Ipsilesional Motor Cortex Plasticity Participates in Spontaneous Hindlimb Recovery after Lateral Hemisection of the Thoracic Spinal Cord in the Rat.

Abstract

After an incomplete spinal cord injury (SCI) spontaneous motor recovery can occur in mammals, but the underlying neural substrates remain poorly understood. The motor cortex is crucial for skilled motor learning and the voluntary control of movement and is known to reorganize after cortical injury to promote recovery. Motor cortex plasticity has also been shown to parallel the recovery of forelimb function after cervical SCI, but whether cortical plasticity participates in hindlimb recovery after SCI remains unresolved. Using intracortical microstimulation (ICMS) mapping, behavioral and cortical inactivation techniques in the female Long-Evans rat, we evaluated the spontaneous cortical mechanisms of hindlimb motor recovery 1-5 weeks after lateral hemisection of the thoracic (T8) spinal cord that ablated the crossed corticospinal tract (CST) from the contralesional motor cortex while sparing the majority of the CST from the ipsilesional motor cortex. Hemisection initially impaired hindlimb motor function bilaterally but significant recovery occurred during the first 3 weeks. ICMS revealed time-dependent changes in motor cortex organization, characterized by a chronic abolishment of hindlimb motor representation in the contralesional motor cortex and the development of transient bilateral hindlimb representation in the ipsilesional motor cortex 3 weeks after hemisection, when significant behavioral recovery occurred. Consistently, reversible inactivation of the ipsilesional, but not the contralesional motor cortex, during skilled ladder walking 3 weeks after hemisection reinstated deficits in both hindlimbs. These findings indicate that the ipsilesional motor cortex transiently reorganizes after lateral hemisection of the thoracic spinal cord to support recovery of hindlimb motor function.SIGNIFICANCE STATEMENT Partial motor recovery can occur after an incomplete spinal cord injury and is hypothesized to result from the reorganization of spared descending motor pathways. The motor cortex is crucial for the control of voluntary movement and contains topographical movement representations (motor maps) that are highly plastic. We examined the organization of hindlimb motor maps bilaterally after a lateral hemisection of the spinal cord to show that while motor maps are abolished in the deefferented cortex, the spared ipsilesional cortex transiently reorganizes to gain a representation of the affected hindlimb after injury that relates to recovery. This finding demonstrates that plasticity in the ipsilesional motor cortex at early time points after spinal cord hemisection is initially important to support motor recovery.