Causal role for sleep-dependent reactivation of learning-activated sensory ensembles for fear memory consolidation

Brittany C. Clawson, Emily J. Pickup, Amy Ensing, Laura Geneseo, James Shaver, John Gonzalez-Amoretti, Meiling Zhao, A. Kane York, Femke Roig Kuhn, Kevin Swift, Jessy D. Martinez, Lijing Wang, Sha Jiang and Sara J. Aton ()
Additional contact information
Brittany C. Clawson: University of Michigan
Emily J. Pickup: University of Michigan
Amy Ensing: University of Michigan
Laura Geneseo: University of Michigan
James Shaver: University of Michigan
John Gonzalez-Amoretti: Recinto de Gurabo
Meiling Zhao: University of Michigan
A. Kane York: University of Michigan
Femke Roig Kuhn: University of Michigan
Kevin Swift: University of Michigan
Jessy D. Martinez: University of Michigan
Lijing Wang: University of Michigan
Sha Jiang: University of Michigan
Sara J. Aton: University of Michigan

Nature Communications, 2021, vol. 12, issue 1, 1-13

Abstract: Abstract Learning-activated engram neurons play a critical role in memory recall. An untested hypothesis is that these same neurons play an instructive role in offline memory consolidation. Here we show that a visually-cued fear memory is consolidated during post-conditioning sleep in mice. We then use TRAP (targeted recombination in active populations) to genetically label or optogenetically manipulate primary visual cortex (V1) neurons responsive to the visual cue. Following fear conditioning, mice respond to activation of this visual engram population in a manner similar to visual presentation of fear cues. Cue-responsive neurons are selectively reactivated in V1 during post-conditioning sleep. Mimicking visual engram reactivation optogenetically leads to increased representation of the visual cue in V1. Optogenetic inhibition of the engram population during post-conditioning sleep disrupts consolidation of fear memory. We conclude that selective sleep-associated reactivation of learning-activated sensory populations serves as a necessary instructive mechanism for memory consolidation.

Date: 2021
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DOI: 10.1038/s41467-021-21471-2

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