1. Neuroscience
Download icon

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
Research Article
  • Cited 4
  • Views 2,144
  • Annotations
Cite this article as: eLife 2020;9:e58321 doi: 10.7554/eLife.58321

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.

Reviewing Editor

  1. Shelly B Flagel, University of Michigan, United States

Publication history

  1. Received: April 27, 2020
  2. Accepted: September 30, 2020
  3. Accepted Manuscript published: October 1, 2020 (version 1)
  4. Version of Record published: October 30, 2020 (version 2)
  5. Version of Record updated: November 30, 2020 (version 3)

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

  • 2,144
    Page views
  • 260
    Downloads
  • 4
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

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)

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

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

Further reading

    1. Neuroscience
    Zhengchao Xu et al.
    Tools and Resources Updated

    The dorsal raphe nucleus (DR) and median raphe nucleus (MR) contain populations of glutamatergic and GABAergic neurons that regulate diverse behavioral functions. However, their whole-brain input-output circuits remain incompletely elucidated. We used viral tracing combined with fluorescence micro-optical sectioning tomography to generate a comprehensive whole-brain atlas of inputs and outputs of glutamatergic and GABAergic neurons in the DR and MR. We found that these neurons received inputs from similar upstream brain regions. The glutamatergic and GABAergic neurons in the same raphe nucleus had divergent projection patterns with differences in critical brain regions. Specifically, MR glutamatergic neurons projected to the lateral habenula through multiple pathways. Correlation and cluster analysis revealed that glutamatergic and GABAergic neurons in the same raphe nucleus received heterogeneous inputs and sent different collateral projections. This connectivity atlas further elucidates the anatomical architecture of the raphe nuclei, which could facilitate better understanding of their behavioral functions.

    1. Neuroscience
    Shankar Ramachandran et al.
    Research Article Updated

    Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here, we show that the Caenorhabditis elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.