http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic) Somatosens Mot Res, 2014; 31(4): 204–208 ! 2014 Informa UK Ltd. DOI: 10.3109/08990220.2014.917292

ORIGINAL ARTICLE

The distribution of the cortical origin of the corticoreticular pathway in the human brain: A diffusion tensor imaging study Sung Ho Jang & Jeong Pyo Seo

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Department of Physical Medicine and Rehabilitation, Yeungnam University, Daegu, Republic of Korea

Abstract

Keywords

We investigated the distribution of the cortical origin of the corticoreticular pathway (CRP) in the human brain. Forty normal subjects were recruited and CRPs from four cortical areas were reconstructed. The first cortical origin area of the CRP was the premotor cortex and the next was the primary motor cortex. Although the CRP fibers also originated from the primary somatosensory cortex and prefrontal cortex, they occupied the smallest portion among four regions of interest.

Cerebral cortex, corticoreticular pathway, diffusion tensor imaging, premotor cortex

Introduction In the human brain, the neural tracts for motor function are classified according to the corticospinal tract (CST) and the non-CST. The corticoreticulospinal tract, one of the nonCSTs in the human brain, innervates the proximal muscles of extremities and axial muscles (Matsuyama et al. 2004; Mendoza and Foundas 2007; Chen et al. 2011). Therefore, it is involved in postural control and gait function (Matsuyama et al. 2004; Mendoza and Foundas 2007; Jang 2010b). The corticoreticulospinal tract consists of the corticoreticular pathway (CRP) and the reticulospinal tract. In general, the neural tracts for sensori-motor function, such as the CST, spinothalamic tract, and medial lemniscus, originate from multiple cortical areas (Russell and Demyer 1961; Davidoff 1990; Simoes et al. 2001; Jang et al. 2012; Seo and Jang 2013). Elucidation of the cortical origins of a neural tract would be important because it could provide a basis for peri-lesional reorganization following cortical injury (Jang 2010a). The CRP is known to originate primarily from the premotor cortex (PMC) and terminates at the pontomedullary reticular formation (Kably and Drew 1998a; Matsuyama et al. 2004; Mendoza and Foundas 2007). Many previous animal and functional neuroimaging studies have suggested that the CRP originates from multiple cerebral areas as well as the PMC (Matsuyama and Drew 1997; Kably and Drew 1998a, 1998b; Drew et al. 2002; Miyai et al. 2002;

History Received 16 December 2013 Revised 10 April 2014 Accepted 15 April 2014 Published online 10 June 2014

Kim et al. 2006; Lee et al. 2013). However, this has not been clearly elucidated in the human brain. Recently developed diffusion tensor tractography (DTT), a technique derived from diffusion tensor imaging (DTI), enables three-dimensional visualization and estimation of the CRP (Yeo et al. 2012). Several studies have reported on injury of the CRP in patients with various pathologies, including stroke and traumatic brain injury (Do et al. 2013; Jang et al. 2013; Yeo and Jang 2013; Yeo et al. 2013b). However, no DTI study on the distribution of the cortical origin of the CRP has been reported. In the current study, using DTT, we attempted to investigate the distribution of the cortical origin of the CRP in normal subjects.

Subjects and methods Subjects A total of 42 right-handed healthy subjects (males: 21, females: 21, mean age: 37.9 years; range: 20–53 years) with no previous history of psychiatric, neurological, or physical illness were enrolled in this study. The Edinburg Handedness Inventory was used for evaluation of handedness (Oldfield 1971). All subjects understood the purpose of the study and provided written, informed consent prior to participation. The study protocol was approved by the Institutional Review Board of a university hospital. Data acquisition

Correspondence: Jeong Pyo Seo, Department of Physical Medicine & Rehabilitation College of Medicine, Yeungnam University, 317-1, Daemyungdong, Namku, Daegu 705-717, South Korea. Tel: 82-53620-4098. Fax: 82-53-623-3259. E-mail: [email protected]

DTI data were acquired using a Synergy-L SENSE head coil on a 1.5 T Gyroscan Intera system (Philips, Best, the Netherlands) equipped with single-shot echo-planar imaging.

DOI: 10.3109/08990220.2014.917292

For each of the 32 non-collinear diffusion sensitizing gradients, we acquired 67 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters were as follows: acquisition matrix ¼ 96  96, reconstructed matrix ¼ 128  128, field of view ¼ 221  221 mm2, TR ¼ 10 726 ms, TE ¼ 76 ms, parallel imaging reduction factor (SENSE factor) ¼ 2, EPI factor ¼ 49, b ¼ 1000 s/ mm2, NEX ¼ 1, slice gap ¼ 0 mm, and slice thickness ¼ 2.3 mm (acquired voxel size 1.73  1.73  2.3 mm3).

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Fiber tracking The Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB) Software Library was used for analysis of diffusion-weighted imaging data. Affine multiscale two-dimensional registration was used for correction of head motion effect and image distortion due to eddy current. A probabilistic tractography method based on a multi-fiber model was used for fiber tracking, and applied in the current study utilizing tractography routines implemented in FMRIB diffusion (0.5 mm step lengths, 5000 streamline samples, curvature thresholds ¼ 0.2) (Behrens et al. 2003, 2007; Smith et al. 2004). For analysis of CRP fibers from the primary somatosensory cortex (S1), primary motor cortex (M1), PMC, and prefrontal cortex (PFC), the seed region of interest (ROI) was placed on the reticular formation of the medulla, the first target ROI was placed on the reticular formation of the midbrain tegmentum. The second target ROIs were placed as follows: (1) S1 (BA 1, 2, and 3—the anterior boundary: central sulcus, the posterior boundary: postcentral sulcus, the medial boundary: the midline between the right and left hemispheres, and the lateral boundary: the lateral sulcus). (2) M1 (BA 4—the anterior boundary: the precentral sulcus, the posterior boundary: the central sulcus, the medial boundary: the midline between the right and left hemispheres, and the lateral boundary: the lateral sulcus). (3) PMC (BA 6— the anterior boundary: the line drawn through the anterior commissure perpendicular to the anterior commissure–posterior commissure line, the posterior boundary: the precentral sulcus, the medial boundary: the midline between the right and left hemispheres, and the lateral boundary: the lateral sulcus). (4) PFC (BA 8—the anterior boundary: the second bank of the dorsolateral prefrontal cortex from the precentral sulcus, the posterior boundary: the anterior margin of BA 6, the medial boundary: the midline between the right and left hemispheres, and the lateral boundary: the inferior frontal sulcus) (Figure 1A) (Brodmann and Gary 2006). Out of 5000 streamline samples, that generated from each seed voxel, were visualized threshold and weightings of tract probability at a minimum of one streamline through each voxel for analysis. Values of fractional anisotropy (FA) and tract volume of each ROI were measured. Statistical analysis SPSS software (v.15.0; SPSS, Chicago, IL, USA) was used for data analysis. One-way ANOVA with least significant difference (LSD) post hoc test was used in determination of differences in value for each DTI parameter (FA and tract volume) between CRP fibers from S1, M1, PMC, and PFC.

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Pearson’s correlation analysis was used in the assessment of any significant correlations between DTI parameters (FA and tract volume) of CRP fibers from each ROI. The significant level for the p-value was set at 0.05.

Results The CRPs from M1 and PMC were reconstructed in all hemispheres (100%). However, the CRPs from S1 and PFC were reconstructed in 64 (76.2%) and 63 (75%) of 84 hemispheres, respectively, and we were not able to reconstruct the CRPs in the other hemispheres. A summary of the mean values for FA and tract volume of the CRPs is shown in Table I. Using the one-way ANOVA test, no significant differences in FA values of CRPs were observed between ROIs (p40.05). By contrast, significant differences in terms of tract volume were observed between ROIs (p50.05). According to the result of the LSD post hoc test, the value for the CRP from the PMC was significantly higher than those from the other ROIs (p50.05) and the CRP value from M1 was higher than those from S1 and PFC (p50.05) (Table II). However, no significant difference was observed between CRPs from S1 and PFC (p40.05).

Discussion In the current study, we investigated the distribution of the cortical origin of the CRP; the results were as follows: (1) no significant differences in FA values of CRPs were observed between ROIs, (2) significant differences in the tract volume of CRPs were observed between ROIs: the largest tract volume of CRP fibers was observed for the PMC (1177.3) and the next largest was from M1 (994.9), however, no significant difference was observed between the other two ROIs (S1: 580.8, PFC: 575.7), and (3) the CRPs from the PMC and M1 were reconstructed in all hemispheres (100%). However, we reconstructed the CRPs from S1 and PFC in 64 (76.2%) and 63 (75%) of 84 hemispheres. The FA value, the most widely used DTI parameter, indicates the degree of directionality and integrity of white matter microstructures such as axons, myelin, and microtubules (Assaf and Pasternak 2008; Neil 2008). Therefore, our results with regard to the FA value appear to indicate that the CRP fibers from each ROI have the characteristic of similar directionality. By contrast, the tract volume is determined by the number of voxels contained within a neural tract (Jang et al. 2013). As a result, a larger number for tract volume of a neural tract suggests a larger fiber number of the neural tract. Our results regarding the tract volume of the CRP indicate that the first cortical origin area of the CRP was the PMC and the next was M1. Although the CRP fibers originated from S1 and PFC, they occupied the smallest portion among four ROIs. The reconstruction rate of the CRPs from each ROI appears to be generally compatible with the results for tract volume. The CRP is known to originate primarily from the PMC; however, the cortical origin of the CRP from other cortical areas is poorly understood (Kably and Drew 1998a; Matsuyama et al. 2004; Mendoza and Foundas 2007). Many clinical studies have suggested that the PMC is the main

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Figure 1. (A) The seed and first target regions of interest (ROIs) were placed on the reticular formation of the medulla and the reticular formation of the midbrain tegmentum (posterior portion of the tegmentum), respectively. The second target ROIs were placed in the primary somatosensory cortex (yellow color), primary motor cortex (blue color), premotor cortex (red color), and prefrontal cortex (green color). (B) CRPs were reconstructed in both hemispheres (yellow—CRP for the primary somatosensory cortex, blue—CRP for the primary motor cortex, red—CRP for the premotor cortex, green—CRP for the prefrontal cortex). (C) CRPs from each ROI were reconstructed in both hemispheres.

Table I. Comparison of diffusion tensor imaging parameters among corticoreticular pathways from the primary somatosensory cortex, primary motor cortex, premotor cortex, and prefrontal cortex. FA S1 M1 PMC PFC

0.434 0.433 0.433 0.438

(0.037) (0.038) (0.034) (0.039)

Tract volume 580.8 994.9 1177.3 575.7

(513.3) (530.1) (737.9) (466.9)

Values represent mean (±standard deviation); FA: fractional anisotropy; S1: primary somatosensory cortex; M1: primary motor cortex; PMC: premotor cortex; PFC: prefrontal cortex.

cortical origin area of the CRP based on evidence indicating that the gait function or proximal muscle weakness (shoulder and hip muscles) in patients with brain injury was closely related to the lesion of PMC (Freund and Hummelsheim

Table II. LSD post hoc test for comparisons of tract volume among corticoreticular pathways from the primary somatosensory cortex, primary motor cortex, premotor cortex, and prefrontal cortex.

S1 M1 PMC PFC

S1

M1

PMC

PFC

– 50.001* 50.001* 0.961

50.001* – 0.044* 50.001*

50.001* 0.044* – 50.001*

0.961 50.001* 50.001* –

Values represent p-value; S1: primary somatosensory cortex; M1: primary motor cortex; PMC: premotor cortex; PFC: prefrontal cortex. *p50.05.

1984, 1985; Freund 1985; Seitz et al. 1998; Hanakawa et al. 1999; Miyai et al. 1999, 2002, 2003; Suzuki et al. 2004, 2008; Chang et al. 2010). In addition, several studies have reported that the medial portion of the PMC is more important to control of posture and gait (Della Sala et al. 2002;

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DOI: 10.3109/08990220.2014.917292

Luft et al. 2005; Iseki et al. 2008; Mihara et al. 2012; Fujimoto et al. 2014). Likewise, several functional neuroimaging studies have suggested that M1 is also an important cortical origin area of the CRP in patients who showed recovery of impaired gait function following stroke (Seitz et al. 1998; Miyai et al. 2002, 2003; Kim et al. 2006). This concept coincided with the results of animal studies demonstrating that M1 was a major cortical origin area of the CRP (Matsuyama and Drew 1997; Kably and Drew 1998a, 1998b; Drew et al. 2002). However, regarding S1 and PFC, relatively fewer studies have suggested an association of activation of these areas with movements of leg or proximal joints in normal subjects or recovery of impaired gait function after brain injury (Miyai et al. 2002; Kim et al. 2006; Lee et al. 2013; Yeo et al. 2013a). Overall, the results of our study showing that the PMC and M1 are the main origins of the PMC and that the CRP originates from other cortexes such as PFC and S1 are compatible with those of previous animal and human studies (Freund and Hummelsheim 1984, 1985; Freund 1985; Matsuyama and Drew 1997; Kably and Drew 1998a, 1998b; Seitz et al. 1998; Hanakawa et al. 1999; Miyai et al. 1999, 2002, 2003; Drew et al. 2002; Suzuki et al. 2004, 2008; Kim et al. 2006; Chang et al. 2010; Lee et al. 2013; Yeo et al. 2013a). In conclusion, we investigated the distribution of the cortical origin of the CRP and found that the first cortical origin area of the CRP was the PMC and the next was M1. Although the CRP fibers also originated from S1 and PFC, they occupied the smallest portion among four ROIs. In addition, the CRP fibers from four ROIs had similar directionality. To the best of our knowledge, this is the first study to investigate the distribution of the cortical origin of CRPs in the human brain. We believe that this study would be helpful in research on normal motor control and recovery mechanisms of the CRP following brain injury. However, several limitations of this study should be considered. First, we did not include the entire area of the PFC and posterior parietal cortex. This was because we could not place the ROI precisely due to the convexity of the anterior portion of the PFC and the posterior portion of the parietal cortex. Therefore, further studies of these areas should be encouraged. The limitations of DTI should be considered (Lee et al. 2005; Parker and Alexander 2005; Wedeen et al. 2008; Yamada et al. 2009). DTI, a powerful anatomic imaging tool, can demonstrate gross fiber architecture. However, DTI can produce false negative results due to crossing fiber or partial volume effect, or false positive results; in particular, probabilistic fiber tracking, which was adopted in the current study, can cause false fiber trajectory (Lee et al. 2005; Parker and Alexander 2005; Wedeen et al. 2008; Yamada et al. 2009). On the other hand, CRP fibers from the lateral portion of the cerebral cortex can be easily affected by crossing fibers such as the superior longitudinal fasciculus. Therefore, further studies would be necessary in order to overcome these limitations of DTI. In addition, further studies on the application of our results in the clinical field should be encouraged.

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Declaration of interest The authors report no conflicts of interest. This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2012R1A1A4A01001873).

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The distribution of the cortical origin of the corticoreticular pathway in the human brain: a diffusion tensor imaging study.

We investigated the distribution of the cortical origin of the corticoreticular pathway (CRP) in the human brain. Forty normal subjects were recruited...
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