Reuniens-hippocampus synchronization is required for successful navigation and decision making

The reciprocal connectivity of the nucleus reuniens (RE) of the ventral midline thalamus with the prefrontal cortex (PFC) and hippocampus (HC) is suggestive of the RE being a critical node within a large-scale brain network underlying spatial cognition. The RE activity has been implicated in navigation, decision making, and spatial memory consolidation. We have previously shown that the RE activity is critical for the retrieval of spatial memory. Yet, the network mechanisms of the RE contribution to the extended prefrontal-thalamo-hippocampal circuit remain to be explored. It has been suggested that the RE facilitates cross-regional communication by synchronizing the PFC-HPC network. To test this hypothesis, we simultaneously recorded local field potentials (LFPs) from rat RE, PFC, and HC while the animals learned a spatial task: Rats were trained to find a fixed reward location in a complex crossword maze with multiple decision points and dead ends over the span of seven days. The LFP-based analysis on cross-regional interaction revealed a strong HC-RE synchronization of the theta (7-12 Hz) and beta (15-25 Hz) bands during the task. Specifically, HC-RE beta coherence gradually increased across training sessions, while theta coherence remained stable. Remarkably, a transient reduction of the HC-RE beta coherence was associated with navigation errors and “vicarious trial-and-error” (VTE), a behavioral marker for indecision or the consideration of options. Our findings support the role of HC-RE synchronization in successful navigation and decision making.