Pathfinding by neuronal growth cones in grasshopper embryos. III. Selective affinity of the G growth cone for the P cells within the A/P fascicle

Abstract

The growth cone of the G neuron selectively fasciculates upon specific axon bundles in a stereotypic sequence as it navigates through the developing central nervous system of the grasshopper embryo. It turns and extends anteriorly in the contralateral neuropil of the second thoracic ganglion at a specific choice point where it fasciculates with the A/P axon bundle which contains the axons of the A1, A2, P1, and P2 neurons. We previously hypothesized (Raper, J. A., M. J. Bastiani, and C. S. Goodman (1983) J. Neurosci. 3: 20-41) that this fascicle, or subsets of axons within it, were specifically labeled and that the G neuron was determined to follow this labeled pathway. Here we report on an ultrastructural analysis of the interactions between the G growth cone and its filopodia with the cells of the A/P fascicle at the choice point. As G reaches its choice point, its filopodia are in more frequent contact with the A/P fascicle in comparison to the other longitudinal axon fascicles. Within the A/P fascicle, the tip of G's growth cone is found to be closely associated with the P and not the A axons. Furthermore, before the G growth cone climbs onto the A/P fascicle, its filopodia show a selective affinity for the P axons as compared to the A axons. Another specific interaction involves selective filopodial insertions; only filopodia from the P cells were found to insert into the G growth cone and induce coated pits and vesicles. These findings suggest that G is able to distinguish the A/P fascicle from other axon bundles and, moreover, is able to distinguish the P axons from the A axons. The companion paper (Raper, J. A., M. J. Bastiani, and C. S. Goodman (1984) J. Neurosci. 4: 2329-2345) presents experimental results based on specific axon ablations that further support this hypothesis.