Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta)

Abstract

Six adult monkeys (Macaca mulatta) received a unilateral lesion of the lateral corticospinal tract (CST) in the thoracic spinal cord. Prior to surgery, the animals were trained to perform quadrupedal stepping on a treadmill, and item retrieval with the foot. Whole body kinematics and electromyogram (EMG) recordings were made prior to, and at regular intervals over a period of 12 weeks after the CST lesion. After 1 week of recovery, all monkeys were able to walk unaided quadrupedally on the treadmill. The animals, however, dragged the hindpaw ipsilateral to the lesion along the treadmill belt during the swing phase and showed a significant reorganization of the spatiotemporal pattern of hindlimb (HL) and forelimb (FL) displacements. The inability to appropriately trigger the swing phase resulted in an increase in the cycle duration and stride length of both HLs. The stance duration decreased in the ipsilateral HL, and increased in the contralateral HL and both FLs. Consequently, there was a dramatic disruption of interlimb and intralimb coupling that was reflected in the limb kinematic and EMG patterns. The CST lesion completely abolished the ability of the monkeys to retrieve items with the foot ipsilateral to the lesion and significantly disrupted the level of performance of the contralateral HL during the first 2 weeks post-lesion. Interestingly, selected HL muscles remained almost quiescent when the monkeys attempted to retrieve items, but were unsuccessful with the affected foot at 1 week post-lesion, whereas the capacity to activate the same muscles was preserved, although reduced, during stepping. Spatial and temporal parameters of gait, kinematics, and EMG patterns recorded during locomotion generally converged toward control values over time, but significant differences persisted up to 12 weeks post-lesion. Although some control was recovered over the distal foot musculature, fine foot grasping remained significantly impaired at the end of the testing period. These findings demonstrate that the CST pathway from the brain normally makes an important contribution to interlimb and intralimb coordination during basic locomotion, and to muscle activation to produce dexterous foot digit movements in the monkey. Furthermore, the present study indicates that the primate has the ability to rapidly accommodate locomotor performance, and to a lesser degree fine foot motor skills, to a reduction in supraspinal control. Identification of the neural substrates mediating the rapid recovery of motor function following injury to the primate spinal cord could provide insight into developing repair strategies to augment functional recovery from neuromotor impairments.