Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways

Abstract

In the previous 2 papers, we focused on the selective affinities that growth cones display for specific axonal pathways. Little is known, however, about how this orthogonal scaffold of axonal pathways in the CNS is established in the first place, and what, if any, role glia might play in these events. Here we show an important relationship between pioneering growth cones and primitive glial cells in the developing longitudinal connectives and peripheral nerve roots of the grasshopper embryo. We describe a preformed glial pathway for the formation of the intersegmental nerve, one of the major roots exiting the CNS. The growth cones that pioneer this nerve display a selective affinity for the segment boundary cell (SBC), a primitive glial cell that establishes the location of this nerve root. Similar glial cells are also found along the pathway where the longitudinal connectives form, and they too may play an important role in the formation of the first longitudinal axonal pathways. Experimental analysis shows that when the SBC is ablated, the growth cones that normally turn laterally to pioneer the intersegmental nerve do not do so, thus confirming the importance of the guiding role of this glial cell. We postulate that a simple orthogonal scaffold of primitive glia is involved in the initial patterning of axonal pathways within and exiting the insect CNS; this concept is remarkably similar to the blueprint hypothesis proposed by Singer et al. (1979) to explain the development of axon pathways in vertebrates.