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Distinct regions of the striatum underlying effort, movement initiation and effort discounting

Abstract

The ventral striatum is believed to encode the subjective value of cost–benefit options; however, this effect has notably been absent during choices that involve physical effort. Previous work in freely moving animals has revealed opposing striatal signals, with greater response to increasing effort demands and reduced responses to rewards requiring effort. Yet, the relationship between these conflicting signals remains unknown. Using functional magnetic resonance imaging with a naturalistic maze-navigation paradigm, we identified functionally segregated regions within the ventral striatum that separately encoded effort activation, movement initiation and effort discounting of rewards. In addition, activity in regions associated with effort activation and discounting oppositely predicted striatal encoding of effort during effort-based decision-making. Our results suggest that the dorsomedial region hitherto associated with action may instead represent the cost of effort and raise fundamental questions regarding the interpretation of striatal ‘reward’ signals in the context of effort demands. This has implications for uncovering the neural architecture underlying motivated behaviour.

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Fig. 1: Maze-navigation task schematic and whole-brain results (N = 29).
Fig. 2: Maze-navigation task ROI analyses and results (N = 29).
Fig. 3: Functional segregation of striatum, and comparison of connectivity profiles with previously identified striatal parcellation based on intrinsic connectivity.
Fig. 4: Schematic and results of effort-based decision-making task (N = 19).
Fig. 5: Cross-paradigm analyses (N = 19).

Data availability

Contrast maps of fMRI data that support the findings of this study are available on NeuroVault (https://neurovault.org/collections/LLQYKRMV/). Other data are available from the corresponding author upon request.

Code availability

Custom code that supports the findings of this study is available from the corresponding author upon request.

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Acknowledgements

This work was supported by funding from the NIMH R00 MH102355 and R01 MH108605 to M.T.T. and F32 MH115692 to J.A.C. and the National Science Foundation Graduate Research Fellowship Program DGE- 1444932 to A.R.A. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank J. Buckholtz and D. Dilks for helpful discussion and commentary. We also thank B. DeVries, M. Nuutinen, E. Hahn, D. Harrison, A. Lu, M. Rehman, J. Yang, K. Kwok, S. Han and N. Ahad for their assistance in data collection.

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S.S. wrote the first draft of the paper; S.S. and M.T.T. designed the research; S.S. performed the research; S.S., V.M.L., J.A.C., A.R.A. and M.T.T. analysed the data; S.S., V.M.L., J.A.C., A.R.A. and M.T.T. wrote the paper.

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Correspondence to Michael T. Treadway.

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The authors report no conflicts of interest, financial or otherwise. In the past three years, M.T.T. has served as a paid consultant to Blackthorn Therapeutics and Avanir Pharmaceuticals. None of these entities supported the current work, and all views expressed herein are solely those of the authors.

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Suzuki, S., Lawlor, V.M., Cooper, J.A. et al. Distinct regions of the striatum underlying effort, movement initiation and effort discounting. Nat Hum Behav 5, 378–388 (2021). https://doi.org/10.1038/s41562-020-00972-y

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