During regeneration of lamprey spinal axons, growth cones lack filopodia and lamellipodia, contain little actin, and elongate much more slowly than do typical growth cones of embryonic neurons. Moreover, these regenerating growth cones are densely packed with neurofilaments (NFs). Therefore, after spinal hemisection the time course of changes in NF mRNA expression was correlated with the probability of regeneration for each of 18 identified pairs of reticulospinal neurons and 12 cytoarchitectonic groups of spinal projecting neurons. During the first 4 weeks after operation, NF message levels were reduced dramatically in all axotomized reticulospinal neurons, on the basis of semiquantitative in situ hybridization for the single lamprey NF subunit (NF-180). Thereafter, NF expression returned toward normal in neurons whose axons normally regenerate beyond the transection but remained depressed in poorly regenerating neurons. The recovery of NF expression in good regenerators was independent of axon growth across the lesion, because excision of a segment of spinal cord caudal to the transection site blocked regeneration but did not prevent the return of NF-180 mRNA. The early decrease in NF mRNA expression was not accompanied by a reduction in NF protein content. Thus the axotomy-induced loss of most of the axonal volume resulted in a reduced demand for NF rather than a reduction in volume-specific NF synthesis. We conclude that the secondary upregulation of NF message during axonal regeneration in the lamprey CNS may be part of an intrinsic growth program executed only in neurons with a strong propensity for regeneration.

The descending spinal projecting system of the lamprey is of interest because it includes axons that activate swimming pattern generators and because regeneration of this system is involved in the behavioral recovery of lampreys following spinal transection. However, little is known about the true size of this projection and of the distribution of its terminations along the spinal cord. Brain neurons with spinal projections were studied in larval sea lampreys by using wholemount preparations labeled retrogradely with horseradish peroxidase (HRP) from spinal injections at 10%, 15%, 25%, 50%, 70%, and 75% of body length from the anterior end. Neurons projecting to different levels of the spinal cord were mapped. A large number of descending axons terminated within nine segments caudal to the last gill. The spinal projection system was divided into 10 bilateral groups based on cytoarchitectural landmarks. All of the lateral nuclear groups had contralateral spinal projections. In addition to the 12 pairs of Müller cells, the pair of Mauthner cells, and the pair of auxiliary Mauthner cells described by previous authors, the study revealed four pairs of smaller neurons that were individually identifiable.

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