Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

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.

References

  1. Bartra, O., McGuire, J. T. & Kable, J. W. The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage 76, 412–427 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Mogenson, G. J., Jones, D. L. & Yim, C. Y. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 14, 69–97 (1980).

    Article  CAS  PubMed  Google Scholar 

  3. Knutson, B., Delgado, M. R. & Phillips, P. E. in Neuroeconomics: Decision Making and the Brain (eds Glimcher, P. W., Fehr, E., Camerer, C., & Poldrack, R. A.) 389–406 (Academic Press, 2009).

  4. Berke, J. D. What does dopamine mean? Nat. Neurosci. 21, 787–793 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Berridge, K. C. & Robinson, T. E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 28, 309–369 (1998).

    Article  CAS  PubMed  Google Scholar 

  6. Schultz, W., Carelli, R. M. & Wightman, R. M. Phasic dopamine signals: from subjective reward value to formal economic utility. Curr. Opin. Behav. Sci. 5, 147–154 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Salamone, J. D., Correa, M., Farrar, A. & Mingote, S. M. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 191, 461–482 (2007).

    Article  CAS  PubMed  Google Scholar 

  8. Wise, R. A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483–494 (2004).

    Article  CAS  PubMed  Google Scholar 

  9. McClure, S. M., Laibson, D. I., Loewenstein, G. & Cohen, J. D. Separate neural systems value immediate and delayed monetary rewards. Science 306, 503–507 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Wittmann, M., Leland, D. S. & Paulus, M. P. Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Exp. Brain Res. 179, 643–653 (2007).

    Article  PubMed  Google Scholar 

  11. Gregorios-Pippas, L., Tobler, P. N. & Schultz, W. Short term temporal discounting of reward value in human ventral striatum. J. Neurophysiol. 101, 1507–1523 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kable, J. W. & Glimcher, P. W. The neural correlates of subjective value during intertemporal choice. Nat. Neurosci. 10, 1625–1633 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Peters, J. & Büchel, C. Overlapping and distinct neural systems code for subjective value during intertemporal and risky decision making. J. Neurosci. 29, 15727–15734 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Prévost, C., Pessiglione, M., Météreau, E., Cléry-Melin, M.-L. & Dreher, J.-C. Separate valuation subsystems for delay and effort decision costs. J. Neurosci. 30, 14080–14090 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Abler, B., Walter, H., Erk, S., Kammerer, H. & Spitzer, M. Prediction error as a linear function of reward probability is coded in human nucleus accumbens. Neuroimage 31, 790–795 (2006).

    Article  PubMed  Google Scholar 

  16. Yacubian, J. et al. Dissociable systems for gain-and loss-related value predictions and errors of prediction in the human brain. J. Neurosci. 26, 9530–9537 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Levy, D. J. & Glimcher, P. W. The root of all value: a neural common currency for choice. Curr. Opin. Neurobiol. 22, 1027–1038 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Croxson, P. L., Walton, M. E., O’Reilly, J. X., Behrens, T. E. & Rushworth, M. F. Effort-based cost–benefit valuation and the human brain. J. Neurosci. 29, 4531–4541 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kurniawan, I. T. et al. Choosing to make an effort: the role of striatum in signaling physical effort of a chosen action. J. Neurophysiol. 104, 313–321 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Schmidt, L., Lebreton, M., Cléry-Melin, M.-L., Daunizeau, J. & Pessiglione, M. Neural mechanisms underlying motivation of mental versus physical effort. PLoS Biol. 10, e1001266 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Burke, C. J., Brünger, C., Kahnt, T., Park, S. Q. & Tobler, P. N. Neural integration of risk and effort costs by the frontal pole: only upon request. J. Neurosci. 33, 1706–1713 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kurniawan, I. T., Guitart-Masip, M., Dayan, P. & Dolan, R. J. Effort and valuation in the brain: the effects of anticipation and execution. J. Neurosci. 33, 6160–6169 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Skvortsova, V., Palminteri, S. & Pessiglione, M. Learning to minimize efforts versus maximizing rewards: computational principles and neural correlates. J. Neurosci. 34, 15621–15630 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Massar, S. A., Libedinsky, C., Weiyan, C., Huettel, S. A. & Chee, M. W. Separate and overlapping brain areas encode subjective value during delay and effort discounting. Neuroimage 120, 104–113 (2015).

    Article  PubMed  Google Scholar 

  25. Scholl, J. et al. The good, the bad, and the irrelevant: neural mechanisms of learning real and hypothetical rewards and effort. J. Neurosci. 35, 11233–11251 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bonnelle, V., Manohar, S., Behrens, T. & Husain, M. Individual differences in premotor brain systems underlie behavioral apathy. Cereb. Cortex 26, 807–819 (2015).

    PubMed  PubMed Central  Google Scholar 

  27. Klein-Flügge, M. C., Kennerley, S. W., Friston, K. & Bestmann, S. Neural signatures of value comparison in human cingulate cortex during decisions requiring an effort-reward trade-off. J. Neurosci. 36, 10002–10015 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Chong, T. T.-J. et al. Neurocomputational mechanisms underlying subjective valuation of effort costs. PLoS Biol. 15, e1002598 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Hauser, T. U., Eldar, E. & Dolan, R. J. Separate mesocortical and mesolimbic pathways encode effort and reward learning signals. Proc. Natl Acad. Sci. USA 114, E7395–E7404 (2017).

    Article  CAS  PubMed  Google Scholar 

  30. Arulpragasam, A. R., Cooper, J. A., Nuutinen, M. R. & Treadway, M. T. Corticoinsular circuits encode subjective value expectation and violation for effortful goal-directed behavior. Proc. Natl Acad. Sci. USA 115, E5233–E5242 (2018).

    Article  CAS  PubMed  Google Scholar 

  31. Aridan, N., Malecek, N. J., Poldrack, R. A. & Schonberg, T. Neural correlates of effort-based valuation with prospective choices. Neuroimage 185, 446–454 (2019).

    Article  PubMed  Google Scholar 

  32. Endepols, H. et al. Effort-based decision making in the rat: an [18F]fluorodeoxyglucose micro positron emission tomography study. J. Neurosci. 30, 9708–9714 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Cousins, M. S. & Salamone, J. D. Nucleus accumbens dopamine depletions in rats affect relative response allocation in a novel cost/benefit procedure. Pharmacol. Biochem. Behav. 49, 85–91 (1994).

    Article  CAS  PubMed  Google Scholar 

  34. Floresco, S. B. The nucleus accumbens: an interface between cognition, emotion, and action. Annu. Rev. Psychol. 66, 25–52 (2015).

    Article  PubMed  Google Scholar 

  35. da Silva, J. A., Tecuapetla, F., Paixão, V. & Costa, R. M. Dopamine neuron activity before action initiation gates and invigorates future movements. Nature 554, 244–248 (2018).

    Article  PubMed  CAS  Google Scholar 

  36. Day, J. J., Jones, J. L., Wightman, R. M. & Carelli, R. M. Phasic nucleus accumbens dopamine release encodes effort-and delay-related costs. Biol. Psychiatry 68, 306–309 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Hamid, A. A. et al. Mesolimbic dopamine signals the value of work. Nat. Neurosci. 19, 117–126 (2016).

    Article  CAS  PubMed  Google Scholar 

  38. Syed, E. C. et al. Action initiation shapes mesolimbic dopamine encoding of future rewards. Nat. Neurosci. 19, 34–39 (2016).

    Article  CAS  PubMed  Google Scholar 

  39. Lau, B. & Glimcher, P. W. Action and outcome encoding in the primate caudate nucleus. J. Neurosci. 27, 14502–14514 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Samejima, K., Ueda, Y., Doya, K. & Kimura, M. Representation of action-specific reward values in the striatum. Science 310, 1337–1340 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Zaborszky, L. et al. Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14, 427–453 (1985).

    Article  CAS  PubMed  Google Scholar 

  42. Penner, M. R. & Mizumori, S. J. Neural systems analysis of decision making during goal-directed navigation. Prog. Neurobiol. 96, 96–135 (2012).

    Article  PubMed  Google Scholar 

  43. Di Chiara, G. et al. Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47, 227–241 (2004).

    Article  PubMed  CAS  Google Scholar 

  44. Van Der Plasse, G., Schrama, R., Van Seters, S. P., Vanderschuren, L. J. & Westenberg, H. G. Deep brain stimulation reveals a dissociation of consummatory and motivated behaviour in the medial and lateral nucleus accumbens shell of the rat. PLoS ONE 7, e33455 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Parkinson, J. A., Willoughby, P. J., Robbins, T. W. & Everitt, B. J. Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical–ventral striatopallidal systems. Behav. Neurosci. 114, 42–63 (2000).

    Article  CAS  PubMed  Google Scholar 

  46. Ko, D. & Wanat, M. J. Phasic dopamine transmission reflects initiation vigor and exerted effort in an action-and region-specific manner. J. Neurosci. 36, 2202–2211 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Choi, E. Y., Yeo, B. T. & Buckner, R. L. The organization of the human striatum estimated by intrinsic functional connectivity. J. Neurophysiol. 108, 2242–2263 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Haber, S. N. & Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26 (2010).

    Article  PubMed  Google Scholar 

  49. Haber, S. N., Kim, K.-S., Mailly, P. & Calzavara, R. Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J. Neurosci. 26, 8368–8376 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Engelhard, B. et al. Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. Nature 570, 509–513 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Gorgolewski, K. J. et al. A high resolution 7-Tesla resting-state fMRI test-retest dataset with cognitive and physiological measures. Sci. Data 2, 140054 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Howe, M. W., Tierney, P. L., Sandberg, S. G., Phillips, P. E. & Graybiel, A. M. Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 500, 575–579 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Roesch, M. R., Singh, T., Brown, P. L., Mullins, S. E. & Schoenbaum, G. Ventral striatal neurons encode the value of the chosen action in rats deciding between differently delayed or sized rewards. J. Neurosci. 29, 13365–13376 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hall, J., Parkinson, J. A., Connor, T. M., Dickinson, A. & Everitt, B. J. Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur. J. Neurosci. 13, 1984–1992 (2001).

    Article  CAS  PubMed  Google Scholar 

  55. Sonkusare, S., Breakspear, M. & Guo, C. Naturalistic stimuli in neuroscience: critically acclaimed. Trends Cogn. Sci. 23, 699–714 (2019).

    Article  PubMed  Google Scholar 

  56. Van Essen, D. C. et al. The WU-Minn human connectome project: an overview. Neuroimage 80, 62–79 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Esterman, M., Tamber-Rosenau, B. J., Chiu, Y.-C. & Yantis, S. Avoiding non-independence in fMRI data analysis: leave one subject out. Neuroimage 50, 572–576 (2010).

    Article  PubMed  Google Scholar 

  58. Pedregosa, F. et al. Scikit-learn: machine learning in Python. J. Mach. Learn. Res. 12, 2825–2830 (2011).

    Google Scholar 

  59. Ojala, M. & Garriga, G. C. Permutation tests for studying classifier performance. J. Mach. Learn. Res. 11, 1833–1863 (2010).

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Michael T. Treadway.

Ethics declarations

Competing interests

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.

Additional information

Peer review information Primary Handling Editor: Jamie Horder.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2 and Supplementary Figs. 1–3.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41562-020-00972-y

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing