IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38475-9.html
   My bibliography  Save this article

Glutamatergic cerebellar neurons differentially contribute to the acquisition of motor and social behaviors

Author

Listed:
  • Meike E. Heijden

    (Baylor College of Medicine
    Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital)

  • Alejandro G. Rey Hipolito

    (Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital
    Baylor College of Medicine)

  • Linda H. Kim

    (Baylor College of Medicine
    Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital)

  • Dominic J. Kizek

    (Baylor College of Medicine
    Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital)

  • Ross M. Perez

    (Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital
    Baylor College of Medicine)

  • Tao Lin

    (Baylor College of Medicine
    Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital)

  • Roy V. Sillitoe

    (Baylor College of Medicine
    Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital
    Baylor College of Medicine
    Baylor College of Medicine)

Abstract

Insults to the developing cerebellum can cause motor, language, and social deficits. Here, we investigate whether developmental insults to different cerebellar neurons constrain the ability to acquire cerebellar-dependent behaviors. We perturb cerebellar cortical or nuclei neuron function by eliminating glutamatergic neurotransmission during development, and then we measure motor and social behaviors in early postnatal and adult mice. Altering cortical and nuclei neurons impacts postnatal motor control and social vocalizations. Normalizing neurotransmission in cortical neurons but not nuclei neurons restores social behaviors while the motor deficits remain impaired in adults. In contrast, manipulating only a subset of nuclei neurons leaves social behaviors intact but leads to early motor deficits that are restored by adulthood. Our data uncover that glutamatergic neurotransmission from cerebellar cortical and nuclei neurons differentially control the acquisition of motor and social behaviors, and that the brain can compensate for some but not all perturbations to the developing cerebellum.

Suggested Citation

  • Meike E. Heijden & Alejandro G. Rey Hipolito & Linda H. Kim & Dominic J. Kizek & Ross M. Perez & Tao Lin & Roy V. Sillitoe, 2023. "Glutamatergic cerebellar neurons differentially contribute to the acquisition of motor and social behaviors," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38475-9
    DOI: 10.1038/s41467-023-38475-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38475-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38475-9?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. Saša Peter & Michiel M. ten Brinke & Jeffrey Stedehouder & Claudia M. Reinelt & Bin Wu & Haibo Zhou & Kuikui Zhou & Henk-Jan Boele & Steven A. Kushner & Min Goo Lee & Michael J. Schmeisser & Tobias M., 2016. "Dysfunctional cerebellar Purkinje cells contribute to autism-like behaviour in Shank2-deficient mice," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    2. Nissim Ben-Arie & Hugo J. Bellen & Dawna L. Armstrong & Alanna E. McCall & Polina R. Gordadze & Qiuxia Guo & Martin M. Matzuk & Huda Y. Zoghbi, 1997. "Math1 is essential for genesis of cerebellar granule neurons," Nature, Nature, vol. 390(6656), pages 169-172, November.
    3. Lauren N. Miterko & Tao Lin & Joy Zhou & Meike E. Heijden & Jaclyn Beckinghausen & Joshua J. White & Roy V. Sillitoe, 2021. "Neuromodulation of the cerebellum rescues movement in a mouse model of ataxia," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Joshua J. White & Roy V. Sillitoe, 2017. "Genetic silencing of olivocerebellar synapses causes dystonia-like behaviour in mice," Nature Communications, Nature, vol. 8(1), pages 1-16, April.
    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. Bérénice Coutant & Jimena Laura Frontera & Elodie Perrin & Adèle Combes & Thibault Tarpin & Fabien Menardy & Caroline Mailhes-Hamon & Sylvie Perez & Bertrand Degos & Laurent Venance & Clément Léna & D, 2022. "Cerebellar stimulation prevents Levodopa-induced dyskinesia in mice and normalizes activity in a motor network," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Nadine Schroeder & Manuela Wuelling & Daniel Hoffmann & Beate Brand-Saberi & Andrea Vortkamp, 2019. "Atoh8 acts as a regulator of chondrocyte proliferation and differentiation in endochondral bones," PLOS ONE, Public Library of Science, vol. 14(8), pages 1-22, August.

    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:14:y:2023:i:1:d:10.1038_s41467-023-38475-9. 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.