Functionally defined white matter of the macaque monkey brain reveals a dorso-ventral attention network

  1. Ilaria Sani  Is a corresponding author
  2. Brent C McPherson
  3. Heiko Stemmann
  4. Franco Pestilli
  5. Winrich A Freiwald  Is a corresponding author
  1. The Rockefeller University, United States
  2. Indiana University, United States
  3. University of Bremen, Germany

Abstract

Classical studies of attention have identified areas of parietal and frontal cortex as sources of attentional control. Recently, a ventral region in the macaque temporal cortex, the posterior infero-temporal dorsal area PITd, has been suggested as a third attentional control area. This raises the question of whether and how spatially distant areas coordinate a joint focus of attention. Here we tested the hypothesis that parieto-frontal attention areas and PITd are directly interconnected. By combining functional MRI with ex-vivo high-resolution diffusion MRI, we found that PITd and dorsal attention areas are all directly connected through three specific fascicles. These results ascribe a new function, the communication of attention signals, to two known fiber-bundles, highlight the importance of vertical interactions across the two visual streams, and imply that the control of endogenous attention, hitherto thought to reside in macaque dorsal cortical areas, is exerted by a dorso-ventral network.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data for Figures 2, 3, 4, 5, have been made available via the Open Science Framework (https://osf.io/8ks5t/).

The following data sets were generated

Article and author information

Author details

  1. Ilaria Sani

    Laboratory of Neural Systems, The Rockefeller University, New York, United States
    For correspondence
    isani01@rockefeller.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4389-7263
  2. Brent C McPherson

    Department of Psychological and Brain Sciences, Programs in Neuroscience and Cognitive Science, Indiana University Network Science Institute, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Heiko Stemmann

    Institute for Brain Research and Center for Advanced Imaging, University of Bremen, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Franco Pestilli

    Department of Psychological and Brain Sciences, Programs in Neuroscience and Cognitive Science, Indiana University Network Science Institute, Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2469-0494
  5. Winrich A Freiwald

    Laboratory of Neural Systems, The Rockefeller University, New York, United States
    For correspondence
    wfreiwald@rockefeller.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8456-5030

Funding

Leon Levy Foundation (https://leonlevyfoundation.org/leon-levy-fellowship-neuroscience)

  • Ilaria Sani

National Science Foundation (BCS-1734853)

  • Franco Pestilli

New York Stem Cell Foundation (https://nyscf.org)

  • Winrich A Freiwald

National Science Foundation (BCS-1057006)

  • Winrich A Freiwald

National Institutes of Health (NIMH ULTTR001108)

  • Franco Pestilli

Indiana Clinical and Translational Sciences Institute (Passthrough)

  • Franco Pestilli

Microsoft Research (Azure Credits Award)

  • Franco Pestilli

Indiana University (Areas of Emergent Research initiative Learning: Brains-Machines-Children)

  • Franco Pestilli

National Institutes of Health (1U54MH091657)

  • Franco Pestilli

National Science Foundation (IIS-1636893)

  • Franco Pestilli

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

Reviewing Editor

  1. Heidi Johansen-Berg, University of Oxford, United Kingdom

Ethics

Animal experimentation: Our Protocols protocol has been approved by The Rockefeller University, Institutional Animal Care and Use Committee. In vivo imaging procedures were performed at the Center for Advanced Imaging of Bremen University. They conformed to the National Institutes of Health Guide for Use and Care of Laboratory Animals, regulations for the welfare of experimental animals issued by the federal government of Germany,and stipulations of local Bremen authorities

Version history

  1. Received: July 29, 2018
  2. Accepted: December 20, 2018
  3. Accepted Manuscript published: January 2, 2019 (version 1)
  4. Version of Record published: January 24, 2019 (version 2)

Copyright

© 2019, Sani 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. Ilaria Sani
  2. Brent C McPherson
  3. Heiko Stemmann
  4. Franco Pestilli
  5. Winrich A Freiwald
(2019)
Functionally defined white matter of the macaque monkey brain reveals a dorso-ventral attention network
eLife 8:e40520.
https://doi.org/10.7554/eLife.40520

Share this article

https://doi.org/10.7554/eLife.40520

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