Martinez M, Delivet-Mongrain H, Leblond H, Rossignol S. Recovery of hindlimb locomotion after incomplete spinal cord injury in the cat involves spontaneous compensatory changes within the spinal locomotor circuitry.

After spinal cord injury (SCI), precise assessment of motor recovery is essential to evaluate the outcome of new therapeutic approaches. Very little is known on the recovery of kinematic parameters after clinically-relevant severe compressive/contusive incomplete spinal cord lesions in experimental animal models. In the present study we evaluated the time-course of kinematic parameters during a 6-week period in rats walking on a treadmill after a severe thoracic clip compression SCI. The effect of daily treadmill training was also assessed. During the recovery period, a significant amount of spontaneous locomotor recovery occurred in 80% of the rats with a return of well-defined locomotor hindlimb pattern, regular plantar stepping, toe clearance and homologous hindlimb coupling. However, substantial residual abnormalities persisted up to 6 weeks after SCI including postural deficits, a bias of the hindlimb locomotor cycle toward the back of the animals with overextension at the swing/stance transition, loss of lateral balance and impairment of weight bearing. Although rats never recovered the antero-posterior (i.e. homolateral) coupling, different levels of decoupling between the fore and hindlimbs were measured. We also showed that treadmill training increased the swing duration variability during locomotion suggesting an activity-dependent compensatory mechanism of the motor control system. However, no effect of training was observed on the main locomotor parameters probably due to a ceiling effect of self-training in the cage. These findings constitute a kinematic baseline of locomotor recovery after clinically relevant SCI in rats and should be taken into account when evaluating various therapeutic strategies aimed at improving locomotor function.

Although a complete thoracic spinal cord section in various mammals induces paralysis of voluntary movements, the spinal lumbosacral circuitry below the lesion retains its ability to generate hindlimb locomotion. This important capacity may contribute to the overall locomotor recovery after partial spinal cord injury (SCI). In rats, it is usually triggered by pharmacological and/or electrical stimulation of the cord while a robot sustains the animals in an upright posture. In the present study we daily trained a group of adult spinal (T7) rats to walk with the hindlimbs for 10 wk (10 min/day for 5 days/wk), using only perineal stimulation. Kinematic analysis and terminal electromyographic recordings revealed a strong effect of training on the reexpression of hindlimb locomotion. Indeed, trained animals gradually improved their locomotion while untrained animals worsened throughout the post-SCI period. Kinematic parameters such as averaged and instant swing phase velocity, step cycle variability, foot drag duration, off period duration, and relationship between the swing features returned to normal values only in trained animals. The present results clearly demonstrate that treadmill training alone, in a normal horizontal posture, elicited by noninvasive perineal stimulation is sufficient to induce a persistent hindlimb locomotor recovery without the need for more complex strategies. This provides a baseline level that should be clearly surpassed if additional locomotor-enabling procedures are added. Moreover, it has a clinical value since intrinsic spinal reorganization induced by training should contribute to improve locomotor recovery together with afferent feedback and supraspinal modifications in patients with incomplete SCI.