Dopamine neuron ensembles signal the content of sensory prediction errors
- National Institute on Drug Abuse, National Institutes of Health, United States
- Northwestern University, United States
- Harvard University, United States
Abstract
Dopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not evident in individual neuron or average neural activity. How then do downstream areas know what to learn in response to these signals? One possibility is that information about content is contained in the pattern of firing across many dopamine neurons. Consistent with this, here we show that the pattern of firing across a small group of dopamine neurons recorded in rats signals the identity of a mis-predicted sensory event. Further, this same information is reflected in the BOLD response elicited by sensory prediction errors in human midbrain. These data provide evidence that ensembles of dopamine neurons provide highly specific teaching signals, opening new possibilities for how this system might contribute to learning.
Data availability
The raw data that went into the analyses shown in Figures 1,2 and 3 are archived athttps://github.com/tastalnaker/dopamine_ensemble_analysis.git
Article and author information
Author details
Geoffrey Schoenbaum
Funding
National Institute on Drug Abuse (ZIA-DA000587)
- Geoffrey Schoenbaum
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee protocols of the NIH. The protocol (#18-CNRB-108) was approved by the NIDA-IRP ACUC. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.
Human subjects: Subjects gave informed consent to participate in the experiment. The protocol (#STU00098371) and consent forms were approved by Northwestern University's Institutional Review Board.
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.
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Dopamine neuron ensembles signal the content of sensory prediction errors
eLife 8:e49315.
https://doi.org/10.7554/eLife.49315
