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Myelination of parvalbumin interneurons shapes the function of cortical sensory inhibitory circuits

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  • Najate Benamer

    (Université de Paris, Institute of Psychiatry and Neuroscience of Paris (IPNP), INSERM U1266, “Team Interactions between neurons and oligodendroglia in myelination and myelin repair”)

  • Marie Vidal

    (Université de Paris, Institute of Psychiatry and Neuroscience of Paris (IPNP), INSERM U1266, “Team Interactions between neurons and oligodendroglia in myelination and myelin repair”)

  • Maddalena Balia

    (Université de Paris, Institute of Psychiatry and Neuroscience of Paris (IPNP), INSERM U1266, “Team Interactions between neurons and oligodendroglia in myelination and myelin repair”
    Institut des Maladies Neurodégénératives, CNRS UMR 5293, Université de Bordeaux, Centre Broca Nouvelle-Aquitaine)

  • María Cecilia Angulo

    (Université de Paris, Institute of Psychiatry and Neuroscience of Paris (IPNP), INSERM U1266, “Team Interactions between neurons and oligodendroglia in myelination and myelin repair”
    GHU PARIS psychiatrie & neurosciences)

Abstract

Myelination of projection neurons by oligodendrocytes is key to optimize action potential conduction over long distances. However, a large fraction of myelin enwraps the axons of parvalbumin-positive fast-spiking interneurons (FSI), exclusively involved in local cortical circuits. Whether FSI myelination contributes to the fine‐tuning of intracortical networks is unknown. Here we demonstrate that FSI myelination is required for the establishment and maintenance of the powerful FSI-mediated feedforward inhibition of cortical sensory circuits. The disruption of GABAergic synaptic signaling of oligodendrocyte precursor cells prior to myelination onset resulted in severe FSI myelination defects characterized by longer internodes and nodes, aberrant myelination of branch points and proximal axon malformation. Consequently, high-frequency FSI discharges as well as FSI-dependent postsynaptic latencies and strengths of excitatory neurons were reduced. These dysfunctions generated a strong excitation-inhibition imbalance that correlated with whisker-dependent texture discrimination impairments. FSI myelination is therefore critical for the function of mature cortical inhibitory circuits.

Suggested Citation

  • Najate Benamer & Marie Vidal & Maddalena Balia & María Cecilia Angulo, 2020. "Myelination of parvalbumin interneurons shapes the function of cortical sensory inhibitory circuits," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18984-7
    DOI: 10.1038/s41467-020-18984-7
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    Cited by:

    1. Li-Pao Fang & Na Zhao & Laura C. Caudal & Hsin-Fang Chang & Renping Zhao & Ching-Hsin Lin & Nadine Hainz & Carola Meier & Bernhard Bettler & Wenhui Huang & Anja Scheller & Frank Kirchhoff & Xianshu Ba, 2022. "Impaired bidirectional communication between interneurons and oligodendrocyte precursor cells affects social cognitive behavior," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Koen Kole & Bas J. B. Voesenek & Maria E. Brinia & Naomi Petersen & Maarten H. P. Kole, 2022. "Parvalbumin basket cell myelination accumulates axonal mitochondria to internodes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Prateek Kumar & Annie M. Goettemoeller & Claudia Espinosa-Garcia & Brendan R. Tobin & Ali Tfaily & Ruth S. Nelson & Aditya Natu & Eric B. Dammer & Juliet V. Santiago & Sneha Malepati & Lihong Cheng & , 2024. "Native-state proteomics of Parvalbumin interneurons identifies unique molecular signatures and vulnerabilities to early Alzheimer’s pathology," Nature Communications, Nature, vol. 15(1), pages 1-26, December.

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