Forward and reverse hippocampal place-cell sequences during ripples

Abstract

We report that temporal spike sequences from hippocampal place neurons of rats on an elevated track recurred in reverse order at the end of a run, but in forward order in anticipation of the run, coinciding with sharp waves. Vector distances between the place fields were reflected in the temporal structure of these sequences. This bidirectional re-enactment of temporal sequences may contribute to the establishment of higher-order associations in episodic memory.

Figure 1

Forward and reverse pre- and replay of place-cell sequences. (a) Spike trains of 13 neurons before, during, and after a single lap (CA1 local field potential shown on top; velocity of the rat shown in the lower panel). The left and right insets magnify 250-ms sections of the spike train, depicting forward preplay and reverse replay, respectively. (b) Histograms show rank-order correlations of the immobility sequences (gray) and an equal number of shuffled surrogate events (white) to the place-field run sequence template. Significantly correlated events are in black. (c) 95% of significant forward correlated events took place before the run (preplay), whereas 85% of significant reverse correlated events took place after the run (replay).

Figure 2

Forward and reverse temporal sequences during ripples reflect distance representations of place cells on the track. (a) Cross-correlograms (CCGs) of forward (preplay) and reverse (replay) events with CA1 sharp-wave ripple events. (b) Temporal offsets between spikes of neuron pairs during significant forward (+) and reverse (o) events were correlated with distance representations between place-field peaks on the track. (c) Temporal offsets of cell pairs were related between track running (‘theta-scale time compression’9) and forward (preplay) and reverse (replay) events.