Dynamic behavior of the locus coeruleus during arousal-related memory processing in a multi-modal 7T fMRI paradigm

  1. Heidi IL Jacobs  Is a corresponding author
  2. Nikos Priovoulos
  3. Benedikt A Poser
  4. Linda HG Pagen
  5. Dimo Ivanov
  6. Frans RJ Verhey
  7. Kâmil Uludağ
  1. Maastricht University, Netherlands
  2. University Health Network, Canada

Abstract

A body of animal and human evidence points to the norepinephrine (NE) locus coeruleus (LC) system in modulating memory for arousing experiences, but whether the LC would recast its role along memory stages remains unknown. Sedation precluded examination of LC dynamics during memory processing in animals. Here, we addressed the contribution of the LC during arousal-associated memory processing through a unique combination of dedicated ultra-high-field LC-imaging methods, a well-established emotional memory task, online physiological and saliva alpha-amylase measurements in young adults. Arousal-related LC activation followed amygdala engagement during encoding. During consolidation and recollection, activation transitioned to hippocampal involvement, reflecting learning and model updating. NE-LC activation is dynamic, plays an arousal-controlling role, and is not sufficient but requires interactions with the amygdala to form adaptive memories of emotional experiences. These findings have implications for understanding contributions of LC dysregulation to disruptions in emotional memory formation, observed in psychiatric and neurocognitive disorders.

Data availability

Processed data to reproduce the figures in this manuscript is provided in the Source data files. Participants did not explicitly consent to their data being made public and therefore, access to their demographic, raw or processed imaging and physiological data is restricted. Requests for the anonymized data should be made to Heidi Jacobs (www.heidijacobs.nl; h.jacobs@maastrichtuniversity.nl or hjacobs@mgh.harvard.edu) and will be reviewed by an independent data access committee, taking into account the research proposal and intended use of the data. Requestors are required to sign a data sharing agreement to ensure participants' confidentiality is maintained prior to release of any data and that procedures conform with the EU legislation on the general data protection regulation and local ethical regulations.

Article and author information

Author details

  1. Heidi IL Jacobs

    School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands
    For correspondence
    h.jacobs@maastrichtuniversity.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7620-3822
  2. Nikos Priovoulos

    School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Benedikt A Poser

    Department of Cognitive Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Linda HG Pagen

    School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Dimo Ivanov

    Department of Cognitive Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Frans RJ Verhey

    School for Mental Health and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Kâmil Uludağ

    Techna Institute & Koerner Scientist in MR Imaging, University Health Network, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (VENI 451-14-035)

  • Heidi IL Jacobs

Universiteit Maastricht (Intramural support FHML)

  • Heidi IL Jacobs

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

Ethics

Human subjects: All participants provided written informed. Approval of the experimental protocol was obtained from the local ethical committee of the Faculty of Psychology and Neuroscience at Maastricht University (#07_11_2014_A1).

Reviewing Editor

  1. Dorothea Hämmerer, UCL, United Kingdom

Publication history

  1. Received: September 20, 2019
  2. Accepted: June 24, 2020
  3. Accepted Manuscript published: June 24, 2020 (version 1)
  4. Version of Record published: July 8, 2020 (version 2)

Copyright

© 2020, Jacobs 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. Heidi IL Jacobs
  2. Nikos Priovoulos
  3. Benedikt A Poser
  4. Linda HG Pagen
  5. Dimo Ivanov
  6. Frans RJ Verhey
  7. Kâmil Uludağ
(2020)
Dynamic behavior of the locus coeruleus during arousal-related memory processing in a multi-modal 7T fMRI paradigm
eLife 9:e52059.
https://doi.org/10.7554/eLife.52059

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