On phasic inhibition during hippocampal theta

Abstract

Two computational models are used to explore the possible implications of recent experimental data (Royer et al. 2012) on phasic inhibition during theta frequency (4-10 Hz) oscillations in the hippocampi of actively behaving rodents. A working hypothesis from previous experimental and modelling studies is that a theta cycle is divided into encoding (when synaptic plasticity is enhanced) and recall (when plasticity is suppressed) half cycles. Using a compartmental model of a CA1 pyramidal cell, including dendritic spines, we demonstrate that out-of-phase perisomatic and dendritic inhibition, respectively, can promote the necessary conditions for these half cycles. Perisomatic inhibition allows dendritic calcium spikes that promote synaptic LTP, while minimising cell output. Dendritic inhibition, on the other hand, both controls cell output and suppresses dendritic calcium spikes, preventing LTP. The exact phase relationship between these sub-cycles may not be fixed. Using a simple sum-of-sinusoids activity model, we suggest an interpretation of the data of Royer et al. (2012) in which a fixed-phase encoding sub-cycle is surrounded by a flexible-phase recall cycle that follows the peak of excitatory drive and consequent phase precession of activity as an animal passes through a pyramidal cell's place field.