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When faced with difficult choices, the possible outcomes are considered through a process known as deliberation. In rats, deliberation is thought to be reflected by pause-and-reorienting behaviors, better known as vicarious trial and errors (VTEs). While VTEs are thought to require medial prefrontal cortex (mPFC) and dorsal hippocampal (dHPC) interactions, no empirical evidence has yet demonstrated such a dual requirement. The nucleus reuniens (Re) of the ventral midline thalamus is anatomically connected with both the mPFC and dHPC, is required for HPC-dependent spatial memory tasks, and is critical for mPFC-dHPC neural synchronization. Currently, it is unclear if, or how, the Re is involved in deliberation. Therefore, by examining the role of the Re on VTE behaviors, we can better understand the anatomical and physiological mechanisms supporting deliberation. Here, we examined the impact of Re suppression on VTE behaviors and mPFC-dHPC theta synchrony during asymptotic performance of a HPC-dependent delayed alternation (DA) task. Pharmacological suppression of the Re increased VTE behaviors that occurred with repetitive choice errors. These errors were best characterized as perseverative behaviors, in which some rats repeatedly selected a goal arm that previously yielded no reward. We then examined the impact of Re suppression on mPFC-dHPC theta synchrony during VTEs. We found that during VTEs, Re inactivation was associated with a reduction in mPFC-dHPC theta coherence and mPFC-to-dHPC theta directionality. Our findings suggest that the Re contributes to deliberation by coordinating mPFC-dHPC neural interactions.

Spatial working memory (SWM) requires the encoding, maintenance, and retrieval of spatially relevant information to guide decision-making. The medial prefrontal cortex (mPFC) has long been implicated in the ability of rodents to perform SWM tasks. While past studies have demonstrated that mPFC ensembles reflect past and future experiences, most findings are derived from tasks that have an experimental overlap between the encoding and retrieval of trajectory specific information. In this study, we recorded single units from the mPFC of rats as they performed a T-maze delayed non-match to position (DNMP) task. This task consists of an encoding dominant sample phase, a memory maintenance delay period, and retrieval dominant choice phase. Using a linear classifier, we investigated whether distinct ensembles collectively reflect various trajectory-dependent experiences. We find that a population of high-firing rate mPFC neurons both predict a future choice and reflect changes in trajectory-dependent behaviors. We then developed a modeling procedure that estimated the number of high and low-firing rate units required to dissociate between various experiences. We find that low firing rate ensembles weakly reflect the direction that rats were forced to turn on the sample phase. This was in contrast to the highly active population that could effectively predict both future decision-making on early stem traversals and trajectory-divergences at T-junction. Finally, we compared the ensemble size necessary to code a forced trajectory to the size required to predict a decision. We provide evidence to suggest that a larger number of highly active neurons are employed during decision-making processes when compared to rewarded forced behaviors. Together, our study provides important insight into how specific ensembles of mPFC units support upcoming choices and ongoing behavior during SWM.