Hippocampal place cell assemblies are speed-controlled oscillators

Abstract

The phase of spikes of hippocampal pyramidal cells relative to the local field oscillation shifts forward (''phase precession'') over a full cycle as the animal crosses the cell's receptive field (''place field''). The linear relationship between the phase of the spikes and the travel distance within the place field is independent of the animal's running speed. This invariance of the phase-distance relationship is likely to be important for coordinated activity of hippocampal cells and space coding, yet the mechanism responsible for it is not known. Here we show that at faster running speeds place cells are active for fewer cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster, yet spatial-phase precession stays unchanged. Interneurons can also show transient-phase precession and contribute to the formation of coherently precessing assemblies. We hypothesize that the speed-correlated acceleration of place cell assembly oscillation is responsible for the phase-distance invariance of hippocampal place cells.cell assembly ͉ interneurons ͉ phase locking ͉ phase precession ͉ oscillations W hile animals navigate in an environment, the hippocampal local field potential (LFP) is characterized by a highly regular oscillation (8-10 Hz). Principal cells in the hippocampus show place-specific firing by two criteria. First, the firing is tuned to a particular location (''place field''), showing a bellshaped tuning curve centered around its preferred location (1). Second, the timing of spikes within subsequent cycles systematically shifts forward (''phase precession''), Ϸ1 full cycle in total, as the rat runs through the place field of the neuron (2, 3) (see also Fig. 1 A and B). Both the firing rate and discharge phase within a cycle are correlated with the rat's position. However, how the rate change and -phase precession of spikes are related is poorly understood. The available experiments support both a rate-phase interdependence (4-6) and independence (7).Several explanations for the place-phase relationship were put forward (4)(5)(6)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). To confront these models, we examined the relationship among running speed, oscillation frequency of place cells and LFP , and timing of spikes within the cycle. We show that principal cells oscillate at a frequency faster than the simultaneously recorded LFP oscillation, and that this oscillation frequency depends on the rat's running speed. Together with the place-and speed-dependent oscillation frequencies of interneurons, the findings support the hypothesis that place coding results from coordinated network activity. We propose that the locomotion speed-dependent oscillation of place cell assemblies may underlie the mechanisms responsible for distance encoding in the hippocampus. ResultsWe recorded the firing patterns of pyramidal cells, interneurons, and the LFP from the CA1 pyramidal layer of rats as they ran on a U-shap...

Altered Phase Precession and Compression of Temporal Sequences by Place Cells in Epileptic Rats

“…There was no difference in interfield distance/running-time lag correlations (CTR: r ϭ 0.868, p Ͻ 0.0001; SE: r ϭ 0.938, p Ͻ 0.0001; CTR-SE comparison: Z ϭ Ϫ0.077, p ϭ 0.11, NS), and no difference in terms of variability (SE: ϭ 41454.55; CTR: ϭ 31049.131; F (35,37) ϭ 1.34; p ϭ 0.61, NS). These results are all the more important that, in contrast to real-time spiking lag, interfield distance is not influenced by behavioral variability (Geisler et al, 2007).…”

“…The time compression index was defined, for all possible pairs of cells, as the ratio of two spike timing measures: (1) the time necessary for the animal to go from one field to the other, and (2) the equivalent compressed time in the theta domain (i.e., the time lag between the spikes of the two corresponding place cells within one theta cycle) (Geisler et al, 2007). It was computed for pairs of simultaneously recorded neurons that shared the same firing directionality, on the basis of their crosscorrelogram (CCG).…”

Local generation of multineuronal spike sequences in the hippocampal CA1 region

“…Interneurons were embedded in the assembly sequences, similar to a previous study examining the stability of sequential activation of pyramidal cells and interneurons during slow oscillations in the neocortex (34). Single interneurons are typically controlled by a limited number of pyramidal cell assemblies (35,36) and suppress the competing assemblies, which can explain their orderly presence in the sequential patterns. In turn, interneuron spiking may provide a scaffold -a temporal backbone -for pyramidal cell spiking.…”

Phase Precession Through Synaptic Facilitation

“…Because the firing rate of hippocampal pyramidal cells is roughly proportional to the running speed of rats (Ekstrom et al, 2001), the number of action potentials fired during a place field traversal is almost constant and independent of running speed (Geisler, Robbe, Zugaro, Sirota, & Buzsáki, 2007). Similar data on the dependence of the firing rate of DG granule cells on running speed are not available.…”

“…Place cells with small place fields exhibit rapid phase precession, whereas cells with large fields display slow phase precession such that the range of firing phases is the same in both cases (Ekstrom et al, 2001;Dragoi & Buzsáki, 2006;Geisler et al, 2007). Mossy fiber facilitation should therefore be strong for small place fields where a CA3 place cell receives only few DG input spikes on average.…”