Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1

  1. Vincent Robert
  2. Ludivine Therreau
  3. Vivien Chevaleyre
  4. Eude Lepicard
  5. Cécile Viollet
  6. Julie Cognet
  7. Arthur JY Huang
  8. Roman Boehringer
  9. Denis Polygalov
  10. Thomas J McHugh
  11. Rebecca Ann Piskorowski  Is a corresponding author
  1. Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266, France
  2. Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266; GHU PARIS psychiatrie & neurosciences, France
  3. RIKEN Center for Brain Science, Japan

Abstract

The hippocampus is critical for memory formation. The hypothalamic supramammillary nucleus (SuM) sends long-range projections to hippocampal area CA2. While the SuM-CA2 connection is critical for social memory, how this input acts on the local circuit is unknown. Using mice, we found that SuM axon stimulation elicited mixed excitatory and inhibitory responses in area CA2 pyramidal neurons (PNs). Parvalbumin-expressing basket cells were largely responsible for the feedforward inhibitory drive of SuM over area CA2. Inhibition recruited by the SuM input onto CA2 PNs increased the precision of action potential firing both in conditions of low and high cholinergic tone. Furthermore, SuM stimulation in area CA2 modulated CA1 activity, indicating that synchronized CA2 output drives a pulsed inhibition in area CA1. Hence, the network revealed here lays basis for understanding how SuM activity directly acts on the local hippocampal circuit to allow social memory encoding.

Data availability

The data analysed for this study are included in the manuscript and supporting files. These are included in tables, and data file for figure 7.

Article and author information

Author details

  1. Vincent Robert

    Team of Synpatic Plasticity and Neural Networks, Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Ludivine Therreau

    Team of Synpatic Plasticity and Neural Networks, Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Vivien Chevaleyre

    Team of Synpatic Plasticity and Neural Networks, Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Eude Lepicard

    Team of Synpatic Plasticity and Neural Networks, Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Cécile Viollet

    Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266; GHU PARIS psychiatrie & neurosciences, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Julie Cognet

    Team of Synpatic Plasticity and Neural Networks, Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Arthur JY Huang

    Laboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Roman Boehringer

    Laboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2856-3262
  9. Denis Polygalov

    Laboratory for Circuit and Behavioral Physiology, RIKEN Center for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8165-5257
  10. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1243-5189
  11. Rebecca Ann Piskorowski

    Institute of Psychiatry and Neuroscience of Paris, INSERM UMRS1266; GHU PARIS psychiatrie & neurosciences, Paris, France
    For correspondence
    rebecca.piskorowski@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0120-2360

Funding

RIKEN Brain Science Institute

  • Thomas J McHugh

Ministry of Education, Culture, Sports, Science and Technology (19H05646)

  • Thomas J McHugh

Ministry of Education, Culture, Sports, Science and Technology (19H05233)

  • Thomas J McHugh

Agence Nationale de la Recherche (ANR-13-JSV4-0002-01)

  • Rebecca Ann Piskorowski

Agence Nationale de la Recherche (ANR-18-CE37-0020-01)

  • Rebecca Ann Piskorowski

Ville de Paris (Programme Emergences)

  • Rebecca Ann Piskorowski

Brain and Behavior Research Foundation (NARSAD Young INvestigator Award)

  • Rebecca Ann Piskorowski

Fondation pour la Recherche Médicale (FRM:FTD20170437387)

  • Vincent Robert

Schizo-Oui

  • Vincent Robert

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All procedures involving animals were performed in accordance with institutional regulations (French Ministry of Research and Education protocol #12406-2016040417305913). Animal sample sizes were estimated using power tests with standard deviations and ANOVA values from pilot experiments. A 15 % failure rate was assumed to account for stereotaxic injection errors and slice preparation complications. Every effort was made to reduce animal suffering.

Reviewing Editor

  1. Katalin Toth, University of Ottawa, Canada

Version history

  1. Received: September 22, 2020
  2. Accepted: May 17, 2021
  3. Accepted Manuscript published: May 18, 2021 (version 1)
  4. Version of Record published: May 26, 2021 (version 2)

Copyright

© 2021, Robert 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. Vincent Robert
  2. Ludivine Therreau
  3. Vivien Chevaleyre
  4. Eude Lepicard
  5. Cécile Viollet
  6. Julie Cognet
  7. Arthur JY Huang
  8. Roman Boehringer
  9. Denis Polygalov
  10. Thomas J McHugh
  11. Rebecca Ann Piskorowski
(2021)
Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
eLife 10:e63352.
https://doi.org/10.7554/eLife.63352

Share this article

https://doi.org/10.7554/eLife.63352

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