Abstract
SummaryNeuronal “replay,” in which place cell firing during rest recapitulates recently experienced trajectories, is thought to mediate the transmission of information from hippocampus to neocortex, but the mechanism for this transmission is unknown. Here, we show that replay uses a phase code to represent spatial trajectories by the phase of firing relative to the 150- to 250-Hz “ripple” oscillations that accompany replay events. This phase code is analogous to the theta phase precession of place cell firing during navigation, in which place cells fire at progressively earlier phases of the 6- to 12-Hz theta oscillation as their place field is traversed, providing information about self-location that is additional to the rate code and a necessary precursor of replay. Thus, during replay, each ripple cycle contains a “forward sweep” of decoded locations along the recapitulated trajectory. Our results indicate a novel encoding of trajectory information during replay and implicates phase coding as a general mechanism by which the hippocampus transmits experienced and replayed sequential information to downstream targets.
Highlights
The mammalian hippocampus is implicated in both spatial cognition and episodic memory function.[1,2] In the rodent hippocampal formation, place and grid cells are active in restricted regions of space—the corresponding place or grid field.[3,4] During active movement, when 6- to 12-Hz theta oscillations dominate the local field potential (LFP), place cells and a subset of grid cells in medial entorhinal cortex (MEC) exhibit a theta phase code for location
The theta phase code for location exhibited by place and grid cells improves the accuracy of decoding location[10] and allows movement direction to be inferred from population activity in each oscillatory cycle.[11,12]
We identified a total of 1,355/1,499 place fields on outbound and 1,256/1,423 place fields on inbound runs along the track that passed our criteria for inclusion (R5 spikes fired within the field on all runs through that field, covering R50% of the place field), with 873/1,044 (83.6%) cells having R1 field included on either outbound or inbound runs along the track
Summary
The mammalian hippocampus is implicated in both spatial cognition and episodic memory function.[1,2] In the rodent hippocampal formation, place and grid cells are active in restricted regions of space—the corresponding place or grid field.[3,4] During active movement, when 6- to 12-Hz theta oscillations dominate the local field potential (LFP), place cells and a subset of grid cells in medial entorhinal cortex (MEC) exhibit a theta phase code for location. These cells fire at progressively earlier phases of the theta cycle as the firing field is traversed.[5,6] Because phase precession is coordinated across cells, this produces theta ‘‘sweeps’’ of activity at the network level that encode a sequence of locations beginning behind and progressing ahead of the animal within each oscillatory cycle.[7,8,9] The theta phase code for location exhibited by place and grid cells improves the accuracy of decoding location[10] and allows movement direction to be inferred from population activity in each oscillatory cycle.[11,12]
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