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Modulation of infraslow oscillation in the dentate gyrus during Non-REM sleep

Gergely F. Turi, Xinyue Chen, Sasa Teng, Emily CY Lim, Carla Dias, Ruining Hu, Fenghua Zhen, View ORCID ProfileYueqing Peng
doi: https://doi.org/10.1101/2023.05.12.540575
Gergely F. Turi
1New York State Psychiatric Institute, Division of Systems Neuroscience New York, NY 10032, USA
2Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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  • For correspondence: [email protected] [email protected]
Xinyue Chen
3Institute for Genomic Medicine, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
4Department of Neuroscience, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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Sasa Teng
3Institute for Genomic Medicine, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
5Department of Pathology and Cell Biology, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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Emily CY Lim
6Columbia College, Columbia University, New York, NY 10027, USA
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Carla Dias
1New York State Psychiatric Institute, Division of Systems Neuroscience New York, NY 10032, USA
2Department of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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Ruining Hu
3Institute for Genomic Medicine, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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Fenghua Zhen
7National Institute of Allergy and Infectious Diseases, Bethesda, MD, 20894, USA
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Yueqing Peng
3Institute for Genomic Medicine, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
5Department of Pathology and Cell Biology, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
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  • ORCID record for Yueqing Peng
  • For correspondence: [email protected] [email protected]
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SUMMARY

The importance of sleep in memory consolidation is well-established, with the hippocampal CA1 and CA3 subregions playing a crucial role in this process. The current working hypothesis postulates that episodic memory traces captured during waking hours are replayed in the hippocampal CA1-CA3 areas and transferred to the cortex for long-term storage during sleep. While the entorhinal cortex provides sensory and spatial information primarily to the hippocampus via the dentate gyrus (DG), the DG has traditionally been regarded as a “silent partner” in memory consolidation. The transfer of captured memory traces from the DG to downstream hippocampal areas remains largely unknown. To investigate this, we used optical imaging tools to record neural activity in the DG during different sleep stages. Strikingly, we found that many of the DG cells are even more active during sleep than wakefulness and the populational activity in the DG slowly oscillates during non-REM (NREM) sleep. The cycles of this oscillatory activity coincided with microarousals and were tightly locked to brief serotonin (5-HT) bursts during NREM sleep. Pharmacological blockade of 5-HT1a receptors abolished the calcium oscillations in the DG. Furthermore, genetic knockdown of 5-HT1a receptors in the DG lead to memory impairment in spatial and contextual memory tasks. Together, our findings suggest that serotonin-driven infraslow calcium oscillations in the DG during NREM sleep are necessary for memory consolidation.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 13, 2023.
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Modulation of infraslow oscillation in the dentate gyrus during Non-REM sleep
Gergely F. Turi, Xinyue Chen, Sasa Teng, Emily CY Lim, Carla Dias, Ruining Hu, Fenghua Zhen, Yueqing Peng
bioRxiv 2023.05.12.540575; doi: https://doi.org/10.1101/2023.05.12.540575
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Modulation of infraslow oscillation in the dentate gyrus during Non-REM sleep
Gergely F. Turi, Xinyue Chen, Sasa Teng, Emily CY Lim, Carla Dias, Ruining Hu, Fenghua Zhen, Yueqing Peng
bioRxiv 2023.05.12.540575; doi: https://doi.org/10.1101/2023.05.12.540575

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