Expression, control, and probable functional significance of the neuronal theta-rhythm.

The data on theta-modulation of neuronal activity in the hippocampus and related structures, obtained by the author and her colleagues have been reviewed. Analysis of extracellularly recorded neuronal activity in alert rabbits, intact and after various brain lesions, in slices and transplants of the hippocampus and septum allow one to make the following conclusions. Integrity of the medial septal area (MS-DB) and its efferent connections are indispensable for theta-modulation of neuronal activity and EEG of the hippocampus. The expression of hippocampal theta depends on the proportion of the MS-DB cells involved in the rhythmic process, and its frequency in the whole theta-range, is determined by the corresponding frequencies of theta-burst in the MS-DB. The neurons of the MS-DB have the properties of endogenous rhythmic burst and regular single spike oscillators. Input signals ascending to the MS-DB from the pontomesencephalic reticular formation increase both the frequency of the MS-DB theta-bursts and the proportion of neurons involved in theta-activity; serotonergic midbrain raphe nuclei have the opposite effect on the MS-DB rhythmic activity and hippocampal EEG theta. Increase of endogenous acetylcholine (by physostigmine) also increases the proportion of the MS-DB neurons discharging in theta-bursts (both in intact and basally-undercut septum), but does not influence the theta-frequency. The primary effect of the MS-DB on hippocampal neurons (pyramidal and non-pyramidal) consists in GABAergic reset inhibition. Reset inhibition, after which theta-modulation follows in constant phase relation, is triggered also by sensory stimuli. About two-thirds of the hippocampal pyramidal neurons are tonically inhibited by sensory stimuli which evoke EEG theta, while others are excited, or do not change their activity. Anticholinergic drugs restrict the population of rhythmic neurons but do not completely suppress theta-bursts in the MS-DB and hippocampus. Under their action, EEG theta can be evoked (presumably through GABAergic MS-DB influences) by strong reticular or sensory stimuli with corresponding high frequency. However information processing in this condition is defective: expression of reset is increased, responses to electrical stimulation of the perforant path and to sensory stimuli are often augmented, habituation to sensory stimuli is absent and tonic responses are curtailed. On a background of continuous theta induced by increase of endogenous acetylcholine, reset is absent or reduced, responsiveness of the hippocampal neurons to electrical and sensory stimulation is strongly reduced.(ABSTRACT TRUNCATED AT 400 WORDS)