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Excitatory synapses and gap junctions cooperate to improve Pv neuronal burst firing and cortical social cognition in Shank2-mutant mice

Author

Listed:
  • Eunee Lee

    (Institute for Basic Science (IBS)
    Yonsei University)

  • Seungjoon Lee

    (Department of Biological Sciences, KAIST)

  • Jae Jin Shin

    (Seoul National University
    Institute for Basic Science (IBS))

  • Woochul Choi

    (Korea Advanced Institute for Science and Technology (KAIST))

  • Changuk Chung

    (Institute for Basic Science (IBS))

  • Suho Lee

    (Department of Biological Sciences, KAIST)

  • Jihye Kim

    (Institute for Basic Science (IBS))

  • Seungmin Ha

    (Institute for Basic Science (IBS))

  • Ryunhee Kim

    (Institute for Basic Science (IBS))

  • Taesun Yoo

    (Institute for Basic Science (IBS))

  • Ye-Eun Yoo

    (Department of Biological Sciences, KAIST)

  • Jisoo Kim

    (Department of Biological Sciences, KAIST)

  • Young Woo Noh

    (Department of Biological Sciences, KAIST)

  • Issac Rhim

    (Institute for Basic Science (IBS))

  • Soo Yeon Lee

    (Department of Biological Sciences, KAIST)

  • Woohyun Kim

    (Department of Biological Sciences, KAIST)

  • Taekyung Lee

    (Institute for Basic Science (IBS))

  • Hyogeun Shin

    (Korea Institute of Science and Technology (KIST))

  • Il-Joo Cho

    (Korea Institute of Science and Technology (KIST))

  • Karl Deisseroth

    (Stanford University)

  • Sang Jeong Kim

    (Seoul National University)

  • Joo Min Park

    (Institute for Basic Science (IBS))

  • Min Whan Jung

    (Institute for Basic Science (IBS)
    Department of Biological Sciences, KAIST)

  • Se-Bum Paik

    (Korea Advanced Institute for Science and Technology (KAIST))

  • Eunjoon Kim

    (Institute for Basic Science (IBS)
    Department of Biological Sciences, KAIST)

Abstract

NMDA receptor (NMDAR) and GABA neuronal dysfunctions are observed in animal models of autism spectrum disorders, but how these dysfunctions impair social cognition and behavior remains unclear. We report here that NMDARs in cortical parvalbumin (Pv)-positive interneurons cooperate with gap junctions to promote high-frequency (>80 Hz) Pv neuronal burst firing and social cognition. Shank2–/– mice, displaying improved sociability upon NMDAR activation, show impaired cortical social representation and inhibitory neuronal burst firing. Cortical Shank2–/– Pv neurons show decreased NMDAR activity, which suppresses the cooperation between NMDARs and gap junctions (GJs) for normal burst firing. Shank2–/– Pv neurons show compensatory increases in GJ activity that are not sufficient for social rescue. However, optogenetic boosting of Pv neuronal bursts, requiring GJs, rescues cortical social cognition in Shank2–/– mice, similar to the NMDAR-dependent social rescue. Therefore, NMDARs and gap junctions cooperate to promote cortical Pv neuronal bursts and social cognition.

Suggested Citation

  • Eunee Lee & Seungjoon Lee & Jae Jin Shin & Woochul Choi & Changuk Chung & Suho Lee & Jihye Kim & Seungmin Ha & Ryunhee Kim & Taesun Yoo & Ye-Eun Yoo & Jisoo Kim & Young Woo Noh & Issac Rhim & Soo Yeon, 2021. "Excitatory synapses and gap junctions cooperate to improve Pv neuronal burst firing and cortical social cognition in Shank2-mutant mice," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25356-2
    DOI: 10.1038/s41467-021-25356-2
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