Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex

  1. Saeedeh Hashemnia
  2. David R Euston
  3. Aaron J Gruber  Is a corresponding author
  1. University of Lethbridge, Canada

Abstract

Psychostimulants such as d-amphetamine (AMPH) often have behavioral effects that appear paradoxical within the framework of optimal choice theory. AMPH typically increases task engagement and the effort animals exert for reward, despite decreasing reward valuation. We investigated neural correlates of this phenomenon in the anterior cingulate cortex (ACC), a brain structure implicated in signaling cost-benefit utility. AMPH decreased signaling of reward, but not effort, in the ACC of freely-moving rats. Ensembles of simultaneously recorded neurons generated task-specific trajectories of neural activity encoding past, present, and future events. Low-dose AMPH contracted these trajectories and reduced their variance, whereas high-dose AMPH expanded both. We propose that under low-dose AMPH, increased network stability balances moderately increased excitability, which promotes accelerated unfolding of a neural 'script' for task execution, despite reduced reward valuation. Noise from excessive excitability at high doses overcomes stability enhancement to drive frequent deviation from the script, impairing task execution.

Data availability

Data and analysis code are available online (https://github.com/SaeedehUleth/AMPH-and-utility-encoding)

Article and author information

Author details

  1. Saeedeh Hashemnia

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. David R Euston

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Aaron J Gruber

    Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Canada
    For correspondence
    aaron.gruber@uleth.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2700-5429

Funding

National Science and Engineering Research Council of Canada

  • Saeedeh Hashemnia
  • David R Euston
  • Aaron J Gruber

Beswick Foundation

  • Saeedeh Hashemnia

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

Reviewing Editor

  1. Geoffrey Schoenbaum, National Institute on Drug Abuse, National Institutes of Health, United States

Ethics

Animal experimentation: All procedures were performed in accordance with the Canadian Council of Animal Care and the Animal Welfare Committee at the University of Lethbridge (AWC# 1512).

Version history

  1. Received: March 9, 2020
  2. Accepted: July 17, 2020
  3. Accepted Manuscript published: August 19, 2020 (version 1)
  4. Version of Record published: August 28, 2020 (version 2)

Copyright

© 2020, Hashemnia 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. Saeedeh Hashemnia
  2. David R Euston
  3. Aaron J Gruber
(2020)
Amphetamine reduces reward encoding and stabilizes neural dynamics in rat anterior cingulate cortex
eLife 9:e56755.
https://doi.org/10.7554/eLife.56755

Share this article

https://doi.org/10.7554/eLife.56755

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