Relationship between structural brainstem and brain plasticity and lower-limb training in spinal cord injury: a longitudinal pilot study.

Michael Villiger,Marie-Claude Hepp-Reymond,Kynan Eng,Daniel Kiper,Spyros Kollias,Patrick Grabher,Armin Curt,Marc Bolliger,Sabina Hotz-Boendermaker,Patrick Freund

doi:10.3389/fnhum.2015.00254

Abstract

Rehabilitative training has shown to improve significantly motor outcomes and functional walking capacity in patients with incomplete spinal cord injury (iSCI). However, whether performance improvements during rehabilitation relate to brain plasticity or whether it is based on functional adaptation of movement strategies remain uncertain. This study assessed training improvement-induced structural brain plasticity in chronic iSCI patients using longitudinal MRI. We used tensor-based morphometry (TBM) to analyze longitudinal brain volume changes associated with intensive virtual reality (VR)-augmented lower limb training in nine traumatic iSCI patients. The MRI data was acquired before and after a 4-week training period (16–20 training sessions). Before training, voxel-based morphometry (VBM) and voxel-based cortical thickness (VBCT) assessed baseline morphometric differences in nine iSCI patients compared to 14 healthy controls. The intense VR-augmented training of limb control improved significantly balance, walking speed, ambulation, and muscle strength in patients. Retention of clinical improvements was confirmed by the 3–4 months follow-up. In patients relative to controls, VBM revealed reductions of white matter volume within the brainstem and cerebellum and VBCT showed cortical thinning in the primary motor cortex. Over time, TBM revealed significant improvement-induced volume increases in the left middle temporal and occipital gyrus, left temporal pole and fusiform gyrus, both hippocampi, cerebellum, corpus callosum, and brainstem in iSCI patients. This study demonstrates structural plasticity at the cortical and brainstem level as a consequence of VR-augmented training in iSCI patients. These structural changes may serve as neuroimaging biomarkers of VR-augmented lower limb neurorehabilitation in addition to performance measures to detect improvements in rehabilitative training.

Highlights

Complete spinal cord injury leads to permanent impairments of motor, sensory, and autonomic function
A survey at the end of every training session indicated that patients enjoyed the Virtual reality (VR)-augmented lower limb tasks and maintained a high level of motivation and attention
This study reveals specific structural brain changes associated with motor performance improvements following intensive VR-augmented lower limb training in chronic incomplete spinal cord injury (iSCI) patients

Summary

Introduction

Complete spinal cord injury leads to permanent impairments of motor, sensory, and autonomic function. In the majority of cases, sensorimotor functions are partially preserved below the lesion level due to an anatomically incomplete lesion, resulting in an incomplete spinal cord injury (iSCI; Wyndaele and Wyndaele, 2006). The ability to relearn successfully a motor action depends on the key concepts for motor learning, i.e., repetition, performance feedback and motivation (Holden, 2005). Virtual reality (VR)-augmented neurorehabilitation interventions in patients with chronic iSCI have shown to improve motor function and neuropathic pain (e.g., Villiger et al, 2011, 2013). The neurophysiological mechanisms underlying performance improvements in patients with acute and chronic iSCI are uncertain

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Discussion

Conclusion