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Long-range GABAergic projections contribute to cortical feedback control of sensory processing

Author

Listed:
  • Camille Mazo

    (Institut Pasteur, Université Paris Cité, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, Perception and Memory Unit
    Champalimaud Foundation)

  • Antoine Nissant

    (Institut Pasteur, Université Paris Cité, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, Perception and Memory Unit)

  • Soham Saha

    (Institut Pasteur, Université Paris Cité, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, Perception and Memory Unit)

  • Enzo Peroni

    (Institut Pasteur, Université Paris Cité, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, Perception and Memory Unit)

  • Pierre-Marie Lledo

    (Institut Pasteur, Université Paris Cité, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, Perception and Memory Unit)

  • Gabriel Lepousez

    (Institut Pasteur, Université Paris Cité, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, Perception and Memory Unit)

Abstract

In the olfactory system, the olfactory cortex sends glutamatergic projections back to the first stage of olfactory processing, the olfactory bulb (OB). Such corticofugal excitatory circuits — a canonical circuit motif described in all sensory systems— dynamically adjust early sensory processing. Here, we uncover a corticofugal inhibitory feedback to OB, originating from a subpopulation of GABAergic neurons in the anterior olfactory cortex and innervating both local and output OB neurons. In vivo imaging and network modeling showed that optogenetic activation of cortical GABAergic projections drives a net subtractive inhibition of both spontaneous and odor-evoked activity in local as well as output neurons. In output neurons, stimulation of cortical GABAergic feedback enhances separation of population odor responses in tufted cells, but not mitral cells. Targeted pharmacogenetic silencing of cortical GABAergic axon terminals impaired discrimination of similar odor mixtures. Thus, corticofugal GABAergic projections represent an additional circuit motif in cortical feedback control of sensory processing.

Suggested Citation

  • Camille Mazo & Antoine Nissant & Soham Saha & Enzo Peroni & Pierre-Marie Lledo & Gabriel Lepousez, 2022. "Long-range GABAergic projections contribute to cortical feedback control of sensory processing," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34513-0
    DOI: 10.1038/s41467-022-34513-0
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    References listed on IDEAS

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    1. Matthew Smear & Roman Shusterman & Rodney O’Connor & Thomas Bozza & Dmitry Rinberg, 2011. "Perception of sniff phase in mouse olfaction," Nature, Nature, vol. 479(7373), pages 397-400, November.
    2. Assunta Diodato & Marion Ruinart de Brimont & Yeong Shin Yim & Nicolas Derian & Sandrine Perrin & Juliette Pouch & David Klatzmann & Sonia Garel & Gloria B Choi & Alexander Fleischmann, 2016. "Molecular signatures of neural connectivity in the olfactory cortex," Nature Communications, Nature, vol. 7(1), pages 1-10, November.
    3. Olivier Gschwend & Jonathan Beroud & Alan Carleton, 2012. "Encoding Odorant Identity by Spiking Packets of Rate-Invariant Neurons in Awake Mice," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-12, January.
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