Dissociated sequential activity and stimulus encoding in the dorsomedial striatum during spatial working memory

Abstract

Several lines of evidence suggest that the striatum has an important role in spatial working memory. The neural dynamics in the striatum have been described in tasks with short delay periods (1-4s), but remain largely uncharacterized for tasks with longer delay periods. We collected and analyzed single unit recordings from the dorsomedial striatum of rats performing a spatial working memory task with delays up to 10s. We found that neurons were activated sequentially, with the sequences spanning the entire delay period. Surprisingly, this sequential activity was dissociated from stimulus encoding activity, which was present in the same neurons, but preferentially appeared towards the onset of the delay period. These observations contrast with descriptions of sequential dynamics during similar tasks in other brains areas, and clarify the contribution of the striatum in spatial working memory.

Article and author information

Author details

  1. Hessameddin Akhlaghpour

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Joost Wiskerke

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jung Yoon Choi

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Joshua P Taliaferro

    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:" 0000-0001-6051-8635
  5. Jennifer Au

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Ilana Witten

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    For correspondence
    iwitten@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0548-2160

Funding

NSF Office of the Director (GRFP)

  • Hessameddin Akhlaghpour

NIH Office of the Director (5R01MH106689-02)

  • Ilana Witten

McKnight Foundation

  • Ilana Witten

Pew Charitable Trusts

  • Ilana Witten

NIH Office of the Director (1 DP2 DA035149-01)

  • Ilana Witten

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 (IACUC) protocols (1876-15) of Princeton University. All surgery was performed under anesthesia, and every effort was made to minimize suffering.

Copyright

© 2016, Akhlaghpour 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

  • 4,433
    views
  • 902
    downloads
  • 85
    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. Hessameddin Akhlaghpour
  2. Joost Wiskerke
  3. Jung Yoon Choi
  4. Joshua P Taliaferro
  5. Jennifer Au
  6. Ilana Witten
(2016)
Dissociated sequential activity and stimulus encoding in the dorsomedial striatum during spatial working memory
eLife 5:e19507.
https://doi.org/10.7554/eLife.19507

Share this article

https://doi.org/10.7554/eLife.19507

Further reading

    1. Neuroscience
    Zeming Fang, Meihua Zhao ... Ru-Yuan Zhang
    Research Article

    Previous studies on reinforcement learning have identified three prominent phenomena: (1) individuals with anxiety or depression exhibit a reduced learning rate compared to healthy subjects; (2) learning rates may increase or decrease in environments with rapidly changing (i.e. volatile) or stable feedback conditions, a phenomenon termed learning rate adaptation; and (3) reduced learning rate adaptation is associated with several psychiatric disorders. In other words, multiple learning rate parameters are needed to account for behavioral differences across participant populations and volatility contexts in this flexible learning rate (FLR) model. Here, we propose an alternative explanation, suggesting that behavioral variation across participant populations and volatile contexts arises from the use of mixed decision strategies. To test this hypothesis, we constructed a mixture-of-strategies (MOS) model and used it to analyze the behaviors of 54 healthy controls and 32 patients with anxiety and depression in volatile reversal learning tasks. Compared to the FLR model, the MOS model can reproduce the three classic phenomena by using a single set of strategy preference parameters without introducing any learning rate differences. In addition, the MOS model can successfully account for several novel behavioral patterns that cannot be explained by the FLR model. Preferences for different strategies also predict individual variations in symptom severity. These findings underscore the importance of considering mixed strategy use in human learning and decision-making and suggest atypical strategy preference as a potential mechanism for learning deficits in psychiatric disorders.

    1. Neuroscience
    Minsik Yun, Do-Hyoung Kim ... Young-Joon Kim
    Research Article

    In birds and insects, the female uptakes sperm for a specific duration post-copulation known as the ejaculate holding period (EHP) before expelling unused sperm and the mating plug through sperm ejection. In this study, we found that Drosophila melanogaster females shortens the EHP when incubated with males or mated females shortly after the first mating. This phenomenon, which we termed male-induced EHP shortening (MIES), requires Or47b+ olfactory and ppk23+ gustatory neurons, activated by 2-methyltetracosane and 7-tricosene, respectively. These odorants raise cAMP levels in pC1 neurons, responsible for processing male courtship cues and regulating female mating receptivity. Elevated cAMP levels in pC1 neurons reduce EHP and reinstate their responsiveness to male courtship cues, promoting re-mating with faster sperm ejection. This study established MIES as a genetically tractable model of sexual plasticity with a conserved neural mechanism.