A Model of the CA1 Field Rhythms

Abstract

We propose a model of the main rhythms in the hippocampal CA1 field: theta rhythm; slow, middle, and fast gamma rhythms; and ripple oscillations. We have based this on data obtained from animals behaving freely. We have considered the modes of neuronal discharges and the occurrence of local field potential oscillations in the theta and non-theta states at different inputs from the CA3 field, the medial entorhinal cortex, and the medial septum. In our work, we tried to reproduce the main experimental phenomena about rhythms in the CA1 field: the coupling of neurons to the phase of rhythms, cross-rhythm phase–phase coupling, and phase–amplitude coupling. Using computational experiments, we have proved the hypothesis that the descending phase of the theta rhythm in the CA1 field is formed by the input from the CA3 field via the Shaffer collaterals, and the ascending phase of the theta rhythm is formed by the IPSPs from CCK basket cells. The slow gamma rhythm is coupled to the descending phase of the theta rhythm, since it also depends on the arrival of the signal via the Shaffer collaterals. The middle gamma rhythm is formed by the EPSPs of the principal neurons of the third layer of the entorhinal cortex, corresponds to experimental data. We were able to unite in a single mathematical model several theoretical ideas about the mechanisms of rhythmic processes in the CA1 field of the hippocampus.

Phase relations of interneuronal activity relative to theta rhythm

“…The copyright holder for this preprint (which this version posted May 11, 2023. ; https://doi.org/10.1101/2023.05.11.540330 doi: bioRxiv preprint Several theoretical studies have investigated the formation of phase relations between neurons of the CA1 field and theta rhythm [6,47]. Despite the detailed nature of these models, the authors were unable to reproduce the form of distribution of most types of interneurons in the theta rhythm phase.…”

“…Most often, one of the populations completely inhibit the other. When considering a larger number of interneuron populations, the problem becomes much more complicated [6,47]. We hypothesized that short-term synaptic plasticity stabilizes the structure of interneuronal activity.…”

“…Models with a few interneuron populations give a good approximation of the distribution of neurons in theta rhythm phases due to input from the medial septum [19,49]. However, with an increase in the number of interneuron classes in models, the quality of the approximation of phase relations decreases [6,21,47]. Although in the cited papers, the authors used a different input structure.…”

Oscillations in the Dentate Gyrus as a Tool for the Functioning of the Hippocampus: Healthy and Epileptic Brain

“…At the same time, the inputs from the medial septum, cholinergic and GABAergic, were found to have only a modulating effect on the theta and gamma activity in the DG through the innervation of EC pyramidal neurons or DG interneurons (Perní a-Andrade and Jonas, 2014). On the other hand, the classical and some modern models of hippocampal theta rhythm generation propose a critical role of inputs from the medial septum/diagonal band (Freund and Antal, 1988;Stewart and Fox, 1990;Buzsá ki, 2002;Nuñez and Buño, 2021;Mysin, 2021) with the participation of the intrinsic recurrent connectivity in the hippocampus (Kocsis et al, 1999). Thus, it is possible that theta oscillations in the hippocampus proper and the DG are generated by different mechanisms.…”

Phase relations of interneuronal activity relative to theta rhythm

“…The mechanisms of formation of phase relations of interneuronal activity and theta rhythm are unknown. Several theoretical studies have investigated the formation of phase relations between neurons of the CA1 field and theta rhythm (Bezaire et al, 2016 ; Mysin, 2021 ). Despite the detailed nature of these models, the authors were unable to reproduce the form of distribution of most types of interneurons in the theta rhythm phase.…”