Incentive valence differentially engages open- and closed-loop basal ganglia circuits during movement initiation.

Overview

1. Department of Psychological and Brain Sciences, University of California, Santa Barbara, CA 93106
2. Aligning Science Across Parkinson’s Collaborative Research Network, Chevy Chase, MD 20815
3. Department of Social and Psychological Sciences, University of Huddersfield, Huddersfield HD1 3DH, United Kingdom
4. Department of Neuroscience, University of California, Berkeley, CA 94720
5. Department of Psychology and Neuroscience, Duke University, Durham, NC 27708
6. BIOPAC Systems, Inc., Goleta, CA 93117
7. Department of Medicine, College of Medicine Tucson, University of Arizona, Tucson, AZ 85724
8. Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213

Abstract

Incentives modulate voluntary movement, yet the circuitry channeling these signals into motor output remains unclear. Classical models emphasize a closed-loop circuit (CLC) linking dorsal putamen (PUTd) with the motor cortex, but this pathway is anatomically segregated from affective processing regions. Anatomical and clinical evidence point to an alternative: an open-loop circuit (OLC) from ventral putamen (PUTv) that may route affective signals to the motor cortex. Here, we conducted two experiments to test whether a functional OLC exists in humans and whether it is differentially engaged by incentive conditions. First, in 7 T resting-state fMRI (multi-echo), PUTv showed robust functional connectivity with both affective and motor regions, including the cingulate motor area, even after accounting for PUTd variance. This connectivity pattern supports the plausibility of an independent pathway linking affective basal ganglia regions to the motor cortex. Second, in 3 T task fMRI (incentivized reaching), jackpot (high-reward) and robber (high-loss avoidance) incentive conditions produced distinct behavioral and neural signatures. Jackpot produced a speed–accuracy trade-off, with faster movement initiation but more false starts. Neurally, this coincided with reduced engagement (BOLD responses relevant for initiation speed) in CLC nodes but not in OLC. Robber, in contrast, eliminated engagement in both OLC and CLC nodes, instead recruiting stopping-related regions (e.g., subthalamic nucleus), consistent with an avoidance phenomenology. Together, these findings support a versatile architecture for movement initiation that flexibly engages distinct cortico-subcortical circuits depending on incentive phenomenology, and offer a candidate mechanism through which affective salience and valence modulate voluntary movement.

Reproduced under the paper's license (CC BY), from the paper cited above.

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Data

Datasets cited

• zenodo:19243767, at Zenodo; found in “Data, Materials, and Software Availability”
• zenodo:19243768, at Zenodo; found in the references

Data, Materials, and Software Availability

Anonymized Behavior and Neural data have been deposited in Zenodo (https://doi.org/10.5281/zenodo.19243767) (70). All other data are included in the manuscript and/or SI Appendix (http://www.pnas.org/lookup/doi/10.1073/pnas.2537314123#supplementary-materials).

Reproduced under the paper's license (CC BY), from the paper cited above.

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Version 1, 28 September 2026: the first record

Recorded: type, language, journal, volume, issue, pages, dates, 15 authors, 5 keywords, 12 MeSH terms, 1 funder, 66 references.

Cite

This paper

Dundon, N. M., Rizor, E. J., Stasiak, J. E., Wang, J., Li, T., Sabugo, K., Villanueva, C., Barandon, P., Babenko, V., Beverly-Aylwin, R., Stump, A., Santander, T., Bostan, A. C., Lapate, R. C., & Grafton, S. T. (2026). Incentive valence differentially engages open- and closed-loop basal ganglia circuits during movement initiation. Proceedings of the National Academy of Sciences of the United States of America, 123(19), e2537314123. https://doi.org/10.1073/pnas.2537314123

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