Olfactory sensory neuron population expansions influence projection neuron adaptation and enhance odour tracking

Suguru Takagi (), Gizem Sancer, Liliane Abuin, S. David Stupski, J. Roman Arguello, Lucia L. Prieto-Godino, David L. Stern, Steeve Cruchet, Raquel Álvarez-Ocaña, Carl F. R. Wienecke, Floris Breugel, James M. Jeanne, Thomas O. Auer () and Richard Benton ()
Additional contact information
Suguru Takagi: University of Lausanne
Gizem Sancer: Yale University
Liliane Abuin: University of Lausanne
S. David Stupski: University of Nevada
J. Roman Arguello: University of Lausanne
Lucia L. Prieto-Godino: University of Lausanne
David L. Stern: Janelia Research Campus of the Howard Hughes Medical Institute
Steeve Cruchet: University of Lausanne
Raquel Álvarez-Ocaña: University of Lausanne
Carl F. R. Wienecke: Stanford University
Floris Breugel: University of Nevada
James M. Jeanne: Yale University
Thomas O. Auer: University of Lausanne
Richard Benton: University of Lausanne

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: 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 olfactory 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 number increases contribute to stronger, more persistent, noni-odour tracking behaviour. These expansions result in increased synaptic connections of sensory neurons with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odour-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 population expansions to explain ecologically-relevant, species-specific behaviour.

Date: 2024
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DOI: 10.1038/s41467-024-50808-w

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