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.

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

  • 3,298
    views
  • 529
    downloads
  • 20
    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. 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

Share this article

https://doi.org/10.7554/eLife.52466

Further reading

    1. Neuroscience
    J Wesley Maddox, Gregory J Ordemann ... Amy Lee
    Research Article

    In congenital stationary night blindness, type 2 (CSNB2)—a disorder involving the Cav1.4 (L-type) Ca2+ channel—visual impairment is mild considering that Cav1.4 mediates synaptic release from rod and cone photoreceptors. Here, we addressed this conundrum using a Cav1.4 knockout (KO) mouse and a knock-in (G369i KI) mouse expressing a non-conducting Cav1.4. Surprisingly, Cav3 (T-type) Ca2+ currents were detected in cones of G369i KI mice and Cav1.4 KO mice but not in cones of wild-type mouse, ground squirrels, and macaque retina. Whereas Cav1.4 KO mice are blind, G369i KI mice exhibit normal photopic (i.e. cone-mediated) visual behavior. Cone synapses, which fail to form in Cav1.4 KO mice, are present, albeit enlarged, and with some errors in postsynaptic wiring in G369i KI mice. While Cav1.4 KO mice lack evidence of cone synaptic responses, electrophysiological recordings in G369i KI mice revealed nominal transmission from cones to horizontal cells and bipolar cells. In CSNB2, we propose that Cav3 channels maintain cone synaptic output provided that the nonconducting role of Cav1.4 in cone synaptogenesis remains intact. Our findings reveal an unexpected form of homeostatic plasticity that relies on a non-canonical role of an ion channel.

    1. Neuroscience
    Jiayun Xu, Mauricio Girardi-Schappo ... Leonard Maler
    Research Article

    Animals navigate by learning the spatial layout of their environment. We investigated spatial learning of mice in an open maze where food was hidden in one of a hundred holes. Mice leaving from a stable entrance learned to efficiently navigate to the food without the need for landmarks. We developed a quantitative framework to reveal how the mice estimate the food location based on analyses of trajectories and active hole checks. After learning, the computed ‘target estimation vector’ (TEV) closely approximated the mice’s route and its hole check distribution. The TEV required learning both the direction and distance of the start to food vector, and our data suggests that different learning dynamics underlie these estimates. We propose that the TEV can be precisely connected to the properties of hippocampal place cells. Finally, we provide the first demonstration that, after learning the location of two food sites, the mice took a shortcut between the sites, demonstrating that they had generated a cognitive map.