Impairment and recovery of hand use after unilateral section of the dorsal columns of the spinal cord in squirrel monkeys

Damage to the ascending forelimb afferents in the dorsal columns (DCs) of the cervical spinal cord in monkeys impairs forelimb use, particularly hand dexterity. Although considerable recovery has been reported, interpretation of the results is complicated by the reproducibility of the lesion and behavioral assessment. Here, we examined the effects of a unilateral DC lesion at the C4-C6 spinal cord level in four adult squirrel monkeys. Behavioral performance was assessed on a reach-to-grasp task over 5-13 weeks after lesion. Retrograde tracers were injected into the skin of the fingertips to determine the distribution of axon terminals in the cuneate nucleus and estimate the effectiveness of lesion at the conclusion of each case. The size and level of DC lesion was reflected in the proportion of spared afferents, which ranged from 1 to 25% across monkeys. The experiments produced two major findings. First, the extent of deafferentation in the DC is directly related to the degree of reaching and grasping impairments, and to the reactivation profile and somatotopic reorganization in contralateral primary somatosensory cortex. Second, considerable behavioral recovery and cortical reorganization occurred even in the monkey with only 1% of axons spared in the DC. Our findings suggest that cutaneous inputs from the hand and forelimb are critical to the integrity of functions such as reaching and grasping. In addition, axon branches from peripheral afferents that terminate on neurons in the dorsal horn of the spinal cord are likely central to the functional recovery.