1. Neuroscience
Download icon

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
Research Article
  • Cited 0
  • Views 1,431
  • Annotations
Cite this article as: eLife 2020;9:e52466 doi: 10.7554/eLife.52466

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.

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.

Metrics

  • 1,431
    Page views
  • 273
    Downloads
  • 0
    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
    Víctor J López-Madrona et al.
    Research Article Updated

    Hippocampal firing is organized in theta sequences controlled by internal memory processes and by external sensory cues, but how these computations are coordinated is not fully understood. Although theta activity is commonly studied as a unique coherent oscillation, it is the result of complex interactions between different rhythm generators. Here, by separating hippocampal theta activity in three different current generators, we found epochs with variable theta frequency and phase coupling, suggesting flexible interactions between theta generators. We found that epochs of highly synchronized theta rhythmicity preferentially occurred during behavioral tasks requiring coordination between internal memory representations and incoming sensory information. In addition, we found that gamma oscillations were associated with specific theta generators and the strength of theta-gamma coupling predicted the synchronization between theta generators. We propose a mechanism for segregating or integrating hippocampal computations based on the flexible coordination of different theta frameworks to accommodate the cognitive needs.

    1. Neuroscience
    Kyle Jasmin et al.
    Research Article

    Individuals with congenital amusia have a lifelong history of unreliable pitch processing. Accordingly, they downweight pitch cues during speech perception and instead rely on other dimensions such as duration. We investigated the neural basis for this strategy. During fMRI, individuals with amusia (N=15) and controls (N=15) read sentences where a comma indicated a grammatical phrase boundary. They then heard two sentences spoken that differed only in pitch and/or duration cues, and selected the best match for the written sentence. Prominent reductions in functional connectivity were detected in the amusia group, between left prefrontal language-related regions and right hemisphere pitch-related regions, which reflected the between-group differences in cue weights in the same groups of listeners. Connectivity differences between these regions were not present during a control task. Our results indicate that the reliability of perceptual dimensions is linked with functional connectivity between frontal and perceptual regions, and suggest a compensatory mechanism.