Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation

Yann Vanrobaeys, Utsav Mukherjee, Lucy Langmack, Stacy E. Beyer, Ethan Bahl, Li-Chun Lin, Jacob J. Michaelson, Ted Abel () and Snehajyoti Chatterjee ()
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Yann Vanrobaeys: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa
Utsav Mukherjee: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa
Lucy Langmack: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa
Stacy E. Beyer: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa
Ethan Bahl: Interdisciplinary Graduate Program in Genetics, University of Iowa
Li-Chun Lin: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa
Jacob J. Michaelson: Iowa Neuroscience Institute, University of Iowa
Ted Abel: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa
Snehajyoti Chatterjee: Department of Neuroscience and Pharmacology, Carver College of Medicine, University of Iowa

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Memory consolidation involves discrete patterns of transcriptional events in the hippocampus. Despite the emergence of single-cell transcriptomic profiling techniques, mapping the transcriptomic signature across subregions of the hippocampus has remained challenging. Here, we utilized unbiased spatial sequencing to delineate transcriptome-wide gene expression changes across subregions of the dorsal hippocampus of male mice following learning. We find that each subregion of the hippocampus exhibits distinct yet overlapping transcriptomic signatures. The CA1 region exhibited increased expression of genes related to transcriptional regulation, while the DG showed upregulation of genes associated with protein folding. Importantly, our approach enabled us to define the transcriptomic signature of learning within two less-defined hippocampal subregions, CA1 stratum radiatum, and oriens. We demonstrated that CA1 subregion-specific expression of a transcription factor subfamily has a critical functional role in the consolidation of long-term memory. This work demonstrates the power of spatial molecular approaches to reveal simultaneous transcriptional events across the hippocampus during memory consolidation.

Date: 2023
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DOI: 10.1038/s41467-023-41715-7

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