Multi-scale mapping along the auditory hierarchy using high-resolution functional UltraSound in the awake ferret

  1. Célian Bimbard
  2. Charlie Demene
  3. Constantin Girard
  4. Susanne Radtke-Schuller
  5. Shihab Shamma
  6. Mickael Tanter  Is a corresponding author
  7. Yves Boubenec  Is a corresponding author
  1. CNRS UMR 8248, École Normale Supérieure, PSL Research University, France
  2. ESPCI ParisTech, PSL Research University, France

Abstract

A major challenge in neuroscience is to longitudinally monitor whole brain activity across multiple spatial scales in the same animal. Functional UltraSound (fUS) is an emerging technology that offers images of cerebral blood volume over large brain portions. Here we show for the first time its capability to resolve the functional organization of sensory systems at multiple scales in awake animals, both within small structures by precisely mapping and differentiating sensory responses, and between structures by elucidating the connectivity scheme of top-down projections. We demonstrate that fUS provides stable (over days), yet rapid, highly-resolved 3D tonotopic maps in the auditory pathway of awake ferrets, thus revealing its unprecedented functional resolution (100/300µm). This was performed in four different brain regions, including very small (1-2mm3 size), deeply situated subcortical (8mm deep) and previously undescribed structures in the ferret. Furthermore, we used fUS to map long-distance projections from frontal cortex, a key source of sensory response modulation, to auditory cortex.

Data availability

The data that support the findings of this study can be found at https://lsp.dec.ens.fr/en/research/supporting-materials-848. The full raw imaging files are >20Tb and are therefore available on request to the corresponding author.

The following data sets were generated

Article and author information

Author details

  1. Célian Bimbard

    Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, École Normale Supérieure, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Charlie Demene

    Institut Langevin, ESPCI ParisTech, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Constantin Girard

    Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, École Normale Supérieure, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Susanne Radtke-Schuller

    Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, École Normale Supérieure, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Shihab Shamma

    Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, École Normale Supérieure, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Mickael Tanter

    Institut Langevin, ESPCI ParisTech, PSL Research University, Paris, France
    For correspondence
    mickael.tanter@espci.fr
    Competing interests
    The authors declare that no competing interests exist.
  7. Yves Boubenec

    Laboratoire des Systèmes Perceptifs, CNRS UMR 8248, École Normale Supérieure, PSL Research University, Paris, France
    For correspondence
    boubenec@ens.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0106-6947

Funding

European Commission (339244-FUSIMAGINE)

  • Charlie Demene
  • Mickael Tanter

European Commission (ADG_20110406-ADAM)

  • Célian Bimbard
  • Constantin Girard
  • Susanne Radtke-Schuller
  • Shihab Shamma
  • Yves Boubenec

Agence Nationale de la Recherche (ANR-10-LABX-0087 IEC)

  • Célian Bimbard
  • Constantin Girard
  • Shihab Shamma
  • Yves Boubenec

Agence Nationale de la Recherche (ANR-10-IDEX-0001-02 PSL*)

  • Célian Bimbard
  • Charlie Demene
  • Constantin Girard
  • Susanne Radtke-Schuller
  • Shihab Shamma
  • Mickael Tanter
  • Yves Boubenec

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

Ethics

Animal experimentation: Experiments were approved by the French Ministry of Agriculture (protocol authorization: 01236.02) and strictly comply with the European directives on the protection of animals used for scientific purposes (2010/63/EU). All surgery was performed under anaesthesia (isoflurane 1%), and every effort was made to minimize suffering.

Reviewing Editor

  1. Andrew J King, University of Oxford, United Kingdom

Publication history

  1. Received: January 13, 2018
  2. Accepted: June 16, 2018
  3. Accepted Manuscript published: June 28, 2018 (version 1)
  4. Version of Record published: July 10, 2018 (version 2)

Copyright

© 2018, Bimbard 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. Célian Bimbard
  2. Charlie Demene
  3. Constantin Girard
  4. Susanne Radtke-Schuller
  5. Shihab Shamma
  6. Mickael Tanter
  7. Yves Boubenec
(2018)
Multi-scale mapping along the auditory hierarchy using high-resolution functional UltraSound in the awake ferret
eLife 7:e35028.
https://doi.org/10.7554/eLife.35028

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