Axial motor organization in postmetamorphic tiger salamanders (Ambystoma tigrinum): a segregation of epaxial and hypaxial motor pools is not necessarily associated with terrestrial locomotion.

Abstract

The axial motor column has undergone a major reorganization during the evolution of vertebrates. In aquatic anamniotes including lampreys, goldfish, and mudpuppies, epaxial and hypaxial motoneurons are intermingled in the column. In contrast, epaxial and hypaxial motoneurons are spatially segregated in water snakes, rats, and monkeys, apparently as a consequence of an isomorphic mapping of motoneuron location onto the position of innervated muscle in the embryonic myotome. The presence of these two very different arrangements of motoneurons requires a major restructuring of the motor column during vertebrate evolution. The time of this reorganization is unknown. All amniotes studied to date have an epaxial/hypaxial segregation, and all anamniotes do not, suggesting that the map arose with the origin of amniotes. All the anamniotes examined previously were permanently aquatic, however, and the map might therefore be associated with terrestrial locomotion. If so, we would expect terrestrial anamniotes to have an arrangement of motoneurons like that in amniotes. We studied the organization of motoneurons innervating the trunk muscles of postmetamorphic, terrestrial tiger salamanders and asked whether their motor columns are more like those of amniotes or those of aquatic anamniotes. The motor column in tiger salamanders is similar to that seen in aquatic anamniotes and very like that in mudpuppies--permanently aquatic salamanders. There are several classes of motoneurons with morphological similarities to the primary and secondary motoneurons characteristic of aquatic anamniotes. Epaxial and hypaxial motoneurons show no obvious morphological differences and occupy extensively overlapping positions in the motor column. The only epaxial/hypaxial distinction is the presence of a few, small, relatively undifferentiated motoneurons located subadjacent to the ependymal layer. These motoneurons are filled only by horseradish peroxidase (HRP) applied to hypaxial nerves. They are probably newly born motoneurons, and their presence suggests continued addition of motoneurons, even in adult salamanders. We conclude that the epaxial/hypaxial segregation seen in amniotes is not necessarily associated with terrestrial locomotion. The segregation and the topographic map it reflects may have arisen in conjunction with the origin of amniotes. If they instead arose prior to the origin of extant amphibians, they must have been secondarily lost in those salamanders studied to date. An examination of the motor column of other amphibians should help to resolve this issue.