Embryonic development of a peripheral nervous system: nerve tract associated cells and pioneer neurons in the antenna of the grasshopper Schistocerca gregaria

Abstract

The grasshopper antenna is an articulated appendage associated with the deutocerebral segment of the head. In the early embryo, the meristal annuli of the antenna represent segment borders and are also the site of differentiation of pioneer cells which found the dorsal and ventral peripheral nerve tracts to the brain. We report here on another set of cells which appear earlier than the pioneers during development and are later found arrayed along these tracts at the border of epithelium and lumen. These so-called nerve tract associated cells differ morphologically from pioneers in that they are bipolar, have shorter processes, and are not segmentally organized in the antenna. Nerve tract associated cells do not express horseradish peroxidase and so are not classical neurons. They do not express antigens such as repo and annulin which are associated with glia cells in the nervous system. Nerve tract associated cells do, however, express the mesodermal/mesectodermal cell surface marker Mes-3 and putatively derive from the antennal coelom and then migrate to the epithelium/lumen border. Intracellular recordings show that such nerve tract associated cells have resting potentials similar to those of pioneer cells and can be dye coupled to the pioneers. Similar cell types are present in the maxilla, a serially homologous appendage on the head. The nerve tract associated cells are organized into a cellular scaffold which we speculate may be relevant to the navigation of pioneer and sensory axons in the early embryonic antennal nervous system.