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Impaired bidirectional communication between interneurons and oligodendrocyte precursor cells affects social cognitive behavior

Author

Listed:
  • Li-Pao Fang

    (University of Saarland)

  • Na Zhao

    (University of Saarland)

  • Laura C. Caudal

    (University of Saarland)

  • Hsin-Fang Chang

    (University of Saarland)

  • Renping Zhao

    (University of Saarland)

  • Ching-Hsin Lin

    (University of Saarland)

  • Nadine Hainz

    (University of Saarland)

  • Carola Meier

    (University of Saarland)

  • Bernhard Bettler

    (University of Basel)

  • Wenhui Huang

    (University of Saarland)

  • Anja Scheller

    (University of Saarland)

  • Frank Kirchhoff

    (University of Saarland
    University of Medicine and Pharmacy of Craiova)

  • Xianshu Bai

    (University of Saarland)

Abstract

Cortical neural circuits are complex but very precise networks of balanced excitation and inhibition. Yet, the molecular and cellular mechanisms that form the balance are just beginning to emerge. Here, using conditional γ-aminobutyric acid receptor B1- deficient mice we identify a γ-aminobutyric acid/tumor necrosis factor superfamily member 12-mediated bidirectional communication pathway between parvalbumin-positive fast spiking interneurons and oligodendrocyte precursor cells that determines the density and function of interneurons in the developing medial prefrontal cortex. Interruption of the GABAergic signaling to oligodendrocyte precursor cells results in reduced myelination and hypoactivity of interneurons, strong changes of cortical network activities and impaired social cognitive behavior. In conclusion, glial transmitter receptors are pivotal elements in finetuning distinct brain functions.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29020-1
    DOI: 10.1038/s41467-022-29020-1
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    References listed on IDEAS

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    1. Fong Kuan Wong & Kinga Bercsenyi & Varun Sreenivasan & Adrián Portalés & Marian Fernández-Otero & Oscar Marín, 2018. "Pyramidal cell regulation of interneuron survival sculpts cortical networks," Nature, Nature, vol. 557(7707), pages 668-673, May.
    2. 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.
    3. Derek G. Southwell & Mercedes F. Paredes & Rui P. Galvao & Daniel L. Jones & Robert C. Froemke & Joy Y. Sebe & Clara Alfaro-Cervello & Yunshuo Tang & Jose M. Garcia-Verdugo & John L. Rubenstein & Scot, 2012. "Intrinsically determined cell death of developing cortical interneurons," Nature, Nature, vol. 491(7422), pages 109-113, November.
    4. Dorien A. Maas & Vivian D. Eijsink & Marcia Spoelder & Josephus A. Hulten & Peter Weerd & Judith R. Homberg & Astrid Vallès & Brahim Nait-Oumesmar & Gerard J. M. Martens, 2020. "Interneuron hypomyelination is associated with cognitive inflexibility in a rat model of schizophrenia," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    5. David Orduz & Najate Benamer & Domiziana Ortolani & Eva Coppola & Lisa Vigier & Alessandra Pierani & María Cecilia Angulo, 2019. "Developmental cell death regulates lineage-related interneuron-oligodendroglia functional clusters and oligodendrocyte homeostasis," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    6. Stanislaw Mitew & Ilan Gobius & Laura R. Fenlon & Stuart J. McDougall & David Hawkes & Yao Lulu Xing & Helena Bujalka & Andrew L. Gundlach & Linda J. Richards & Trevor J. Kilpatrick & Tobias D. Merson, 2018. "Pharmacogenetic stimulation of neuronal activity increases myelination in an axon-specific manner," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    7. Balint Nagy & Anahit Hovhannisyan & Ruxandra Barzan & Ting-Jiun Chen & Maria Kukley, 2017. "Different patterns of neuronal activity trigger distinct responses of oligodendrocyte precursor cells in the corpus callosum," PLOS Biology, Public Library of Science, vol. 15(8), pages 1-32, August.
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    Cited by:

    1. Qilin Guo & Davide Gobbo & Na Zhao & Hong Zhang & Nana-Oye Awuku & Qing Liu & Li-Pao Fang & Tanja M. Gampfer & Markus R. Meyer & Renping Zhao & Xianshu Bai & Shan Bian & Anja Scheller & Frank Kirchhof, 2024. "Adenosine triggers early astrocyte reactivity that provokes microglial responses and drives the pathogenesis of sepsis-associated encephalopathy in mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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