Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat.

We examined the activity of single cells of the supramammillary nucleus (SUM), the mammillary body (MB), and adjacent regions of the diencephalon with respect to the hippocampal electroencephalogram (EEG) in urethane-anesthetized rats. Twenty-nine of 170 cells were found to discharge synchronously with the theta rhythm of the hippocampus (theta-related neurons). All of the 29 theta-related cells were localized to the SUM or MB. A subset of theta-related cells of SUM and MB discharged in short-duration bursts comparable to the pyramidal complex spike cells of the hippocampus. In contrast to hippocampal complex spikes, however, which predominantly exhibit this mode of firing during non-theta states, the burst firing of SUM/MB cells was strongly correlated with the theta rhythm. The proportion of bursting neurons was higher in MB than in SUM. Using partial coherence analysis, we examined the relationship between SUM/MB theta-related cells and the two generators of theta of the dorsal hippocampus. The theta-related cells of MB showed a stronger correlation with "CA1" than with "dentate" theta, whereas no such asymmetry was found in the relationship between neuronal firing of SUM cells and the two generators of theta in the hippocampus. The foregoing suggests that the theta-related cells of MB are driven by descending projections from the hippocampal formation (CA1), whereas those of the SUM are not. The SUM and MB are intimately connected with the hippocampal formation--the SUM mainly via ascending projections to the dentate gyrus, and the MB via direct descending projections from the subiculum. Theta-related SUM/MB cells may be directly involved in the generation of theta and/or the transfer of theta rhythmicity to various parts of the limbic system and forebrain.