1. Neuroscience

Subpopulations of neurons in lOFC encode previous and current rewards at time of choice

  1. David L Hocker  Is a corresponding author
  2. Carlos D Brody
  3. Cristina Savin
  4. Christine M Constantinople
  1. New York University, United States
  2. Princeton University, United States
https://doi.org/10.7554/eLife.70129
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  1. David L Hocker
  2. Carlos D Brody
  3. Cristina Savin
  4. Christine M Constantinople
(2021)
Subpopulations of neurons in lOFC encode previous and current rewards at time of choice
eLife 10:e70129.
https://doi.org/10.7554/eLife.70129
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Abstract

Studies of neural dynamics in lateral orbitofrontal cortex (lOFC) have shown that subsets of neurons that encode distinct aspects of behavior, such as value,may project to common downstreamtargets. However, it is unclear whether reward history, which may subserve lOFC's well-documented role in learning, is represented by functional subpopulations in lOFC. Previously, we analyzed neural recordings from rats performing a value-based decision-making task, and we documented trial-by-trial learning that required lOFC (Constantinople et al., 2019). Here we characterize functional subpopulations of lOFC neurons during behavior, including their encoding of task variables. We found five distinct clusters of lOFC neurons, either based on clustering of their trial-averaged peristimulus time histograms (PSTHs), or a feature space defined by their average conditional firing rates aligned to different task variables. We observed weak encoding of reward attributes, but stronger encoding of reward history, the animal's left or right choice, and reward receipt across all clusters. Only one cluster, however, encoded the animal's reward history at the time shortly preceding the choice, suggesting a possible role in integrating previous and current trial outcomes at the time of choice. This cluster also exhibits qualitatively similar responses to identified corticostriatal projection neurons in a recent study (Hirokawa et al., 2019), and suggests a possible role for subpopulations of lOFC neurons in mediating trial-by-trial learning.

Data availability

Physiology, behavior, GLM statistical modeling, and clustering results source data are publicly available on Zenodo. https://doi.org/10.5281/zenodo.5592702.Code for the GLM model fit, clustering, and all subsequent analysis will also be provided publicly via Github atgithub.com/constantinoplelab/published/

The following data sets were generated

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Author details

  1. David L Hocker

    Center for Neural Science, New York University, New York, United States
    For correspondence
    dh148@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3091-421X

  2. Carlos D Brody

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4201-561X

  3. Cristina Savin

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Christine M Constantinople

    Center for Neural Science, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4435-4460

Funding

National Institute of Mental Health (R00MH111926)

  • Christine M Constantinople

National Institute of Mental Health (R01MH125571)

  • Cristina Savin
  • Christine M Constantinople

Alfred P. Sloan Foundation

  • Christine M Constantinople

Klingenstein-Simons Fellowship Award in Neuroscience

  • Christine M Constantinople

National Science Foundation (1922658)

  • Cristina Savin

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 accordance with the National Institutes of Health standards. Animal use procedures were approved by the Princeton University Institutional Animal Care and Use Committee (protocol #1853).

Copyright

© 2021, Hocker 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. David L Hocker
  2. Carlos D Brody
  3. Cristina Savin
  4. Christine M Constantinople
(2021)
Subpopulations of neurons in lOFC encode previous and current rewards at time of choice
eLife 10:e70129.
https://doi.org/10.7554/eLife.70129

Share this article

https://doi.org/10.7554/eLife.70129

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Further reading

    1. Neuroscience

    Lateral orbitofrontal cortex promotes trial-by-trial learning of risky, but not spatial, biases

    Christine M Constantinople, Alex T Piet ... Carlos D Brody
    Research Article

    Individual choices are not made in isolation but are embedded in a series of past experiences, decisions, and outcomes. The effects of past experiences on choices, often called sequential biases, are ubiquitous in perceptual and value-based decision-making, but their neural substrates are unclear. We trained rats to choose between cued guaranteed and probabilistic rewards in a task in which outcomes on each trial were independent. Behavioral variability often reflected sequential effects, including increased willingness to take risks following risky wins, and spatial ‘win-stay/lose-shift’ biases. Recordings from lateral orbitofrontal cortex (lOFC) revealed encoding of reward history and receipt, and optogenetic inhibition of lOFC eliminated rats’ increased preference for risk following risky wins, but spared other sequential effects. Our data show that different sequential biases are neurally dissociable, and the lOFC’s role in adaptive behavior promotes learning of more abstract biases (here, biases for the risky option), but not spatial ones.