Various cognitive functions have long been known to require the hippocampus. Recently, progress has been made in identifying the hippocampal neural activity patterns that implement these functions. One such pattern is the sharp wave–ripple (SWR), an event associated with highly synchronous neural firing in the hippocampus and modulation of neural activity in distributed brain regions. Hippocampal spiking during SWRs can represent past or potential future experience, and SWR-related interventions can alter subsequent memory performance. These findings and others suggest that SWRs support both memory consolidation and memory retrieval for processes such as decision-making. In addition, studies have identified distinct types of SWR based on representational content, behavioural state and physiological features. These various findings regarding SWRs suggest that different SWR types correspond to different cognitive functions, such as retrieval and consolidation. Here, we introduce another possibility — that a single SWR may support more than one cognitive function. Taking into account classic psychological theories and recent molecular results that suggest that retrieval and consolidation share mechanisms, we propose that the SWR mediates the retrieval of stored representations that can be utilized immediately by downstream circuits in decision-making, planning, recollection and/or imagination while simultaneously initiating memory consolidation processes.
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The authors thank J. Andreas, A. E. Comrie, T. Davidson, J. Guidera, T. H. Joo, K. Kay, H. Liang, B. P. Nachman and all other members of the Frank Lab for helpful discussion and close reading of sections of this text. The authors apologize to those whose work was not cited because of limited space. This work was supported by National Institue of Mental Health (NIMH) award number F30MH115582 (H.R.J.), National Institute of General Medical Sciences Medical Scientist Training Program grant #T32GM007618 (H.R.J.), NIMH grant R01 MH10517 (L.M.F.) and the Howard Hughes Medical Institute (L.M.F.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Nature Reviews Neuroscience thanks L. Colgin, L. Menendez de la Prida and the other anonymous reviewer for their contribution to the peer review of this work.
The authors declare no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
- Retrograde amnesia
An inability to access previously formed memories.
- Anterograde amnesia
An inability to form new memories.
- Fear conditioning
The process by which an animal learns to associate a cue (cued fear conditioning) or environment (contextual fear conditioning) with a negative outcome, such as a foot shock, and as a result expresses fear in response to the cue or environment alone.
The conscious recall of a past experience.
- Stimulus–response association
A conditioned relationship that supports an organism executing an action (the response) in reaction to a stimulus.
The process of setting future goals and determining the actions required to accomplish them, such as predetermining a route to a target location.
The possibly subconscious mental act of considering possible future or alternative scenarios.
- Local field potential
(LFP). The electrical potential measured by an extracellular electrode that results from the summed membrane currents of nearby neurons.
- Rapid eye movement (REM) sleep
The ‘paradoxical’, wake-like phase of sleep that is marked by reduced synchrony in the LFP and REM and that is associated in humans with dreaming.
- Slow-wave sleep
The phase of sleep marked by low-frequency oscillations in the LFP that is strongly associated with memory consolidation.
- Trace eyeblink conditioning
A hippocampus-dependent classical conditioning task in which a conditioned stimulus such as a tone or flash of light is followed, after a delay, by a blink-inducing unconditioned stimulus, such as a corneal air puff.
A behaviourally defined loss of a previously learned association, typically thought to require new learning.
- Place fields
A place field is the location in an environment where a given cell increases its rate of action potential firing when the animal is in that location.
- Place cells
Pyramidal cells of the hippocampus that fire action potentials at a higher rate when the animal is in a particular location in an environment.
- NMDA receptor-mediated AMPA receptor trafficking
The process by which glutamatergic NMDA receptor activation leads to preparation of glutamatergic AMPA receptors for insertion in the membrane to result in increased synaptic weight.
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Joo, H.R., Frank, L.M. The hippocampal sharp wave–ripple in memory retrieval for immediate use and consolidation. Nat Rev Neurosci 19, 744–757 (2018). https://doi.org/10.1038/s41583-018-0077-1
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