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[Preprint]. 2024 Feb 28:2023.09.15.556782. Originally published 2023 Sep 15. [Version 3] doi: 10.1101/2023.09.15.556782

Sensory neuron population expansion enhances odor tracking without sensitizing projection neurons

Suguru Takagi, Gizem Sancer, Liliane Abuin, S David Stupski, J Roman Arguello, Lucia L Prieto-Godino, David L Stern, Steeve Cruchet, Raquel Alvarez-Ocana, Carl F R Wienecke, Floris van Breugel, James M Jeanne, Thomas O Auer, Richard Benton
PMCID: PMC10515935  PMID: 37745467

Abstract

The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous neural pathways of Drosophila melanogaster and its close relative Drosophila sechellia , an extreme specialist for Morinda citrifolia noni fruit. D. sechellia has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN population increases contribute to stronger, more persistent, noni-odor tracking behavior. These sensory neuron expansions result in increased synaptic connections with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odor-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron expansions to explain ecologically-relevant, species-specific behavior.

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