1. Neuroscience
Download icon

Stable and dynamic representations of value in the prefrontal cortex

  1. Pierre Enel  Is a corresponding author
  2. Joni D Wallis
  3. Erin L Rich
  1. Icahn School of Medicine at Mount Sinai, United States
  2. University of California, Berkeley, United States
Research Article
  • Cited 9
  • Views 2,741
  • Annotations
Cite this article as: eLife 2020;9:e54313 doi: 10.7554/eLife.54313

Abstract

Optimal decision-making requires that stimulus-value associations are kept up to date by constantly comparing the expected value of a stimulus with its experienced outcome. To do this, value information must be held in mind when a stimulus and outcome are separated in time. However, little is known about the neural mechanisms of working memory (WM) for value. Contradicting theories have suggested WM requires either persistent or transient neuronal activity, with stable or dynamic representations respectively. To test these hypotheses, we recorded neuronal activity in the orbitofrontal and anterior cingulate cortex of two monkeys performing a valuation task. We found that features of all hypotheses were simultaneously present in prefrontal activity, and no single hypothesis was exclusively supported. Instead, mixed dynamics supported robust, time invariant value representations while also encoding the information in a temporally specific manner. We suggest that this hybrid coding is a critical mechanism supporting flexible cognitive abilities.

Data availability

The neural recording data analyzed in this paper is available online at https://doi.org/10.5061/dryad.4j0zpc88b

The following data sets were generated

Article and author information

Author details

  1. Pierre Enel

    Department of Neurosience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, United States
    For correspondence
    pierre.enel@mssm.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8983-6223
  2. Joni D Wallis

    Helen Wills Neuroscience Institute, Department of Psychology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Erin L Rich

    Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute of Mental Health (R01-MH121448)

  • Joni D Wallis

National Institute of Mental Health (R01-MH097990)

  • Joni D Wallis

Hilda and Preston Davis Foundation (Postdoctoral fellowship)

  • Erin L Rich

National Institute on Drug Abuse (K08-DA039051)

  • Erin L Rich

National Institute of Mental Health (R01-MH117763)

  • Joni D Wallis

Whitehall Foundation Research Grant (Postdoctoral fellowship)

  • Erin L Rich

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 (Assurance Number A3084-01). All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (Protocol Number R283) of the University of California at Berkeley. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

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

Publication history

  1. Received: December 10, 2019
  2. Accepted: July 6, 2020
  3. Accepted Manuscript published: July 6, 2020 (version 1)
  4. Accepted Manuscript updated: July 8, 2020 (version 2)
  5. Version of Record published: July 29, 2020 (version 3)

Copyright

© 2020, Enel 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.

Metrics

  • 2,741
    Page views
  • 409
    Downloads
  • 9
    Citations

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

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)

Further reading

    1. Neuroscience
    Debora Fusca, Peter Kloppenburg
    Research Article

    Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

    1. Neuroscience
    Wanhui Sheng et al.
    Research Article Updated

    Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here, we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes; however, activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.