A diffusible signal attracts olfactory sensory axons toward their target in the developing brain of the moth

Abstract

The signals that olfactory receptor axons use to navigate to their target in the CNS are still not well understood. In the moth Manduca sexta, the primary olfactory pathway develops postembryonically, and the receptor axons navigate from an experimentally accessible sensory epithelium to the brain along a pathway long enough for detailed study of regions in which axon behavior changes. The current experiments ask whether diffusible factors contribute to receptor axon guidance. Explants were made from the antennal receptor epithelium and co-cultured in a collagen gel matrix with slices of various regions of the brain. Receptor axons were attracted toward the central regions of the brain, including the protocerebrum and antennal lobe. Receptor axons growing into a slice of the most proximal region of the antennal nerve, where axon sorting normally occurs, showed no directional preference. When the antennal lobe was included in the slice, the receptor axons entering the sorting region grew directly toward the antennal lobe. Taken together with the previous in vivo experiments, the current results suggest that an attractive diffusible factor can serve as one cue to direct misrouted olfactory receptor axons toward the medial regions of the brain, where local cues guide them to the antennal lobe. They also suggest that under normal circumstances, in which the receptor axons follow a pre-existing pupal nerve to the antennal lobe, the diffusible factor emanating from the lobe acts in parallel and at short range to maintain the fidelity of the path into the antennal lobe.

Development of A-type allatostatin immunoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta

“…These released neuropeptides could provide a diffusible signal for the incoming ORN axons to find the AL and then to explore their way around the AL neuropil finally targeting their specific glomerular template sites. Diffusible signals of unknown identity released from the AL may attract ORN axons toward the forming AL, as has been described recently in a study using a combination of AL slices and cocultured ORNs (Oland et al 2003). Similarly, long-term culture studies with mouse olfactory explants have suggested the presence of a diffusible signal from the olfactory bulb; this might attract ORNs and thus act as a neurotropic factor (Goetze et al 2002).…”

Morphological and functional plasticity of olfactory ensheathing cells

“…The guidance mechanisms controlling OEC migration to the presumptive olfactory bulb during development are ultimately responsible for the directional guidance of the pioneer axons and subsequent establishment of the olfactory nerve tracts (Key & St John, 2002). This migration may be mediated by a bulbderived chemoattractant (Liu et al, 1995), similar to that required by olfactory axons in the moth, Manduca sexta (Oland et al, 2003). The same or related factors may be responsible in rats for attracting neuronal precursors from the subventricular zone to their olfactory destinations (Liu & Rao, 2003).…”

Target tissue influences the peripheral trajectory of mouse primary sensory olfactory axons

“…Both Goetze et al (2002) and Oland et al (2003) have recently observed directed growth from explants of isolated olfactory neuroepithelium that were cocultured with explants or slices of the target tissue, suggesting that the target tissue produces a soluble factor to attract the growing axons. Whether the target tissue influences the growth and guidance of primary olfactory axons as they navigate within the native extracellular environment of the nasal septum was unknown.…”

“…Apart from these molecules we still do not understand how axons follow discrete peripheral trajectories to reach the olfactory bulb. Recent in vitro studies examining the behavior of primary olfactory axon outgrowth suggest that the target tissue provides an attractive cue for these growing axons, in both the mouse and moth olfactory systems (Goetze et al, 2002;Oland et al, 2003). How does the olfactory bulb influence the peripheral trajectory of growing olfactory axons in vivo?…”