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

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 (nad2018@med.cornell.edu) and Alicia Che (alicia.che@yale.edu)
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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
Zhe Ran S. Duan: Weill Cornell Medicine
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

Nature Communications, 2025, vol. 16, issue 1, 1-15

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-024-55783-w

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