A memory transcriptome time course reveals essential long-term memory transcription factors

Spencer G. Jones, Beatriz Gil-Martí, Eva Sacristán-Horcajada, Abigail C. Edison, Emily F. Butler, Neda Miandashti, Camilla Roselli, Enrique Turiégano, Tamara Boto, Jamie M. Kramer () and Francisco A. Martin ()
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Spencer G. Jones: Dalhousie University
Beatriz Gil-Martí: Spanish National Research Council (CSIC)
Eva Sacristán-Horcajada: Spanish National Research Council (CSIC)
Abigail C. Edison: Dalhousie University
Emily F. Butler: Dalhousie University
Neda Miandashti: Dalhousie University
Camilla Roselli: Trinity College Dublin
Enrique Turiégano: Autonomous University of Madrid
Tamara Boto: Trinity College Dublin
Jamie M. Kramer: Dalhousie University
Francisco A. Martin: Spanish National Research Council (CSIC)

Nature Communications, 2025, vol. 16, issue 1, 1-18

Abstract: Abstract Long-term memory (LTM) requires transcription and translation of new proteins, yet the transcriptional control of memory remains poorly understood. Here, we performed a transcriptome time-course during LTM formation in Drosophila melanogaster exposed to courtship conditioning. We identified a mushroom body-specific transcriptional memory trace that becomes activated during memory consolidation. Using scRNAseq of CREB-activated cells we were able to detect a persistent transcriptional response in MB neurons after LTM consolidation and retrieval. As a proof of causality, we conducted a loss-of-function screen for genes comprising the transcriptional memory trace, finding 16 positive hits whose disruption impaired LTM. Among them, we identified two neuron activity-regulated genes, Hr38 and sr, which encode transcription factors that are activated by courtship LTM training, required for LTM, and bind to many genes comprising the transcriptional memory trace. Overall, we further define the transcriptional response to LTM and identify transcription factors that may help shape it.

Date: 2025
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DOI: 10.1038/s41467-025-64379-x

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