Initial formation and secondary condensation of nerve pathways in the medicinal leech.
Invertebrates have proved to be important experimental systems for examining questions related to growth cone navigation and nerve formation, in large part because of their simpler nervous systems. However, such apparent simplicity can be deceiving because the final stereotyped patterns may be the result of multiple developmental mechanisms and not necessarily the sole consequence of the pathway choices of individual growth cones. We have examined the normal sequence of events that are involved in the formation of the major peripheral nerves in leech embryos by employing (1) an antibody directed against acetylated tubulin to label neurons growing out from the central nervous system, (2) the Lan3-2 antibody to label a specific population of peripheral neurons growing into the central nervous system, and (3) intracellular dye filling of single cells. We found that the mature pattern of nerves was characterized by a pair of large nerve roots, each of which branched into two major tracts. The earliest axonal projections did not, however, establish this pattern definitively. Rather, each of the four nerves initially formed as discrete, roughly parallel tracts without bifurcation, with the final branching pattern of the nerve roots being generated by a secondary condensation. In addition, we found that some of the nerves were pioneered in different ways and by different groups of neurons. One of the nerves was established by central neurons growing peripherally, another by peripheral neurons growing centrally. These results suggest that the formation of common nerves and neuronal pathfinding in the leech involves multiple sets of growth cone guidance strategies and morphogenetic mechanisms that belie its apparent simplicity.
Jellies
J
J
Department of Biological Sciences, Western Michigan University, Kalamazoo 49008, USA. john.jellies@wmich.edu
Kopp
D M
DM
Johansen
K M
KM
Johansen
J
J
D000344:Afferent Pathways / Q000648:ultrastructure; D000818:Animals; D000911:Antibodies, Monoclonal; D001369:Axons / Q000648:ultrastructure*; D002490:Central Nervous System / Q000166:cytology; D004525:Efferent Pathways / Q000648:ultrastructure; D004625:Embryo, Nonmammalian / Q000648:ultrastructure; D017952:Ganglia, Invertebrate / Q000196:embryology; D007865:Leeches; D008959:Models, Neurological; D009024:Morphogenesis; D009434:Neural Pathways / Q000196:embryology*; D009474:Neurons / Q000648:ultrastructure*; D017933:Peripheral Nervous System / Q000166:cytology; D014404:Tubulin / Q000276:immunology
D000911:Antibodies, Monoclonal; D014404:Tubulin