Dopaminergic challenge dissociates learning from primary versus secondary sources of information

  1. Alicia I Rybicki  Is a corresponding author
  2. Sophie L Sowden
  3. Bianca Schuster
  4. Jennifer L Cook
  1. University of Birmingham, United Kingdom

Abstract

Some theories of human cultural evolution posit that humans have social-specific learning mechanisms that are adaptive specialisations moulded by natural selection to cope with the pressures of group living. However, the existence of neurochemical pathways that are specialised for learning from social information and from individual experience is widely debated. Cognitive neuroscientific studies present mixed evidence for social-specific learning mechanisms: some studies find dissociable neural correlates for social and individual learning whereas others find the same brain areas and, dopamine-mediated, computations involved in both. Here we demonstrate that, like individual learning, social learning is modulated by the dopamine D2 receptor antagonist haloperidol when social information is the primary learning source, but not when it comprises a secondary, additional element. Two groups (total N = 43) completed a decision-making task which required primary learning, from own experience, and secondary learning from an additional source. For one group the primary source was social, and secondary was individual; for the other group this was reversed. Haloperidol affected primary learning irrespective of social/individual nature, with no effect on learning from the secondary source. Thus, we illustrate that dopaminergic mechanisms underpinning learning can be dissociated along a primary-secondary but not a social-individual axis. These results resolve conflict in the literature and support an expanding field showing that, rather than being specialised for particular inputs, neurochemical pathways in the human brain can process both social and non-social cues and arbitrate between the two depending upon which cue is primarily relevant for the task at hand.

Data availability

All raw data and analysis scripts can be accessed at the Open Science Framework data repository:​​https://osf.io/398w4/?view_only=08c062a9694a4b00ac7cbc52ee333628

Article and author information

Author details

  1. Alicia I Rybicki

    Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, United Kingdom
    For correspondence
    axr783@bham.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6668-1214
  2. Sophie L Sowden

    Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9913-0515
  3. Bianca Schuster

    Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Jennifer L Cook

    Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4916-8667

Funding

Biotechnology and Biological Sciences Research Council (Midlands Integrative Biosciences Training Partnership (MIBTP) Doctoral Funding)

  • Alicia I Rybicki

H2020 European Research Council (757583 - Brain2Bee)

  • Sophie L Sowden
  • Bianca Schuster
  • Jennifer L Cook

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

Ethics

Human subjects: Informed consent was obtained from each subject. The study was in line with the local ethical guidelines approved by the local ethics committee (ERN_18_1588) and in accordance with the Helsinki Declaration of 1975.

Reviewing Editor

  1. Steve W C Chang, Yale University, United States

Version history

  1. Received: October 20, 2021
  2. Preprint posted: December 3, 2021 (view preprint)
  3. Accepted: March 14, 2022
  4. Accepted Manuscript published: March 15, 2022 (version 1)
  5. Accepted Manuscript updated: March 16, 2022 (version 2)
  6. Version of Record published: April 21, 2022 (version 3)

Copyright

© 2022, Rybicki 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

  • 1,205
    Page views
  • 129
    Downloads
  • 7
    Citations

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

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. Alicia I Rybicki
  2. Sophie L Sowden
  3. Bianca Schuster
  4. Jennifer L Cook
(2022)
Dopaminergic challenge dissociates learning from primary versus secondary sources of information
eLife 11:e74893.
https://doi.org/10.7554/eLife.74893

Share this article

https://doi.org/10.7554/eLife.74893

Further reading

    1. Neuroscience
    E Nicholas Petersen, Mahmud Arif Pavel ... Scott B Hansen
    Research Article

    Rapid conversion of force into a biological signal enables living cells to respond to mechanical forces in their environment. The force is believed to initially affect the plasma membrane and then alter the behavior of membrane proteins. Phospholipase D2 (PLD2) is a mechanosensitive enzyme that is regulated by a structured membrane-lipid site comprised of cholesterol and saturated ganglioside (GM1). Here we show stretch activation of TWIK-related K+ channel (TREK-1) is mechanically evoked by PLD2 and spatial patterning involving ordered GM1 and 4,5-bisphosphate (PIP2) clusters in mammalian cells. First, mechanical force deforms the ordered lipids, which disrupts the interaction of PLD2 with the GM1 lipids and allows a complex of TREK-1 and PLD2 to associate with PIP2 clusters. The association with PIP2 activates the enzyme, which produces the second messenger phosphatidic acid (PA) that gates the channel. Co-expression of catalytically inactive PLD2 inhibits TREK-1 stretch currents in a biological membrane. Cellular uptake of cholesterol inhibits TREK-1 currents in culture and depletion of cholesterol from astrocytes releases TREK-1 from GM1 lipids in mouse brain. Depletion of the PLD2 ortholog in flies results in hypersensitivity to mechanical force. We conclude PLD2 mechanosensitivity combines with TREK-1 ion permeability to elicit a mechanically evoked response.

    1. Developmental Biology
    2. Neuroscience
    Athina Keramidioti, Sandra Schneid ... Charles N David
    Research Article

    The Hydra nervous system is the paradigm of a ‘simple nerve net’. Nerve cells in Hydra, as in many cnidarian polyps, are organized in a nerve net extending throughout the body column. This nerve net is required for control of spontaneous behavior: elimination of nerve cells leads to polyps that do not move and are incapable of capturing and ingesting prey (Campbell, 1976). We have re-examined the structure of the Hydra nerve net by immunostaining fixed polyps with a novel antibody that stains all nerve cells in Hydra. Confocal imaging shows that there are two distinct nerve nets, one in the ectoderm and one in the endoderm, with the unexpected absence of nerve cells in the endoderm of the tentacles. The nerve nets in the ectoderm and endoderm do not contact each other. High-resolution TEM (transmission electron microscopy) and serial block face SEM (scanning electron microscopy) show that the nerve nets consist of bundles of parallel overlapping neurites. Results from transgenic lines show that neurite bundles include different neural circuits and hence that neurites in bundles require circuit-specific recognition. Nerve cell-specific innexins indicate that gap junctions can provide this specificity. The occurrence of bundles of neurites supports a model for continuous growth and differentiation of the nerve net by lateral addition of new nerve cells to the existing net. This model was confirmed by tracking newly differentiated nerve cells.