Dissociable encoding of motivated behavior by parallel thalamo-striatal projections

The successful pursuit of goals requires the coordinated execution and termination of actions that lead to positive outcomes. This process is thought to rely on motivational states that are guided by internal drivers, such as hunger or fear. However, the mechanisms by which the brain tracks motivational states to shape instrumental actions are not fully understood. The paraventricular nucleus of the thalamus (PVT) is a midline thalamic nucleus that shapes motivated behaviors via its projections to the nucleus accumbens (NAc)(1–9) and monitors internal state via interoceptive inputs from the hypothalamus and brainstem(10–14). Recent studies have revealed two major PVT neuronal subpopulations, Type1(PVT) and Type2(PVT), which differ in genetic identity, functionality, and anatomical connectivity to other brain regions, including the NAc(15–17). In this study, we used fiber photometry to investigate the in vivo dynamics of these two distinct PVT neuronal types in mice performing a reward foraging task. We discovered that Type1(PVT) and Type2(PVT) neurons encode the execution and termination of goal-oriented actions, respectively. Furthermore, unlike Type2(PVT) cells, activity in the Type1(PVT) neuronal population mirrored motivation parameters such as vigor and satiety. Interestingly, these features were largely preserved when activity in PVT projections to the NAc was selectively assessed. Collectively, our results highlight the existence of two parallel thalamo-striatal projections that participate in the dynamic regulation of goal pursuits and provide insight into the mechanisms by which the brain tracks motivational states to shape instrumental actions.