Regeneration of descending projections to the spinal motor neurons after spinal hemisection in the goldfish.

Following spinal transection, descending spinal projections from goldfish brainstem neurons spontaneously regenerate beyond the lesion site. The nucleus of the medial longitudinal fasciculus (nFLM), which has a critical role in swimming, also sends regenerated axons over a long distance to the ipsilateral spinal cord. To examine whether regenerated axons re-innervate the appropriate targets, we injected rhodamine dextran amine (RDA) into the nFLM of spinally transected goldfish and examined anterogradely labeled axons in the spinal cord. In intact controls, there were many RDA-labeled boutons or varicosities in the spinal cord in close apposition to both neurons positive for calcitonin gene-related peptide (CGRP), and those negative for CGRP. This suggests that the nFLM neurons project axons directly to the motoneurons and interneurons in the spinal cord. Four days after hemisection 1 mm caudal to the rostral end of the spinal cord, the number of RDA-labeled boutons in close apposition to the spinal neurons was significantly decreased on the side ipsilateral to the injection. Six to twelve weeks after spinal hemisection, regenerated axons ran through the repaired lesion site, and the number of RDA-labeled boutons or varicosities in close apposition to the ipsilateral spinal neurons had returned to the control level. These findings suggest that the midbrain-spinal pathway, critical for locomotion in fish, spontaneously regenerates beyond the lesion site to re-innervate the appropriately innervated targets after spinal lesion.