Elsevier

NeuroImage

Volume 54, Issue 2, 15 January 2011, Pages 1254-1261
NeuroImage

Cerebral activation is correlated to regional atrophy of the spinal cord and functional motor disability in spinal cord injured individuals

https://doi.org/10.1016/j.neuroimage.2010.09.009Get rights and content

Abstract

Recovery of function following lesions in the nervous system requires adaptive changes in surviving circuitries. Here we investigate whether changes in cerebral activation are correlated to spinal cord atrophy and recovery of functionality in individuals with incomplete spinal cord injury (SCI).

19 chronic SCI individuals and 7 age-comparable controls underwent functional magnetic resonance imaging (fMRI) while performing rhythmic dorsiflexion of the ankle. A significant negative correlation was found between the activation in the ipsilateral motor (M1) and bilateral premotor cortex (PMC) on one hand and the functional ability of the SCI participants measured by the clinical motor score on the other. There was no significant correlation between activation in any other cerebral area and the motor score.

Activation in ipsilateral somatosensory cortex (S1), M1 and PMC was negatively correlated to the width of the spinal cord in the left–right direction, where the corticospinal tract is located, but not in the antero-posterior direction. There was a tendency for a negative correlation between cerebral activation in ipsilateral S1, M1 and PMC and the amplitude of motor evoked potentials in the tibialis anterior muscle elicited by transcranial magnetic stimulation, but this did not reach statistical significance. There was no correlation between motor score or spinal cord dimensions and the volume of the cortical motor areas.

The observations show that lesion of descending tracts in the lateral part of the spinal cord results in increased activation in ipsilateral motor and sensory areas, which may help to compensate for the functional deficit following SCI.

Research Highlights

► Cerebral activation in sensory and motor areas is negatively correlated with the extent of lesion in the lateral columns of the spinal cord. ► Cerebral activation in sensory and motor areas is negatively correlated with motor function. ► Ipsilateral cortical activation is correlated to lateralized ipsilateral atrophy.

Introduction

There is little potential for regeneration of central motor and sensory fibres following spinal cord injury (SCI) in human individuals (Raineteau and Schwab, 2001). Attempts at promoting regeneration of damaged fibres have so far shown relatively little effect (Priestley et al., 2002, Raisman and Li, 2007) and recovery of function following SCI therefore still relies mainly on reorganisation and adaptation of surviving neural circuitries below and above the lesion (Raineteau and Schwab, 2001). Reorganisation of circuitries in the motor cortex has been relatively well characterized in individuals with stroke and there is accumulating evidence that this reorganisation is of importance for the long-term potential for functional recovery (Ward et al., 2003a, Ward et al., 2003b). One of the main functional adaptations in stroke patients appears to be recruitment of additional motor areas, in particular the premotor cortex (PMC) in order to compensate for reduced capacity of the primary motor cortex (M1) to generate sufficient motor output during task performance in severely affected and badly recovered patients (Ward et al., 2003a, Ward et al., 2003b). Comparatively little is known about the significance of cortical reorganisation for functional recovery following SCI. Dong et al. (2008) demonstrated in 8 patients that the activated volume was larger in ipsilateral sensorimotor cortex and that the magnitude of activation was larger in the contralateral dorsal PMC during wrist movement in individuals with spinal cord compression than in healthy individuals. Following decompression the activation was normalized. A similar finding was also reported for cerebral activation during wrist and ankle movements by Holly et al. (2007) in 4 individuals with myelopathy. Jurkiewicz et al. (2007) demonstrated that the volume of activation in M1 increased and the activation of associated cortical sensorimotor areas decreased as their six examined individuals recovered functionally following SCI. In another study the same group has recently demonstrated that individuals who did not recover functional ability showed reduced activation in M1 as well as in associated cortical areas (Jurkiewicz et al., 2010).

A question, which has not been addressed in previous studies, is how the cerebral reorganisation relates to the extent of lesion of the spinal cord. So far imaging techniques have not permitted a detailed analysis of lesion of specific pathways in the spinal cord, even with the development of new techniques such as diffusion tensor imaging, but in a recent study it was reported that atrophy of the lateral part of the spinal cord, where the corticospinal tract is located, was correlated to the clinical motor deficit in SCI individuals, whereas atrophy in the posterior part of the spinal cord was correlated to the clinical sensory deficit (Lundell et al., 2010). Based on this, it was the purpose of the present study to test the hypothesis that changes in cerebral activation following spinal cord lesion are better correlated to atrophy of the lateral parts of the spinal cord than the anterior and posterior parts.

We consequently recorded cerebral activation using Blood Oxygenation Level dependent functional magnetic resonance imaging (BOLD fMRI) in a group of SCI individuals during standardized movements of the foot that all individuals were able to accomplish. We then investigated the correlation of the cerebral activation to the extent of damage in the spinal cord (measured as a directional specific atrophy of the spinal cord) and the functional recovery of the individuals (measured as clinical motor and sensory scores). We also investigated the correlation of cerebral activation with functional transmission in the corticospinal tract measured as the amplitude and latency of motor evoked potentials elicited by transcranial magnetic stimulation. We finally analysed whether spinal cord lesion was related to changes in the volume of the cortical motor areas. The main new finding of the study was that activation in the motor areas was correlated to the extent of lesion in the lateral part of the spinal cord suggesting that lesion of corticospinal fibres following SCI is functionally compensated by activity in neighbouring motor areas.

Section snippets

Participants

We enrolled 7 male healthy volunteers with no known history of neurological disorders (mean (SD) 42 (18) years) and 19 individuals with chronic incomplete SCI (mean (SD) 46 (12) years, gender: 1 female/18 male) including lesions on cervical (nc = 15), thoracic (nt = 3), and lumbar (nl = 1) spinal cord levels. Time from injury spanned from 1 to 28 years (mean 13 years). Two SCI participants were not included in the group analyses because they showed no significant cortical activation when moving the

Results

All participants were able to move the foot to some extent. Fig. 1B shows examples of the ankle movements in a healthy control participant (upper panel), an SCI participant with little atrophy of the lateral parts of the spinal cord (middle panel) and a SCI participant with pronounced atrophy of the lateral parts of the spinal cord (lower panel). All participants moved the foot at the same frequency in response to the visual pacing signal, but the movement amplitude was much lower for the SCI

Discussion

In this study we have demonstrated that atrophy of the lateral parts of the spinal cord following spinal cord lesion is correlated with larger activation in the ipsilateral somatosensory–motor cortex. This suggests that the brain may partly compensate damage to lateral column motor fibres, such as the corticospinal tract, by increased activity in cortical neuronal populations, which are not normally involved in the control of dorsiflexion.

Participants with the largest atrophy of the lateral

Conclusion

This study has demonstrated that lesion of the lateral parts of the spinal cord where the corticospinal tract and other descending pathways are located is correlated to reduced motor ability and increased cerebral activation in the ipsilateral S1 and M1 as well as the PMC bilaterally. This suggests that reorganisation of cerebral control of leg muscle activity following spinal cord lesion involves increased activation of cortical areas that are normally not recruited during movement.

Acknowledgments

This study was supported by a grant from the Ludvig and Sara Elsass Foundation and a fellowship for DB from the Canadian Institutes of Health Research. The MR scanner was donated by the Simon Spies Foundation.

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