Mapping the human subcortical auditory system using histology, post mortem MRI and in vivo MRI at 7T

  1. Kevin R Sitek  Is a corresponding author
  2. Omer Faruk Gulban  Is a corresponding author
  3. Evan Calabrese
  4. G Allan Johnson
  5. Agustin Lage-Castellanos
  6. Michelle Moerel
  7. Satrajit S Ghosh
  8. Federico de Martino
  1. Massachusetts Institute of Technology, United States
  2. Maastricht University, Netherlands
  3. Duke University, United States

Abstract

Studying the human subcortical auditory system non-invasively is challenging due to its small, densely packed structures deep within the brain. Additionally, the elaborate three-dimensional (3-D) structure of the system can be difficult to understand based on currently available 2-D schematics and animal models. We addressed these issues using a combination of histological data, post mortem magnetic resonance imaging (MRI), and in vivo MRI at 7 Tesla. We created anatomical atlases based on state-of-the-art human histology (BigBrain) and post mortem MRI (50 μm). We measured functional MRI (fMRI) responses to natural sounds and demonstrate that the functional localization of subcortical structures is reliable within individual participants who were scanned in two different experiments. Further, a group functional atlas derived from the functional data locates these structures with a median distance below 2mm. Using diffusion MRI tractography, we revealed structural connectivity maps of the human subcortical auditory pathway both in vivo (1050 μm isotropic resolution) and post mortem (200 μm isotropic resolution). This work captures current MRI capabilities for investigating the human subcortical auditory system, describes challenges that remain, and contributes novel, openly available data, atlases, and tools for researching the human auditory system.

Data availability

In vivo data are available on OpenNeuro: https://openneuro.org/datasets/ds001942Derivatives (including histology-based, post mortem MRI-based, and fMRI-based atlases) are available on the Open Science Framework: https://osf.io/c4m82/Analysis code, flowcharts, and other auxiliary files are available on Github: https://github.com/sitek/subcortical-auditory-atlas

The following data sets were generated

Article and author information

Author details

  1. Kevin R Sitek

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    ksitek@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2172-5786
  2. Omer Faruk Gulban

    Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    For correspondence
    faruk.gulban@maastrichtuniversity.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7761-3727
  3. Evan Calabrese

    Center for In Vivo Microscopy, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. G Allan Johnson

    Center for In Vivo Microscopy, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Agustin Lage-Castellanos

    Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Michelle Moerel

    Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Satrajit S Ghosh

    McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5312-6729
  8. Federico de Martino

    Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.

Funding

NWO (864-13-012)

  • Omer Faruk Gulban
  • Federico de Martino

National Institutes of Health (5R01EB020740)

  • Satrajit S Ghosh

National Institutes of Health (P41EB019936)

  • Satrajit S Ghosh

National Institutes of Health (5F31DC015695)

  • Kevin R Sitek

Eaton Peabody Laboratory at Mass Eye and Ear (Amelia Peabody Scholarship)

  • Kevin R Sitek

Harvard Brain Science Initiative (Travel Grant)

  • Kevin R Sitek

National Institutes of Health (P41EB015897)

  • G Allan Johnson

National Institutes of Health (1S10OD010683-01)

  • G Allan Johnson

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

Ethics

Human subjects: The experimental procedures were approved by the ethics committee of the Faculty for Psychology and Neuroscience at Maastricht University (reference number: ERCPN-167_09_05_2016), and were performed in accordance with the approved guidelines and the Declaration of Helsinki. Written informed consent was obtained for every participant before conducting the experiments. All participants reported to have normal hearing, had no history of hearing disorder/impairments or neurological disease.

Reviewing Editor

  1. Jonathan Erik Peelle, Washington University in St. Louis, United States

Publication history

  1. Received: May 30, 2019
  2. Accepted: July 28, 2019
  3. Accepted Manuscript published: August 1, 2019 (version 1)
  4. Version of Record published: August 23, 2019 (version 2)

Copyright

© 2019, Sitek 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. Kevin R Sitek
  2. Omer Faruk Gulban
  3. Evan Calabrese
  4. G Allan Johnson
  5. Agustin Lage-Castellanos
  6. Michelle Moerel
  7. Satrajit S Ghosh
  8. Federico de Martino
(2019)
Mapping the human subcortical auditory system using histology, post mortem MRI and in vivo MRI at 7T
eLife 8:e48932.
https://doi.org/10.7554/eLife.48932

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