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 relies 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)1,2,3,4,5,6,7,8 and monitors internal state via interoceptive inputs from the hypothalamus and brainstem.3,9,10,11,12,13,14 Recent studies indicate that the PVT can be subdivided into two major neuronal subpopulations, namely PVTD2(+) and PVTD2(−), which differ in genetic identity, functionality, and anatomical connectivity to other brain regions, including the NAc.4,15,16 In this study, we used fiber photometry to investigate the in vivo dynamics of these two distinct PVT neuronal types in mice performing a foraging-like behavioral task. We discovered that PVTD2(+) and PVTD2(−) neurons encode the execution and termination of goal-oriented actions, respectively. Furthermore, activity in the PVTD2(+) neuronal population mirrored motivation parameters such as vigor and satiety. Similarly, PVTD2(−) neurons also mirrored some of these parameters, but to a much lesser extent. Importantly, 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. [Display omitted] •PVTD2(+)-NAc pathway encodes the execution of goal-oriented actions•PVTD2(−)-NAc pathway encodes the termination of goal-oriented actions•The activity of PVTD2(+) neurons correlated with motivation parameters•PVTD2(−) neuronal activity correlated with motivation, but to a lesser degree Beas et al. identify two thalamo-striatal pathways, PVTD2(+)-NAc and PVTD2(−)-NAc, that display distinct in vivo dynamics throughout different times of a foraging-like task. These two pathways act synergistically, enabling the execution of specific elements needed to engage, track, and terminate rewarded goal-oriented behavior.