Dissociable encoding of motivated behavior by parallel thalamo-striatal projections

Sofia Beas; Isbah Khan; Claire Gao; Gabriel Loewinger; Emma Macdonald; Alison Bashford; Shakira Rodriguez-Gonzalez; Francisco Pereira; Mario A Penzo

doi:10.1016/j.cub.2024.02.037

Dissociable encoding of motivated behavior by parallel thalamo-striatal projections

Curr Biol. 2024 Apr 8;34(7):1549-1560.e3. doi: 10.1016/j.cub.2024.02.037. Epub 2024 Mar 7.

Authors

Sofia Beas¹, Isbah Khan², Claire Gao², Gabriel Loewinger³, Emma Macdonald², Alison Bashford², Shakira Rodriguez-Gonzalez², Francisco Pereira³, Mario A Penzo⁴

Affiliations

¹ Unit on the Neurobiology of Affective Memory, National Institute of Mental Health, Convent Drive, Bethesda, MD 20892, USA; Department of Neurobiology, University of Alabama at Birmingham, University Boulevard, Birmingham, AL 35294, USA. Electronic address: sbeas@uab.edu.
² Unit on the Neurobiology of Affective Memory, National Institute of Mental Health, Convent Drive, Bethesda, MD 20892, USA.
³ Machine Learning Team, National Institute of Mental Health, Convent Drive, Bethesda, MD 20892, USA.
⁴ Unit on the Neurobiology of Affective Memory, National Institute of Mental Health, Convent Drive, Bethesda, MD 20892, USA. Electronic address: mario.penzo@nih.gov.

PMID: 38458192
PMCID: PMC11003833 (available on 2025-04-08)
DOI: 10.1016/j.cub.2024.02.037

Abstract

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 PVT^D2(+) and PVT^D2(-), 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 PVT^D2(+) and PVT^D2(-) neurons encode the execution and termination of goal-oriented actions, respectively. Furthermore, activity in the PVT^D2(+) neuronal population mirrored motivation parameters such as vigor and satiety. Similarly, PVT^D2(-) 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.

Keywords: FLMM analysis; food-seeking; goal termination; motivation; nucleus accumbens; paraventricular nucleus of the thalamus; reward approach.

MeSH terms

Animals
Hypothalamus
Mice
Midline Thalamic Nuclei / physiology
Motivation*
Nucleus Accumbens* / physiology
Thalamus

Abstract

MeSH terms

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