Abstract
Understanding the mechanisms involved in maintaining lifelong neurogenesis has a clear biological and clinical interest. In the present study, we performed olfactory nerve transection on larval Xenopus to induce severe damage to the olfactory circuitry. We surveyed the timing of the degeneration, subsequent rewiring and functional regeneration of the olfactory system following injury. A range of structural labeling techniques and functional calcium imaging were performed on both tissue slices and whole brain preparations. Cell death of olfactory receptor neurons and proliferation of stem cells in the olfactory epithelium were immediately increased following lesion. New olfactory receptor neurons repopulated the olfactory epithelium and once again showed functional responses to natural odorants within 1 week after transection. Reinnervation of the olfactory bulb (OB) by newly formed olfactory receptor neuron axons also began at this time. Additionally, we observed a temporary increase in cell death in the OB and a subsequent loss in OB volume. Mitral/tufted cells, the second order neurons of the olfactory system, largely survived, but transiently lost dendritic tuft complexity. The first odorant-induced responses in the OB were observed 3 weeks after nerve transection and the olfactory network showed signs of major recovery, both structurally and functionally, after 7 weeks.
Highlights
While many mammalian species appear to have lost regenerative capacity of neuronal tissue during evolution, early diverging vertebrates exhibit elevated neuroregenerative potential and have been shown to be capable of restoring entire brain regions after lesion
We show that olfactory nerves (ONs) transection targets Olfactory receptor neurons (ORNs) for cell death, leaving other components of this system involved in the process of regeneration largely unperturbed
To observe structural changes occurring in the main olfactory epithelium (MOE) after bilateral ON transection, we visualized major cell populations of the MOE, namely supporting cells (SCs), proliferative basal cells (BCs) and ORNs
Summary
While many mammalian species appear to have lost regenerative capacity of neuronal tissue during evolution, early diverging vertebrates exhibit elevated neuroregenerative potential and have been shown to be capable of restoring entire brain regions after lesion (for review Ferretti, 2011). This ability is variable among species and has a strong developmental component. The stem cell population located in the subventricular zone is mainly responsible for supplying the OB with new interneurons (Lim and Alvarez-Buylla, 2016), which has been shown to be essential in adjusting olfactory performance (Mouret et al, 2009)
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