Dopamine promotes instrumental motivation, but reduces reward-related vigour

  1. John P Grogan  Is a corresponding author
  2. Timothy R Sandhu
  3. Michele T Hu
  4. Sanjay G Manohar
  1. University of Oxford, United Kingdom
  2. University of Cambridge, United Kingdom

Abstract

We can be motivated when reward depends on performance, or merely by the prospect of a guaranteed reward. Performance-dependent (contingent) reward is instrumental, relying on an internal action-outcome model, whereas motivation by guaranteed reward may minimise opportunity cost in reward-rich environments. Competing theories propose that each type of motivation should be dependent on dopaminergic activity. We contrasted these two types of motivation with a rewarded saccade task, in patients with Parkinson’s disease (PD). When PD patients were ON dopamine, they had greater response vigour (peak saccadic velocity residuals) for contingent rewards, whereas when PD patients were OFF medication, they had greater vigour for guaranteed rewards. These results support the view that reward expectation and contingency drive distinct motivational processes, and can be dissociated by manipulating dopaminergic activity. We posit that dopamine promotes goal-directed motivation, but dampens reward-driven vigour, contradictory to the prediction that increased tonic dopamine amplifies reward expectation

Data availability

Anonymised data are available on OSF (https://osf.io/2k6x3)

The following data sets were generated

Article and author information

Author details

  1. John P Grogan

    Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford, United Kingdom
    For correspondence
    john.grogan@ndcn.ox.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0463-8904
  2. Timothy R Sandhu

    Department of Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
  3. Michele T Hu

    Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford, United Kingdom
    Competing interests
    Michele T Hu, MTH is a consultant advisor to the Roche Prodromal Advisory, Biogen Digital Advisory Board, Evidera, and CuraSen Therapeutics, Inc..
  4. Sanjay G Manohar

    Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0735-4349

Funding

MRC (MR/P00878X)

  • Sanjay G Manohar

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Ethical approval was granted by the South Central Oxford A REC (18/SC/0448). All participants gave written informed consent.

Copyright

© 2020, Grogan et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 5,931
    views
  • 415
    downloads
  • 26
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. John P Grogan
  2. Timothy R Sandhu
  3. Michele T Hu
  4. Sanjay G Manohar
(2020)
Dopamine promotes instrumental motivation, but reduces reward-related vigour
eLife 9:e58321.
https://doi.org/10.7554/eLife.58321

Share this article

https://doi.org/10.7554/eLife.58321

Further reading

    1. Neuroscience
    Agnieszka Glica, Katarzyna Wasilewska ... Katarzyna Jednoróg
    Research Article

    The neural noise hypothesis of dyslexia posits an imbalance between excitatory and inhibitory (E/I) brain activity as an underlying mechanism of reading difficulties. This study provides the first direct test of this hypothesis using both electroencephalography (EEG) power spectrum measures in 120 Polish adolescents and young adults (60 with dyslexia, 60 controls) and glutamate (Glu) and gamma-aminobutyric acid (GABA) concentrations from magnetic resonance spectroscopy (MRS) at 7T MRI scanner in half of the sample. Our results, supported by Bayesian statistics, show no evidence of E/I balance differences between groups, challenging the hypothesis that cortical hyperexcitability underlies dyslexia. These findings suggest that alternative mechanisms must be explored and highlight the need for further research into the E/I balance and its role in neurodevelopmental disorders.

    1. Neuroscience
    Paul I Jaffe, Gustavo X Santiago-Reyes ... Russell A Poldrack
    Research Article

    Evidence accumulation models (EAMs) are the dominant framework for modeling response time (RT) data from speeded decision-making tasks. While providing a good quantitative description of RT data in terms of abstract perceptual representations, EAMs do not explain how the visual system extracts these representations in the first place. To address this limitation, we introduce the visual accumulator model (VAM), in which convolutional neural network models of visual processing and traditional EAMs are jointly fitted to trial-level RTs and raw (pixel-space) visual stimuli from individual subjects in a unified Bayesian framework. Models fitted to large-scale cognitive training data from a stylized flanker task captured individual differences in congruency effects, RTs, and accuracy. We find evidence that the selection of task-relevant information occurs through the orthogonalization of relevant and irrelevant representations, demonstrating how our framework can be used to relate visual representations to behavioral outputs. Together, our work provides a probabilistic framework for both constraining neural network models of vision with behavioral data and studying how the visual system extracts representations that guide decisions.