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

  • 2,221
    views
  • 300
    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
    Vincent Huson, Wade G Regehr
    Research Article

    Unipolar brush cells (UBCs) are excitatory interneurons in the cerebellar cortex that receive mossy fiber (MF) inputs and excite granule cells. The UBC population responds to brief burst activation of MFs with a continuum of temporal transformations, but it is not known how UBCs transform the diverse range of MF input patterns that occur in vivo. Here, we use cell-attached recordings from UBCs in acute cerebellar slices to examine responses to MF firing patterns that are based on in vivo recordings. We find that MFs evoke a continuum of responses in the UBC population, mediated by three different types of glutamate receptors that each convey a specialized component. AMPARs transmit timing information for single stimuli at up to 5 spikes/s, and for very brief bursts. A combination of mGluR2/3s (inhibitory) and mGluR1s (excitatory) mediates a continuum of delayed, and broadened responses to longer bursts, and to sustained high frequency activation. Variability in the mGluR2/3 component controls the time course of the onset of firing, and variability in the mGluR1 component controls the duration of prolonged firing. We conclude that the combination of glutamate receptor types allows each UBC to simultaneously convey different aspects of MF firing. These findings establish that UBCs are highly flexible circuit elements that provide diverse temporal transformations that are well suited to contribute to specialized processing in different regions of the cerebellar cortex.

    1. Neuroscience
    Choongheon Lee, Mohammad Shokrian ... Jong-Hoon Nam
    Research Article

    We hypothesized that active outer hair cells drive cochlear fluid circulation. The hypothesis was tested by delivering the neurotoxin, kainic acid, to the intact round window of young gerbil cochleae while monitoring auditory responses in the cochlear nucleus. Sounds presented at a modest level significantly expedited kainic acid delivery. When outer-hair-cell motility was suppressed by salicylate, the facilitation effect was compromised. A low-frequency tone was more effective than broadband noise, especially for drug delivery to apical locations. Computational model simulations provided the physical basis for our observation, which incorporated solute diffusion, fluid advection, fluid–structure interaction, and outer-hair-cell motility. Active outer hair cells deformed the organ of Corti like a peristaltic tube to generate apically streaming flows along the tunnel of Corti and basally streaming flows along the scala tympani. Our measurements and simulations coherently suggest that active outer hair cells in the tail region of cochlear traveling waves drive cochlear fluid circulation.