The Ventral Midline Thalamus Mediates Successful Deliberation by Coordinating Prefrontal and Hippocampal Neural Activity

Abstract

AbstractWhen faced with difficult choices, the possible outcomes are considered through a process known as deliberation. In rats, deliberation can 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 work has 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 well-learned performance of a HPC-dependent delayed alternation (DA) task. Pharmacological suppression of the Re increased VTE behaviors that resulted in erroneous choices. These errors were best characterized as perseverative behaviors, where at the decision-point, some rats repeatedly turned in the direction that previously yielded no reward, while simultaneously deliberating. These ‘failed’ deliberations were associated with a reduction in mPFC-dHPC theta coherence at the choice-point. Importantly, the reduction in mPFC-dHPC theta synchrony observed during VTE behaviors was almost entirely driven by Re-suppression induced changes to the mPFC theta oscillation. Our findings suggest that the Re is important for successful deliberation, and mPFC-dHPC interactions, by coordinating local theta oscillations in the mPFC.