Neonatal midthoracic spinal cord injury disrupts the development of postural reflexes and hindlimb locomotion. The recovery of rhythmical alternating movements, such as locomotion, is enhanced in injured animals receiving fetal spinal cord transplants. Neonatal cervical spinal cord injury disrupts not only locomotion but also skilled forelimb movement. The aims of this study were to determine the consequences of cervical spinal cord injury on forelimb motor function and to determine whether transplants of fetal spinal cord support normal development of skilled forelimb use after this injury. Three-day-old rats received a cervical spinal cord lesion at C3, with or without a transplant of fetal cervical spinal cord (embryonic day 14); unoperated pups served as controls. Animals were examined daily during the first month of life using a behavioral protocol that assessed reflexes, postural reactions, and forelimb motor skills. They also were trained and tested as adults to assess performance in goal-directed reaching tasks. The onset of postural reflexes was delayed in the lesion-only group, and goal-directed reaching and associated postural adjustments failed to develop. The transplant group developed reflex responses and skilled forelimb activity that resembled normal movement patterns. Transplant animals developed both target reaching and accompanying postural adjustments. Target reaching requires integration of segmental, intersegmental, and supraspinal input to propriospinal and motor neurons over many spinal cord levels. Transplants may support the reestablishment of input onto these neurons, permitting the development of skilled forelimb activity after neonatal cervical spinal cord injury. The neuroanatomical reorganization of descending and propriospinal input was examined in the companion paper (Diener and Bregman, 1998).

Cervical spinal cord injury at birth permanently disrupts forelimb function in goal-directed reaching. Transplants of fetal spinal cord tissue permit the development of skilled forelimb use and associated postural adjustments (, companion article). The aim of this study was to determine whether transplants of fetal spinal cord tissue support the remodeling of supraspinal and segmental pathways that may underlie recovery of postural reflexes and forelimb movements. Although brainstem-spinal and segmental projections to the cervical spinal cord are present at birth, skilled forelimb reaching has not yet developed. Three-day-old rats received a cervical spinal cord overhemisection with or without transplantation of fetal spinal cord tissue (embryonic day 14); unoperated pups served as normal controls. Neuroanatomical tracing techniques were used to examine the organization of CNS pathways that may influence target-directed reaching. In animals with hemisections only, corticospinal, brainstem-spinal, and dorsal root projections within the spinal cord were decreased in number and extent. In contrast, animals receiving hemisections plus transplants exhibited growth of these projections throughout the transplant and over long distances within the host spinal cord caudal to the transplant. Raphespinal axons were apposed to numerous propriospinal neurons in control and transplant animals; these associations were greatly reduced in the lesion-only animals. These observations suggest that after neonatal cervical spinal cord injury, embryonic transplants support axonal growth of CNS pathways and specifically supraspinal input to propriospinal neurons. We suggest that after neonatal spinal injury in the rat, the transplant-mediated reestablishment of supraspinal input to spinal circuitry is the mechanism underlying the development of target-directed reaching and associated postural adjustments.

The normal development of the somatosensory system requires intact sensory inputs from the periphery during a critical window of time early in development. Here we determined how the removal of only part of the ascending spinal inputs early in development affects the anatomical and neurophysiological development of the somatosensory system. We performed spinal overhemisections in rat pups at C3/C4 levels on the third day after birth. This procedure hemisects the spinal cord on one side and transects the dorsal funiculus on the other side. When the rats were 6-8 months old, the responsiveness and somatotopy of the primary somatosensory cortex (S1) contralateral to the hemisection were determined using standard multiunit mapping techniques. Sections of the flattened cortex were processed for cytochrome oxidase activity, Nissl substance, or myelin. We found that histologically apparent modules that are normally present in the regions of the forepaw and the hindpaw representations were absent, whereas the lateral barrel field representing the face was completely normal. The neurons in the forepaw regions of S1 either did not respond to the stimulation of the skin of any region of the body or responded to the stimulation of the upper arm afferents that enter the spinal cord rostral to the site of the lesion. The results show that a lack of normal sensory inputs via ascending pathways in the dorsal spinal cord during early development results in massive anatomical and neurophysiological abnormalities in the cortex. Intact crossed spinothalamic pathways are unable to support the normal development of the forepaw barrels.