Cited by 80Neurobiology and Insect Physiology ResearchOlfactory and Sensory Function StudiesInsect Pheromone Research and Control

Generating parallel representations of position and identity in the olfactory system

Open access
Taisz, István, Donà, Erika, Münch, Daniel, Bailey, Shanice N., Morris, Billy J., Meechan, Kimberly I., Stevens, Katie M., Varela-Martínez, Irene +5 more·2023·Cell

Published version of a preprint

Abstract

In Drosophila , a dedicated olfactory channel senses a male pheromone, cis -vaccenyl acetate (cVA), promoting female courtship while repelling males. Here, we show that separate cVA-processing streams extract qualitative and positional information. cVA sensory neurons respond to concentration differences in a 5-mm range around a male. Second-order projection neurons encode the angular position of a male by detecting inter-antennal differences in cVA concentration, which are amplified through contralateral inhibition. At the third circuit layer, we identify 47 cell types with diverse input-output connectivity. One population responds tonically to male flies, a second is tuned to olfactory looming, while a third integrates cVA and taste to coincidentally promote female mating. The separation of olfactory features resembles the mammalian what and where visual streams; together with multisensory integration, this enables behavioral responses appropriate to specific ethological contexts.

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Crossref · 10.1016/j.cell.2023.04.038

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  • GRNs respond to specific taste categories, such as appetitive sugar or aversive bitter compounds, resulting in acceptance or avoidance.

    “GRNs respond to specific taste categories, such as appetitive sugar or aversive bitter compounds, resulting in acceptance (that is, proboscis extension and feeding) or avoidance, respectively24,33,35,38.”

    From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [38]

    The Results section (“Integrating cVA and taste is key to controlling female receptivity”; page unavailable) reports that Ir94e GRNs respond to particular stimuli, especially compounds on male genitals. It does not address sugar or bitter responses, or link those taste categories to feeding acceptance or avoidance; its behavioral finding concerns female receptivity. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • Ir94e neurons respond to salt and the presentation of male genitals, but the exact tastants Ir94e neurons respond to are not well understood.

    “Ir94e neurons respond to salt and the presentation of male genitals, but the exact tastants Ir94e neurons respond to are not well understood31,33,37,38.”
  • Ir94e GRNs in virgin females respond to the presentation of male genitals.

    “Ir94e GRNs in virgin females have been shown to respond to the presentation of male genitals38.”
  • MuJoCo is known for better stability and performance.

    “We changed the underlying physics engine because (i) MuJoCo is known for better stability and performance 46 ,”

    From NeuroMechFly v2: simulating embodied sensorimotor control in adult Drosophila (2024) · cites this paper as [46]

    The Key resources table and Method details (page numbers unavailable in our copy) describe software for fly tracking, imaging, and analysis, but do not address MuJoCo. Searches for MuJoCo and for physics-engine stability and performance found no passage supporting the cited claim. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

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Authors
Taisz, I., Donà, E., Münch, D., Bailey, S. N., Morris, B. J., Meechan, K. I., Stevens, K. M., Varela-Martínez, I., Gkantia, M., Schlegel, P., Ribeiro, C., Jefferis, G. S. X. E., & Galili, D. S.
Affiliations
  • MRC Laboratory of Molecular Biology (GB)
  • Champalimaud Foundation (PT)
  • University of Cambridge (GB)
Corresponding author
  • Jefferis, Gregory S.X.E.
  • Galili, Dana S.
Venue
Cell
Publisher
Elsevier BV
Published
2023-06
Volume
186
Issue
12
Pages
2556-2573.e22
ISSN
0092-8674 (ISSN-L)
OpenAlex
W4378213119
Cited by
79
References
130
Citations by year
2026: 14 · 2025: 27 · 2024: 21 · 2023: 13 · 2022: 4
FWCI
9.09
Type
journal article
Language
en
Open access
Locations
  • Cell (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • SSRN Electronic Journal (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Wellcome Trust (110232, 203261, 110232/Z/15/Z, /Z/15/Z, 649111, 203261/Z/16/Z)
  • UK Research and Innovation
  • Fundação Champalimaud
  • Horizon 2020 Framework Programme (H2020-IF-748478, 649111)
  • Medical Research Council (MC-U105188491, U105188491)
  • Fundação para a Ciência e a Tecnologia (PTDC/MED-NEU/4001/2021, H2020)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect Pheromone Research and Control
Keywords
cis-vaccenyl acetate, male pheromones, Drosophila olfactory system, positional information, identity information, contralateral inhibition, projection neurons, multisensory integration
MeSH terms
Acetates, Animals, Drosophila, Drosophila melanogaster, Female, Male, Mammals, Oleic Acids, Pheromones, Sexual Behavior, Animal, Smell, Receptors, Odorant, Drosophila Proteins

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