Engram-specific transcriptome profiling of contextual memory consolidation

Priyanka Rao-Ruiz, Jonathan J. Couey, Ivo M. Marcelo, Christian G. Bouwkamp, Denise E. Slump, Mariana R. Matos, Rolinka J. Loo, Gabriela J. Martins, Mirjam Hout, Wilfred F. IJcken, Rui M. Costa, Michel C. Oever () and Steven A. Kushner ()
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Priyanka Rao-Ruiz: Erasmus MC University Medical Center
Jonathan J. Couey: Erasmus MC University Medical Center
Ivo M. Marcelo: Erasmus MC University Medical Center
Christian G. Bouwkamp: Erasmus MC University Medical Center
Denise E. Slump: Erasmus MC University Medical Center
Mariana R. Matos: Vrije Universiteit Amsterdam
Rolinka J. Loo: Vrije Universiteit Amsterdam
Gabriela J. Martins: Champalimaud Centre for the Unknown
Mirjam Hout: Erasmus MC University Medical Center
Wilfred F. IJcken: Erasmus MC University Medical Center
Rui M. Costa: Champalimaud Centre for the Unknown
Michel C. Oever: Vrije Universiteit Amsterdam
Steven A. Kushner: Erasmus MC University Medical Center

Nature Communications, 2019, vol. 10, issue 1, 1-14

Abstract: Abstract Sparse populations of neurons in the dentate gyrus (DG) of the hippocampus are causally implicated in the encoding of contextual fear memories. However, engram-specific molecular mechanisms underlying memory consolidation remain largely unknown. Here we perform unbiased RNA sequencing of DG engram neurons 24 h after contextual fear conditioning to identify transcriptome changes specific to memory consolidation. DG engram neurons exhibit a highly distinct pattern of gene expression, in which CREB-dependent transcription features prominently (P = 6.2 × 10−13), including Atf3 (P = 2.4 × 10−41), Penk (P = 1.3 × 10−15), and Kcnq3 (P = 3.1 × 10−12). Moreover, we validate the functional relevance of the RNAseq findings by establishing the causal requirement of intact CREB function specifically within the DG engram during memory consolidation, and identify a novel group of CREB target genes involved in the encoding of long-term memory.

Date: 2019
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DOI: 10.1038/s41467-019-09960-x

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