Catecholaminergic modulation of meta-learning

  1. Jennifer L Cook  Is a corresponding author
  2. Jennifer C Swart
  3. Monja I Froböse
  4. Andreea Oliviana Diaconescu
  5. Dirk EM Geurts
  6. Hanneke EM den Ouden
  7. Roshan Cools
  1. University of Birmingham, United Kingdom
  2. Radboud University Nijmegen, Netherlands
  3. University of Basel, Switzerland

Abstract

The remarkable expedience of human learning is thought to be underpinned by meta-learning, whereby slow accumulative learning processes are rapidly adjusted to the current learning environment. To date, the neurobiological implementation of meta-learning remains unclear. A burgeoning literature argues for an important role for the catecholamines dopamine and noradrenaline in meta-learning. Here we tested the hypothesis that enhancing catecholamine function modulates the ability to optimise a meta-learning parameter (learning rate) as a function of environmental volatility. 102 participants completed a task which required learning in stable phases, where the probability of reinforcement was constant, and volatile phases, where probabilities changed every 10-30 trials. The catecholamine transporter blocker methylphenidate enhanced participants' ability to adapt learning rate: Under methylphenidate, compared with placebo, participants exhibited higher learning rates in volatile relative to stable phases. Furthermore, this effect was significant only with respect to direct learning based on the participants' own experience, there was no significant effect on inferred-value learning where stimulus values had to be inferred. These data demonstrate a causal link between catecholaminergic modulation and the adjustment of the meta-learning parameter learning rate.

Data availability

All raw data and analysis scripts can be accessed at the Open Science Framework data repository: https://osf.io/z59us/?view_only=0ffe62256536421489d6aeddedeb2ba6

The following data sets were generated

Article and author information

Author details

  1. Jennifer L Cook

    School of Psychology, University of Birmingham, Birmingham, United Kingdom
    For correspondence
    j.l.cook@bham.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4916-8667
  2. Jennifer C Swart

    Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0989-332X
  3. Monja I Froböse

    Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.
  4. Andreea Oliviana Diaconescu

    Department of Psychiatry, University of Basel, Basel, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3633-9757
  5. Dirk EM Geurts

    Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.
  6. Hanneke EM den Ouden

    Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    Hanneke EM den Ouden, has acted as consultant for Eleusis benefit corps but does not own shares. Eleusis have no involvement in this study.
  7. Roshan Cools

    Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    Roshan Cools, has acted as a consultant for Pfizer and Abbvie but does not own shares. Pfizer and Abbvie have no involvement in this study.

Funding

H2020 European Research Council (ERC Starting Grant 757583)

  • Jennifer L Cook

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Research talent grant 406-14-028)

  • Jennifer C Swart

University of Birmingham (Birmingham Fellows Programme)

  • Jennifer L Cook

ZonMw (92003576)

  • Dirk EM Geurts

James S. McDonnell Foundation (James McDonnell scholar award)

  • Roshan Cools

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Vici Award 53-14-005)

  • Roshan Cools

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Veni Grant 451-11-004)

  • Hanneke EM den Ouden

Swiss National Foundation (PZ00P3_167952)

  • Andreea Oliviana Diaconescu

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

Ethics

Human subjects: Human subjects: Informed consent, and consent to publish, was obtained prior to participation. The study was in line with the local ethical guidelines approved by the local ethics committee (CMO / METC Arnhem Nijmegen: protocol NL47166.091.13), pre-registered (trial register NTR4653, http://www.trialregister.nl/trialreg/admin/rctview.asp?TC=4653), and in accordance with the Helsinki Declaration of 1975.

Copyright

© 2019, Cook 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

  • 2,254
    views
  • 308
    downloads
  • 27
    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. Jennifer L Cook
  2. Jennifer C Swart
  3. Monja I Froböse
  4. Andreea Oliviana Diaconescu
  5. Dirk EM Geurts
  6. Hanneke EM den Ouden
  7. Roshan Cools
(2019)
Catecholaminergic modulation of meta-learning
eLife 8:e51439.
https://doi.org/10.7554/eLife.51439

Share this article

https://doi.org/10.7554/eLife.51439

Further reading

    1. Neuroscience
    Yisi Liu, Pu Wang ... Hongwei Zhou
    Short Report

    The increasing use of tissue clearing techniques underscores the urgent need for cost-effective and simplified deep imaging methods. While traditional inverted confocal microscopes excel in high-resolution imaging of tissue sections and cultured cells, they face limitations in deep imaging of cleared tissues due to refractive index mismatches between the immersion media of objectives and sample container. To overcome these challenges, the RIM-Deep was developed to significantly improve deep imaging capabilities without compromising the normal function of the confocal microscope. This system facilitates deep immunofluorescence imaging of the prefrontal cortex in cleared macaque tissue, extending imaging depth from 2 mm to 5 mm. Applied to an intact and cleared Thy1-EGFP mouse brain, the system allowed for clear axonal visualization at high imaging depth. Moreover, this advancement enables large-scale, deep 3D imaging of intact tissues. In principle, this concept can be extended to any imaging modality, including existing inverted wide-field, confocal, and two-photon microscopy. This would significantly upgrade traditional laboratory configurations and facilitate the study of connectomes in the brain and other tissues.

    1. Neuroscience
    Damian Koevoet, Laura Van Zantwijk ... Christoph Strauch
    Research Article

    What determines where to move the eyes? We recently showed that pupil size, a well-established marker of effort, also reflects the effort associated with making a saccade (‘saccade costs’). Here, we demonstrate saccade costs to critically drive saccade selection: when choosing between any two saccade directions, the least costly direction was consistently preferred. Strikingly, this principle even held during search in natural scenes in two additional experiments. When increasing cognitive demand experimentally through an auditory counting task, participants made fewer saccades and especially cut costly directions. This suggests that the eye-movement system and other cognitive operations consume similar resources that are flexibly allocated among each other as cognitive demand changes. Together, we argue that eye-movement behavior is tuned to adaptively minimize saccade-inherent effort.