The effect of descending theta rhythmic input from the septohippocampal system on firing in the supramammillary nucleus.

The supramammillary nucleus (SUM) is part of an ascending pathway conveying behavior-dependent drive to the septal generator of limbic theta rhythm. The SUM is, however, reciprocally connected to the septohippocampal system and there is strong evidence that both septum and SUM are capable of generating theta rhythmic activity. The present study examined the possible role of a descending rhythmic input to the SUM using simultaneously recorded hippocampal EEG and SUM neuronal activity in anesthetized rats. Fourier based phase analysis was performed on recordings in which fast theta rhythmic activity was elicited by tail pinch and in which a slower theta rhythm persisted after cessation of the sensory stimulus. It was found that the firing of a subpopulation of SUM neurons followed the hippocampal theta waves with a constant time delay, rather than a constant phase, suggesting that during deceleration associated with a shift from sensory-elicited theta to spontaneous theta rhythm they followed a descending rhythmic input, most likely from the medial septum. Neurons of a second group, which fired at the hippocampal theta peaks, did not show such relationship demonstrating heterogeneity in the population of rhythmic SUM neurons and their possible roles in theta generation. Combined with previous studies focusing on the role of the ascending theta drive from the SUM, these results demonstrate dynamic bidirectional coupling between subcortical theta generators. Thus, during certain states, rhythmically firing SUM neurons lead the septal theta oscillator, in others the direction may reverse and SUM follows a theta drive of septal origin.