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Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb

Author

Listed:
  • Jane S. Huang

    (University of Pittsburgh)

  • Tenzin Kunkhyen

    (University of Pittsburgh)

  • Alexander N. Rangel

    (University of Pittsburgh)

  • Taryn R. Brechbill

    (University of Pittsburgh)

  • Jordan D. Gregory

    (University of Pittsburgh)

  • Emily D. Winson-Bushby

    (University of Pittsburgh)

  • Beichen Liu

    (University of Pittsburgh
    Carnegie Mellon University)

  • Jonathan T. Avon

    (University of Pittsburgh)

  • Ryan J. Muggleton

    (University of Pittsburgh
    Carnegie Mellon University)

  • Claire E. J. Cheetham

    (University of Pittsburgh
    Carnegie Mellon University)

Abstract

Postnatal neurogenesis provides an opportunity to understand how newborn neurons integrate into circuits to restore function. Newborn olfactory sensory neurons (OSNs) wire into highly organized olfactory bulb (OB) circuits throughout life, enabling lifelong plasticity and regeneration. Immature OSNs form functional synapses capable of evoking firing in OB projection neurons but what contribution, if any, they make to odor processing is unknown. Here, we show that immature OSNs provide odor input to the mouse OB, where they form monosynaptic connections with excitatory neurons. Importantly, immature OSNs respond as selectively to odorants as mature OSNs and exhibit graded responses across a wider range of odorant concentrations than mature OSNs, suggesting that immature and mature OSNs provide distinct odor input streams. Furthermore, mice can successfully perform odor detection and discrimination tasks using sensory input from immature OSNs alone. Together, our findings suggest that immature OSNs play a previously unappreciated role in olfactory-guided behavior.

Suggested Citation

  • Jane S. Huang & Tenzin Kunkhyen & Alexander N. Rangel & Taryn R. Brechbill & Jordan D. Gregory & Emily D. Winson-Bushby & Beichen Liu & Jonathan T. Avon & Ryan J. Muggleton & Claire E. J. Cheetham, 2022. "Immature olfactory sensory neurons provide behaviourally relevant sensory input to the olfactory bulb," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33967-6
    DOI: 10.1038/s41467-022-33967-6
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    References listed on IDEAS

    as
    1. Claire E. J. Cheetham & Una Park & Leonardo Belluscio, 2016. "Rapid and continuous activity-dependent plasticity of olfactory sensory input," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
    2. Jinsong Li & Tomohiro Ishii & Paul Feinstein & Peter Mombaerts, 2004. "Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons," Nature, Nature, vol. 428(6981), pages 393-399, March.
    3. Stuart Firestein, 2001. "How the olfactory system makes sense of scents," Nature, Nature, vol. 413(6852), pages 211-218, September.
    4. Ezequiel M. Arneodo & Kristina B. Penikis & Neil Rabinowitz & Angela Licata & Annika Cichy & Jingji Zhang & Thomas Bozza & Dmitry Rinberg, 2018. "Stimulus dependent diversity and stereotypy in the output of an olfactory functional unit," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
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