710 Integrative systems
Anatomical location and somatotopic organization of the corticospinal tract in the corona radiata of the normal human brain: a diffusion tensor tractography study Hyeok Gyu Kwona, Jeong-Hee Yangb, Jun Bum Parkc, Min Ho Kime, Soon Ho Choif and Dong Seok Yangd The anatomical location and somatotopic organization of the corticospinal tract (CST) in the corona radiata (CR) of the normal human brain have not been studied using diffusion tensor tractography so far. In this study, the anatomical location and somatotopic organization of the CST in the CR were evaluated by determining the highest probabilistic locations and distances between the upper and lower extremities in the slices of upper and lower CR in the brain. In the mediolateral direction, the average of the highest probabilistic locations for the upper and lower extremities were 40.27 and 37.16% at the upper CR level and 38.19 and 37.14% at the lower CR level, respectively. In the anteroposterior direction, the average of the highest probabilistic locations for the upper and lower extremities were 62.52 and 75.65% at the upper CR level and 60.19 and 68.12% at the lower CR level, respectively. The average distances between upper and lower extremities for the mediolateral direction were 2.41 mm at the upper CR level and 1.21 mm at the lower CR level. The average distances between upper and lower extremities for the anteroposterior direction were 5.23 mm at the upper CR level and 4.47 mm at the lower CR level, respectively.
Our findings suggest that the anatomical location and somatotopic organization for the upper extremity are located anterolaterally to the lower extremity in the CR of a normal human brain and distances between the upper and lower extremities become decreased as the CST descends from the upper to the lower CR c 2014 Wolters Kluwer level. NeuroReport 25:710–714 Health | Lippincott Williams & Wilkins.
Introduction
Diffusion tensor tractography (DTT) is based on DTI and allows localizing the neural tract at the subcortical level in three dimensions [9–11]. In addition, it is a very useful tool for the measurement of an anatomical location and somatotopic organization of the CST.
The corticospinal tract (CST) is composed of long axonal bundles and is the major neural pathway. It is believed to be crucial for skillful finger movement and walking pattern simultaneously [1]. Several studies have previously suggested somatotopy of the CST in which separate upper and lower extremities may be present by brain dissection or clinic–radiologic findings [2–5]. Furthermore, specifically isolated upper extremity weakness or lower extremity weakness in a patient after a stroke using a computed tomography or an MRI has confirmed the anatomical location and somatotopic organization of the upper and lower extremities at multiple levels of the CST [6–8]. Nevertheless, those methods have several limitations in terms of lack of accuracy, indirect findings, or invasiveness. It would be a major clinical advantage to gain knowledge of the exact anatomical location and somatotopic organization of the CST for surgical planning near the CST, prediction for the prognosis of motor weakness, and a scientific rehabilitation strategy after stroke. Diffusion tensor imaging (DTI) is an advanced technique of MRI for assessment of the integrity of the neural tract in a noninvasive manner. c 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins 0959-4965
NeuroReport 2014, 25:710–714 Keywords: corona radiata, corticospinal tract, diffusion tensor tractography, somatotopic organization a Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Taegu, bDepartment of Biological Science, College of Natural Science, Sungkyunkwan University, Suwon, Departments of cNeurosurgery, dPhysical Medicine and Rehabilitation, University of Ulsan College of Medicine, eBiomedical Research Center, Ulsan University Hospital and fDepartment of Physical Therapy, Ulsan College East Campus, Ulsan, Korea
Correspondence to Dong Seok Yang, MD, PhD, Department of Physical Medicine and Rehabilitation, University of Ulsan College of Medicine, Ulsan University Hospital, 290-3 Jeonha-dong, Dong-gu, Ulsan 682-714, Korea Tel: + 82 52 250 7210; fax: + 82 52 250 8940; e-mails: [email protected]; [email protected] Received 24 February 2014 accepted 14 March 2014
To date, the anatomical location and somatotopic organization of the CSTs in the normal human brain have been confirmed from the centrum semiovale to the medullar level, not in the corona radiata (CR) [12–18]. Although the CR is known to be one of the most important sites of ischemic stroke [19], to our knowledge, there has been no study as yet on the CST in the CR of the normal human brain. Thus, we have attempted to investigate the anatomical location and somatotopic organization of the CST for the upper and lower extremities quantitatively at the upper and lower CR level using DTT.
Materials and methods Participants
We recruited 47 right-handed healthy individuals (men: 23, mean age: 33.45 years, range: 20–54 years) who had no DOI: 10.1097/WNR.0000000000000170
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Location and organization of corticospinal tract Kwon et al. 711
previous history of physical, neurological, or psychiatric illness. The Edinburgh Handedness inventory was used for the handedness [20]. This study protocol was approved by the Institutional Review Board of Yeungnam University Hospital (Daegu, Korea). Data acquisition
DTI data were obtained using a multichannel head coil on a 1.5-T Philips Gyroscan intera (Hoffman-LaRoche Ltd, Best, the Netherlands) with single-shot echo-planar imaging. Imaging was performed using a six-channel head coil. For each of the 32 noncollinear diffusion sensitizing gradients, we acquired 65 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters were as follows: acquisition matrix = 96 96 matrix, reconstructed to matrix = 128 128 matrix, field of view = 221 221 mm2, TE = 76 ms, TR = 10 726 ms, EPI factor = 49, parallel imaging reduction factor (SENSE factor) = 2, b-value = 1000 s/mm2, NEX = 1, and a slice thickness of 2.3 mm. Fiber tracking
Diffusion-weighted imaging data were analyzed using the Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB) Software Library. The head motion effect and image distortion because of eddy current were corrected by affine multiscale two-dimensional registration. The probabilistic tractography method based on a multifiber model was used for fiber tracking and applied to the present study utilizing tractography routines implemented in FMRIB diffusion (0.5 mm step lengths, 5000 streamline samples, curvature thresholds = 0.2) [21]. CSTs for both upper and lower extremities were determined by the selection of fiber passing through two regions of interests (ROIs) on the basis of studies by Kwon et al. [13] and Seo et al. [18]. The seed ROIs for the upper and lower extremities were placed on the precentral knob (somatotopy for the upper extremity) and the dorsomedial part (somatotopy for the lower extremity) of the primary motor cortex on the axial slices map, respectively (Fig. 1a, left top). The target ROI was located at the anterior portion of pontine on the color map (part of the anterior blue color) (Fig. 1a, left bottom). Measurement of the corticospinal tract location at the upper and lower corona radiata level
The anatomical location of the CST in the CR was evaluated as the highest probabilistic location (%) in the slices of the upper and lower CR for each participant. As shown in Fig. 1b, we defined the boundary as follows: the most anterior point of the lateral ventricle (anterior boundary), the most posterior point of the lateral ventricle (posterior boundary), and midline (medial boundary), and the most lateral point of the cerebral cortex (lateral boundary). The anatomical location of the CST was measured laterally from the medial boundary in the mediolateral (ML) direction and posteriorly from the
anterior boundary in the anteroposterior (AP) direction. CST probabilistic maps were acquired by overlapping of the highest probabilistic location. The probabilistic map was superimposed on a mean non-diffusion-weighted image to create a mean of all participants of nondiffusion-weighted images using the SPM19 software (SPSS Inc., Chicago, Illinois, USA). Measurement of average distance for the highest probability location between the upper and the lower extremities
The average distance for the highest probability location between the upper and the lower extremities was measured as each location of the point. It was calculated as a pixel unit and then converted into millimeters. The pixel unit is 1.73 mm (X) 1.73 mm (Y). Statistical analysis
The highest probabilistic location of the CSTs was used for performance of an independent t-test for determination of variances. The significance level of the P value was set at P value less than 0.05.
Results The probabilistic tracking of the CSTs for the upper and lower extremities was visualized in three dimensions from the cortex to the pons in all participants (Fig. 1a, right). We confirmed that CSTs for the upper and lower extremities run from the cortex to the medulla along the known pathway of the CST separately. In the ML direction, the highest probabilistic locations for the upper and lower extremities were 40.72% : 37.16%, 40.27% : 36.80%, and 41.20% : 37.52% (average, right, left) from the medial boundary at the upper CR level, and 38.19% : 37.14%, 37.72% : 36.90%, and 38.65% : 37.38% (average, right, left) from the medial boundary at the lower CR level, respectively. In the AP direction, the highest probabilistic locations for the upper and lower extremities were 62.52% : 75.65%, 62.14% : 76.63%, and 62.90% : 74.68% (average, right, left) from the anterior boundary at the upper CR level, and 69.19% : 68.12%, 60.30% : 69.24%, and 60.08% : 67.00% (average, right, left) from the anterior boundary at the lower CR level, respectively (Table 1). In comparison with the highest probabilistic locations of the upper extremity or the lower extremity, there were no significant differences between the right and left in both ML and AP directions at the upper and the lower CR level (P > 0.05). In contrast, significant differences in the highest probabilistic locations were observed between the upper and the lower extremities in both ML and AP directions at the upper and the lower CR level (P < 0.05) (Table 1). The distances between the upper and lower extremities of the CST in the CR were evaluated in the ML and AP directions. In the ML direction, the distances for the highest probability location of the CST between the upper and the lower extremities were 2.41, 2.32, and
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712 NeuroReport 2014, Vol 25 No 9
Fig. 1
(a)
(b)
ROI
Medial boundary
Lateral boundary Anterior boundary R Posterior boundary
R
R
Green : Hand for CST Red : Leg for CST (c)
(d)
R
R
Diffusion tensor tractography shows locations for the upper and lower extremities of the corticospinal tract (CST), and measurement of somatotopic organization at the different corona radiata (CR) levels. (a) The seed regions of interests (ROIs) are given at the precentral knob (green) for the upper extremity and at the mediodorsal part (red) for the lower extremity. Target ROI is given at the anterior portion of the pontine, and the CSTs are reconstructed in both hemispheres (green: upper extremity for the CST, red: lower extremity for the CST). (b) Measurement of the CST location – the most anterior point of the lateral ventricle (anterior boundary), the most posterior point of the lateral ventricle (posterior boundary), midline (medial boundary), and the most lateral point of the cerebral cortex (lateral boundary). (c) CST probabilistic maps are shown at the upper CR level. (d) CST probabilistic maps are shown at the lower CR level (green: highest probabilistic locations for the upper extremity, red: highest probabilistic locations for the lower extremity).
Table 1
Results of average locations of the highest probability point of the corticospinal tract at the corona radiata Right
Upper CR level Mediolateral Anteroposterior Lower CR level Mediolateral Anteroposterior
Left
Average
Upper extremity
Lower extremity
Upper extremity
Lower extremity
Upper extremity
Lower extremity
40.27 (2.36) 62.14 (11.01)
36.80 (3.11) 76.63 (12.68)
41.20 (2.40) 62.90 (11.20)
37.52 (3.00) 74.68 (9.45)
40.72 (2.41) 62.52 (11.05)
37.16 (3.06) 75.65 (11.16)
37.72 (2.57) 60.30 (6.02)
36.9 (2.46) 69.24 (6.39)
38.65 (2.95) 60.08 (6.14)
37.38 (2.68) 67.00 (6.32)
38.19 (2.64) 60.19 (6.05)
37.14 (2.11) 68.12 (6.42)
Values represent mean (±SD) %, location (percent). CR, corona radiata.
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Location and organization of corticospinal tract Kwon et al. 713
Table 2
Average distance for the highest probability locations of the corticospinal tract between upper and lower extremities Upper CR level
Mediolateral direction Anteroposterior direction
Lower CR level
Right
Left
Average
Right
Left
Average
2.32 (2.20) 5.45 (3.21)
2.50 (1.87) 5.01 (3.17)
2.41 (2.03) 5.23 (3.18)
1.18 (1.58) 4.86 (3.91)
1.25 (1.72) 4.09 (3.17)
1.21 (1.64) 4.47 (3.56)
Values represent mean (±SD)mm. Each location of the point was calculated as a pixel unit and converted into millimeters. The voxel size is 1.73 mm 1.73 mm 2.3 mm. CR, corona radiata.
2.50 mm (average, right, left) at the upper CR level, and 1.21, 1.18, and 1.25 mm (average, right, left) at the lower CR level, respectively. In the AP direction, distances between the upper and lower extremities were 5.23, 5.45, and 5.01 mm (average, right, left) at the upper CR level, and 4.47, 4.86, and 4.09 mm (average, right, left) at the lower CR level, respectively (Table 2).
Discussion In this study, we have confirmed the anatomic location and somatotopic organization of the CST at the upper and lower CR level using DTT with a quantitative analysis. It appears that the upper extremity of the CST in all CR levels is always located anterolateral to the lower extremity. In addition, ML and AP distances between the upper and lower extremities decrease as the CST passes from the upper to the lower CR level. Several clinic–radiologic correlation studies have shown the anatomical location and somatotopic organization of the CST in the CR [3,4,22,23]. In these studies, patients with a cerebral infarct associated with prominent upper or lower extremity weakness were analyzed. Using threedimensional anisotropy derived from a diffusion-weighted MRI, 13 patients with CR infarcts with a degree of dominant motor dysfunction of their extremities were investigated [3]. The results of the study are as follows: seven patients with an upper extremity-dominant motor dysfunction had an infarct in the middle third of the CST; one patient with a lower extremity-dominant motor dysfunction in the posterior third of the CST; and five patients with equal motor dysfunction in both the middle and posterior third of the CST [3]. Nevertheless, these results could not provide an exact anatomical location of the CST in detail because a standard point in the CR was not defined. Actually, three studies have established a standard point after analyzing a conventional MRI, which enabled the measurement of a relative distance to the center of an infarct from the anterior pole or posterior pole of the lateral ventricle [4,22,23]. On the basis of their results, we used the anterior pole of the lateral ventricle as a standard point, and then the average AP distance ratios of the arm : leg were measured as 0.45 : 0.49, 0.64 : 0.71, and 0.60 : 0.70, respectively. These values indicate that the upper extremity is consistently located anterior to the lower extremity and the latter two values are also in good agreement with our results, which show ratios of the upper extremity: lower extremity,
0.62 : 0.75 at the upper CR level, and 0.60 : 0.68 at the lower CR level. In 2007, Song [23], for the first time, measured the somatotopy of ML distance as well as AP distance. In his study, the ML location of the lesion was assessed using the laterality index, which was defined as the LV/IV ratio (I, the gray matter margin of the insular cortex; V, the lateral ventricle wall; and L, center of the lesion). The laterality index of lesions in stroke patients with dominant motor weakness of the bulbofacial, arm, and leg was 0.68, 0.66, and 0.50, respectively. These results suggest that the motor subserving the bulbofacial–arm–leg paresis is in anterolateral-to-posteromedial alignment. In agreement with Song, our study has confirmed that the upper extremity is located symmetrical and anterolateral to the lower extremity in all CR levels as shown in Fig. 1c and d and Tables 1 and 2. In terms of the correspondence between the right and the left brain, we found that there were some variations; however, they did not affect the results. Similarly, studies carried out by Seo et al. [18] and Pan et al. [17] showed the laterality on the anatomical location of CST in the normal human brain using the same methodological approach as this study [17,18]. They found no significant difference between the right and the left hemispheres in the centrum semiovale and the posterior limb of the internal capsule. As for the CR level of a normal brain, there are only two studies on the somatotopic organization of the CST. One study used a fusion of fMRI and DTT and showed that only hemispheres from four of seven patients had a hand that is located anterolateral to the leg [24]. The other study reported that the upper extremity of the CST is anterior to the lower extremity [25]. In that study, all CSTs rotated anteriorly close to the 12 o’clock position as they coursed toward the posterior limb of the internal capsule (PLIC). In terms of the clinical application, however, these results have some limitations because a small number of patients were studied, and they were not analyzed quantitatively. In this study, we found characteristics of the upper and lower extremities of the CST in the CR descending from the upper to the lower CR level, and carried out quantitative analysis. First, all average distances between the upper and lower extremities in the AP and ML directions were decreased. The average distances for the highest probability point of the CST between the upper and lower extremities were 2.41 and 5.45 mm (ML and AP direction) at the upper CR level and 1.21 and 4.47 mm (ML and AP direction) at the lower CR level, respectively
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714 NeuroReport 2014, Vol 25 No 9
(Table 2). This is not surprising because the lower CR level is located close to the PLIC, a very compact axonal area of the CST. Second, the anatomical locations of both lower extremities in the ML direction showed almost no interval change (average lower extremity: D0.02 = 37.16 – 37.14/right lower extremity: D0.10 = 36.80 – 36.90/ left lower extremity: D0.14 = 37.52 – 37.38) (Table 1). Thus, it is possible to establish the lower extremity as the axis of rotation, which indicates that the upper extremity rotates close to 01, the 12 o’clock position. Third, average distances between the upper and lower extremities in the ML direction are 1.21 mm (right: 1.18 mm, left: 1.25 mm), respectively, suggesting that the upper extremity is slightly located lateral to the lower extremity, although it maintains the location anteriorly. These results may represent a preparation step for the somatotopically organized upper extremity, which is located anteromedial to the lower extremity in the PLIC. Recently, Lee et al. [16] confirmed these somatotopies of the CST for the hand and leg in the PLIC using a fusion of fMRI and DTT. In addition, somatotopies in the centrum semiovale – the structure situated just above the CR – show that the hand of the CST is located anterolateral to the foot of the CST using the same method as that applied in our study [18]. Thus, when the CST passes from the cortex to the PLIC, the upper extremity of CST is always anterior to the lower extremity of CST in the AP direction, but that of CST is shifted from the lateral area to the medial area in the ML direction. To the best of our knowledge, this is the first study of the anatomical location and somatotopic organization of the CST in the CR of a normal human brain using DTT with a quantitative analysis. We expect that our data may be useful for clinical applications. However, some limitations of this study should be considered. First, DTT cannot show functional or synaptic connections. Second, the measurements of highest probability location were operator dependent on the selection of boundaries and the CR level. Third, we did not reconstruct the CST from the supplementary motor area and premotor area. Finally, all participants did not show a good correspondence between the right and the left brain.
Conclusion We elucidate the anatomical location and somatotopic organization of the CST in the CR of a normal human brain using DTT. The upper extremity of the CST is arranged anterolateral to the lower extremity, and the upper and lower extremities of the CST become closer to each other as the CST descends from the upper to the lower CR level.
Acknowledgements This study was supported by Ulsan University Hospital, Ulsan, Korea (Biomedical Research Center Promotion Fund UUH-2009-#9-05).
Conflicts of interest
There are no conflicts of interest.
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Anatomical location and somatotopic organization of the corticospinal tract in the corona radiata of the normal human brain: a diffusion tensor tractography study Hyeok Gyu Kwona, Jeong-Hee Yangb, Jun Bum Parkc, Min Ho Kime, Soon Ho Choif and Dong Seok Yangd The anatomical location and somatotopic organization of the corticospinal tract (CST) in the corona radiata (CR) of the normal human brain have not been studied using diffusion tensor tractography so far. In this study, the anatomical location and somatotopic organization of the CST in the CR were evaluated by determining the highest probabilistic locations and distances between the upper and lower extremities in the slices of upper and lower CR in the brain. In the mediolateral direction, the average of the highest probabilistic locations for the upper and lower extremities were 40.27 and 37.16% at the upper CR level and 38.19 and 37.14% at the lower CR level, respectively. In the anteroposterior direction, the average of the highest probabilistic locations for the upper and lower extremities were 62.52 and 75.65% at the upper CR level and 60.19 and 68.12% at the lower CR level, respectively. The average distances between upper and lower extremities for the mediolateral direction were 2.41 mm at the upper CR level and 1.21 mm at the lower CR level. The average distances between upper and lower extremities for the anteroposterior direction were 5.23 mm at the upper CR level and 4.47 mm at the lower CR level, respectively.
Our findings suggest that the anatomical location and somatotopic organization for the upper extremity are located anterolaterally to the lower extremity in the CR of a normal human brain and distances between the upper and lower extremities become decreased as the CST descends from the upper to the lower CR c 2014 Wolters Kluwer level. NeuroReport 25:710–714 Health | Lippincott Williams & Wilkins.
Introduction
Diffusion tensor tractography (DTT) is based on DTI and allows localizing the neural tract at the subcortical level in three dimensions [9–11]. In addition, it is a very useful tool for the measurement of an anatomical location and somatotopic organization of the CST.
The corticospinal tract (CST) is composed of long axonal bundles and is the major neural pathway. It is believed to be crucial for skillful finger movement and walking pattern simultaneously [1]. Several studies have previously suggested somatotopy of the CST in which separate upper and lower extremities may be present by brain dissection or clinic–radiologic findings [2–5]. Furthermore, specifically isolated upper extremity weakness or lower extremity weakness in a patient after a stroke using a computed tomography or an MRI has confirmed the anatomical location and somatotopic organization of the upper and lower extremities at multiple levels of the CST [6–8]. Nevertheless, those methods have several limitations in terms of lack of accuracy, indirect findings, or invasiveness. It would be a major clinical advantage to gain knowledge of the exact anatomical location and somatotopic organization of the CST for surgical planning near the CST, prediction for the prognosis of motor weakness, and a scientific rehabilitation strategy after stroke. Diffusion tensor imaging (DTI) is an advanced technique of MRI for assessment of the integrity of the neural tract in a noninvasive manner. c 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins 0959-4965
NeuroReport 2014, 25:710–714 Keywords: corona radiata, corticospinal tract, diffusion tensor tractography, somatotopic organization a Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Taegu, bDepartment of Biological Science, College of Natural Science, Sungkyunkwan University, Suwon, Departments of cNeurosurgery, dPhysical Medicine and Rehabilitation, University of Ulsan College of Medicine, eBiomedical Research Center, Ulsan University Hospital and fDepartment of Physical Therapy, Ulsan College East Campus, Ulsan, Korea
Correspondence to Dong Seok Yang, MD, PhD, Department of Physical Medicine and Rehabilitation, University of Ulsan College of Medicine, Ulsan University Hospital, 290-3 Jeonha-dong, Dong-gu, Ulsan 682-714, Korea Tel: + 82 52 250 7210; fax: + 82 52 250 8940; e-mails: [email protected]; [email protected] Received 24 February 2014 accepted 14 March 2014
To date, the anatomical location and somatotopic organization of the CSTs in the normal human brain have been confirmed from the centrum semiovale to the medullar level, not in the corona radiata (CR) [12–18]. Although the CR is known to be one of the most important sites of ischemic stroke [19], to our knowledge, there has been no study as yet on the CST in the CR of the normal human brain. Thus, we have attempted to investigate the anatomical location and somatotopic organization of the CST for the upper and lower extremities quantitatively at the upper and lower CR level using DTT.
Materials and methods Participants
We recruited 47 right-handed healthy individuals (men: 23, mean age: 33.45 years, range: 20–54 years) who had no DOI: 10.1097/WNR.0000000000000170
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Location and organization of corticospinal tract Kwon et al. 711
previous history of physical, neurological, or psychiatric illness. The Edinburgh Handedness inventory was used for the handedness [20]. This study protocol was approved by the Institutional Review Board of Yeungnam University Hospital (Daegu, Korea). Data acquisition
DTI data were obtained using a multichannel head coil on a 1.5-T Philips Gyroscan intera (Hoffman-LaRoche Ltd, Best, the Netherlands) with single-shot echo-planar imaging. Imaging was performed using a six-channel head coil. For each of the 32 noncollinear diffusion sensitizing gradients, we acquired 65 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters were as follows: acquisition matrix = 96 96 matrix, reconstructed to matrix = 128 128 matrix, field of view = 221 221 mm2, TE = 76 ms, TR = 10 726 ms, EPI factor = 49, parallel imaging reduction factor (SENSE factor) = 2, b-value = 1000 s/mm2, NEX = 1, and a slice thickness of 2.3 mm. Fiber tracking
Diffusion-weighted imaging data were analyzed using the Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB) Software Library. The head motion effect and image distortion because of eddy current were corrected by affine multiscale two-dimensional registration. The probabilistic tractography method based on a multifiber model was used for fiber tracking and applied to the present study utilizing tractography routines implemented in FMRIB diffusion (0.5 mm step lengths, 5000 streamline samples, curvature thresholds = 0.2) [21]. CSTs for both upper and lower extremities were determined by the selection of fiber passing through two regions of interests (ROIs) on the basis of studies by Kwon et al. [13] and Seo et al. [18]. The seed ROIs for the upper and lower extremities were placed on the precentral knob (somatotopy for the upper extremity) and the dorsomedial part (somatotopy for the lower extremity) of the primary motor cortex on the axial slices map, respectively (Fig. 1a, left top). The target ROI was located at the anterior portion of pontine on the color map (part of the anterior blue color) (Fig. 1a, left bottom). Measurement of the corticospinal tract location at the upper and lower corona radiata level
The anatomical location of the CST in the CR was evaluated as the highest probabilistic location (%) in the slices of the upper and lower CR for each participant. As shown in Fig. 1b, we defined the boundary as follows: the most anterior point of the lateral ventricle (anterior boundary), the most posterior point of the lateral ventricle (posterior boundary), and midline (medial boundary), and the most lateral point of the cerebral cortex (lateral boundary). The anatomical location of the CST was measured laterally from the medial boundary in the mediolateral (ML) direction and posteriorly from the
anterior boundary in the anteroposterior (AP) direction. CST probabilistic maps were acquired by overlapping of the highest probabilistic location. The probabilistic map was superimposed on a mean non-diffusion-weighted image to create a mean of all participants of nondiffusion-weighted images using the SPM19 software (SPSS Inc., Chicago, Illinois, USA). Measurement of average distance for the highest probability location between the upper and the lower extremities
The average distance for the highest probability location between the upper and the lower extremities was measured as each location of the point. It was calculated as a pixel unit and then converted into millimeters. The pixel unit is 1.73 mm (X) 1.73 mm (Y). Statistical analysis
The highest probabilistic location of the CSTs was used for performance of an independent t-test for determination of variances. The significance level of the P value was set at P value less than 0.05.
Results The probabilistic tracking of the CSTs for the upper and lower extremities was visualized in three dimensions from the cortex to the pons in all participants (Fig. 1a, right). We confirmed that CSTs for the upper and lower extremities run from the cortex to the medulla along the known pathway of the CST separately. In the ML direction, the highest probabilistic locations for the upper and lower extremities were 40.72% : 37.16%, 40.27% : 36.80%, and 41.20% : 37.52% (average, right, left) from the medial boundary at the upper CR level, and 38.19% : 37.14%, 37.72% : 36.90%, and 38.65% : 37.38% (average, right, left) from the medial boundary at the lower CR level, respectively. In the AP direction, the highest probabilistic locations for the upper and lower extremities were 62.52% : 75.65%, 62.14% : 76.63%, and 62.90% : 74.68% (average, right, left) from the anterior boundary at the upper CR level, and 69.19% : 68.12%, 60.30% : 69.24%, and 60.08% : 67.00% (average, right, left) from the anterior boundary at the lower CR level, respectively (Table 1). In comparison with the highest probabilistic locations of the upper extremity or the lower extremity, there were no significant differences between the right and left in both ML and AP directions at the upper and the lower CR level (P > 0.05). In contrast, significant differences in the highest probabilistic locations were observed between the upper and the lower extremities in both ML and AP directions at the upper and the lower CR level (P < 0.05) (Table 1). The distances between the upper and lower extremities of the CST in the CR were evaluated in the ML and AP directions. In the ML direction, the distances for the highest probability location of the CST between the upper and the lower extremities were 2.41, 2.32, and
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712 NeuroReport 2014, Vol 25 No 9
Fig. 1
(a)
(b)
ROI
Medial boundary
Lateral boundary Anterior boundary R Posterior boundary
R
R
Green : Hand for CST Red : Leg for CST (c)
(d)
R
R
Diffusion tensor tractography shows locations for the upper and lower extremities of the corticospinal tract (CST), and measurement of somatotopic organization at the different corona radiata (CR) levels. (a) The seed regions of interests (ROIs) are given at the precentral knob (green) for the upper extremity and at the mediodorsal part (red) for the lower extremity. Target ROI is given at the anterior portion of the pontine, and the CSTs are reconstructed in both hemispheres (green: upper extremity for the CST, red: lower extremity for the CST). (b) Measurement of the CST location – the most anterior point of the lateral ventricle (anterior boundary), the most posterior point of the lateral ventricle (posterior boundary), midline (medial boundary), and the most lateral point of the cerebral cortex (lateral boundary). (c) CST probabilistic maps are shown at the upper CR level. (d) CST probabilistic maps are shown at the lower CR level (green: highest probabilistic locations for the upper extremity, red: highest probabilistic locations for the lower extremity).
Table 1
Results of average locations of the highest probability point of the corticospinal tract at the corona radiata Right
Upper CR level Mediolateral Anteroposterior Lower CR level Mediolateral Anteroposterior
Left
Average
Upper extremity
Lower extremity
Upper extremity
Lower extremity
Upper extremity
Lower extremity
40.27 (2.36) 62.14 (11.01)
36.80 (3.11) 76.63 (12.68)
41.20 (2.40) 62.90 (11.20)
37.52 (3.00) 74.68 (9.45)
40.72 (2.41) 62.52 (11.05)
37.16 (3.06) 75.65 (11.16)
37.72 (2.57) 60.30 (6.02)
36.9 (2.46) 69.24 (6.39)
38.65 (2.95) 60.08 (6.14)
37.38 (2.68) 67.00 (6.32)
38.19 (2.64) 60.19 (6.05)
37.14 (2.11) 68.12 (6.42)
Values represent mean (±SD) %, location (percent). CR, corona radiata.
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Location and organization of corticospinal tract Kwon et al. 713
Table 2
Average distance for the highest probability locations of the corticospinal tract between upper and lower extremities Upper CR level
Mediolateral direction Anteroposterior direction
Lower CR level
Right
Left
Average
Right
Left
Average
2.32 (2.20) 5.45 (3.21)
2.50 (1.87) 5.01 (3.17)
2.41 (2.03) 5.23 (3.18)
1.18 (1.58) 4.86 (3.91)
1.25 (1.72) 4.09 (3.17)
1.21 (1.64) 4.47 (3.56)
Values represent mean (±SD)mm. Each location of the point was calculated as a pixel unit and converted into millimeters. The voxel size is 1.73 mm 1.73 mm 2.3 mm. CR, corona radiata.
2.50 mm (average, right, left) at the upper CR level, and 1.21, 1.18, and 1.25 mm (average, right, left) at the lower CR level, respectively. In the AP direction, distances between the upper and lower extremities were 5.23, 5.45, and 5.01 mm (average, right, left) at the upper CR level, and 4.47, 4.86, and 4.09 mm (average, right, left) at the lower CR level, respectively (Table 2).
Discussion In this study, we have confirmed the anatomic location and somatotopic organization of the CST at the upper and lower CR level using DTT with a quantitative analysis. It appears that the upper extremity of the CST in all CR levels is always located anterolateral to the lower extremity. In addition, ML and AP distances between the upper and lower extremities decrease as the CST passes from the upper to the lower CR level. Several clinic–radiologic correlation studies have shown the anatomical location and somatotopic organization of the CST in the CR [3,4,22,23]. In these studies, patients with a cerebral infarct associated with prominent upper or lower extremity weakness were analyzed. Using threedimensional anisotropy derived from a diffusion-weighted MRI, 13 patients with CR infarcts with a degree of dominant motor dysfunction of their extremities were investigated [3]. The results of the study are as follows: seven patients with an upper extremity-dominant motor dysfunction had an infarct in the middle third of the CST; one patient with a lower extremity-dominant motor dysfunction in the posterior third of the CST; and five patients with equal motor dysfunction in both the middle and posterior third of the CST [3]. Nevertheless, these results could not provide an exact anatomical location of the CST in detail because a standard point in the CR was not defined. Actually, three studies have established a standard point after analyzing a conventional MRI, which enabled the measurement of a relative distance to the center of an infarct from the anterior pole or posterior pole of the lateral ventricle [4,22,23]. On the basis of their results, we used the anterior pole of the lateral ventricle as a standard point, and then the average AP distance ratios of the arm : leg were measured as 0.45 : 0.49, 0.64 : 0.71, and 0.60 : 0.70, respectively. These values indicate that the upper extremity is consistently located anterior to the lower extremity and the latter two values are also in good agreement with our results, which show ratios of the upper extremity: lower extremity,
0.62 : 0.75 at the upper CR level, and 0.60 : 0.68 at the lower CR level. In 2007, Song [23], for the first time, measured the somatotopy of ML distance as well as AP distance. In his study, the ML location of the lesion was assessed using the laterality index, which was defined as the LV/IV ratio (I, the gray matter margin of the insular cortex; V, the lateral ventricle wall; and L, center of the lesion). The laterality index of lesions in stroke patients with dominant motor weakness of the bulbofacial, arm, and leg was 0.68, 0.66, and 0.50, respectively. These results suggest that the motor subserving the bulbofacial–arm–leg paresis is in anterolateral-to-posteromedial alignment. In agreement with Song, our study has confirmed that the upper extremity is located symmetrical and anterolateral to the lower extremity in all CR levels as shown in Fig. 1c and d and Tables 1 and 2. In terms of the correspondence between the right and the left brain, we found that there were some variations; however, they did not affect the results. Similarly, studies carried out by Seo et al. [18] and Pan et al. [17] showed the laterality on the anatomical location of CST in the normal human brain using the same methodological approach as this study [17,18]. They found no significant difference between the right and the left hemispheres in the centrum semiovale and the posterior limb of the internal capsule. As for the CR level of a normal brain, there are only two studies on the somatotopic organization of the CST. One study used a fusion of fMRI and DTT and showed that only hemispheres from four of seven patients had a hand that is located anterolateral to the leg [24]. The other study reported that the upper extremity of the CST is anterior to the lower extremity [25]. In that study, all CSTs rotated anteriorly close to the 12 o’clock position as they coursed toward the posterior limb of the internal capsule (PLIC). In terms of the clinical application, however, these results have some limitations because a small number of patients were studied, and they were not analyzed quantitatively. In this study, we found characteristics of the upper and lower extremities of the CST in the CR descending from the upper to the lower CR level, and carried out quantitative analysis. First, all average distances between the upper and lower extremities in the AP and ML directions were decreased. The average distances for the highest probability point of the CST between the upper and lower extremities were 2.41 and 5.45 mm (ML and AP direction) at the upper CR level and 1.21 and 4.47 mm (ML and AP direction) at the lower CR level, respectively
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714 NeuroReport 2014, Vol 25 No 9
(Table 2). This is not surprising because the lower CR level is located close to the PLIC, a very compact axonal area of the CST. Second, the anatomical locations of both lower extremities in the ML direction showed almost no interval change (average lower extremity: D0.02 = 37.16 – 37.14/right lower extremity: D0.10 = 36.80 – 36.90/ left lower extremity: D0.14 = 37.52 – 37.38) (Table 1). Thus, it is possible to establish the lower extremity as the axis of rotation, which indicates that the upper extremity rotates close to 01, the 12 o’clock position. Third, average distances between the upper and lower extremities in the ML direction are 1.21 mm (right: 1.18 mm, left: 1.25 mm), respectively, suggesting that the upper extremity is slightly located lateral to the lower extremity, although it maintains the location anteriorly. These results may represent a preparation step for the somatotopically organized upper extremity, which is located anteromedial to the lower extremity in the PLIC. Recently, Lee et al. [16] confirmed these somatotopies of the CST for the hand and leg in the PLIC using a fusion of fMRI and DTT. In addition, somatotopies in the centrum semiovale – the structure situated just above the CR – show that the hand of the CST is located anterolateral to the foot of the CST using the same method as that applied in our study [18]. Thus, when the CST passes from the cortex to the PLIC, the upper extremity of CST is always anterior to the lower extremity of CST in the AP direction, but that of CST is shifted from the lateral area to the medial area in the ML direction. To the best of our knowledge, this is the first study of the anatomical location and somatotopic organization of the CST in the CR of a normal human brain using DTT with a quantitative analysis. We expect that our data may be useful for clinical applications. However, some limitations of this study should be considered. First, DTT cannot show functional or synaptic connections. Second, the measurements of highest probability location were operator dependent on the selection of boundaries and the CR level. Third, we did not reconstruct the CST from the supplementary motor area and premotor area. Finally, all participants did not show a good correspondence between the right and the left brain.
Conclusion We elucidate the anatomical location and somatotopic organization of the CST in the CR of a normal human brain using DTT. The upper extremity of the CST is arranged anterolateral to the lower extremity, and the upper and lower extremities of the CST become closer to each other as the CST descends from the upper to the lower CR level.
Acknowledgements This study was supported by Ulsan University Hospital, Ulsan, Korea (Biomedical Research Center Promotion Fund UUH-2009-#9-05).
Conflicts of interest
There are no conflicts of interest.
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