Phase relations of rhythmic neuronal firing in the supramammillary nucleus and mammillary body to the hippocampal theta activity in urethane anesthetized rats

Structures in the caudal diencephalon including the posterior hypothalamic nucleus, the supramammillary nucleus (SUM) and the nuclei of the mammillary body (MB) occupy a strategic position in the crossroads of ascending and descending traffic between the brainstem and the limbic forebrain (septum/hippocampus). In this study we analyzed the phase relations of rhythmically discharging SUM/MB cells to hippocampal theta rhythm in urethane anesthetized rats with a dual aim of separating different functional types of SUM and MB neurons and characterizing their coupling to septohippocampal theta oscillators. We found that rhythmically firing neurons in the SUM/MB represent a functionally heterogenous population of cells that are coupled with forebrain theta oscillators at different preferred phases. Based on their phase relations to hippocampal theta four groups of rhythmic SUM/MB cells were identified. Neurons of the first and second groups fired out-of-phase relative to each other and synchronously with the positive (8 degrees +/- 7) or negative peaks (-177 degrees +/- 7) of theta field activity in the hippocampus, recorded above the CA1 pyramidal layer. Cells of the other two groups, also forming out-of-phase counter-parts, fired on the rising (97 degrees +/- 9) or falling segments (-97 degrees +/- 6) of CA1 theta waves. The peaks in the phase distribution histogram were well separated, and the empty zones between them were wider (40-70 degrees) than those comprising the phase data for different groups. The variations of phase values for individual neurons, when tested during several theta epochs, did not exceed the range of a single group. Theta field potentials were also recorded in the SUM/MB and were advanced by one quarter of the cycle (79 degrees +/- 9, range 56-99 degrees) relative to CA1 theta oscillations. The present results indicate that, similar to other theta-generating structures, rhythmically firing neurons can be classified on the basis of their phase relations in the SUM/MB as well. Different classes of SUM/MB neurons might play different roles in generating and/or transmitting theta rhythmic activity of the limbic system.