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Spatial and single-cell transcriptomics reveal neuron-astrocyte interplay in long-term memory

View ORCID ProfileWenfei Sun, Zhihui Liu, Xian Jiang, Michelle B. Chen, Hua Dong, Jonathan Liu, Thomas C. Südhof, Stephen R. Quake
doi: https://doi.org/10.1101/2023.03.20.533566
Wenfei Sun
1Department of Bioengineering, Stanford University, Stanford, CA
2Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA
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  • ORCID record for Wenfei Sun
Zhihui Liu
2Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA
3Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA
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Xian Jiang
2Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA
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Michelle B. Chen
1Department of Bioengineering, Stanford University, Stanford, CA
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Hua Dong
4Institute for Stem Cell Biology and Regenerative Medicine, Stanford University School of Medicine, Stanford, CA
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Jonathan Liu
5Chan Zuckerberg Biohub, Stanford, CA
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Thomas C. Südhof
2Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA
3Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA
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  • For correspondence: steve@quake-lab.org tcs1@stanford.edu
Stephen R. Quake
1Department of Bioengineering, Stanford University, Stanford, CA
5Chan Zuckerberg Biohub, Stanford, CA
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  • For correspondence: steve@quake-lab.org tcs1@stanford.edu
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Abstract

Memory encodes past experiences, thereby enabling future plans. The basolateral amygdala (BLA) is a center of salience networks that underlie emotional experience and thus plays a key role in long-term fear memory formation1, 2. Here we used spatial and single-cell transcriptomics to illuminate the cellular and molecular architecture of the role of the basolateral amygdala in long-term memory. We identified transcriptional signatures in subpopulations of neurons and astrocytes that were memory-specific and persisted for weeks. These transcriptional signatures implicate neuropeptide signaling, mitogen-activated protein kinase (MAPK), brain-derived neurotrophic factor (BDNF), cAMP response element-binding protein (CREB), ubiquitination pathways, and synaptic connectivity in long-term memory. We also discovered that a neuronal sub-population, defined by increased Penk expression and decreased Tac expression, constitutes the most prominent component of the BLA’s memory engram. These transcriptional changes were observed both with single-cell RNAseq and with single-molecule spatial transcriptomics in intact slices, thereby providing a rich spatial map of a memory engram. The spatial data enabled us to show that this neuronal subpopulation further interacts with spatially related astrocytes that are essential for memory consolidation, indicating that neurons require interactions with astrocytes to encode long term memory.

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 March 21, 2023.
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Spatial and single-cell transcriptomics reveal neuron-astrocyte interplay in long-term memory
Wenfei Sun, Zhihui Liu, Xian Jiang, Michelle B. Chen, Hua Dong, Jonathan Liu, Thomas C. Südhof, Stephen R. Quake
bioRxiv 2023.03.20.533566; doi: https://doi.org/10.1101/2023.03.20.533566
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Spatial and single-cell transcriptomics reveal neuron-astrocyte interplay in long-term memory
Wenfei Sun, Zhihui Liu, Xian Jiang, Michelle B. Chen, Hua Dong, Jonathan Liu, Thomas C. Südhof, Stephen R. Quake
bioRxiv 2023.03.20.533566; doi: https://doi.org/10.1101/2023.03.20.533566

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