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A corticalhippocampalcortical loop of information processing during memory consolidation
Gideon Rothschild1, Elad Eban2 & Loren M Frank1,3
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 corticalhippocampalcortical 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.
2017 Nature America, Inc., part of Springer Nature. All rights reserved.
The hippocampus is critical for forming memories of daily life events, but over time memories can become independent of the hippocampus13. This transition of memory representations from being strongly dependent on the hippocampus to being fully or mostly engrained in cortical networks is termed memory consolidation. According to the influential two-stage model4,5 of consolidation, the first stage occurs during behavior, when the hippocampus rapidly encodes various aspects of the experience via changes of synaptic strengths. In the second stage, during slow-wave sleep and consummatory behaviors, the newly acquired hippocampal information is replayed repeatedly, driving plasticity in neocortex and allowing for the longer-term storage of the memory. The hippocampus has therefore been referred to as the fast learner, which teaches the cortex, the slow learner1,6.
A number of studies have implicated hippocampal replay during SWRs as a potential mechanism of hippocampalcortical communication underlying memory consolidation4,711. SWRs originate in the hippocampus5,12,13, and sequences of hippocampal place cell firing that occurred during wakefulness are repeatedly reactivated on an accelerated timescale during SWRs. Importantly, reactivated hippocampal representations have been suggested to engage cortical networks, as SWRs can drive excitatory responses in cortical output regions14,15, and reactivation in...