Independent rate and temporal coding in hippocampal pyramidal cells

Abstract

In the brain, hippocampal pyramidal cells use temporal as well as rate coding to signal spatial aspects of the animal's environment or behaviour. The temporal code takes the form of a phase relationship to the concurrent cycle of the hippocampal electroencephalogram theta rhythm. These two codes could each represent a different variable. However, this requires the rate and phase to vary independently, in contrast to recent suggestions that they are tightly coupled, both reflecting the amplitude of the cell's input. Here we show that the time of firing and firing rate are dissociable, and can represent two independent variables: respectively the animal's location within the place field, and its speed of movement through the field. Independent encoding of location together with actions and stimuli occurring there may help to explain the dual roles of the hippocampus in spatial and episodic memory, or may indicate a more general role of the hippocampus in relational/declarative memory.

Figure 1

(a) Behavioural task: rat shuttles back and forth along linear track between food rewards contained in cups attached to moveable walls. (b) False-colour firing field of a place cell created from multiple runs in the eastward direction. (c) EEG theta rhythm and place cell firing (in red) for the same cell on a single eastward run. Ticks above the spikes indicate + to − zero crossings (0°/360° phase) for each theta wave, lines through theta waves indicate 270°. Bursts of spikes occur at higher than theta frequency causing each successive burst to move to an earlier phase of the theta cycle, despite initially rising, then falling firing rate. Theta cycle phase of spikes from multiple runs is plotted against position (d), time (e) and instantaneous firing rate (f) in the place field. g) Phase (adjusted for circularity, see Methods) is better correlated with location than with time or firing rate across the population of cells. Here and in subsequent figures, vertical bars represent +/− s.e.m.

Figure 2

Phase precession is independent of instantaneous firing rate. (a) Phase depends on location, being highest in the early third of each field, lower in the middle third, and lowest in the late third. (b) Temporal derivative of phase is negative in each portion of the field (68/76 fields in the early portion, p< 1 × 10^-12; 57/76 in the middle, p<1 × 10^-5; 46/76 late, p< 0.05, binomial test). (c) Instantaneous firing rate starts low, increases in the middle third and then decreases in the late part of the field. (d) Temporal derivative of instantaneous firing starts high, falls towards zero in the middle third, and then goes negative in the last third. Here and in subsequent figures, * denotes p < 0.05 & ** denotes p < 0.01.

Figure 3

Phase is correlated with track location on low as well as high firing rate runs. (a) A single cell for which average firing rate on high rate runs (below) is four times that on lower rate ones (above) with no discernible effect on the phase precession. (b) The same analysis for the cell shown in Figure 1. Phase precession can occur despite very low firing rates. Above: 35 spikes from 66 low-rate runs, mean spikes/run .53, SEM 0.09, range 0-2 (0 spikes on 41 runs, 1 on 15, and 2 on 10); Below: 194 spikes from 36 high-rate runs mean spikes/run 5.40, SEM 0.53, range 2-14. (c) Population data (n=34): phase precesses across early, middle and late parts of the field on both high and low rate runs.

Figure 4

Firing rates differ on fast and slow runs through the field. (a) Significant difference in average peak firing rates but no difference in (b) rate of phase precession, (c) total phase shift. (d) Firing rate is the only variable measured that consistently correlates with running speed (1.5 metre track, mean r= 0.223, 23/29 fields with significant positive correlations p< 0.05)

Figure 5

Phase Precession on the shortened tracks. Single cell: (a) phase angle vs position (green) gets steeper as the field size shrinks and the firing rate (spikes dividing by dwell time, in red) drops due to shortening of the track. Bottom panel shows the second baseline trial on full-length track carried out after short track trials. Population: slope of phase precession (i.e. rate of change in space) increases with shorter track length (b) in the absence of systematic changes in other correlations such as firing rate (c), ‘Delta’ values refer to the change from the preceding baseline trial to the trial on the shortened track, see Methods.