Abstract
SummaryReactivation of hippocampal place cell sequences during behavioral immobility and rest has been linked with both memory consolidation and navigational planning. Yet it remains to be investigated whether these functions are temporally segregated, occurring during different behavioral states. During a self-paced spatial task, awake hippocampal replay occurring either immediately before movement toward a reward location or just after arrival at a reward location preferentially involved cells consistent with the current trajectory. In contrast, during periods of extended immobility, no such biases were evident. Notably, the occurrence of task-focused reactivations predicted the accuracy of subsequent spatial decisions. Additionally, during immobility, but not periods preceding or succeeding movement, grid cells in deep layers of the entorhinal cortex replayed coherently with the hippocampus. Thus, hippocampal reactivations dynamically and abruptly switch between operational modes in response to task demands, plausibly moving from a state favoring navigational planning to one geared toward memory consolidation.
Highlights
Prominent theories of hippocampal function place it at the center of networks supporting memory and navigation (O’Keefe and Nadel, 1978; Scoville and Milner, 1957)
Numerous studies have shown that cortical local field potential (LFP) patterns associated with sleep, such as delta waves (Maingret et al, 2016; Mednick et al, 2013) and spindles (Johnson et al, 2010), are temporally coordinated with sharp-wave ripple complexes (SWRs) (Battaglia et al, 2004; Peyrache et al, 2011; Sirota et al, 2003), and they have indicated that cortico-hippocampal dialogue may be important for learning (Maingret et al, 2016)
After pausing, rats transition rapidly from a state in which they preferentially exhibit replay associated with the ongoing task to a disengaged state, in which replay was directed toward remote sections of the track and incorporated grid cells from deep layers of the medial entorhinal cortex
Summary
Prominent theories of hippocampal function place it at the center of networks supporting memory and navigation (O’Keefe and Nadel, 1978; Scoville and Milner, 1957). At the time of discovery, replay was proposed as the mechanism supporting systems-level memory consolidation (Wilson and McNaughton, 1994), the process by which memories are transferred out of the hippocampus, becoming less susceptible to hippocampal damage (Marr, 1971; Scoville and Milner, 1957) Consistent with this hypothesis, replay typically reflects recent experiences, novel ones (Cheng and Frank, 2008; Foster and Wilson, 2006; O’Neill et al, 2008; van de Ven et al, 2016), is dependent on the NMDA receptor (Dupret et al, 2010; Silva et al, 2015), and is associated with cortical reactivations (Ji and Wilson, 2007; Rothschild et al, 2017; Wierzynski et al, 2009). Hippocampal reactivation during rest enhances learning (de Lavilleon et al, 2015; Rasch et al, 2007)
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