Abstract
Development of the adult olfactory system of the moth Manduca sexta depends on reciprocal interactions between olfactory receptor neuron (ORN) axons growing in from the periphery and centrally-derived glial cells. Early-arriving ORN axons induce a subset of glial cells to proliferate and migrate to form an axon-sorting zone, in which later-arriving ORN axons will change their axonal neighbors and change their direction of outgrowth in order to travel with like axons to their target areas in the olfactory (antennal) lobe. These newly fasciculated axon bundles will terminate in protoglomeruli, the formation of which induces other glial cells to migrate to surround them. Glial cells do not migrate unless ORN axons are present, axons fail to fasciculate and target correctly without sufficient glial cells, and protoglomeruli are not maintained without a glial surround. We have shown previously that Epidermal Growth Factor receptors and the IgCAMs Neuroglian and Fasciclin II play a role in the ORN responses to glial cells. In the present work, we present evidence for the importance of glial Fibroblast Growth Factor receptors in glial migration, proliferation, and survival in this developing pathway. We also report changes in growth patterns of ORN axons and of the dendrites of olfactory (antennal lobe) neurons following blockade of glial FGFR activation that suggest that glial FGFR activation is important in reciprocal communication between neurons and glial cells.
Highlights
The past decade has seen a growing appreciation of the importance of neuron-glia signaling in nervous system development, and glial cells have been shown to play numerous roles affecting axon outgrowth or growth arrest, course changes, fasciculation, and targeting [1,2,3,4,5,6,7,8,9,10]
Because we find no evidence for Fibroblast Growth Factor Receptors (FGFRs) on olfactory receptor neuron (ORN), this suggests that activation of glial FGFRs is important in glia-to-ORN signaling
The primary olfactory pathway of M. sexta consists of a small number of cell types: a) ORNs, whose cell bodies are located distally in the antennae and whose axons extend to form the antennal nerves and antennal lobes, b) antennal-lobe neurons, whose cell bodies are clustered entirely outside of the antennal lobe neuropil and whose dendrites form synapses with each other and with the terminal arborizations of ORN axons in the glomeruli, c) centrally-derived glial cells which populate the sorting zone (SZ glia) and which surround the glomeruli (NP glia), and d) peripheral glia (antennal nerve (AN) glia), which migrate toward the antennal lobes along the antennal nerves and extend processes that surround small groups of ORN axons [16]
Summary
The past decade has seen a growing appreciation of the importance of neuron-glia signaling in nervous system development, and glial cells have been shown to play numerous roles affecting axon outgrowth or growth arrest, course changes, fasciculation, and targeting [1,2,3,4,5,6,7,8,9,10]. Olfactory receptor neurons (ORNs) send their axons in the antennal nerve (AN) toward the nascent adult antennal lobe of the brain where the first axons to arrive induce a change in a subset of central glial cells, causing them to proliferate and migrate outward a short distance into the nerve (Fig. 1A). These glial cells define an axonal sorting zone (SZ); their presence induces subsequently arriving ORN axons to change course and fasciculate with other ORN axons with which they travel to a given region of the antennal lobe (AL) (Fig. 1B). Glial deficiency in the sorting zone causes defects in axon fasciculation and targeting [16]
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