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Understanding morphological, molecular, and functional adaptations of the amphibian olfactory system demanded by transition from aquatic to terrestrial habitats

Subject Area Cognitive, Systems and Behavioural Neurobiology
Molecular Biology and Physiology of Neurons and Glial Cells
Term from 2018 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 356132378
 
Final Report Year 2024

Final Report Abstract

The Xenopus olfactory system exhibits several interesting structural, molecular, and functional peculiarities compared to the mammalian olfactory system. It is unknown whether these features are common to all amphibian species. Also, it is still elusive which adaptations of the olfactory system are beneficial for a successful transition from an aquatic to a terrestrial habitat. Here, we set out to investigate the olfactory system of other amphibian species with lifestyles different from Xenopus. Furthermore, we continued to study the olfactory system of Xenopus. We found that, as in Xenopus laevis, axonal projections of olfactory receptor neurons of the axolotl (Caudata; Ambystoma mexicanum) and all investigated larval frog species (Pipidae: Xenopus tropicalis; Bufonidae: Rhinella arenarum; Hylidae: Scinax granulatus; Dendrobatidae: Ranitomeya imitator) predominantly bifurcate before entering a glomerulus and connect to multiple glomeruli. Bifurcating olfactory receptor neuron axons have also been observed in juveniles of the terrestrial Rhinella arenarum and the arboreal Scinax granulatus. Our results show that bifurcating receptor neuron axons are a common feature of amphibians, independent of developmental stage, lifestyle, and adaptations to specific habitats. These results challenge the unbranched axon concept as a universal vertebrate feature. We found that S100Z, a calcium-binding protein, is exclusively associated with the main olfactory system in Xenopus laevis and not with the vomeronasal organ as in mammals. We also found that glomerular clustering in the olfactory bulb is remarkably conserved in all investigated species. Some minor differences between the glomerular clusters in different species could reflect adaptation to specific ecological niches. We thoroughly investigated the morphology of projection neurons of the olfactory bulb of larval Xenopus laevis. We found that projection neurons in the dorsal postmetamorphic olfactory bulb regularly connect to multiple glomeruli, while at least half of the projection neurons in the postmetamorphic ventral olfactory bulb, similarly as in the olfactory bulb of premetamorphic animals, connect to only one glomerulus. This result suggests that different coding strategies are necessary for waterborne and airborne odorant detection. We investigated the impact of the unusual wiring in the olfactory system of larval Xenopus laevis on glomerular module organization and odor representations in the olfactory bulb network. We found that the glomerular odor map to amino acids is neither stereotypic between animals nor chemotopically organized. This is an unexpected finding whose functional significance is still unknown. Finally, we developed behavioral assays to test the behavioral relevance of odorants in amphibian larvae. We found that attractive behavior elicited by amino acid odorants persists throughout the metamorphosis of Xenopus. Also, we found that this attractive behavior is reestablished after transection and regeneration of the olfactory nerves in larval Xenopus. Despite the several problems that we experienced during this project (funding from the Argentinian agency; global Covid-19 pandemic), we obtained excellent results and, without a doubt, gained valuable results that contribute to a better understanding of the anatomy, morphology, and function of the olfactory system of amphibians.

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