Figure 6.

Interleaved cell assemblies. A. Spiking activity of two hippocampal neurons (blue and green ticks) and LFP theta in a single run (1 second is shown). Temporal distance T is the time needed for the rat to run the distance between the peaks of the two place fields (‘real time’). Tau, time offset between the two neurons within the theta cycle (‘theta time’). B. Distribution of oscillation frequencies of CA1 pyramidal cells (n>1000) during running on the maze relative to the reference LFP theta (8.09 Hz=0 Hz). Gray dashed line: mean oscillation frequency of pyramidal cells (8.61 Hz=0.52 Hz). Note that nearly all place cells oscillate faster than the frequency of the concurrent LFP theta. C. Three example model neurons (color-coded) with identical oscillation frequency but different phase onset, according to their maximal discharge location. Bottom, the summed activity of the entire population of model neurons (black dashed line) oscillates slower than each transiently active individual neuron (color-coded). D. The phase of the three example neurons with respect to the oscillation of the population is plotted against time. Note that the neuronal spikes phase-precess approximately 360° (O’Keefe and Recce, 1993). Right: spike density for the example neurons. E. Correlation between the distances of place fields peaks and theta-scale time lag for >3000 pairs of neurons (as in A). Above and right: histograms of distance and time lag, respectively. F. Interleaved neuron sequences represent position and distance relationships. The width of the bars indicates firing intensity of the hypothesized assemblies while the theta-time scale temporal differences between assemblies reflect their respective distance representations. In successive theta cycles, assemblies representing overlapping place fields (P1 to P8) shift together in time and sustain a temporal order relationship with each other so that the assembly that fires on the earliest phase represents a place field whose center the animal traverses first. The temporal compression mechanism (Skaggs et al., 1996) allows distances to be translated into time. Approximately, 7±2 assemblies/gamma cycles, are present in a given theta period (Bragin et al., 1995; Lisman and Idiart, 1995). The assembly sequences within theta cycles could be conceived as a neural word. Note that neighboring overlapping words differ only by one assembly. The rat has to travel 7±2 theta cycles until a word with entirely different assemblies appear. A to E, modified after Geisler et al. (2010). F, modified after Dragoi and Buzsáki (2006).