Spatial learning strengthens hippocampal but not prefrontal influence on nucleus reuniens in rats

Coordinated interactions between the hippocampus (HC) and prefrontal cortex (PFC) that are essential for spatial navigation occur despite relatively asymmetric anatomical connectivity. The midline thalamic nucleus reuniens (RE) is reciprocally connected with both regions and has been proposed to support HC-PFC communication.

Here, we examined local and long-range neural dynamics within the HC-RE-PFC circuit while adult male rats learned to navigate a complex maze across multiple days. Using spectral power, coherence, and Granger causality analyses within linear mixed-effects models to control for locomotion.

We observed learning-related decreases in theta power across all regions, despite increased velocity with better task performance. In contrast, beta (15-30 Hz) increased in HC but decreased in RE and PFC. Notably, HC-to-RE information flow in theta, beta, and low-gamma bands increased with learning, while RE-to-HC influences decreased. Direct HC-PFC interactions remained comparatively stable, and PFC-RE beta coherence decreased with learning.

These findings reveal a dynamic reconfiguration of HC-RE-PFC network interactions during spatial learning, driven primarily by a selective increase in hippocampal, but not prefrontal, influence on RE. The directional asymmetry between HC-RE and RE-PFC pathways is inconsistent with a simple relay account and instead supports a role for RE as an active participant in spatial cognition.