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Two spatiotemporally distinct value systems shape reward-based learning in the human brain

Author

Listed:
  • Elsa Fouragnan

    (Institute of Neuroscience & Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK)

  • Chris Retzler

    (Institute of Neuroscience & Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK
    University of Huddersfield)

  • Karen Mullinger

    (Sir Peter Mansfield Magnetic Resonance Center, School of Physics and Astronomy, University of Nottingham
    Birmingham University Imaging Centre, School of Psychology, University of Birmingham)

  • Marios G. Philiastides

    (Institute of Neuroscience & Psychology, University of Glasgow, 58 Hillhead Street, Glasgow G12 8QB, UK)

Abstract

Avoiding repeated mistakes and learning to reinforce rewarding decisions is critical for human survival and adaptive actions. Yet, the neural underpinnings of the value systems that encode different decision-outcomes remain elusive. Here coupling single-trial electroencephalography with simultaneously acquired functional magnetic resonance imaging, we uncover the spatiotemporal dynamics of two separate but interacting value systems encoding decision-outcomes. Consistent with a role in regulating alertness and switching behaviours, an early system is activated only by negative outcomes and engages arousal-related and motor-preparatory brain structures. Consistent with a role in reward-based learning, a later system differentially suppresses or activates regions of the human reward network in response to negative and positive outcomes, respectively. Following negative outcomes, the early system interacts and downregulates the late system, through a thalamic interaction with the ventral striatum. Critically, the strength of this coupling predicts participants’ switching behaviour and avoidance learning, directly implicating the thalamostriatal pathway in reward-based learning.

Suggested Citation

  • Elsa Fouragnan & Chris Retzler & Karen Mullinger & Marios G. Philiastides, 2015. "Two spatiotemporally distinct value systems shape reward-based learning in the human brain," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9107
    DOI: 10.1038/ncomms9107
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    Cited by:

    1. Chen Qu & Elise Météreau & Luigi Butera & Marie Claire Villeval & Jean-Claude Dreher & Matthew Rushworth, 2019. "Neurocomputational mechanisms at play when weighing concerns for extrinsic rewards, moral values, and social image," Post-Print halshs-02193425, HAL.
    2. M. A. Pisauro & E. F. Fouragnan & D. H. Arabadzhiyska & M. A. J. Apps & M. G. Philiastides, 2022. "Neural implementation of computational mechanisms underlying the continuous trade-off between cooperation and competition," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Elsa F. Fouragnan & Billy Hosking & Yin Cheung & Brooke Prakash & Matthew Rushworth & Alejandra Sel, 2024. "Timing along the cardiac cycle modulates neural signals of reward-based learning," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Johannes Algermissen & Jennifer C. Swart & René Scheeringa & Roshan Cools & Hanneke E. M. den Ouden, 2024. "Prefrontal signals precede striatal signals for biased credit assignment in motivational learning biases," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. Tarryn Balsdon & M. Andrea Pisauro & Marios G. Philiastides, 2024. "Distinct basal ganglia contributions to learning from implicit and explicit value signals in perceptual decision-making," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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