A cortical-hippocampal-cortical loop of information processing during memory consolidation
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Hippocampal replay during sharp-wave ripple events (SWRs) is thought to drive memory consolidation in hippocampal and cortical circuits. Changes in neocortical activity can precede SWR events, but whether and how these changes influence the content of replay remains unknown. Here we show that during sleep there is a rapid cortical-hippocampal-cortical loop of information flow around the times of SWRs. We recorded neural activity in auditory cortex (AC) and hippocampus of rats as they learned a sound-guided task and during sleep. We found that patterned activation in AC precedes and predicts the subsequent content of hippocampal activity during SWRs, while hippocampal patterns during SWRs predict subsequent AC activity. Delivering sounds during sleep biased AC activity patterns, and sound-biased AC patterns predicted subsequent hippocampal activity. These findings suggest that activation of specific cortical representations during sleep influences the identity of the memories that are consolidated into long-term stores.
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TMR in rodent studies confirmed that auditory cues paired to specific trajectories during spatial learning enhance hippocampal reactivation of the associated trajectory when delivered during subsequent sleep.
“TMR has also been used in rodent studies, confirming that auditory cues, which had been paired to specific trajectories dur-ing a spatial learning task, enhance hippocampal reactivation of the associated trajectory when delivered during subsequent sleep.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [89]
The Results describe rats learning a sound-guided Y-track task and show that sounds delivered during sleep biased auditory-cortex patterns that predicted subsequent hippocampal CA1 activity. They do not establish enhanced reactivation of the trajectory associated with a cue: the Results state that sound identity could not be significantly decoded from CA1 ensembles. The Discussion distinguishes this paper’s finding from a previous study showing that sleep sounds can bias hippocampal reactivation. (LLM, conf=0.88)
Experimental — accuracy not yet measuredMemory reactivation is observed in many brain regions beyond hippocampus, including sensory, motor, entorhinal, parietal, prefrontal, and subcortical areas.
“memory reactivation is a far more ubiquitous phenomenon, as it is observed in many brain regions, ranging from early sensory [87][88][89] and motor cortices, 65,90 over medial entorhinal cortex [91][92][93] and higher-order association areas like the parietal [94][95][96] and prefrontal cortices [97][98][99] to different subcortical areas.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [89]
Information flow during coordinated reactivation events appears organized in a loop-like manner, with cortical activity predicting hippocampal reactivations during SPW-Rs, and hippocampal reactivations leading extrahippocampal regions.
“information flow during such coordinated reactivation events appears be organized in a loop-like manner, with activity in cortical regions predicting the content of hippocampal reactivations during SPW-Rs, 89 and hippocampal reactivations, in turn, leading reactivations in extrahippocampal regions.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [89]
TMR biases the content of memory reactivations toward targeted memory information but does not appear to increase the overall number of reactivation events.
“these studies revealed that, while biasing the content of memory reactivations toward the targeted memory information, TMR does not appear to increase the overall number of reactivation events.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [89]
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- Authors
- Rothschild, G., Eban, E., & Frank, L. M.
- Affiliations
- University of California, San Francisco (US)
- Google (United States) (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Frank, Loren M
- Venue
- Nature Neuroscience
- Published
- 2016-12-12
- Volume
- 20
- Issue
- 2
- Pages
- 251-259
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5783826
- OpenAlex
- W2561545741
- Cited by
- 387
- References
- 54
- Citations by year
- 2026: 27 · 2025: 39 · 2024: 40 · 2023: 40 · 2022: 37 · 2021: 33 · 2020: 50 · 2019: 58 · 2018: 41 · 2017: 22
- FWCI
- 25.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Mental Health (R01MH105174, R01MH090188)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- memory consolidation, hippocampal ripples, hippocampal replay, auditory cortex, sleep, memory reactivation
- MeSH terms
- Memory Consolidation, Animals, Auditory Cortex, Hippocampus, Learning, Male, Nerve Net, Neurons, Sleep, Wakefulness, Rats, Long-Evans
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