The evolving concept of the intrinsic hippocampal theta/gamma oscillator

Three main types of electrical oscillations are recorded from the hippocampus in vivo: theta (θ), gamma (γ) and sharp wave ripples with frequency bands of 4-12, 25-100 and 110-250 Hz, respectively. Theta activity is the more robust of them, and has important physiological roles because it is involved in spatial navigation, memory formation and memory retrieval. Classical lesion studies in vivo have suggested that the hippocampus passively follows the θ  rhythm generated in the septum by neurons that are synaptically connected with hippocampal neurons though septo-hippocampal connections. This view has been questioned since several studies have shown that oscillations in the θ range can be recorded in in vitro hippocampal preparations thus indicating that the hippocampus itself can act as a θ oscillator. In this review, we will describe how the paradigm of the intrinsic θ oscillator has been changing over the years from simple models that have proposed single hippocampal lamellae to contain the θ oscillator to the current models that include some degree of septo-temporal integration.