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DOI: 10.1148/radiol.2423060297
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(Radiology 2007;242:840-845.)
© RSNA, 2007

Neuroradiology

Somatotopic Organization of Thalamocortical Projection Fibers as Assessed with MR Tractography1

Kei Yamada, MD, PhD, Yoshinari Nagakane, MD, Kenji Yoshikawa, MD, PhD, Osamu Kizu, MD, PhD, Hirotoshi Ito, MD, PhD, Takao Kubota, MD, PhD, Kentaro Akazawa, MD, Hiroyuki Oouchi, MD, Shigenori Matsushima, MD, Masanori Nakagawa, MD and Tsunehiko Nishimura, MD, PhD

1 From the Departments of Radiology (K. Yamada, O.K., H.I., T.K., K.A., H.O., S.M., T.N.) and Neurology (Y.N., K. Yoshikawa, M.N.), Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kajii-cyo, Kawaramachi Hirokoji Sagaru, Kamigyo-ku, Kyoto City, Kyoto 602-8566, Japan. Received February 15, 2006; revision requested April 20; revision received April 27; accepted May 31; final version accepted June 29. Address correspondence to K. Yamada. (e-mail: kyamada{at}koto.kpu-m.ac.jp).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively evaluate the course of sensory fibers through the supratentorial brain with diffusion-tensor–based tractography.

Materials and Methods: This study was approved by the institutional review board. Informed consent was obtained. Seven healthy volunteers (five men, two women; age range, 20–55 years) underwent 1.5-T magnetic resonance imaging. Diffusion-tensor images with isotropic voxels (2 x 2 x 2 mm) were obtained by using a single-shot echo-planar imaging technique, with a motion-probing gradient in 15 orientations, a b value of 1000 sec/mm2, and nine signals acquired. The total imaging time was approximately 30 minutes. Fiber tracking of the sensorimotor pathways was performed with the fiber assignment by continuous tracking method.

Results: All the pyramidal tracts rotated anteriorly as they traveled through the centrum semiovale. On the other hand, the sensory tracts rotated posteriorly as they coursed through the centrum semiovale toward the cortex. When the sensorimotor tracts were viewed as a unit, the tracts of the lower extremity formed the axis of rotation around which the other parts of the pyramidal and sensory homunculus rotated.

Conclusion: Sensorimotor fibers of the lower extremity form an axis of rotation, around which the pyramidal fibers rotate anteriorly and the sensory fibers rotate posteriorly.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Somatotopic representations of the homunculus of the primary motor cortex have been well documented in textbooks and in the literature (1–3). The face and tongue parts of the homunculus are located at the most inferolateral part of the precentral gyrus on the lateral surface of the cerebral hemisphere, whereas the lower extremity part is located on the medial surface of the cerebral hemisphere. As the corticospinal tract courses caudally through the centrum semiovale, the face and tongue parts of the homunculus turn anteriorly relative to the leg and trunk parts. (We refer to this as "anterior rotation.") Thus, the homunculus appears upright at the level of the centrum semiovale on transverse images of the brain. As the tract passes through the internal capsule, the homunculus continues to turn further in the same direction (2,3). When the corticospinal tract reaches the internal capsule, the motor homunculus has turned medially by approximately 90°.

The corresponding sensory homunculus of the primary sensory cortex in the parietal lobe lies posterior to the motor homunculus at the level of the sensory cortex of the parietal lobe, which is where the projection fibers from the ipsilateral thalamus terminate. The sensory homunculus at the level of the thalamus lies such that the head part of the homunculus is medial (at the ventroposteromedial nucleus) and the lower extremity part of the homunculus is lateral (within the ventroposterolateral nucleus). The thalamocortical projection starts from this head-medial homunculus, courses through the posterior quarter of the internal capsule (4–6), and ends at the cortex in a head-lateral position.

The course of the corticospinal tract through the centrum semiovale has been demonstrated; however, to our knowledge, the course of the thalamocortical projection through the centrum semiovale has not been fully documented in an experimental or clinical study (4,6–8). In certain textbooks, the trajectory of the thalamocortical projection is shown as being completely parallel to that of the pyramidal tract (2). In this case, the head part of the homunculus turns anteriorly to the lower extremity part of the homunculus (anterior rotation) as it courses through the centrum semiovale. However, to our knowledge, it has not been determined whether the sensory homunculus at the thalamus turns anteriorly to reach the lateral position or whether it turns posteriorly. Thus, the purpose of our study was to prospectively evaluate the course of sensory fibers through the supratentorial region of the brain with diffusion-tensor–based tractography (9,10).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Volunteers
This study was approved by the institutional review board. Seven healthy volunteers (five men, two women) were recruited and gave informed consent. These volunteers ranged in age from 20 to 55 years. None of the subjects had any known neurologic abnormality or history of severe head trauma. No abnormalities were found on the magnetic resonance (MR) images.

Imaging
All images were obtained with a 1.5-T whole-body MR imager (Gyroscan Intera; Philips Medical Systems, Best, the Netherlands). An acquisition time of approximately 30 minutes was used for diffusion-tensor imaging. Images were acquired by using a single-shot echo-planar imaging technique with the following parameters: 6000/88 (repetition time msec/echo time msec), with a motion-probing gradient in 15 orientations; b value, 1000 sec/mm2; and nine signals acquired. A parallel imaging technique was used to record data with a 128 x 128 spatial resolution for a 256 x 256-mm field of view. A total of 41 sections were obtained, with a section thickness of 2 mm and no intersection gap. Thus, the pixel size was isotropic (2 x 2 x 2 mm).

Image Analysis
We transferred the diffusion-tensor imaging data to an offline workstation (Precision 530; Dell, Round Rock, Tex); Pride software (Philips Medical Systems) was used for image analysis. Anisotropy values were calculated for each pixel, and color maps were created by using a previously described method (11–13). We used the Runge-Kutta method for interpolation of the tensors. Eigenvectors were translated into neuronal trajectories with the fiber assignment by continuous tracking method; the brute force approach was not used (9). The step size was 0.9 voxel. The procedure for mapping neural connections began with the designation of two regions of interest (ROIs) in a three-dimensional space. Fiber tracts that passed through both ROIs were designated the final tracts of interest. Tracking was terminated (stop criteria) when a pixel with low fractional anisotropy, a predetermined trajectory curvature between two contiguous vectors, or both was reached. We used a fractional anisotropy value of 0.3 and an inner product of 0.8 as our default stop criteria.

When tracking the pyramidal tract, we placed the ROIs so that they covered the unilateral ventral pons and part of the motor cortex (Fig 1). The motor cortex was identified on the basis of morphologic features of the sulci at the vertex. An ROI was placed on the color-coded vector map to facilitate identification of subcortical white matter. For the sensory tract, a pair of ROIs was placed at the dorsal part of the midbrain, pons, or both and the sensory cortex. The ROIs in the cortex were divided into three regions to characterize the rotation of the homunculus (Fig 1). The ROIs were placed by one operator (K.Yamada).


Figure 1
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  		Figure 1: Schematic illustrations of an ROI setting for sensory and pyramidal tractography. We used the same brainstem ROI for all three corresponding cortical ROIs. The upper extremity region of the cortical ROI is purple, the trunk region is blue, and the lower extremity region is orange. C = caudate nucleus, P = putamen, Th = thalamus, and VP = ventropostero nuclei.

 
The course of both the pyramidal tract and the sensory tract was assessed on transverse sections. Section-by-section measurements of the rotational angles of these tracts were obtained to enable characterization of the course of these tracts (Fig 2). Angles were measured on the transverse images, with 0° representing the 12 o'clock position. To incorporate the results obtained in both hemispheres, we measured the rotational angles in a clockwise fashion in the left hemisphere and in a counterclockwise fashion in the right hemisphere.


Figure 2
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  		Figure 2: Schematic illustrations of sensorimotor tracts at four levels of the brain. Triangles represent motor tracts, and circles represent sensory tracts. The color scheme is similar to that of Figure 1 (orange, lower extremity tract; blue, trunk tract; and purple, upper extremity tract). When we measured the rotational angles, we defined 0° as the 12 o'clock position (blue line). The angles formed between the sensorimotor tracts and the 0° line were recorded every 6 mm from the vertex to the level of the thalamus.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Seven pairs of pyramidal and sensory tracts were successfully depicted (Fig 3). All the pyramidal tracts had an anterior rotation, which corresponded to the known trajectory of the pyramidal tract through the centrum semiovale (2,3). This finding enabled us to confirm that tractography is a valid technique for depicting the normal anatomy of white matter bundles in the brain.


Figure 3
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  		Figure 3: Representative sensorimotor tracts of the left cerebral hemisphere are shown. Depicted fiber tracts are superimposed on transverse diffusion-weighted MR images (6000/88). The color tracts represent the homunculus tracts (orange, lower extremity; blue, trunk; and purple, upper extremity). The pyramidal tract has an anterior rotation (green arrows), whereas the sensory tract has a posterior rotation (blue arrows). Circles were placed on the sensory and motor fibers, respectively.

 
On the other hand, the thalamocortical projection of the sensory fibers had a posterior rotation as it coursed through the centrum semiovale. The sensory homunculus at the level of the thalamus was oriented in a horizontal fashion, with the head-medial homunculus. As the sensory homunculus rotated posteriorly as it traveled through the centrum semiovale, it became inverted when it reached the level of the lateral ventricle. The sensory homunculus turned further in the same direction until it reached the sensory cortex.

Section-by-section measurements of the rotational angles of the sensory and pyramidal tracts were plotted (Fig 4). When the path of the sensorimotor tracts through the supratentorial brain was divided into three segments of equal length (ie, vertex, centrum semiovale, and thalamus), an acute rotation was typically observed at the levels of the vertex and thalamus. In the middle compartment (centrum semiovale), there was no substantial change in angle. In the middle part of the sensorimotor tracts, both the sensory and the pyramidal tracts were aligned in the anteroposterior direction (0° for the pyramidal tract and 180° for the sensory tract).


Figure 4
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  		Figure 4: Schematic illustration shows the rotation angles of the sensorimotor tracts in each case. The angles of the fiber tracts from both hemispheres are incorporated. The sensory tract shows a posterior rotation of approximately 200°. The pyramidal tract (PT) shows an anterior rotation of approximately 90°.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
ADVANCES IN KNOWLEDGE
 References
 
In our study, we used diffusion-tensor–based tractography to demonstrate the course of the thalamocortical projection fibers through the internal capsule and centrum semiovale; to our knowledge, this has not been previously studied in detail. The sensory trajectory from the thalamus starts at both the ventroposteromedial and the ventroposterolateral nuclei. When viewed on a transverse section of the MR image, the sensory homunculus at the level of the thalamus is situated in a horizontally oriented position, with the head part of the homunculus at the medial aspect and the leg and trunk parts at the lateral aspect. Our tractographic findings show that the thalamocortical projection of this thalamic homunculus rotates posteriorly into an inverted position as it travels through the centrum semiovale. As the tract progresses further toward the cortex, it turns further in the same direction until it reaches the sensory cortex.

On the other hand, the motor homunculus rotates anteriorly as it travels toward the internal capsule. This has been documented in textbooks and in the literature (2,3). There is more information regarding the anatomy of the pyramidal tract than the anatomy of the sensory tract (14–18); this imbalance is probably due to the clinical importance of the pyramidal tract for daily activity.

When the sensory and motor fibers are observed as a unit, it becomes apparent that the sensorimotor fibers of the lower extremity are in close proximity as they travel through the supratentorial region of the brain. In other words, the sensorimotor fibers of the lower extremity form an axis of rotation, around which the pyramidal fibers rotate anteriorly and the sensory fibers rotate posteriorly. There are possible clinical implications of this somatotopic organization of the sensorimotor tracts.

Radical surgical removal of supratentorial gliomas is advantageous in terms of survival rate and quality of life (19,20). The avoidance of pyramidal tract damage during surgery in such cases is of primary importance to maintain postsurgical activities of daily living; the MR tractographic technique is an attractive tool for such cases (21,22). However, even with such advanced imaging guidance, the border between healthy brain tissue and the infiltrating tumor is often unclear during surgery. Thus, intraoperative neurophysiologic tests are increasingly being used to minimize the danger of damaging vital areas of the brain (22,23). Knowledge of the somatotopic organization of the sensory and pyramidal tracts obtained in our study may further aid in the effective use of these intraoperative electrophysiologic examinations.

For example, when a surgeon performs surgical resection of a tumor located near the pyramidal tract at the level of the centrum semiovale, the disappearance of sensory-evoked potential of the lower extremity may indicate that the surgeon is coming close to the pyramidal tract of the lower extremity, since we now know that the sensorimotor fibers of the lower extremity are aligned tightly together throughout their trajectory through the supratentorial region of the brain.

The anteroposterior alignment of the pyramidal fibers at the level of the centrum semiovale may be another characteristic feature that may aid in the use of the motor-evoked potential. It may be assumed that when one approaches the pyramidal tract from the anterior aspect, the motor-evoked potential of the face and tongue parts of the homunculus will react earlier than will the upper or lower extremity parts. Thus, it can be presumed that face and tongue fibers are more sensitive than upper or lower extremity fibers, and thus physicians may wish to monitor the face and tongue fibers to avoid damaging the main body of the pyramidal tract.

The second clinical implication of this study is that the somatotopic organization of the sensorimotor tracts may help explain the mechanism of certain clinical symptoms encountered in patients with small infarcts involving the centrum semiovale. For instance, pure motor hemiparesis is a type of acute stroke that involves the face, arm, and leg on one side of the body and occurs in the absence of a sensory deficit, homonymous hemianopsia, aphasia, agnosia, or apraxia (24). This type of stroke was studied extensively in the era before MR imaging, and it was found that involvement of the lower extremity alone is a rare event in patients with pure motor hemiparesis (25). The paucity of such cases may be explained by the fact that the sensorimotor fibers of the lower extremity are spatially situated close together; this makes it difficult for an infarct to involve the pyramidal tract but spare the adjacent sensory tract. Thus, the incidence of certain stroke types may simply be a reflection of the characteristic somatotopic organization of the sensorimotor fibers in certain regions of the brain.

There was a recent retrospective clinicoradiologic correlation study of 54 cases with small infarcts involving the centrum semiovale (26). The authors indicated that there could be an anteroposterior organization of the pyramidal tract, as suggested by the correlation of the location of the infarct and the clinical symptoms. Their findings are in good agreement with the findings of our study, which showed a similar anteroposterior organization. Further clinicoradiologic correlations with diffusion-weighted imaging and MR tractography (27,28) may lead to a better understanding of the anatomy and symptoms.

There were some study limitations that deserve comment. First, tractography is currently able to depict only part of the pyramidal tract, since fibers cross at the level of the centrum semiovale (29–32). Thus, the fibers that are depicted with the current imaging technique include only those that originate from the vertex—namely the arm, leg, and trunk fibers of the primary motor cortex. Other parts of the pyramidal tract can be depicted only with more advanced techniques (29,30,33,34). Thus, it must be kept in mind that in this study we analyzed only a limited part of the entire set of fan-shaped sensory and pyramidal tracts. Second, the sensory system consists of multiple modalities, including heat, pain, touch, and deep sensation. The organization of these different modalities was not considered in this study, as it is impossible to discriminate the fibers associated with these modalities with current spatial resolution. We did not consider imaging sensory fibers that originate from the thalamus and end at the prefrontal or motor cortices. Third, we did not perform a direct correlation of MR imaging and histologic analysis findings. A direct comparison between dissected brain specimens and MR tractographic images is the next step to consolidate our knowledge.

In summary, the sensory and pyramidal fibers of the lower extremity form an axis of rotation, around which the pyramidal tract rotates anteriorly to reach the internal capsule and the sensory fibers rotate posteriorly from the thalamus toward the sensory cortex of the parietal lobe. To our knowledge, this organization of the sensorimotor tracts through the centrum semiovale has not been described previously, and it could have clinical implications for neurosurgery and neurology. Future prospective studies that address the clinicoradiologic correlation of data in patients who have experienced a stroke will be necessary to confirm the anatomic organization of the sensory and pyramidal fibers that we found.


   ADVANCES IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
References
 


   FOOTNOTES
 

Abbreviations: ROI = region of interest

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, K. Yamada, T.K.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, Y.N., K. Yoshikawa, O.K., H.I., T.K., K.A., H.O., S.M., M.N., T.N.; clinical studies, Y.N., K. Yoshikawa, O.K., H.I., T.K., K.A., H.O., S.M., M.N., T.N.; and manuscript editing, K. Yamada, M.N., T.N.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

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