Abstract
Individual receptor neurons in the peripheral olfactory organ extend long axons into the olfactory bulb forming synapses with projection neurons in spherical neuropil regions, called glomeruli. Generally, odor map formation and odor processing in all vertebrates is based on the assumption that receptor neuron axons exclusively connect to a single glomerulus without any axonal branching. We comparatively tested this hypothesis in multiple fish and amphibian species (both sexes) by applying sparse cell electroporation to trace single olfactory receptor neuron axons. Sea lamprey (jawless fish) and zebrafish (bony fish) support the unbranched axon concept, with 94% of axons terminating in single glomeruli. Contrastingly, axonal projections of the axolotl (salamander) branch extensively before entering up to six distinct glomeruli. Receptor neuron axons labeled in frog species (Pipidae, Bufonidae, Hylidae, and Dendrobatidae) predominantly bifurcate before entering a glomerulus and 59 and 50% connect to multiple glomeruli in larval and postmetamorphotic animals, respectively. Independent of developmental stage, lifestyle, and adaptations to specific habitats, it seems to be a common feature of amphibian olfactory receptor neuron axons to frequently bifurcate and connect to multiple glomeruli. Our study challenges the unbranched axon concept as a universal vertebrate feature and it is conceivable that also later diverging vertebrates deviate from it. We propose that this unusual wiring logic evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and could be the basis of an alternative way of odor processing.
Highlights
Vertebrates are equipped with a sophisticated olfactory system to detect relevant chemical information about their environment
Axonal tracings obtained from the tadpoles of the clawed frog (23 ± 8.1, n = 10) showed a significantly higher degree of branching when compared to the zebrafish (p = 0.0013)
The collected data indicates that olfactory receptor neurons (ORNs) axonal projections in larval and juvenile amphibians are much more heterogeneous than what has been reported in rodents and what we found in fishes
Summary
Vertebrates are equipped with a sophisticated olfactory system to detect relevant chemical information about their environment. The majority of examined axons were shown to be connecting to more than one glomerulus in larval animals [26] and this alternative pattern was retained after metamorphosis [27] It remains elusive whether this multi-glomerular wiring is a specific adaptation of the secondarily aquatic Xenopus or if it is a more conserved evolutionary feature present in other vertebrate lineages. We could show that multi-glomerular innervation of single ORN axons are the predominant pattern in the axolotl salamander, which suggests that this feature might be present in all amphibians Both the main olfactory system of the sea lamprey (jawless fish) as well as the olfactory system of zebrafish (teleost fish) follow the unbranched ORN axon paradigm with a single ORN axon only arborizing within the confines of a single glomerulus. We propose that the unusual wiring logic found in amphibians evolved around the divergence of the terrestrial tetrapod lineage from its aquatic ancestors and forms the basis of an alternative way of odor processing
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