The role of the brain in metamorphosis of the olfactory epithelium in the frog, Xenopus laevis

Abstract

Retrograde signaling from the brain to the olfactory sensory epithelium is important for neuronal survival, but the importance of the olfactory bulb in retrograde signaling during the naturally-induced, neuronal plasticity occurring during metamorphosis is unclear. The olfactory system of the African clawed frog ( Xenopus laevis) undergoes dramatic rearrangements during metamorphosis, making this an ideal system in which to examine interactions between the brain and the olfactory sensory epithelium. The main olfactory epithelium of larvae, located in the principal cavity (PC), changes at metamorphosis in function, receptor neuron morphology, biochemistry, and axon termination sites. A new, “middle”, cavity forms during metamorphosis that assumes all the characteristics of the larval PC. Using a combination of bulbectomy and olfactory transplantation, we investigated changes in expression of a marker protein (E7) and in apical ultrastructure in olfactory receptor neurons either (1) connected to the olfactory bulb, (2) connected to non-olfactory brain regions, or (3) with no apparent central nervous system (CNS) connections. We find that neurons in the middle cavity (MC) lacking connections with the CNS appear mature but neurons in the PC do not. Supporting cells in the PC undergo the changes normally observed during metamorphosis. Neurons connected to non-olfactory brain regions, either after bulbectomy or transplantation, appeared normal with regard to the changes normally expected after metamorphosis. These results suggest that influence from the brain is necessary for metamorphic changes in the X. laevis olfactory epithelium, but that these signals are not confined to the olfactory bulb; non-olfactory brain regions can also support these metamorphic changes.