Location of the corticospinal tract at the corona radiata in human brain

doi:10.1016/j.brainres.2010.02.050

Brain Research

Volume 1326, 22 April 2010, Pages 75-80

https://doi.org/10.1016/j.brainres.2010.02.050 Get rights and content

Abstract

Little is known about the location of the corticospinal tract (CST) at the corona radiata (CR). In the current study we attempted to elucidate the location of the CST for the hand at the CR using diffusion tensor tractography analysis based on functional MRI activation results. Functional MRI was performed at 1.5-T with timed hand grasp-release movements, and diffusion tensor tractography was performed using a Synergy-L Sensitivity Encoding (SENSE) head coil. Probabilistic mapping was obtained for 16 normal subjects using areas of functional MRI activation as the first region of interest (ROI 1) and the CST area in the lower pons as the second region of interest (ROI 2). The authors measured the antero-posterior and medio-lateral locations of pixels in the CST in two areas of the CR (CR 1 — the first axial image to show the septum pellucidum and the body of the fornix from the vertex, and CR 2 — the axial image showing the insular gyrus). The most probable locations in the medio-lateral direction (from the most medial point of the lateral ventricle wall to the most lateral point of the cerebral cortex) were 24.2% in both CR 1 and 2, and the most probable locations in the antero-posterior direction (from the most anterior point of the lateral ventricle to the most posterior point of the lateral ventricle) were 66.7 and 63.6% in CR 1 and 2, respectively. It was found that the CST for the hand descended through about one quarter (medio-lateral direction) and two-thirds (antero-posterior direction) at the CR.

Introduction

The corticospinal tract (CST) is the most important motor pathway in the human brain. Therefore, elucidating the state of the CST is mandatory for the rehabilitation of patients with weakness following brain injury. In the past, many studies have attempted to elucidate the location of the CST in the human brain using post-mortem dissection, electrophysiological, or clinico-radiologic correlation methods (Bertrand et al., 1965, Hanaway and Young, 1977, Kim and Pope, 2005, Kretschmann, 1988, Ross, 1980, Song, 2007). However, these methods have significant limitations in that they cannot visualize or identify the CST in the live brain. By contrast, diffusion tensor tractography (DTT), which is derived from diffusion tensor imaging (DTI), allows the visualization and localization of neural tracts at the subcortical level in three dimensions. Several DTT studies have been published on this topic (Holodny et al., 2005, Ino et al., 2007, Westerhausen et al., 2007, Yamada et al., 2007). However, DTT can lead to erroneous results due to operator-dependent bias that might occur during manual analysis (Lee et al., 2005). To overcome this limitation, some researchers have used the activation of functional MRI for analysis of DTT as a region of interest (ROI) instead of manually selecting an ROI (Guye et al., 2003, Kim et al., 2008). This suggests that DTT analyzed in conjunction with the results of fMRI activation would provide a more accurate localization of the CST.

Among the several regions through which the CST passes, the corona radiata (CR) is important because it is an area that is commonly affected by stroke, and its involvement is related to poor motor outcome in stroke patients (Kwon et al., 2007, Shelton and Reding, 2001). After the initial introduction of DTT, only a single DTT study has been conducted to determine the location of the CST in the CR, and there has been no combined fMRI and DTT study on this topic (Yamada et al., 2007). In the current study, we attempted to elucidate the location of the CST for the hand at the CR in the normal human brain using a combined fMRI/DTT method. To determine the locations of the individual CSTs in the CR, the CSTs are needed to be spatially normalized into a standard anatomical reference space by coregistering them with a standard anatomical template such as Montreal Neurological Institute (MNI) EPI template. However, the normalization is not easy to be applied in the clinical sites. Therefore, we defined the relative coordinates system by using anatomical landmarks as described in the Experimental procedures section for the easiness of clinical application. The locations of CSTs at CR were presented as a probabilistic map in the relative coordinates systems.

Section snippets

Results

The probabilistic functional activation maps for left hand and right hand movements are shown in Figs. 1A and B in order. Because we were interested in the activation in the primary sensori-motor cortex in which the pixels were anticipated to have high probabilities other activated areas with probability less than or equal to 10% were eliminated in the Fig. 1 for better visualization. The activated areas in the left and right hemispheres successfully located in the primary sensori-motor cortex

Discussion

In the current study we investigated the location of the hand CST at the right CR. This approach can be applied in a clinical setting, by analyzing DTT in conjunction with fMRI activation results. It is well-known that there is a somatotopical anterior-to-posterior arrangement of the CST in the CR (Inoue et al., 2001, Kim and Pope, 2005, Song, 2007, Tohgi et al., 1996, Yamada et al., 2007). Recently, Yamada et al. (Yamada et al., 2007), conducted a DTT study to evaluate the location of the CST

Subjects

Sixteen right-handed normal volunteers (14 men, 2 women, mean age = 28 years, range 24–33 years) with no history of neurological disorder were included in this study. All subjects provided signed, informed consent prior to the commencement of the study, and our institutional review board approved the study protocol.

Data acquisition

All data were acquired on a 1.5 T scanner (Hoffman-LaRoche, Ltd, Best, The Netherlands) using a Synergy-L Sensitivity Encoding (SENSE) head coil. The fMRI data were acquired using a

Acknowledgment

This work was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD)KRF-2005-003-H00026.

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However, the fact that we did not find any involvement of the posterior corona radiata in mild RLS/WED indicates that the AD decrease might be a result of the disease progress. The corona radiata consists of a mixture of associative and projection tracts and its posterior part is known to include descending pathways, such as the CST [115–117], but thalamocortical fibers from somatosensory nuclei also make a large contribution [90]. Therefore, this result points to possible changes in sensorimotor integration [38–40] underlying the syndrome.
Restless Legs Syndrome, a potentially disabling sleep disorder, also known as Willis-Ekbom disease (RLS/WED), may be caused by loss of inhibitory modulation of descending central motor pathways, structural changes in the somatosensory cortex, abnormal connectivity between motor and sensory areas, as well as by subtle abnormalities in white matter micro-organization.
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TBSS analysis revealed decreased axial diffusivity (AD) in the left posterior thalamic radiation in RLS/WED. In subjects with severe RLS/WED, AD was reduced in the left posterior corona radiata and this reduction was negatively correlated with severity of symptoms. ROI-based analysis showed that radial diffusivity (RD) was increased in the superior cerebellar peduncles of individuals with severe RLS/WED. Tractography did not show between-group or subgroup differences.
Our results are consistent with subtle white matter changes, prominently in RLS/WED subjects with more severe symptoms, in areas related to sensory or motor function, as well as to sensorimotor integration, compared to controls. These findings support the hypothesis, raised by prior pathophysiological studies, of defective integration within these networks.
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Of note, the occurrence of bilateral corona radiata infarcts is very rare, and in previous studies, only 1.2%-1.6% of patients were presented with first-ever stroke in this location.6,7 Furthermore, it is well known that pyramidal tract fibers are somatotopically arranged in the human corona radiata and corticobulbar and corticospinal tracts are located from an anterior to posterior direction.8-10 However, little is known about the location of the corticolingual tract (also referred to as cortico-hypoglossal) at this level.
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The corona radiata is connected to the cortical spinal tract, passing through the basal ganglia structures, and the posterior limb of the internal capsule (Wang et al., 2014). This tract is reported to play a role in various gross motor functions, particularly with respect to limb movement (Han et al., 2010). Given evidence for the disruption of fine motor speech processes when gross motor hand movements are required (Hirschfeld and Zwitserlood, 2012), our results showing that increases in FA of the right corona radiata are associated with slower response times, may be a reflection of the specialization and subsequent interference that occurs between gross and fine motor movements.
In this study, we examined the relationship between tractography-based measures of white matter integrity (ex. fractional anisotropy [FA]) from diffusion tensor imaging (DTI) and five reading-related tasks, including rapid automatized naming (RAN) of letters, digits, and objects, and reading of real words and nonwords. Twenty university students with no reported history of reading difficulties were tested on all five tasks and their performance was correlated with diffusion measures extracted through DTI tractography. A secondary analysis using whole-brain Tract-Based Spatial Statistics (TBSS) was also used to find clusters showing significant negative correlations between reaction time and FA. Results showed a significant relationship between the left inferior fronto-occipital fasciculus FA and performance on the RAN of objects task, as well as a strong relationship to nonword reading, which suggests a role for this tract in slower, non-automatic and/or resource-demanding speech tasks. There were no significant relationships between FA and the faster, more automatic speech tasks (RAN of letters and digits, and real word reading). These findings provide evidence for the role of the inferior fronto-occipital fasciculus in tasks that are highly demanding of orthography–phonology translation (e.g., nonword reading) and semantic processing (e.g., RAN object). This demonstrates the importance of the inferior fronto-occipital fasciculus in basic naming and suggests that this tract may be a sensitive predictor of rapid naming performance within the typical population. We discuss the findings in the context of current models of reading and speech production to further characterize the white matter pathways associated with basic reading processes.
Functional MRI vs. navigated TMS to optimize M1 seed volume delineation for DTI tractography. A prospective study in patients with brain tumours adjacent to the corticospinal tract
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DTI-based tractography is an increasingly important tool for planning brain surgery in patients suffering from brain tumours. However, there is an ongoing debate which tracking approaches yield the most valid results. Especially the use of functional localizer data such as navigated transcranial magnetic stimulation (nTMS) or functional magnetic resonance imaging (fMRI) seem to improve fibre tracking data in conditions where anatomical landmarks are less informative due to tumour-induced distortions of the gyral anatomy. We here compared which of the two localizer techniques yields more plausible results with respect to mapping different functional portions of the corticospinal tract (CST) in brain tumour patients.
The CSTs of 18 patients with intracranial tumours in the vicinity of the primary motor area (M1) were investigated by means of deterministic DTI. The core zone of the tumour-adjacent hand, foot and/or tongue M1 representation served as cortical regions of interest (ROIs). M1 core zones were defined by both the nTMS hot-spots and the fMRI local activation maxima. In addition, for all patients, a subcortical ROI at the level of the inferior anterior pons was implemented into the tracking algorithm in order to improve the anatomical specificity of CST reconstructions. As intra-individual control, we additionally tracked the CST of the hand motor region of the unaffected, i.e., non-lesional hemisphere, again comparing fMRI and nTMS M1 seeds. The plausibility of the fMRI-ROI- vs. nTMS-ROI-based fibre trajectories was assessed by a-priori defined anatomical criteria. Moreover, the anatomical relationship of different fibre courses was compared regarding their distribution in the anterior-posterior direction as well as their location within the posterior limb of the internal capsule (PLIC).
Overall, higher plausibility rates were observed for the use of nTMS- as compared to fMRI-defined cortical ROIs (p < 0.05) in tumour vicinity. On the non-lesional hemisphere, however, equally good plausibility rates (100%) were observed for both localizer techniques. fMRI-originated fibres generally followed a more posterior course relative to the nTMS-based tracts (p < 0.01) in both the lesional and non-lesional hemisphere.
NTMS achieved better tracking results than fMRI in conditions when the cortical tract origin (M1) was located in close vicinity to a brain tumour, probably influencing neurovascular coupling. Hence, especially in situations with altered BOLD signal physiology, nTMS seems to be the method of choice in order to identify seed regions for CST mapping in patients.
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There is, however, little consensus where — along the course of the CST — to place a second ROI. Two alternative positions have been suggested, one at the level of the internal capsule (posterior limb; Han et al., 2010; Holodny et al., 2005a and 2005b; Pan et al., 2012) and the other at the level of the brain stem (usually midbrain) (Gerardin et al., 2003; Lazar et al., 2003; Nimsky et al., 2006; Frey et al., 2012). However, thus far, it remains unknown which of the two positions yield more accurate tracking results in brain tumour patients.
Imaging of the course of the corticospinal tract (CST) by diffusion tensor imaging (DTI) is useful for function-preserving tumour surgery. The integration of functional localizer data into tracking algorithms offers to establish a direct structure–function relationship in DTI data. However, alterations of MRI signals in and adjacent to brain tumours often lead to spurious tracking results. We here compared the impact of subcortical seed regions placed at different positions and the influences of the somatotopic location of the cortical seed and clinical co-factors on fibre tracking plausibility in brain tumour patients.
The CST of 32 patients with intracranial tumours was investigated by means of deterministic DTI and neuronavigated transcranial magnetic stimulation (nTMS). The cortical seeds were defined by the nTMS hot spots of the primary motor area (M1) of the hand, the foot and the tongue representation. The CST originating from the contralesional M1 hand area was mapped as intra-individual reference. As subcortical region of interests (ROI), we used the posterior limb of the internal capsule (PLIC) and/or the anterior inferior pontine region (aiP). The plausibility of the fibre trajectories was assessed by a-priori defined anatomical criteria. The following potential co-factors were analysed: Karnofsky Performance Scale (KPS), resting motor threshold (RMT), T1-CE tumour volume, T2 oedema volume, presence of oedema within the PLIC, the fractional anisotropy threshold (FAT) to elicit a minimum amount of fibres and the minimal fibre length.
The results showed a higher proportion of plausible fibre tracts for the aiP-ROI compared to the PLIC-ROI. Low FAT values and the presence of peritumoural oedema within the PLIC led to less plausible fibre tracking results. Most plausible results were obtained when the FAT ranged above a cut-off of 0.105. In addition, there was a strong effect of somatotopic location of the seed ROI; best plausibility was obtained for the contralateral hand CST (100%), followed by the ipsilesional hand CST (>95%), the ipsilesional foot (>85%) and tongue (>75%) CST. In summary, we found that the aiP-ROI yielded better tracking results compared to the IC-ROI when using deterministic CST tractography in brain tumour patients, especially when the M1 hand area was tracked. In case of FAT values lower than 0.10, the result of the respective CST tractography should be interpreted with caution with respect to spurious tracking results. Moreover, the presence of oedema within the internal capsule should be considered a negative predictor for plausible CST tracking.
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Research ReportLocation of the corticospinal tract at the corona radiata in human brain

Abstract

Introduction

Section snippets

Results

Discussion

Subjects

Data acquisition

Acknowledgment

Neuroimage

Neuroimage

J. Neurol. Sci.

Neurosci. Lett.

Neuroimage

Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging

Nat. Neurosci.

Electrical exploration of the internal capsule and neighbouring structures during stereotaxic procedures

J. Neurosurg.

Diffusion-tensor MR tractography of somatotopic organization of corticospinal tracts in the internal capsule: initial anatomic results in contradistinction to prior reports

Radiology

Somatotopy of corticospinal tract in the internal capsule shown by functional MRI and diffusion tensor images

Neuroreport

Research Report
Location of the corticospinal tract at the corona radiata in human brain