Supramammillary Theta Oscillations in Water Maze Learning

The supramammillary nucleus (SuM) in the hypothalamus, in conjunction with the hippocampus (HPC), has been implicated through theta oscillations in various brain functions ranging from locomotion to learning and memory. While the indispensable role of the SuM in HPC theta generation in anesthetized animals is well-characterized, the SuM is not always necessary for HPC theta in awake animals. This raises questions on the precise behavioral relevance of SuM theta activity and its interaction with HPC theta activity. We used simultaneously recorded SuM and HPC local field potentials (LFPs) in a one-day water maze (WM) learning paradigm in rats (n = 8), to show that theta activities recorded from the SuM itself were not positively correlated with locomotor (swimming) speed nor acceleration, but the individual relationship between acceleration and SuM theta frequency is correlated with WM learning rates. In contrast, we found that SuM-HPC theta phase coherence is strongly correlated with swimming speed and acceleration, but these do not relate to WM learning. SuM-HPC-directed coherence analysis demonstrated no swimming kinetics nor learning rate associations, but revealed that periods of high SuM-HPC theta phase coherence are driven by the SuM at relatively low (~6.2 Hz) frequencies. Additionally, we demonstrate that the SuM and the HPC also engage in non-random, non-coherent phase coupling modes where either structure preferentially displays a ± 2 Hz difference with the other. Our data indicate SuM theta LFPs do not appear to be related to either speed coding or spatial learning in swimming rats and display non-random out-of-phase theta frequency coupling with the HPC.