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Slow stabilization of concurrently acquired hippocampal context representations.

ABSTRACT: Hippocampal neurons exhibit spatially localized firing patterns that, at the population level, represent a particular environment or context. Many studies have examined how hippocampal neurons switch from an existing representation to a new one when the environment is changed, a process referred to as remapping. New representations were commonly thought to emerge rapidly, within a few minutes and then remain remarkably stable thereafter. However, a number of recent studies suggest that hippocampal representations may be more fluid than previously thought and most of the previous studies only required that subjects switch from a familiar environment to a novel one. In the present study, we examined the concurrent development of two distinct hippocampal representations by exposing rats to two distinct environmental contexts in an ABAB pattern and we recorded neuronal activity for eight daily training sessions. Hippocampal neurons exhibited normal place fields with typical firing properties during the initial exposure to each context on the first day. However, when the rats were returned to the original context after having spent 15 min in the second context, many of the neurons fired in new locations (i.e., they remapped) as if the rat had encountered a new environment. By the third day, the representations had stabilized and were highly consistent across visits to the same context. These results suggest that when subjects concurrently encode multiple contexts, hippocampal representations may require repeated experiences to fully stabilize. © 2016 Wiley Periodicals, Inc.

SUBMITTER: Law LM

PROVIDER: S-EPMC5138051 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Slow stabilization of concurrently acquired hippocampal context representations.

Law L Matthew LM Bulkin David A DA Smith David M DM

Hippocampus 20161003 12

Hippocampal neurons exhibit spatially localized firing patterns that, at the population level, represent a particular environment or context. Many studies have examined how hippocampal neurons switch from an existing representation to a new one when the environment is changed, a process referred to as remapping. New representations were commonly thought to emerge rapidly, within a few minutes and then remain remarkably stable thereafter. However, a number of recent studies suggest that hippocamp ...[more]

PMID: 27650572

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Project description:BackgroundThere is evidence that slow wave sleep (SWS) promotes the consolidation of memories that are subserved by mediotemporal- and hippocampo-cortical neural networks. In contrast to implicit memories, explicit memories are accompanied by conscious (attentive and controlled) processing. Awareness at pre-sleep encoding has been recognized as critical for the off-line memory consolidation. The present study elucidated the role of task-dependent cortical activation guided by attentional control at pre-sleep encoding for the consolidation of hippocampus-dependent memories during sleep.MethodologyA task with a hidden regularity was used (Number Reduction Task, NRT), in which the responses that can be implicitly predicted by the hidden regularity activate hippocampo-cortical networks more strongly than responses that cannot be predicted. Task performance was evaluated before and after early-night sleep, rich in SWS, and late-night sleep, rich in rapid eye movement (REM) sleep. In implicit conditions, slow cortical potentials (SPs) were analyzed to reflect the amount of controlled processing and the localization of activated neural task representations.Principal findingsDuring implicit learning before sleep, the amount of controlled processing did not differ between unpredictable and predictable responses, nor between early- and late-night sleep groups. A topographic re-distribution of SPs indicating a spatial reorganization occurred only after early, not after late sleep, and only for predictable responses. These SP changes correlated with the amount of SWS and were covert because off-line RT decrease did not differentiate response types or sleep groups.ConclusionsIt is concluded that SWS promotes the neural reorganization of task representations that rely on the hippocampal system despite absence of conscious access to these representations.SignificanceOriginal neurophysiologic evidence is provided for the role of SWS in the consolidation of memories encoded with hippocampo-cortical interaction before sleep. It is demonstrated that this SWS-mediated mechanism does not depend critically on explicitness at learning nor on the amount of controlled executive processing during pre-sleep encoding.

Dataset Information

Slow stabilization of concurrently acquired hippocampal context representations.

Publications

Slow stabilization of concurrently acquired hippocampal context representations.

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