The reorganization and reactivation of hippocampal maps predict spatial memory performance

By David Dupret, J. O’Neill, Barty Pleydell-Bouverie, J. Csicsvari. 2010

692 citations recorded by the source corpus.

The hippocampus is an important brain circuit for spatial memory and the spatially selective spiking of hippocampal neuronal assemblies is thought to provide a mnemonic representation of space. We found that remembering newly learnt goal locations required NMDA receptor–dependent stabilization and enhanced reactivation of goal-related hippocampal assemblies. During spatial learning, place-related firing patterns in the CA1, but not CA3, region of the rat hippocampus were reorganized to represent new goal locations. Such reorganization did not occur when goals were marked by visual cues. The stabilization and successful retrieval of these newly acquired CA1 representations of behaviorally relevant places was NMDAR dependent and necessary for subsequent memory retention performance. Goal-related assembly patterns associated with sharp wave/ripple network oscillations, during both learning and subsequent rest periods, predicted memory performance. Together, these results suggest that the reorganization and reactivation of assembly firing patterns in the hippocampus represent the formation and expression of new spatial memory traces.

Subfields: Cell Biology, Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Hippocampal replay in the awake state: a potential physiological substrate of memory consolidation and retrieval (2011, positive): “Consistent with this possibility, a recent study demonstrated that the strength of awake reactivation predicts subsequent memor”
About sleep's role in memory. (2013, background): “This contrasts with findings indicating that an external triggering of memory reactivations during sleep enhances memory performance the next day (295, 959, 1018) and that spontaneous memory reactivations during sleep correlate with later memory performance (335, 448, 449).”
Memory consolidation. (2015, background): “However, both awake and sleep replay do seem to contribute to later memory performance (Dupret et al. 2010), with awake replay, perhaps, serving to initially stabilize memory but with sleep replay operating in association with systems consolidation.”
A dedicated population for reward coding in the hippocampus (2018, positive): “Although the presence of a goal can alter hippocampal activity in many respects (Ranck, 1973; Gothard et al., 1996; Hollup et al., 2001; Hok et al., 2007; Dupret et al., 2010; McKenzie et al., 2013, 2014; Danielson et al., 2016; Sarel et al., 2017), and in some cases, activity is correlated with goa”
Cellular and Systems Consolidation of Declarative Memory (2017, background): “Replay during task execution has been related to working memory (Jadhav et al. 2012) and replay during quiet rest seems to stabilise the hippocampal memory trace (Dupret et al. 2010).”
The Role of Hippocampal Replay in Memory and Planning (2018, background): “(C) Online replay can depict locations proximal to the animal’s current location (‘local’ replay, left) [71,85,122] or be distant to the animal (‘remote’ replay, right) [63,64,122].”
The restless engram: consolidations never end. (2012, background): “The reactivation of hippocampal maps during post-training rest/sleep periods was further reported to predict performance on hippocampal-dependent matching-to-place reward tasks (Dupret et al. 2010).”
Synaptic Plasticity Forms and Functions. (2020, background): “Recent data suggest that CA1 may be involved in producing a map related to the value of a given environment, where salient regions are more densely represented by particular neurons (Hollup et al. 2001, Dupret et al. 2010, Zaremba et al. 2017, Turi et al. 2019).”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “devoted a series of elegant experiments to address some of these issues (O’Neill et al., 2006, 2008; Csicsvari et al., 2007; Dupret et al., 2010; cf., O’Neill et al., 2010; Csicsvari et al., 2014; Csicsvari and Dupret, 2014).”
Reverse replay of hippocampal place cells is uniquely modulated by changing reward (2016, positive): “Previous studies that reported effects of reward and/or goal on SWRs or on replay have tended to utilize complex behaviors dependent on rather demanding learned tasks (Dupret et al., 2010; Pfeiffer and Foster, 2013; Singer and Frank, 2009).”
Biasing the content of hippocampal replay during sleep (2012, neutral): “From top to bottom, (1) the onsets of acoustic stimuli, (2) animal’s velocity (green), (3) a raster plot of place cell activity (data are presented as in a), (4) MUA, and (5) awake/sleep classification.”