1. Neuroscience
Download icon

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
Short Report
  • Cited 55
  • Views 2,872
  • Annotations
Cite this article as: eLife 2016;5:e13665 doi: 10.7554/eLife.13665

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).

Reviewing Editor

  1. Timothy EJ Behrens, University College London, United Kingdom

Publication history

  1. Received: December 9, 2015
  2. Accepted: March 3, 2016
  3. Accepted Manuscript published: March 7, 2016 (version 1)
  4. Version of Record published: March 16, 2016 (version 2)

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

  • 2,872
    Page views
  • 761
    Downloads
  • 55
    Citations

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

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

  1. Further reading

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
    Anita E Autry et al.
    Research Article Updated

    While recent studies have uncovered dedicated neural pathways mediating the positive control of parenting, the regulation of infant-directed aggression and how it relates to adult-adult aggression is poorly understood. Here we show that urocortin-3 (Ucn3)-expressing neurons in the hypothalamic perifornical area (PeFAUcn3) are activated during infant-directed attacks in males and females, but not other behaviors. Functional manipulations of PeFAUcn3 neurons demonstrate the role of this population in the negative control of parenting in both sexes. PeFAUcn3 neurons receive input from areas associated with vomeronasal sensing, stress, and parenting, and send projections to hypothalamic and limbic areas. Optogenetic activation of PeFAUcn3 axon terminals in these regions triggers various aspects of infant-directed agonistic responses, such as neglect, repulsion, and aggression. Thus, PeFAUcn3 neurons emerge as a dedicated circuit component controlling infant-directed neglect and aggression, providing a new framework to understand the positive and negative regulation of parenting in health and disease.