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Adaptive stimulus selection for consolidation in the hippocampus

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Associative memories guide behavioural adaptation by binding together outcome-predictive sensory stimuli 1 , 2 . However, in a feature-rich environment, only a subset of stimuli may predict a desired outcome… Click to show full abstract

Associative memories guide behavioural adaptation by binding together outcome-predictive sensory stimuli 1 , 2 . However, in a feature-rich environment, only a subset of stimuli may predict a desired outcome 3 , 4 . How neural circuits enable behavioural adaptation by selectively and durably representing subsets of sensory stimuli that are pertinent to a specific outcome is not known. We investigated this feature selection process in the hippocampus during memory acquisition and subsequent consolidation. Two-photon calcium imaging of CA3 axonal projections to CA1 combined with simultaneous local field potential recordings revealed that CA3 projections that encode behaviourally informative sensory stimuli were selectively recruited during the memory replay events that underlie hippocampal memory consolidation 5 . These axonal projections formed sequential assemblies that conjunctively link sensory features to spatial location and thus reward proximity. By contrast, axons encoding uninformative, peripatetic sensory cues were notably suppressed during memory replay. Thus, while the hippocampus comprehensively encodes the real-time sensory environment, it implements a flexible filtering mechanism to maximize the utility of memories destined for long-term storage. We propose that utility-dependent recruitment of sensory experience during memory consolidation is a general coding principle for associative learning. In memory consolidation, the hippocampus has a unique way to preferentially amplify behaviour-relevant information that entails ‘replaying’ this information during periods of rest.

Keywords: consolidation; sensory stimuli; memory; selection; consolidation hippocampus

Journal Title: Nature
Year Published: 2021

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