IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33967-6.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33967-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33967-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Stuart Firestein, 2001. "How the olfactory system makes sense of scents," Nature, Nature, vol. 413(6852), pages 211-218, September.
    2. 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.
    3. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Hao-Ching Jiang & Sung Jin Park & I-Hao Wang & Daniel M. Bear & Alexandra Nowlan & Paul L. Greer, 2024. "CD20/MS4A1 is a mammalian olfactory receptor expressed in a subset of olfactory sensory neurons that mediates innate avoidance of predators," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Agnes, Everton J. & Erichsen, Rubem & Brunnet, Leonardo G., 2012. "Model architecture for associative memory in a neural network of spiking neurons," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 391(3), pages 843-848.
    3. Carles Bosch & Tobias Ackels & Alexandra Pacureanu & Yuxin Zhang & Christopher J. Peddie & Manuel Berning & Norman Rzepka & Marie-Christine Zdora & Isabell Whiteley & Malte Storm & Anne Bonnin & Chris, 2022. "Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron microtomography and volume electron microscopy," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Anastasiia Gusach & Yang Lee & Armin Nikpour Khoshgrudi & Elizaveta Mukhaleva & Ning Ma & Eline J. Koers & Qingchao Chen & Patricia C. Edwards & Fanglu Huang & Jonathan Kim & Filippo Mancia & Dmitry B, 2024. "Molecular recognition of an odorant by the murine trace amine-associated receptor TAAR7f," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Marylène Rugard & Thomas Jaylet & Olivier Taboureau & Anne Tromelin & Karine Audouze, 2021. "Smell compounds classification using UMAP to increase knowledge of odors and molecular structures linkages," PLOS ONE, Public Library of Science, vol. 16(5), pages 1-17, May.
    6. Silva, Joaquim & Sá, Elisabete Sampaio & Escadas, Marco & Carvalho, Joana, 2021. "The influence of ambient scent on the passengers’ experience, emotions and behavioral intentions: An experimental study in a Public Bus service," Transport Policy, Elsevier, vol. 106(C), pages 88-98.
    7. Kevin W. Zhu & Shawn D. Burton & Maira H. Nagai & Justin D. Silverman & Claire A. March & Matt Wachowiak & Hiroaki Matsunami, 2022. "Decoding the olfactory map through targeted transcriptomics links murine olfactory receptors to glomeruli," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Chulwon Choi & Jungnam Bae & Seonghan Kim & Seho Lee & Hyunook Kang & Jinuk Kim & Injin Bang & Kiheon Kim & Won-Ki Huh & Chaok Seok & Hahnbeom Park & Wonpil Im & Hee-Jung Choi, 2023. "Understanding the molecular mechanisms of odorant binding and activation of the human OR52 family," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33967-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.