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Salient experiences are represented by unique transcriptional signatures in the mouse brain

  1. Diptendu Mukherjee
  2. Bogna Marta Ignatowska-Jankowska
  3. Eyal Itskovits
  4. Ben Jerry Gonzales
  5. Hagit Turm
  6. Liz Izakson
  7. Doron Haritan
  8. Noa Bleistein
  9. Chen Cohen
  10. Ido Amit
  11. Tal Shay
  12. Brad Grueter
  13. Alon Zaslaver
  14. Ami Citri Is a corresponding author
  1. The Hebrew University of Jerusalem, Israel
  2. Weizmann Institute of Science, Israel
  3. Ben-Gurion University of the Negev, Israel
  4. Vanderbilt University School of Medicine, United States
Research Article
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Cite as: eLife 2018;7:e31220 doi: 10.7554/eLife.31220

Abstract

It is well established that inducible transcription is essential for the consolidation of salient experiences into long-term memory. However, whether inducible transcription relays information about the identity and affective attributes of the experience being encoded, has not been explored. To this end, we analyzed transcription induced by a variety of rewarding and aversive experiences, across multiple brain regions. Our results describe the existence of robust transcriptional signatures uniquely representing distinct experiences, enabling near-perfect decoding of recent experiences. Furthermore, experiences with shared attributes display commonalities in their transcriptional signatures, exemplified in the representation of valence, habituation and reinforcement. This study introduces the concept of a neural transcriptional code, which represents the encoding of experiences in the mouse brain. This code is comprised of distinct transcriptional signatures that correlate to attributes of the experiences that are being committed to long-term memory.

Article and author information

Author details

  1. Diptendu Mukherjee

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Bogna Marta Ignatowska-Jankowska

    The Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Eyal Itskovits

    Department of Genetics, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Ben Jerry Gonzales

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Hagit Turm

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Liz Izakson

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Doron Haritan

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  8. Noa Bleistein

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  9. Chen Cohen

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  10. Ido Amit

    Department of Immunology, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  11. Tal Shay

    Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel
    Competing interests
    The authors declare that no competing interests exist.
  12. Brad Grueter

    Department of Anesthesiology, Vanderbilt University School of Medicine, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-4224-3866
  13. Alon Zaslaver

    Department of Genetics, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  14. Ami Citri

    Department of Biological Chemistry, Silberman Institute for Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
    For correspondence
    ami.citri@mail.huji.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 0000-0002-9914-0278

Funding

Israel Science Foundation (Personal Grant 393/12 & I-CORE 1796/12)

  • Ami Citri

The Lady Davis Postdoctoral Fellowship (Postdoctoral stipend)

  • Bogna Marta Ignatowska-Jankowska

German-Israeli Foundation for Scientific Research and Development (Young Investigator Award 2299-2291.1./2011)

  • Ami Citri

Brain and Behavior Research Foundation (Young Investigator Award #18795)

  • Ami Citri

Canadian Institute for Advanced Research (Research Support)

  • Ami Citri

Binational United-States Israel Research Foundation (Research Grant #2011266)

  • Ami Citri

Milton Rosenbaum Research Foundation (Research Grant)

  • Ami Citri

National Institutes for Psychobiology in Israel (Research Grant 109-15-16)

  • Ami Citri

Shimon Peres Postdoctoral Award (Postdoctoral stipend)

  • Bogna Marta Ignatowska-Jankowska

ELSC Postdoctoral Award (Postdoctoral stipend)

  • Bogna Marta Ignatowska-Jankowska

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 (#NS-13-13895-3 ; NS-15-14668-3 ; NS-14-14088-3 ; NS-15-14312-3 ; NS-15-14348-3) of the Hebrew University of Jerusalem. The protocol was approved by the Committee on the Ethics of Animal Experiments of the Hebrew University. Every effort was made to minimize suffering.

Reviewing Editor

  1. Sacha B Nelson, Reviewing Editor, Brandeis University, United States

Publication history

  1. Received: September 4, 2017
  2. Accepted: February 5, 2018
  3. Accepted Manuscript published: February 7, 2018 (version 1)

Copyright

© 2018, Mukherjee 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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