Theta synchronization in the limbic system: the role of Gudden's tegmental nuclei

Abstract

Theta rhythm is most prominent in the hippocampus but has also been recorded in other cortical and limbic structures and can play an important role in functional coupling of widely separated structures responsible for different components of the memory building process. Here we demonstrate in the rat that neuronal activity exhibiting strong state-dependent synchrony with rhythmic hippocampal electroencephalogram is present also at the brainstem level, specifically in the relatively small tegmental nuclei of Gudden intimately connected with the limbic forebrain. We found that during theta states, either occurring spontaneously or triggered by sensory stimulation in the urethane anaesthetized rat, all neurons in the anterior and ventral tegmental nuclei exhibited a consistent switch from irregular discharges to rhythmic bursts. The switch between these patterns closely matched the analogous transformations in the hippocampal EEG, but the level of synchrony between the two signals varied depending on the level of theta activation. During sensory stimulation, when theta is faster and more regular, the rhythmic bursts in the tegmentum showed extremely high coherence (up to 0.96) with hippocampal field potentials. During spontaneous theta, the average coherence was lower but still highly significant (0.62). Gudden's nuclei are reciprocally connected to the mammillary body complex (MB) occupying a strategic position at the gateway of hippocampofugal connections organized in the Papez circuit. Thus, coupling between the MB-Gudden circuit and the hippocampus and consequently the neuronal traffic through the Papez circuit and hence the assembly of limbic structures connected to the hippocampus may vary according to the activity in these specific brainstem nuclei.