METAMORPHOSIS OF SPINAL-PROJECTING NEURONS IN THE BRAIN OF THE SEA LAMPREY DURING TRANSFORMATION OF THE LARVA TO ADULT - NORMAL ANATOMY ANDRESPONSE TO AXOTOMY

The spinal projecting system of the sea lamprey (Petromyzon marinus) h as been used extensively in studies of axonal regeneration in both lar vae and adults. However, little is known about the changes that are un dergone by this system during metamorphosis. In order to determine the developmental changes in the size of the descending spinal projection and in the morphology of its neurons, larval, transforming, and adult lamprey brains were labeled by retrograde transport of horseradish pe roxidase (HRP) injected into the spinal cord at 25% of body length. Ex amination of brain wholemount preparations revealed that the total num ber of labeled neurons doubled during metamorphosis. Most of this incr ease could be explained by elongation of reticulospinal axons from the rostralmost segments of the spinal cord to locations caudal to the in jection site. There were no additions or deletions of either identifie d reticulospinal neurons or of reticulospinal nuclear groups between t he larval and the adult stages. The proportions of Muller and Mauthner cells that were labeled reached a maximum of 93% during the early sta ges of metamorphosis. Axons of these neurons are known to project almo st the entire length of the cord, even in larvae. Therefore, the effic iency of retrograde transport appears to be greater during metamorphos is than during larval or adult stages. While changes in efficiency of retrograde transport could account for some of the apparent increase i n reticulospinal neuron numbers between larvae and animals undergoing metamorphosis, this could not contribute to the further increase in th e apparent size of the reticulospinal system in the adult, since effic iency of retrograde labeling in these animals was lower than that at e arlier stages. With retrograde labeling, a significant increase was se en in the profusion of dendritic arborization of some Muller and Mauth ner cells during the early stages of metamorphosis. This correlated wi th an increase in the incidence of extreme axonal die-back, as indicat ed by the presence of retraction bulbs within the brainstem. However, intracellular injection of Neurobiotin in untransected animals showed similar degrees of dendritic arborization at all examined stages of de velopment. Therefore, the dendritic profusion did not reflect developm ental changes in neuronal morphology but rather reflected an increased sensitivity to axotomy during metamorphosis. We conclude that, during the transformation of the lamprey from the large larval to the adult form, there is little change in either the size or the dendritic morph ology of the identified giant reticulospinal neurons. With respect to the smaller reticulospinal neurons, the distance of projection of many of their axons increases during metamorphosis, but there is very litt le increase in the number of reticulospinal neurons. (C) 1995 Wiley-Li ss, Inc.