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A connectional hub in the rostral anterior cingulate cortex links areas of emotion and cognitive control

  1. Wei Tang
  2. Saad Jbabdi
  3. Ziyi Zhu
  4. Michiel Cottaar
  5. Giorgia Grisot
  6. Julia F Lehman
  7. Anastasia Yendiki
  8. Suzanne N Haber  Is a corresponding author
  1. McLean Hospital / Harvard Medical School, United States
  2. University of Oxford, United Kingdom
  3. University of Rochester School of Medicine, United States
  4. Massachusetts General Hospital, United States
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Cite this article as: eLife 2019;8:e43761 doi: 10.7554/eLife.43761

Abstract

We investigated afferent inputs from all areas in the frontal cortex (FC) to different subregions in the rostral anterior cingulate cortex (rACC). Using retrograde tracing in macaque monkeys, we quantified projection strength by counting retrogradely labeled cells in each FC area. The projection from different FC regions varied across injection sites in strength, following different spatial patterns. Importantly, a site at the rostral end of the cingulate sulcus stood out as having strong inputs from many areas in diverse FC regions. Moreover, it was at the integrative conjunction of three projection trends across sites. This site marks a connectional hub inside the rACC that integrates FC inputs across functional modalities. Tractography with monkey diffusion magnetic resonance imaging (dMRI) located a similar hub region comparable to the tracing result. Applying the same tractography method to human dMRI data, we demonstrated that a similar hub can be located in the human rACC.

Article and author information

Author details

  1. Wei Tang

    Basic Neuroscience Division, McLean Hospital / Harvard Medical School, Belmont, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Saad Jbabdi

    Centre for Functional MRI of the Brain, Department of Clinical Neurology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Ziyi Zhu

    Department of Pharmacology and Physiology, University of Rochester School of Medicine, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michiel Cottaar

    Centre for Functional MRI of the Brain, Department of Clinical Neurology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Giorgia Grisot

    Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4349-1201
  6. Julia F Lehman

    Department of Pharmacology and Physiology, University of Rochester School of Medicine, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Anastasia Yendiki

    Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Suzanne N Haber

    Department of Pharmacology and Physiology, University of Rochester School of Medicine, Rochester, United States
    For correspondence
    Suzanne_Haber@urmc.rochester.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5237-1941

Funding

National Institute of Mental Health (MH106435)

  • Wei Tang
  • Ziyi Zhu
  • Julia F Lehman
  • Suzanne N Haber

National Institute of Mental Health (MH045573)

  • Wei Tang
  • Ziyi Zhu
  • Julia F Lehman
  • Suzanne N Haber

Medical Research Council (MR/L009013/1)

  • Saad Jbabdi

National Institute of Mental Health (U01-MH109589)

  • Michiel Cottaar

NIH Blueprint for Neuroscience Research (U01-MH093765)

  • Giorgia Grisot
  • Anastasia Yendiki

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 nonhuman primate experiments were performed in accordance with the Institute of Laboratory Animal Resources Guide for the Care and Use of Laboratory Animals and approved by the University Committee on Animal Resources at University of Rochester (Protocol Number UCAR-2008-122R).

Human subjects: The human data were obtained from the publicly available Human Connectome Project database. All procedures conformed to ethical standards approved by the Institutional Review Board of Partners Healthcare. All human subjects have provided written informed consent.

Reviewing Editor

  1. David Badre, Brown University, United States

Publication history

  1. Received: November 19, 2018
  2. Accepted: June 18, 2019
  3. Accepted Manuscript published: June 19, 2019 (version 1)
  4. Version of Record published: July 11, 2019 (version 2)

Copyright

© 2019, Tang 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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