Coordinated memory replay in the visual cortex and hippocampus during sleep

Abstract

Sleep replay of awake experience in the cortex and hippocampus has been proposed to be involved in memory consolidation. However, whether temporally structured replay occurs in the cortex and whether the replay events in the two areas are related are unknown. Here we studied multicell spiking patterns in both the visual cortex and hippocampus during slow-wave sleep in rats. We found that spiking patterns not only in the cortex but also in the hippocampus were organized into frames, defined as periods of stepwise increase in neuronal population activity. The multicell firing sequences evoked by awake experience were replayed during these frames in both regions. Furthermore, replay events in the sensory cortex and hippocampus were coordinated to reflect the same experience. These results imply simultaneous reactivation of coherent memory traces in the cortex and hippocampus during sleep that may contribute to or reflect the result of the memory consolidation process.

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Figure 1: Experimental design.
Figure 2: Visual cortical and hippocampal spiking activities were organized as frames during SWS.
Figure 3: Visual cortical cells displayed localized firing fields.
Figure 4: Sleep frames replayed multicell firing sequences during RUN in both the visual cortex and the hippocampus.
Figure 5: Frame replays occurred significantly more often than chance in POST in both the visual cortex and hippocampus.
Figure 6: Visual cortical and hippocampal frames that replayed the same trajectories tended to occur at the same time.
Figure 7: Cortical and hippocampal frames co-replayed the same running trajectory as revealed by interval analysis.

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Acknowledgements

We thank E. Miller, C. Moore, J. Fisher and F.-M. Zhou for critical readings on the manuscript, and Wilson laboratory members for technical help and suggestions and comments on the project and manuscript. Supported by grants to M.A.W. from the Brain Science Institute at the Institute of Physical and Chemical Research (RIKEN) in Japan and the US National Institutes of Health.

Author information

Correspondence to Daoyun Ji or Matthew A Wilson.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Hippocampal frames were related to hippocampal EEG ripples. (PDF 212 kb)

Supplementary Fig. 2

Temporal relationship between cortical and hippocampal frames was not significantly different between PRE and POST, and was not sensitive to frame definition parameters. (PDF 85 kb)

Supplementary Fig. 3

Cell pairs between the visual cortex and hippocampus that had high correlation during RUN also had high correlation in POST, but not in PRE. (PDF 28 kb)

Supplementary Fig. 4

High but not low correlation during RUN boosted correlation in POST between the visual cortex and hippocampus, and within the hippocampus. (PDF 78 kb)

Supplementary Fig. 5

Firing patterns in the visual cortex and hippocampus during RUN were replayed in sleep frames during POST. (PDF 36 kb)

Supplementary Fig. 6

Frame replays were compressed during sleep. (PDF 85 kb)

Supplementary Fig. 7

Difference in frame properties did not significantly contribute to increase in replaying ratio from PRE to POST. (PDF 87 kb)

Supplementary Fig. 8

There were no significant differences in distribution of frame duration, within-frame multiunit firing rate per tetrode, and within frame active cell firing rate between replaying and non-replaying candidate frames in either the visual cortex or the hippocampus. (PDF 22 kb)

Supplementary Fig. 9

Shuffling procedure to determine significance (p value) of the overlapping replaying frame pairs. (PDF 65 kb)

Supplementary Fig. 10

Temporal relationship between cortical and hippocampal sequence replays. (PDF 69 kb)

Supplementary Fig. 11

Sleep stage classification. (PDF 38 kb)

Supplementary Fig. 12

Frame boundary determination. (PDF 69 kb)

Supplementary Table 1

Minimum matching indices (I) required for significant frame sequences, given the number of cells in a frame. (PDF 26 kb)

Supplementary Table 2

Comparison in replaying frame ratio between PRE and POST in the visual cortex for each of the 12 trajectories. (PDF 19 kb)

Supplementary Table 3

Comparison in replaying frame ratio between PRE and POST in the hippocampus for each of the 15 trajectories. (PDF 19 kb)

Supplementary Methods (PDF 53 kb)

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Ji, D., Wilson, M. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10, 100–107 (2007). https://doi.org/10.1038/nn1825

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