Firing of place cells in the exploring rat conveys doubly coded spatial
information: both the rate of spikes and their timing relative to the
phase of the ongoing field theta oscillation are correlated with the
location of the animal. Specifically, the firing rate of a place cell
waxes and wanes, while the timing of spikes precesses monotonically as
the animal traverses the portion of the environment preferred by the
cell. We propose a mechanism for the generation of this firing pattern
that can be applied for place cells in all three hippocampal subfields
and that encodes spatial information in the output of the cell without
relying on topographical connections or topographical input. A single
pyramidal cell was modeled so that the cell received rhythmic
inhibition in phase with theta field potential oscillation on the soma
and was excited on the dendrite with input depending on the speed of
the rat. The dendrite sustained an intrinsic membrane potential
oscillation, frequency modulated by its input. Firing probability of
the cell was determined jointly by somatic and dendritic oscillations.
Results were obtained on different levels of abstraction: a purely
analytical derivation was arrived at, corroborated by numerical
simulations of rate neurons, and an extension of these simulations to
spiking neurons was also performed. Realistic patterns of rate and
temporal coding emerged and were found to be inseparable. These results
may have implications on the robustness of information coding in place
cell firing and on the ways information is processed in structures
downstream to the hippocampus. (C) 2003 Wiley-Liss, Inc.
