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

Author

Listed:
  • 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
    University of Lausanne
    Queen Mary University of London)

  • Lucia L. Prieto-Godino

    (University of Lausanne
    The Francis Crick Institute)

  • 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
    Harvard Medical School)

  • Floris Breugel

    (University of Nevada)

  • James M. Jeanne

    (Yale University)

  • Thomas O. Auer

    (University of Lausanne
    University of Fribourg)

  • Richard Benton

    (University of Lausanne)

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.

Suggested Citation

  • 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 Bre, 2024. "Olfactory sensory neuron population expansions influence projection neuron adaptation and enhance odour tracking," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50808-w
    DOI: 10.1038/s41467-024-50808-w
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    References listed on IDEAS

    as
    1. Juan Antonio Sánchez-Alcañiz & Giovanna Zappia & Frédéric Marion-Poll & Richard Benton, 2017. "A mechanosensory receptor required for food texture detection in Drosophila," Nature Communications, Nature, vol. 8(1), pages 1-9, April.
    2. Quentin Gaudry & Elizabeth J. Hong & Jamey Kain & Benjamin L. de Bivort & Rachel I. Wilson, 2013. "Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila," Nature, Nature, vol. 493(7432), pages 424-428, January.
    3. Kaitlyn Elizabeth Ellis & Sven Bervoets & Hayley Smihula & Ishani Ganguly & Eva Vigato & Thomas O. Auer & Richard Benton & Ashok Litwin-Kumar & Sophie Jeanne Cécile Caron, 2024. "Evolution of connectivity architecture in the Drosophila mushroom body," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Phing Chian Chai & Steeve Cruchet & Leonore Wigger & Richard Benton, 2019. "Sensory neuron lineage mapping and manipulation in the Drosophila olfactory system," Nature Communications, Nature, vol. 10(1), pages 1-17, December.
    5. Thomas O. Auer & Mohammed A. Khallaf & Ana F. Silbering & Giovanna Zappia & Kaitlyn Ellis & Raquel Álvarez-Ocaña & J. Roman Arguello & Bill S. Hansson & Gregory S. X. E. Jefferis & Sophie J. C. Caron , 2020. "Olfactory receptor and circuit evolution promote host specialization," Nature, Nature, vol. 579(7799), pages 402-408, March.
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