Theta oscillations represent collective dynamics of multineuronal membrane potentials of murine hippocampal pyramidal cells

A deep neural network model predicts theta oscillations in the mouse hippocampal CA1 area based on in vivo membrane potentials of as few as three pyramidal cells. Theta (theta) oscillations are one of the characteristic local field potentials (LFPs) in the hippocampus that emerge during spatial navigation, exploratory sniffing, and rapid eye movement sleep. LFPs are thought to summarize multineuronal events, including synaptic currents and action potentials. However, no in vivo study to date has directly interrelated theta oscillations with the membrane potentials (Vm) of multiple neurons, and it remains unclear whether LFPs can be predicted from multineuronal Vms. Here, we simultaneously patch-clamp up to three CA1 pyramidal neurons in awake or anesthetized mice and find that the temporal evolution of the power and frequency of theta oscillations in Vms (theta(Vm)s) are weakly but significantly correlate with LFP theta oscillations (theta(LFP)) such that a deep neural network could predict the theta(LFP) waveforms based on the theta(Vm) traces of three neurons. Therefore, individual neurons are loosely interdependent to ensure freedom of activity, but they partially share information to collectively produce theta(LFP).