Pausing and reorienting behaviors enhance the performance of a spatial working memory task.

During spatial working memory tasks, animals need to retain information about a previous trial in order to successfully select their next trajectory. Specifically, the delayed non-match to position task requires rats to follow a cued sample trajectory, then select the opposite route after a delay period. When faced with this choice, rats will occasionally exhibit complex behaviors, such as pausing and sweeping their head back and forth. These behaviors, called vicarious trial and error (VTE), are thought to be a behavioral manifestation of deliberation. However, we identified similarly complex behaviors during sample-phase traversals, despite the fact that these laps do not require a decision. First, we identified that these behaviors occurred more often after incorrect trials than before them, indicating that rats are retaining information between trials. Next, we determined that these pause-and-reorient (PAR) behaviors increased the likelihood of the next choice being selected correctly, suggesting that these behaviors assist the rat in successful task performance. Finally, we identified similarities between PARs and choice-phase VTEs, suggesting that VTEs may not only be reflective of deliberation, but may also contribute to a strategy for successful performance of spatial working memory tasks.

The ventral midline thalamus coordinates prefrontal-hippocampal neural synchrony during vicarious trial and error.

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.