[ARTICLE] Body-Machine Interfaces after Spinal Cord Injury: Rehabilitation and Brain Plasticity – Full Text HTML

Abstract

The purpose of this study was to identify rehabilitative effects and changes in white matter microstructure in people with high-level spinal cord injury following bilateral upper-extremity motor skill training. Five subjects with high-level (C5–C6) spinal cord injury (SCI) performed five visuo-spatial motor training tasks over 12 sessions (2–3 sessions per week). Subjects controlled a two-dimensional cursor with bilateral simultaneous movements of the shoulders using a non-invasive inertial measurement unit-based body-machine interface. Subjects’ upper-body ability was evaluated before the start, in the middle and a day after the completion of training. MR imaging data were acquired before the start and within two days of the completion of training. Subjects learned to use upper-body movements that survived the injury to control the body-machine interface and improved their performance with practice. Motor training increased Manual Muscle Test scores and the isometric force of subjects’ shoulders and upper arms. Moreover, motor training increased fractional anisotropy (FA) values in the cingulum of the left hemisphere by 6.02% on average, indicating localized white matter microstructure changes induced by activity-dependent modulation of axon diameter, myelin thickness or axon number. This body-machine interface may serve as a platform to develop a new generation of assistive-rehabilitative devices that promote the use of, and that re-strengthen, the motor and sensory functions that survived the injury.

1. Introduction

Despite progress in the field of assistive technologies for people who suffered an injury to the spinal cord, most of the current devices to control computers and wheelchairs are set in place to require as little physical effort from the user as possible, and little attention has been paid to maintaining and strengthening the neural and muscular resources that survived the injury [1,2,3,4]. Spinal cord injury (SCI) leads to motor impairment, weakness, muscular and cortical atrophy and altered reflexes, and these have been shown to progress further with lack of exercise [5,6,7,8,9,10]. Even in individuals with injuries to the cervical spinal cord, some motor and sensory capacities may remain available in the upper body. Several studies have shown that using their remaining functions and keeping an active body is critical for people with SCI in order to avoid the collateral effects of paralysis and to potentially recover some of the lost mobility [5,6,7,11]. Therefore, it is crucial to develop the next generation of assistive-rehabilitative devices that promote learning through upper-body coordination.
Acquisition, retention and refinement of motor skills all rely on the capability of the nervous system to create new patterns of neural activation for accomplishing new tasks and for recovering lost motor functions [12]. Recent advances in neural imaging have allowed learning studies on juggling [13], balance [14] and body-machine interfaces (BMIs) by our group [15], to demonstrate motor skill learning-induced structural changes of cortical and subcortical areas in both gray matter and white matter by using diffusion tensor imaging (DTI). DTI non-invasively measures the direction and rate of water diffusion within tissue. White matter integrity is commonly measured by fractional anisotropy (FA), a normalized measure of the variance of the diffusion ellipsoid at each voxel [16]. FA values for white matter tissue have been shown to be affected by physiological parameters, such as axon diameter, axon number and myelin thickness [17].
Loss of somatosensory afference leads to functional cortical reorganization [18,19,20]. SCI has been shown to lead to spinal cord atrophy, cortical atrophy of primary and sensory cortex [8], descending motor tracts [9] and cortical reorganization of the sensorimotor system [8,10], and the degree of cortical reorganization is associated with the level of disability. Although the goal of most SCI treatments is to re-establish neural connections in order to restore motor function, it is unclear whether the anatomical and functional changes that follow injury can be reversed.
In this study, we investigated the rehabilitative effects and learning-induced changes in the brain white matter microstructure of people with high-level SCI after they practiced coordinated upper-body movements to control a computer cursor through a novel body-machine interface. Subjects learned to use the remaining ability of their shoulders and upper arms to perform movements that controlled a computer cursor to complete different related tasks. Complementary to [15], the purpose of this study was to identify changes in motor function and white matter by comparing clinical scores and FA values pre- and post-bilateral upper-body motor skill training in people with a high-level spinal cord injury. We started from the assumption that motor learning is likely to be associated with different brain reorganization in unimpaired subjects compared to subjects with tetraplegia, in consideration also of the greater need for the reorganization of motor functions in the latter group.

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Figure 5. Regions showing lower fractional anisotropy (FA) in spinal cord injury (SCI) subjects compared to controls. (A) Brain regions associated with motor function used to perform tract-based spatial statistics (TBSS) and ROI analyses; (B) TBSS results. Regions showing significantly higher (red-yellow) and lower (blue-light blue) FA values in SCI versus control subjects overlaid over the standard Montreal Neurological Institute (MNI)152 T1-weighted anatomical scan (p < 0.05, uncorrected). The location of each slice in Montreal Neurological Institute space is shown at the lower left section. a-s-pCR, anterior, superior and posterior corona radiata; CG, cingulum; g-bCC, genu and body of corpus callosum; a-pIC, anterior and posterior limbs of internal capsule.

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