Hippocampal-prefrontal communication subspaces align with behavioral and network patterns in a spatial memory task.

Rhythmic network states have been theorized to facilitate communication between brain regions, but how these oscillations influence communication subspaces, i.e. the low-dimensional neural activity patterns that mediate inter-regional communication, and in turn how subspaces impact behavior remains unclear. Using a spatial memory task in rats (male Long-Evans rats), we simultaneously recorded ensembles from hippocampal CA1 and the prefrontal cortex (PFC) to address this question. We found that task behaviors best aligned with low-dimensional, shared subspaces between these regions, rather than local activity in either region. Critically, both network oscillations and speed modulated the structure and performance of this communication subspace. To understand the communication space, we visualized shared CA1-PFC communication geometry using manifold techniques and found ring-like structures. We hypothesize that these shared activity manifolds are utilized to mediate the task behavior. These findings suggest that memory-guided behaviors are driven by shared CA1-PFC interactions that are dynamically modulated by oscillatory states, offering a novel perspective on the interplay between rhythms and behaviorally relevant neural communication. This study reveals that shared communication subspaces between the hippocampus and prefrontal cortex are aligned with both behavioral patterns and network oscillations during a spatial memory task. We demonstrate that these shared subspaces robustly predict task behavior, while local activity in either region alone does not. The organization of these task subspaces into differing manifolds demonstrates task information in interregional coordination, thought to be critical for memory-guided behavior. Moreover, our findings highlight the significance of theta power in modulating these communication dynamics. These insights provide a deeper understanding of the interregional neural mechanisms underlying mnemonic and behavioral processes, which are of broad interest to the neuroscience community.