The hippocampus encodes delay and value information during delay-discounting decision making

  1. Akira Masuda  Is a corresponding author
  2. Chie Sano
  3. Qi Zhang
  4. Hiromichi Goto
  5. Thomas J McHugh
  6. Shigeyoshi Fujisawa
  7. Shigeyoshi Itohara  Is a corresponding author
  1. Doshisha University, Japan
  2. RIKEN Center for Brain Science, Japan
  3. University of Tsukuba, Japan

Abstract

The hippocampus, a region critical for memory and spatial navigation, has been implicated in delay discounting, the decline in subjective reward value when a delay is imposed. However, how delay information is encoded in the hippocampus is poorly understood. Here we recorded from CA1 of mice performing a delay-discounting decision-making task, where delay lengths, delay positions, and reward amounts were changed across sessions, and identified subpopulations of CA1 neurons which increased or decreased their firing rate during long delays. The activity of both delay-active and -suppressive cells reflected delay length, delay position, and reward amount; however manipulating reward amount differentially impacted the two populations, suggesting distinct roles in the valuation process. Further, genetic deletion of NMDA receptor in hippocampal pyramidal cells impaired delay-discount behavior and diminished delay-dependent activity in CA1. Our results suggest that distinct subclasses of hippocampal neurons concertedly support delay-discounting decisions in a manner dependent on NMDA receptor function.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Akira Masuda

    Organization for Research Initiatives and Development, Doshisha University, Kyotanabe, Japan
    For correspondence
    amasuda@mail.doshisha.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8659-6356
  2. Chie Sano

    Laboratory for Behavioral Genetics, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Qi Zhang

    Faculty of Human Science, University of Tsukuba, Tsukuba, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Hiromichi Goto

    Laboratory for Behavioral Genetics, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Thomas J McHugh

    Laboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Shigeyoshi Fujisawa

    Laboratory for Systems Neurophysiology, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Shigeyoshi Itohara

    Laboratory for Behavioral Genetics, RIKEN Center for Brain Science, Wako, Japan
    For correspondence
    shigeyoshi.itohara@riken.jp
    Competing interests
    The authors declare that no competing interests exist.

Funding

Japan Society for the Promotion of Science (16K15196)

  • Akira Masuda

Japan Agency for Medical Research and Development (Brain/MINDS)

  • Shigeyoshi Fujisawa

Uehara Memorial Foundation

  • Akira Masuda

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 Institute of Health. The study was approved by the Institutional Animal Care and Use Committee of the RIKEN Institute in Wako (approval number H27-2-239(6)), in conformity with Article 24 of the RIKEN regulations for animal experiments. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Matthijs (Matt) van der Meer

Publication history

  1. Received: October 4, 2019
  2. Accepted: February 19, 2020
  3. Accepted Manuscript published: February 20, 2020 (version 1)
  4. Version of Record published: March 2, 2020 (version 2)

Copyright

© 2020, Masuda 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. Akira Masuda
  2. Chie Sano
  3. Qi Zhang
  4. Hiromichi Goto
  5. Thomas J McHugh
  6. Shigeyoshi Fujisawa
  7. Shigeyoshi Itohara
(2020)
The hippocampus encodes delay and value information during delay-discounting decision making
eLife 9:e52466.
https://doi.org/10.7554/eLife.52466

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