Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex
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 prepar...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2025-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55783-w |
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| author | 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. De Marco García Alicia Che |
| author_facet | 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. De Marco García Alicia Che |
| author_sort | John Vargas-Ortiz |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-30bd6209a6b047a8bd0cdd5d781928ef |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-30bd6209a6b047a8bd0cdd5d781928ef2025-02-09T12:44:01ZengNature PortfolioNature Communications2041-17232025-02-0116111510.1038/s41467-024-55783-wTranslaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortexJohn Vargas-Ortiz0Lin Lin1Vena K. Martinez2Rong-jian Liu3Rachel Babij4Zhe Ran S. Duan5Sam Wacks6Liyuan Sun7Amanda Wang8Sajida Khan9John Lee Soto-Vargas10Natalia V. De Marco García11Alicia Che12Department of Psychiatry, Yale School of MedicineDepartment of Psychiatry, Yale School of MedicineDepartment of Psychiatry, Yale School of MedicineDepartment of Psychiatry, Yale School of MedicineCenter for Neurogenetics, Feil Family Brain and Mind Research Institute, Weill Cornell MedicineCenter for Neurogenetics, Feil Family Brain and Mind Research Institute, Weill Cornell MedicineCenter for Neurogenetics, Feil Family Brain and Mind Research Institute, Weill Cornell MedicineDepartment of Psychiatry, Yale School of MedicineDepartment of Psychiatry, Yale School of MedicineDepartment of Psychiatry, Yale School of MedicineDepartment of Psychiatry, Yale School of MedicineCenter for Neurogenetics, Feil Family Brain and Mind Research Institute, Weill Cornell MedicineDepartment of Psychiatry, Yale School of MedicineAbstract 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.https://doi.org/10.1038/s41467-024-55783-w |
| spellingShingle | 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. De Marco García Alicia Che Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex Nature Communications |
| title | Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex |
| title_full | Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex |
| title_fullStr | Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex |
| title_full_unstemmed | Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex |
| title_short | Translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex |
| title_sort | translaminar synchronous neuronal activity is required for columnar synaptic strengthening in the mouse neocortex |
| url | https://doi.org/10.1038/s41467-024-55783-w |
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