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Lateral presynaptic inhibition mediates gain control in an olfactory circuit

Author

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  • Shawn R. Olsen

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

  • Rachel I. Wilson

    (Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA)

Abstract

Olfactory signals are transduced by a large family of odorant receptor proteins, each of which corresponds to a unique glomerulus in the first olfactory relay of the brain. Crosstalk between glomeruli has been proposed to be important in olfactory processing, but it is not clear how these interactions shape the odour responses of second-order neurons. In the Drosophila antennal lobe (a region analogous to the vertebrate olfactory bulb), we selectively removed most interglomerular input to genetically identified second-order olfactory neurons. Here we show that this broadens the odour tuning of these neurons, implying that interglomerular inhibition dominates over interglomerular excitation. The strength of this inhibitory signal scales with total feedforward input to the entire antennal lobe, and has similar tuning in different glomeruli. A substantial portion of this interglomerular inhibition acts at a presynaptic locus, and our results imply that this is mediated by both ionotropic and metabotropic receptors on the same nerve terminal.

Suggested Citation

  • Shawn R. Olsen & Rachel I. Wilson, 2008. "Lateral presynaptic inhibition mediates gain control in an olfactory circuit," Nature, Nature, vol. 452(7190), pages 956-960, April.
    • Handle: RePEc:nat:nature:v:452:y:2008:i:7190:d:10.1038_nature06864
    DOI: 10.1038/nature06864
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    Cited by:

    1. Inga Petelski & Yannick Günzel & Sercan Sayin & Susanne Kraus & Einat Couzin-Fuchs, 2024. "Synergistic olfactory processing for social plasticity in desert locusts," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Christian Keck & Cristina Savin & Jörg Lücke, 2012. "Feedforward Inhibition and Synaptic Scaling – Two Sides of the Same Coin?," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-15, March.
    3. Yilun Zhang & Tatyana O Sharpee, 2016. "A Robust Feedforward Model of the Olfactory System," PLOS Computational Biology, Public Library of Science, vol. 12(4), pages 1-15, April.
    4. Eyal Rozenfeld & Merav Tauber & Yair Ben-Chaim & Moshe Parnas, 2021. "GPCR voltage dependence controls neuronal plasticity and behavior," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Burak Gür & Luisa Ramirez & Jacqueline Cornean & Freya Thurn & Sebastian Molina-Obando & Giordano Ramos-Traslosheros & Marion Silies, 2024. "Neural pathways and computations that achieve stable contrast processing tuned to natural scenes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Tyler R. Sizemore & Julius Jonaitis & Andrew M. Dacks, 2023. "Heterogeneous receptor expression underlies non-uniform peptidergic modulation of olfaction in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    7. Jean-Pierre Rospars & Alexandre Grémiaux & David Jarriault & Antoine Chaffiol & Christelle Monsempes & Nina Deisig & Sylvia Anton & Philippe Lucas & Dominique Martinez, 2014. "Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-16, December.
    8. Mami Nakamizo-Dojo & Kenichi Ishii & Jiro Yoshino & Masato Tsuji & Kazuo Emoto, 2023. "Descending GABAergic pathway links brain sugar-sensing to peripheral nociceptive gating in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    9. Eyal Rozenfeld & Nadine Ehmann & Julia E. Manoim & Robert J. Kittel & Moshe Parnas, 2023. "Homeostatic synaptic plasticity rescues neural coding reliability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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