Midbrain dopamine neurons compute inferred and cached value prediction errors in a common framework

  1. Brian F Sadacca
  2. Joshua L Jones
  3. Geoffrey Schoenbaum  Is a corresponding author
  1. National Institutes of Health, United States

Abstract

Midbrain dopamine neurons have been proposed to signal reward prediction errors as defined in temporal difference (TD) learning algorithms. While these models have been extremely powerful in interpreting dopamine activity, they typically do not use value derived through inference in computing errors. This is important because much real world behavior - and thus many opportunities for error-driven learning - is based on such predictions. Here, we show that error-signaling rat dopamine neurons respond to the inferred, model-based value of cues that have not been paired with reward and do so in the same framework as they track the putative cached value of cues previously paired with reward. This suggests that dopamine neurons access a wider variety of information than contemplated by standard TD models and that, while their firing conforms to predictions of TD models in some cases, they may not be restricted to signaling errors from TD predictions.

Article and author information

Author details

  1. Brian F Sadacca

    Intramural Research program of the National Institute on Drug Abuse, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Joshua L Jones

    Intramural Research program of the National Institute on Drug Abuse, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Geoffrey Schoenbaum

    Intramural Research program of the National Institute on Drug Abuse, National Institutes of Health, Bethesda, United States
    For correspondence
    geoffrey.schoenbaum@nih.gov
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: Experiments were performed at the National Institute on Drug Abuse Intramural Research Program in accordance with NIH guidelines and an approved institutional animal care and use committee protocol (15-CNRB-108). The protocol was approved by the ACUC at NIDA-IRP (Assurance Number: A4149-01).

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 3,485
    views
  • 851
    downloads
  • 98
    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. Brian F Sadacca
  2. Joshua L Jones
  3. Geoffrey Schoenbaum
(2016)
Midbrain dopamine neurons compute inferred and cached value prediction errors in a common framework
eLife 5:e13665.
https://doi.org/10.7554/eLife.13665

Share this article

https://doi.org/10.7554/eLife.13665

Further reading

    1. Neuroscience
    Bradley B Doll, Nathaniel D Daw
    Insight

    Evidence increasingly suggests that dopaminergic neurons play a more sophisticated role in predicting rewards than previously thought.

    1. Neuroscience
    Cristina Gil Avila, Elisabeth S May ... Markus Ploner
    Research Article

    Chronic pain is a prevalent and debilitating condition whose neural mechanisms are incompletely understood. An imbalance of cerebral excitation and inhibition (E/I), particularly in the medial prefrontal cortex (mPFC), is believed to represent a crucial mechanism in the development and maintenance of chronic pain. Thus, identifying a non-invasive, scalable marker of E/I could provide valuable insights into the neural mechanisms of chronic pain and aid in developing clinically useful biomarkers. Recently, the aperiodic component of the electroencephalography (EEG) power spectrum has been proposed to represent a non-invasive proxy for E/I. We, therefore, assessed the aperiodic component in the mPFC of resting-state EEG recordings in 149 people with chronic pain and 115 healthy participants. We found robust evidence against differences in the aperiodic component in the mPFC between people with chronic pain and healthy participants, and no correlation between the aperiodic component and pain intensity. These findings were consistent across different subtypes of chronic pain and were similarly found in a whole-brain analysis. Their robustness was supported by preregistration and multiverse analyses across many different methodological choices. Together, our results suggest that the EEG aperiodic component does not differentiate between people with chronic pain and healthy individuals. These findings and the rigorous methodological approach can guide future studies investigating non-invasive, scalable markers of cerebral dysfunction in people with chronic pain and beyond.