Identification of the Rubro-Olivary Tract in the Human Brain: a Diffusion Tensor Tractography Study

Original Article J. Phys. Ther. Sci. 22: 7–10, 2010 Identification of the Rubro-Olivary Tract in the Human Brain: a Diffusion Tensor Tractography Study

SUNG HO JANG, MD1), JI HEON HONG, PT, MS1), YONG HYUN KWON, PT, PhD2)

1)Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University 2)Department of Physical Therapy, Yeungnam College of Science & Technology: 1737, Daemyung 7-Dong, Namgu, Daegu, 705-703, Republic of Korea. TEL +82 53-650-9702, FAX: +82 53-629-5048

Abstract. [Purpose] Little is known about the rubro-olivary tract (ROT) in the human brain. We attempted to identify the ROT using diffusion tensor tractography (DTT). [Subjects and Methods] We obtained ROT data from 11 healthy subjects with no history of neurological disorder. For tracking of the ROT, a seed region of interest (ROI) was selected in the red nucleus, and a target ROI was found in the inferior olive of each subject. [Results] The ROT, originated in the red nucleus, and passed laterally to the decussation of the superior cerebellar peduncle in the lower midbrain. In the pons, it descended through the area adjacent to the medial lemnicus in the posterior direction. Within the medulla, the ROT ended in the inferior olive, which was located lateral to the medial lemnicus and posterior to the pyramid. [Conclusion] We identified the ROT in the human brain using DTT. These results will be informative for research into the ROT in the human brain. Key words: Diffusion tensor image, Red nucleus, Inferior olive

(This article was submitted Jul. 24, 2009, and was accepted Sep. 3, 2009)

INTRODUCTION few studies have attempted to identify the ROT in the human brain, however, there has been no The rubro-olivary tract (ROT) is one of central detailed DTT study of the ROT11,12). In the current tegmental tracts which are efferent pathways of the study, we attempted to identify the ROT in the extrapyramidal motor system1). Little is known human brain using DTT. about the pathway and function of the ROT in the human brain. According to a previous study, the SUBJECTS AND METHODS ROT seems to work as a switcher between the corticospinal tract and the rubrospinal tract2). Subjects Therefore, the ROT is an important neural pathway We obtained information on the ROT from 11 in motor control and has the potential to contribute subjects (8 men, mean age: 37.1 ± 14.3 years) with to motor recovery following brain injury. Many no history of neurological or psychiatric illness, studies have reported identification of the ROT in who were right-handed as verified by the modified the mammalian brain3–7). With the introduction of Edinburg Handedness Inventory13). All subjects diffusion tensor tractography (DTT), we are able to understood the purpose of this study, and provided visualize neural tracts in three dimensions8–10). A their written informed consent prior to participation 8 J. Phys. Ther. Sci. Vol. 22, No. 1, 2010 in the experiments. This study was approved by the The structural characteristics of the ROT, the red institutional review board of our university. nucleus, and the inferior olive are described in Table 1. The mean FA value of the ROT was 0.51, Diffusion tensor imaging: and the mean FA value of the red nucleus (0.50) was Diffusion tensor images were acquired in a higher than that of the inferior olive (0.37). single-shot spin echo-planar imaging sequences Statistical analysis showed that the FA and ADC using a 1.5-T Philips Gyroscan Intera equipped with values of the ROT were not significantly different a Synergy-L Sensitivity Encoding (SENSE) head between the right and the left hemispheres (p>0.05). coil. For each of the 32 non-collinear and non- Similar results were obtained for the right and left coplanar diffusion-sensitizing gradients, we hemispheres of the red nucleus and the inferior acquired 60 contiguous slices parallel to the anterior olive (p>0.05). commissure-posterior commissure line. The imaging parameters used were: matrix = 128 × 128, DISCUSSION field of view = 221 × 221 mm2, TE = 76 ms, TR = 10,726 ms, SENSE factor = 2, EPI factor = 67, b = In the current study, we identified the ROT in 600 mm2s-1, and slice thickness = 2.3 mm. We also three dimensions from the red nucleus to the evaluated the fiber connectivity using FACT (fiber inferior olive in healthy subjects using DTT. assignment by continuous tracking), a 3-D fiber Several studies reported the pathway of the ROT in reconstruction algorithm contained within Philips the mammalian and the human brain3–7,11,12) and PRIDE software10). The termination criteria used some of these studies described the pathway of the were fractional anisotrophy (FA) <0.2 and direction ROT6,11,12). Strominger et al. reported the detailed threshold 750. A seed ROI was drawn in the red pathway of the ROT in the rhesus monkey brain6). nucleus, and another ROI was drawn in the inferior The ROT passes dorsal to the lateral part of the olive of the medulla. Fiber tracts passing through decussation of the superior cerebellar peduncle, and both ROIs were designated as the final tracts of then descends through the central part of the interest. FA and apparent diffusion coefficients tegmentum. It subsequently passes dorsal to the (ADC) were measured in each of the ROIs and the trapezoid body, and then between the medial ROT. lemnicus and the facial nucleus to the inferior olive. For statistical analysis, right and left hemispheres In 2007, Habas and Cabanis reported the pathway in were compared by the paired t-test. Analysis was their preliminary probabilistic tractography study of performed with SPSS version 14.0 software four human subjects11). They described the ROT (Chicago, IL), and statistical significance was descending within the dorsal pontine tegmentum chosen as p< 0.05. dorsal to the medial lemniscus. Recently, Kamali et al. described the pathway briefly for five human RESULTS subjects, as originating in the red nucleus and descending in the posterior area of the medial The ROT, originated in the red nucleus, and lemniscus to the lower pons12). These findings are passed laterally to the decussation of the superior compatible with our results in general, which found cerebellar peduncle in the lower midbrain. In the that the ROT descended laterally to the decussation pons, it descended through the area adjacent to the of the superior cerebellar peduncle in the lower medial lemnicus in the posterior direction. Within midbrain and descended through the area adjacent the medulla, it ended in the inferior olive, which to the medial lemnicus in the posterior direction in was located lateral to the medial lemnicus and the pons. In quantitative analysis of the ROT, we posterior to the pyramid. However, there were found that the FA value of the ROT (0.51) was some variations at the decussation of the superior slightly lower than that of the CST, as reported in cerebellar peduncle: in the lower midbrain (it previous studies (0.54–0.71)14,15). This finding passed postero-laterally in 4 hemispheres; and in the suggests that the ROT is less developed than the pons it descended lateral to the medial lemniscus in CST. the lower pons in 7 hemispheres, and postero- In conclusion, we identified the ROT in the laterally to the medial lemniscus in the mid-pons in human brain using DTT. These results will be 4 hemispheres). informative for research into motor control in the 9

Fig. 1. The pathway of the rubrospinal tract (ROT, 1: right, 2: left) in a subject (34-year-old man). The ROT, originates in the red nucleus (3), and passes laterally to the decussation of the superior cerebellar peduncle in the lower midbrain (4). In the pons, it descends through the area adjacent to the medial lemniscus in the posterior direction (5, 6). Within the medulla, it ends in the inferior olive, which is located lateral to the medial lemnicus and posterior to the pyramid (7, 8).

Table 1. Quantitative data for the rubro-olivary tract, the red nucleus, and the inferior olive Right Left Total FA Tract 0.51 ± 0.02 0.51 ± 0.02 0.51 ± 0.02 Red 0.50 ± 0.78 0.48 ± 0.05 0.49 ± 0.06 Olive 0.37 ± 0.08 0.36 ± 0.07 0.37 ± 0.08 ADC Tract 0.87 ± 0.08 0.85 ± 0.06 0.86 ± 0.07 Red 0.78 ± 0.07 0.81 ± 0.09 0.80 ± 0.08 Olive 0.90 ± 0.10 0.87 ± 0.10 0.89 ± 0.10 FA: fractional anisotropy. ADC: apparent diffusion coefficients. Values: mean ± standard deviation. Non significance of differences between the right and left hemispheres. 10 J. Phys. Ther. Sci. Vol. 22, No. 1, 2010 normal human brain and the motor recovery a retrograde and an anterograde neuronal tracer. mechanism following brain injury. We believe that Neuroscience, 1981, 6: 2379–2391. further, more detailed studies of the anatomy and 8) Itoh D, Aoki S, Maruyama K, et al.: Corticospinal function of the ROT are needed. tracts by diffusion tensor tractography in patients with arteriovenous malformations. J Comput Assist Tomogr, 2006, 30: 618–623. ACKNOWLEDGEMENT 9) Lee SK, Kim DI, Kim J, et al.: Diffusion-tensor MR imaging and fiber tractography: a new method of This work was supported by National Research describing aberrant fiber connections in developmental Foundation of Korea Grant funded by the Korean CNS anomalies. Radiographics, 2005, 25: 53–65; Government (KRF-2008-314-E00173). discussion 66–68. 10) Mori S, Crain BJ, Chacko VP, et al.: Three- dimensional tracking of axonal projections in the brain REFERENCES by magnetic resonance imaging. Ann Neurol, 1999, 45: 265–269. 1) Kahle W, Frotscher M: Nervous anatomy and sensory 11) Habas C, Cabanis EA: Anatomical parcellation of the organs. 5th ed. New York: Theme flexibook, 2003. brainstem and cerebellar white matter: a preliminary 2) Kennedy PR: Corticospinal, rubrospinal and rubro- probabilistic tractography study at 3 T. olivary projections: a unifying hypothesis. Trends Neuroradiology, 2007, 49: 849–863. Neurosci, 1990, 13: 474–479. 12) Kamali A, Kramer LA, Butler IJ, et al.: Diffusion 3) Conde F, Conde H: The rubro-olivary tract in the cat, tensor tractography of the somatosensory system in the as demonstrated with the method of retrograde human brainstem: initial findings using high isotropic transport of horseradish peroxidase. Neuroscience, spatial resolution at 3.0 T. Eur Radiol, 2009, 19: 1480– 1982, 7: 715–724. 1488. 4) Linauts M, Martin GF: An autoradiographic study of 13) Oldfield RC: The assessment and analysis of midbrain-diencephalic projections to the inferior handedness: the Edinburgh inventory. olivary nucleus in the opossum (Didelphis virginiana). Neuropsychologia, 1971, 9: 97–113. J Comp Neurol, 1978, 179: 325–353. 14) Ahn YH, Kim SH, Han BS, et al.: Focal lesions of the 5) Strominger NL, Nelson LR, Strominger RN: Banding corticospinal tract demonstrated by diffusion tensor of rubro-olivary terminations in the principal inferior imaging in patients with diffuse axonal injury. olivary nucleus of the chimpanzee. Brain Res, 1985, NeuroRehabilitation, 2006, 21: 239–243. 343: 185–187. 15) Wong JC, Concha L, Beaulieu C, et al.: Spatial 6) Strominger NL, Truscott TC, Miller RA, et al.: An profiling of the corticospinal tract in amyotrophic autoradiographic study of the rubroolivary tract in the lateral sclerosis using diffusion tensor imaging. J rhesus monkey. J Comp Neurol, 1979, 183: 33–45. Neuroimaging, 2007, 17: 234–240. 7) Walberg F, Nordby T: A re-examination of the rubro- olivary tract in the cat, using horseradish peroxidase as