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

Author

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  • 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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
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