Phase relations of theta oscillations in a computer model of the hippocampal CA1 field: Key role of Schaffer collaterals.

The hippocampal theta rhythm (4-12 Hz) is one of the most important electrophysiological processes in the hippocampus, it participates in cognitive hippocampal functions, such as navigation in space, novelty detection, and declarative memory. We use neural network modeling to study the mechanism of theta rhythm emergence in the CA1 microcircuitry. Our model of the CA1 field includes biophysical representation of major cell types related to the theta rhythm emergence: excitatory pyramidal cells and two types of inhibitory interneurons, PV+ basket cells and oriens lacunosum-moleculare (OLM) cells. The main inputs to the CA1 cells come from the entorhinal cortex via perforant pathway, the CA3 field via Schaffer collaterals, and the medial septum via fimbria-fornix. By computer simulations we investigated the influence of each input, intrinsic parameters of neurons, and connections between neurons on phase coupling between the theta rhythm and the firing of pyramidal, PV+ basket and OLM cells in the CA1. We found that the input from the CA3 field via Schaffercollaterals plays a major role in the formation of phase relations that have been observed in experiments in vivo. The direct input from the medial septum participates in the formation of proper phase relations, but it is not crucial for the production of the theta rhythm in CA1 neural populations.

Modeling synchronous theta activity in the medial septum: key role of local communications between different cell populations.

It is widely believed that the theta rhythm in the hippocampus is caused by the rhythmic input from the medial septum-diagonal band of Broca (MSDB). The main MSDB output is formed by GABAergic projection neurons which are divided into two subpopulations and fire at different phases of the hippocampal theta rhythm. The MSDB also contains projection cholinergic, glutamatergic, and non-projection GABAergic neurons. These cell populations innervate each other and also GABAergic projection neurons and participate in the formation of the synchronous rhythmic output to the hippocampus. The purpose of this study is to work out a model of interactions between all neural populations of the MSDB that underlie the formation of the synchronous septal theta signal. The model is built from biologically plausible neurons of the Hodgkin-Huxley type and its architecture reflects modern data on the morphology of neural connections in the MSDB. The model satisfies the following requirements: (1) a large portion of neurons is fast-spiking; (2) the subpopulations of GABAergic projection neurons contain endogenous pacemaker neurons; (3) the phase shift of activity between subpopulations of GABAergic projection neurons is equal to about 150°; and (4) the strengths of bidirectional connections between the subpopulations of GABAergic projection cells are different. It is shown that the theta rhythm generation can be performed by a system of glutamatergic and GABAergic non-projection neurons. We also show that bursting pacemaker neurons in the subpopulation of projection GABAergic neurons play a significant role in the formation of stable antiphase outputs from the MSDB to the hippocampus.