Supramammillary Nucleus Modulates Spike-Time Coordination in the Prefrontal-Thalamo-Hippocampal Circuit during Navigation.

During navigation, hippocampal spatial maps are thought to interact with action-planning systems in other regions of cortex. We here report a key role for spike-time coordination in functional coupling of the medial prefrontal cortex (mPFC) to the hippocampus through the thalamic nucleus reuniens (NR). When rats perform a T-maze alternation task, spikes of neurons in mPFC and NR exhibit enhanced coordination to the CA1 theta rhythm before the choice point on the maze. A similar coordination to CA1 theta rhythm was observed in neurons of the supramammillary nucleus (SUM). Optogenetic silencing of SUM neurons reduced the temporal coordination in the mPFC-NR-CA1 circuit. Following SUM inactivation, trajectory representations were impaired in both NR and CA1, but not in mPFC, indicating a failure in transmission of action plans from mPFC to the hippocampus. The findings identify theta-frequency spike-time coordination as a mechanism for gating of information flow in the mPFC-NR-CA1 circuit.