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Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex

Author

Listed:
  • John Vargas-Ortiz

    (Yale School of Medicine)

  • Lin Lin

    (Yale School of Medicine)

  • Vena K. Martinez

    (Yale School of Medicine)

  • Rong-jian Liu

    (Yale School of Medicine)

  • Rachel Babij

    (Weill Cornell Medicine
    Weill Cornell/Rockefeller/Sloan Kettering Tri-Institutional MD-PhD Program)

  • Zhe Ran S. Duan

    (Weill Cornell Medicine
    Weill Cornell/Rockefeller/Sloan Kettering Tri-Institutional MD-PhD Program)

  • Sam Wacks

    (Weill Cornell Medicine)

  • Liyuan Sun

    (Yale School of Medicine)

  • Amanda Wang

    (Yale School of Medicine)

  • Sajida Khan

    (Yale School of Medicine)

  • John Lee Soto-Vargas

    (Yale School of Medicine)

  • Natalia V. Marco García

    (Weill Cornell Medicine)

  • Alicia Che

    (Yale School of Medicine
    Wu Tsai Institute, Yale University)

Abstract

Synchronous neuronal activity is a hallmark of the developing mouse primary somatosensory cortex. While the patterns of synchronous neuronal activity in cortical layer 2/3 have been well described, the source of the robust layer 2/3 activity is still unknown. Using a novel microprism preparation and in vivo 2-photon imaging in neonatal mice, we show that synchronous neuronal activity is organized in barrel columns across layers. Monosynaptic rabies tracing and slice electrophysiology experiments reveal that layer 2/3 pyramidal neurons receive significant layer 5 inputs during the first postnatal week, and silencing layer 5 synaptic outputs results in a significant reduction in spontaneous activity, abnormal sensory-evoked activity and disrupted layer 4-layer 2/3 connectivity. Our results demonstrate that translaminar layer 5-layer 2/3 connectivity plays an important role in synchronizing the developing barrel column to ensure the strengthening of layer 4-layer 2/3 connections, supporting the formation of the canonical cortical organization in barrel cortex.

Suggested Citation

  • John Vargas-Ortiz & Lin Lin & Vena K. Martinez & Rong-jian Liu & Rachel Babij & Zhe Ran S. Duan & Sam Wacks & Liyuan Sun & Amanda Wang & Sajida Khan & John Lee Soto-Vargas & Natalia V. Marco García & , 2025. "Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex," Nature Communications, Nature, vol. 16(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-024-55783-w
    DOI: 10.1038/s41467-024-55783-w
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    1. Yong-Chun Yu & Shuijin He & She Chen & Yinghui Fu & Keith N. Brown & Xing-Hua Yao & Jian Ma & Kate P. Gao & Gina E. Sosinsky & Kun Huang & Song-Hai Shi, 2012. "Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly," Nature, Nature, vol. 486(7401), pages 113-117, June.
    2. Stephen C. Noctor & Alexander C. Flint & Tamily A. Weissman & Ryan S. Dammerman & Arnold R. Kriegstein, 2001. "Neurons derived from radial glial cells establish radial units in neocortex," Nature, Nature, vol. 409(6821), pages 714-720, February.
    3. Balazs Lendvai & Edward A. Stern & Brian Chen & Karel Svoboda, 2000. "Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo," Nature, Nature, vol. 404(6780), pages 876-881, April.
    4. James B. Ackman & Timothy J. Burbridge & Michael C. Crair, 2012. "Retinal waves coordinate patterned activity throughout the developing visual system," Nature, Nature, vol. 490(7419), pages 219-225, October.
    5. Knut Kirmse & Michael Kummer & Yury Kovalchuk & Otto W. Witte & Olga Garaschuk & Knut Holthoff, 2015. "GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    6. Laura A. B. Elias & Doris D. Wang & Arnold R. Kriegstein, 2007. "Gap junction adhesion is necessary for radial migration in the neocortex," Nature, Nature, vol. 448(7156), pages 901-907, August.
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