Intrinsically regulated learning is modulated by synaptic dopamine signaling

  1. Pablo Ripollés  Is a corresponding author
  2. Laura Ferreri
  3. Ernest Mas-Herrero
  4. Helena Alicart
  5. Alba Gómez-Andrés
  6. Josep Marco-Pallares
  7. Rosa Maria Antonijoan
  8. Toemme Noesselt  Is a corresponding author
  9. Marta Valle
  10. Jordi Riba
  11. Antoni Rodriguez-Fornells  Is a corresponding author
  1. New York University, United States
  2. L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Spain
  3. McGill University, Canada
  4. Universitat Autònoma de Barcelona, Spain
  5. Otto-von-Guericke University, Germany
  6. Sant Pau Institute of Biomedical Research, Spain

Abstract

We recently provided evidence that an intrinsic reward-related signal-triggered by successful learning in absence of any external feedback-modulated the entrance of new information into long-term memory via the activation of the dopaminergic midbrain, hippocampus, and ventral striatum (the SN/VTA-Hippocampal loop; Ripollés et al., 2016). Here, we used a double-blind, within-subject randomized pharmacological intervention to test whether this learning process is indeed dopamine-dependent. A group of healthy individuals completed three behavioural sessions of a language-learning task after the intake of different pharmacological treatments: a dopaminergic precursor, a dopamine receptor antagonist or a placebo. Results show that the pharmacological intervention modulated behavioral measures of both learning and pleasantness, inducing memory benefits after 24 hours only for those participants with a high sensitivity to reward. These results provide causal evidence for a dopamine-dependent mechanism instrumental in intrinsically regulated learning and further suggest that subject-specific reward sensitivity drastically alters learning success.

Data availability

Data is available via Dryad (https://dx.doi.org/10.5061/dryad.g5f7v1j)

The following data sets were generated

Article and author information

Author details

  1. Pablo Ripollés

    Department of Psychology, New York University, New York, United States
    For correspondence
    pabloripollesvidal@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8463-3723
  2. Laura Ferreri

    Cognition and Brain Plasticity Group, L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Ernest Mas-Herrero

    Montreal Neurological Institute, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Helena Alicart

    Cognition and Brain Plasticity Group, L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Alba Gómez-Andrés

    Cognition and Brain Plasticity Group, L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Josep Marco-Pallares

    Cognition and Brain Plasticity Group, L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Rosa Maria Antonijoan

    Department of Pharmacology and Therapeutics, Universitat Autònoma de Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Toemme Noesselt

    Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany
    For correspondence
    toemme@med.ovgu.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9611-9713
  9. Marta Valle

    Department of Pharmacology and Therapeutics, Universitat Autònoma de Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Jordi Riba

    Human Neuropsychopharmacology Group, Sant Pau Institute of Biomedical Research, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  11. Antoni Rodriguez-Fornells

    Cognition and Brain Plasticity Group, L'Institut d'Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain
    For correspondence
    antoni.rodriguez@icrea.cat
    Competing interests
    The authors declare that no competing interests exist.

Funding

Ministerio de Industria, Economía y Competitividad (PSI2011-29219)

  • Antoni Rodriguez-Fornells

Ministerio de Industria, Economía y Competitividad (AP2010-4179)

  • Pablo Ripollés

Morelly-Rotary Postdoctoral Fellowship

  • Laura Ferreri

Ministerio de Sanidad, Servicios Sociales e Igualdad (CP04/00 121)

  • Marta Valle

Deutsche Forschungsgemeinschaft (DFG-SFB-779/A15)

  • Toemme Noesselt

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

Ethics

Human subjects: This study was performed according to local ethics and to the Declaration of Helsinki. It was approved by the Ethics Committee of Hospital Sant Pau and by the Spanish Medicines and Medical Devices Agency (EudraCT 2016-000801-35). All participants gave informed written consent and received compensation for their participation in the study according to Spanish legislation.

Reviewing Editor

  1. Vishnu Murty, Temple University, United States

Publication history

  1. Received: May 9, 2018
  2. Accepted: August 29, 2018
  3. Accepted Manuscript published: August 30, 2018 (version 1)
  4. Version of Record published: September 11, 2018 (version 2)

Copyright

© 2018, Ripollés 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.

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  1. Pablo Ripollés
  2. Laura Ferreri
  3. Ernest Mas-Herrero
  4. Helena Alicart
  5. Alba Gómez-Andrés
  6. Josep Marco-Pallares
  7. Rosa Maria Antonijoan
  8. Toemme Noesselt
  9. Marta Valle
  10. Jordi Riba
  11. Antoni Rodriguez-Fornells
(2018)
Intrinsically regulated learning is modulated by synaptic dopamine signaling
eLife 7:e38113.
https://doi.org/10.7554/eLife.38113

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