A mechanism for hippocampal place cell firing during the hyperpolarizing phases of the theta rhythm

Victoria Booth and Gina R. Poe

University of Michigan

During phase precession, hippocampal place cells fire over a range of phases of the population theta rhythm. The majority of spikes occur, however, around the peaks of the theta rhythm when the somatic membrane of the cell is presumably most depolarized. During REM sleep, on the other hand, place cells associated with familiar environments fire preferentially at the troughs of the theta rhythm when the somatic membrane of the cell is most hyperpolarized (Poe et al, Brain Research, 2000). A locus of similar place cell firing in the theta trough has been identified in a recent analysis of phase precession data from awake animals (Yamaguchi et al, J Neurophysiol, 2002). We propose that such preferential firing in the theta trough could result from a gating of synaptic inputs by the 180 degree phase differential in the theta rhythm at the distal dendritic and cellular layers. In particular, distal dendritic synaptic inputs (from layer III of the entorhinal cortex) arriving at the peak of the dendritic theta rhythm, equivalently the trough of the somatic theta rhythm, would be successfully propagated to generate an action potential while those arriving at the trough of dendritic theta, equivalently the peak of somatic theta, would generate only subthreshold responses. We use a realistic, multicompartment CA1 pyramidal cell model (Migliore, J Comput Neurosci, 2002) to investigate this proposed mechanism.