Dynamic and selective engrams emerge with memory consolidation.

Tomé DF
Zhang Y
Aida T
Mosto O
Lu YL
Chen M
Sadeh S
Roy DS

Scientific Abstract

Episodic memories are encoded by experience-activated neuronal ensembles that remain necessary and sufficient for recall. However, the temporal evolution of memory engrams after initial encoding is unclear. In this study, we employed computational and experimental approaches to examine how the neural composition and selectivity of engrams change with memory consolidation. Our spiking neural network model yielded testable predictions: memories transition from unselective to selective as neurons drop out of and drop into engrams; inhibitory activity during recall is essential for memory selectivity; and inhibitory synaptic plasticity during memory consolidation is critical for engrams to become selective. Using activity-dependent labeling, longitudinal calcium imaging and a combination of optogenetic and chemogenetic manipulations in mouse dentate gyrus, we conducted contextual fear conditioning experiments that supported our model's predictions. Our results reveal that memory engrams are dynamic and that changes in engram composition mediated by inhibitory plasticity are crucial for the emergence of memory selectivity.

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Dynamic and selective engrams emerge with memory consolidation.

Tomé DF
Zhang Y
Aida T
Mosto O
Lu YL
Chen M
Sadeh S
Roy DS

Scientific Abstract

Episodic memories are encoded by experience-activated neuronal ensembles that remain necessary and sufficient for recall. However, the temporal evolution of memory engrams after initial encoding is unclear. In this study, we employed computational and experimental approaches to examine how the neural composition and selectivity of engrams change with memory consolidation. Our spiking neural network model yielded testable predictions: memories transition from unselective to selective as neurons drop out of and drop into engrams; inhibitory activity during recall is essential for memory selectivity; and inhibitory synaptic plasticity during memory consolidation is critical for engrams to become selective. Using activity-dependent labeling, longitudinal calcium imaging and a combination of optogenetic and chemogenetic manipulations in mouse dentate gyrus, we conducted contextual fear conditioning experiments that supported our model's predictions. Our results reveal that memory engrams are dynamic and that changes in engram composition mediated by inhibitory plasticity are crucial for the emergence of memory selectivity.

Citation

2024. Nat Neurosci, 27(3):561-572.

DOI

10.1038/s41593-023-01551-w

Free Full Text at Europe PMC

PMC10917686

Downloads

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Similar content

Preprint
Mederos S, Vissers N, Blakely P, Clopath C, Hofer SB

Overwriting an instinct: visual cortex instructs learning to suppress fear responses

Preprint
Delamare G, Zaki Y, Cai DJ, Clopath C

Drift of neural ensembles driven by slow fluctuations of intrinsic excitability

Preprint
Boboeva V, Pezzotta A, Clopath C, Akrami A

From recency to central tendency biases in working memory: a unifying network model