Infant lesion effect: III. Anatomical correlates of sparing and recovery of function after spinal cord damage in newborn and adult cats.

We have demonstrated that sparing of tactile placing occurs after neonatal but not adult spinal cord damage and that the spared tactile placing of one limb depends on the corresponding (contralateral) sensorimotor cortex. In order to determine whether anatomical reorganization of the corticospinal or brainstem-spinal pathways also occurred which might account for the sparing of the tactile placing response, we used retrograde transport of horseradish peroxidase to map supraspinal neurons which project caudal to a spinal hemisection made either neonatally or in adulthood. The pattern of HRP labeling in the brainstem was identical in both the neonatal and adult operates. Neonatal operates, however, showed severe retrograde cell loss in brainstem nuclei which projected to the damaged side of the cord. This massive retrograde cell loss was not seen when lesions were made in the adult. In contrast, sparing of corticospinal projections and anatomical reorganization of the corticospinal tract were found after neonatal, but not adult spinal cord lesions. In adult operates, this lesion abolished HRP labeling in the contralateral sensorimotor cortex, while in all of the neonatal operates, HRP labeled cells were found throughout these cortical areas. The labeled cells had many characteristics in common with those of the normal CST. They were located in lamina V of cytoarchitectonic areas 4, 3, 1-2, and 5. Although the range of cell diameter was normal, the mean diameter of these spared neurons was below normal. Although the 'spared' CST may share many characteristics with the normal CST, its axons must have reached caudal segments of the cord by an abnormal pathway, since the normal route for the CST was destroyed by the lesion. The results indicate that two different regions of the CNS responded differently to the same neonatal lesion. Growing CST axons exhibited anatomical plasticity, contrasting with the retrograde death of the brainstem spinal tracts. We suggest that this difference between the two classes of pathways is due to the difference in time of their development. Only the latest developing pathways displayed anatomical sparing. The difference may also be seen in terms of the behavioral results. Only late-developing motor patterns were spared after neonatal lesions.