tracking– based parcellation
results substantially aided in the identification of these tracts on the color
map. The core of the cingulum below
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the cingulate gyrus could be easily identified on the color map due to the characteristic intense green color adjacent
to the corpus callosum. Along its
course, the cingulum collects prominent projections from the cingulate gyrus, although it is possible that the cingulum may contain some fibers from
the corpus callosum. Posterior to the
splenium of the corpus callosum (Figs
8, O–R; Fig 9, S and T), the cingulum
turns sharply (the color becomes blue
on the color map) toward the temporal
lobe and travels along the ventral surface of the hippocampus (Fig 8, G–L; Fig
9, K–T) until it reaches the amygdala.
The projection in the temporal lobe can
also be appreciated in Figures 9, G–J,
and 10, E–H.
The fornix originates in the hypothalamic area, and its anterior and posterior projections in the hypothalamus
can be identified on the color map (Fig
8, M and N). The body of the fornix can
be easily identified in Figure 9, G–P.
However, as the projection turned laterally (Fig 9, Q and R) and approached
the hippocampus, the fornix–stria terminalis distinction became obscure at
the current image resolution. Figure 10,
G–J, shows the projection of the fornix
and stria terminalis along the dorsal
surface, while the cingulum travels
along the ventral surface.
Short-Range Association Fibers
On the 2D parcellation maps shown in
Figures 8–10, there were several white matter areas that were not classified in any of
the tract families examined in this study.
Most notable is a frontal white matter area
indicated by a single asterisk (Fig 8, S and
U; Fig 9, I and K; Fig 10, G) and an area in
the lateral occipital lobe indicated by double asterisks (Fig 8, S; Fig 9, W; Fig 10, I).
Figure 12 shows results of 3D tracking performed by placing ROIs in these areas
(ROIs are shown in Fig 12). The results indicated the presence of short-range association fibers (U fibers) in these areas. The
proximity of these tracts to the superior
longitudinal fasciculus (see Fig 8, S and T)
suggests that they could be a part of that
fascicle, which is known to consist of both
short- and long-range axonal fibers (31);
the tract in the occipital lobe corresponded
to what is called the vertical occipital fasciculus (33).
DISCUSSION
Other authors have reported 3D reconstructions of white matter tracts and 2D
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color map assignments (5,13,25–27,34).
In the present study, we extended their
findings with a systematic comparison of
the 3D tract reconstruction and 2D presentation by using high-spatial-resolution DT imaging datasets.
Compared with conventional T1- and
T2-weighted MR images, the DT-based
color map provides far more information
about white matter architecture. Owing
to the increasing availability of DT imaging capabilities on clinical MR units, 2D
DT color mapping is expected to be an
important diagnostic tool in the near future. In this article, we have provided a
2D color map atlas with structural assignments, which should aid the interpretation of color maps in clinical studies. The
3D tract reconstructions served two purposes. First, they allowed us to visualize
the trajectories of a tract of interest and
the relationship of that tract with other
tracts and gray matter nuclei. Second,
once the trajectories of various tracts
were reconstructed, the assignment of
the color map structures became more
straightforward by observing the coincidence of the trajectories in the 2D plane
of interest. The 3D tract reconstruction
protocols used in this study were based
on those in previous publications by different groups (25–27), and the results
were qualitatively identical, which confirmed the high reproducibility of the reconstruction method.
The color map was created directly
from the diffusion tensor vector field,
and various tracts could be identified on
the basis of the orientation information.
Two tract systems may have the same
color if their in-plane fiber orientations
are the same, while the same tract system
often changes color if it changes orientation. On the white matter parcellation
map, the white matter was color coded
differently for each tract. As a result, the
same tract always has the same color and
different tracts have different colors, simplifying the interpretation. However,
clinical application of this approach is
less straightforward, because the parcellation map requires 3D tract reconstruction, the result of which depends on ROI
placement. The tracking result is also affected by image resolution and signal-tonoise ratio. For reproducible generation
of the parcellation map, rather strict protocols for imaging and tract reconstruction must be defined and followed.
In this study, 3D coordinate information
for each tract was superimposed on
MPRAGE images to create the parcellation
map. Although the sensitivity-encoding
acquisition drastically reduced image dis-
Figure 12. Left lateral view of 3D reconstruction shows short-range association fibers.
White boxes indicate approximate locations of
ROIs used for reconstruction. Tracts shown in
blue and magenta are white matter regions
indicated by a single asterisk in Figures 8 –10;
those shown in orange are regions indicated by
double asterisks in Figures 8 –10.
tortion related to inhomogeneity of the B0
constant magnetic induction field, a small
amount of mismatch between DT and
MPRAGE images remained around the sinus areas; thus, care must be taken when
interpreting data in these regions.
Various visible white matter structures
on the DT imaging color map were assigned. Most of these white matter tract
systems cannot be delineated on conventional MR images. The 2D and 3D white
matter atlas presented in this article should
be useful for teaching and clinical uses. The
color map used in this study delineated not
only detailed white matter anatomy but
also gray matter structures such as the deep
cerebellar nuclei and intrathalamic structures, which are difficult to identify on T1and T2-weighted MR images. The thalamus could be roughly divided into three
regions. Dorsomedial regions appeared
green (anterior-posterior orientation) and
received projections from the frontal lobe,
ventrolateral regions appeared blue (superior-inferior orientation) and received projections from superior areas of frontal and
parietal lobes, and posterior regions (pulvinar) appeared red (right-left orientation)
and received projections from the occipital
lobes. As also pointed out by Wiegell et al
(35), it may be possible to study thalamic
structures by using DT imaging in the future, when even higher resolution DT imaging maps may become available with improved technical capabilities, such as
higher magnetic field strength.
In addition to the neuroanatomy revealed by the DT images, the atlas can
provide important information for conventional MR imaging studies. For example, it has been a common practice to
place an ROI in a white matter area to
quantify such MR parameters as T1, T2,
magnetization transfer rate, and diffuWakana et al
Radiology
sion anisotropy. In this process, care
must be taken because some white matter
areas consist of a mixture of various types
of tracts or because, in some areas, a
small amount of shift in ROI placement
results in measurement of very different
white matter tracts. The atlas can be used
as a guide for the ROI placement strategy.
Although the DT and 3D reconstruction
techniques provide exciting new information about neuroanatomy, the limitations
should also be emphasized. One of the
most important limitations stems from
that fact that DT imaging reflects the averaged water diffusion property within a
pixel, which is an indirect indicator of the
axonal structures. In fact, Wedeen et al (36)
have convincingly shown that use of the
diffusion tensor calculation to delineate
the underlying axonal structures is often
an oversimplification. In many cases, DT
imaging results are biased by the dominant
axonal component. For example, it has
been reported (29,30) that callosal connections should extend not only to cortical
areas close to the midline but also to more
lateral areas. Our results failed to show
these lateral projections, probably because
of the massive projection fibers (corona radiata) located laterally to the callosal fibers.
Similarly, branches of the projection fibers
toward lateral cortical areas could not be
observed, probably because of the large
tract of association fibers running in the
anterior-posterior orientation. Therefore,
as mentioned earlier in this report, our atlases should be considered as maps of the
core of the major white matter bundles,
rather than as connectivity maps.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
CONCLUSION
Various white matter tract systems were
reconstructed by using high-spatial-resolution DT MR data sets with the goal of understanding 3D relationships between different tracts and between tracts and gray
matter structures. In order to appreciate
the detailed coordinates of the tracts of
interest, the 3D trajectories were superimposed on MPRAGE MR images and were
compared with 2D DT imaging color maps
at various section levels and orientations.
On the basis of the comparison, the color
map structures were assigned, and a 2D
color map atlas was created. The atlas may
prove useful for teaching purposes and for
future application of DT color mapping in
clinical studies.
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