Anatomy of nerve fiber bundles at micrometer-resolution in the vervet monkey visual system

  1. Hiromasa Takemura  Is a corresponding author
  2. Nicola Palomero-Gallagher  Is a corresponding author
  3. Markus Axer
  4. David Gräßel
  5. Matthew J Jorgensen
  6. Roger Woods
  7. Karl Zilles
  1. National Institute of Information and Communications Technology, Japan
  2. Research Centre Jülich, Germany
  3. Wake Forest School of Medicine, United States
  4. University of California, Los Angeles, United States

Abstract

Although the primate visual system has been extensively studied, detailed spatial organization of white matter fiber tracts carrying visual information between areas has not been fully established. This is mainly due to the large gap between tracer studies and diffusion-weighted MRI studies, which focus on specific axonal connections and macroscale organization of fiber tracts, respectively. Here we used 3D polarization light imaging (3D-PLI), which enables direct visualization of fiber tracts at micrometer resolution, to identify and visualize fiber tracts of the visual system, such as stratum sagittale, inferior longitudinal fascicle, vertical occipital fascicle, tapetum and dorsal occipital bundle in vervet monkey brains. Moreover, 3D-PLI data provide detailed information on cortical projections of these tracts, distinction between neighboring tracts, and novel short-range pathways. This work provides essential information for interpretation of functional and diffusion-weighted MRI data, as well as revision of wiring diagrams based upon observations in the vervet visual system.

Data availability

Original data is publicly available via the EBRAINS platform of the Human Brain Project (Axer et al., 2020; DOI: 10.25493/AFR3-KDK).

The following data sets were generated

Article and author information

Author details

  1. Hiromasa Takemura

    Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology, Suita-shi, Osaka, Japan
    For correspondence
    htakemur@nict.go.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2096-2384
  2. Nicola Palomero-Gallagher

    Institute of Neuroscience and Medicine INM-1, Research Centre Jülich, Jülich, Germany
    For correspondence
    n.palomero-gallagher@fz-juelich.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4463-8578
  3. Markus Axer

    Institute of Neuroscience and Medicine INM-1, Research Centre Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. David Gräßel

    Institute of Neuroscience and Medicine INM-1, Research Centre Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3228-8048
  5. Matthew J Jorgensen

    Department of Pathology, Section on Comparative Medicine, Wake Forest School of Medicine, Winston-Salem, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Roger Woods

    Ahmanson-Lovelace Brain Mapping Center, Departments of Neurology and of Psychiatry and Biobehavioral Sciences, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Karl Zilles

    Institute of Neuroscience and Medicine INM-1, Research Centre Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Japan Society for the Promotion of Science (JP17H04684)

  • Hiromasa Takemura

Japan Society for the Promotion of Science (JP15J00412)

  • Hiromasa Takemura

European Union's Horizon 2020 Research and Innovation Programme (785907 (HBP SGA2))

  • Markus Axer
  • Karl Zilles

National Institutes of Health (R01 MH092311)

  • Roger Woods

P40 grant (OD010965)

  • Matthew J Jorgensen

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

Ethics

Animal experimentation: Vervet monkeys (Chlorocebus aethiops sabaeus) used in this study were part of the Vervet Research Colony and were housed at the Wake Forest School of Medicine. Macaque monkeys (Macaca fascicularis) were obtained from Covance (Münster, Germany). Animals were colony-born, of known age and were mother-reared in species-typical social groups. The present study did not include experimental procedures with live animals. Brains were obtained when animals were sacrificed to reduce the size of the colony, where they were maintained in accordance with the guidelines of the Directive 2010/63/eu of the European Parliament and of the Council on the protection of animals used for scientific purposes or the Wake Forest Institutional Animal Care and Use Committee IACUC #A11-219. Euthanasia procedures conformed to the AVMA Guidelines for the Euthanasia of Animals.

Copyright

© 2020, Takemura 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.

Metrics

  • 2,900
    views
  • 315
    downloads
  • 27
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Hiromasa Takemura
  2. Nicola Palomero-Gallagher
  3. Markus Axer
  4. David Gräßel
  5. Matthew J Jorgensen
  6. Roger Woods
  7. Karl Zilles
(2020)
Anatomy of nerve fiber bundles at micrometer-resolution in the vervet monkey visual system
eLife 9:e55444.
https://doi.org/10.7554/eLife.55444

Share this article

https://doi.org/10.7554/eLife.55444

Further reading

    1. Neuroscience
    William T Redman, Santiago Acosta-Mendoza ... Michael J Goard
    Research Article

    Although grid cells are one of the most well-studied functional classes of neurons in the mammalian brain, whether there is a single orientation and spacing value per grid module has not been carefully tested. We analyze a recent large-scale recording of medial entorhinal cortex to characterize the presence and degree of heterogeneity of grid properties within individual modules. We find evidence for small, but robust, variability and hypothesize that this property of the grid code could enhance the encoding of local spatial information. Performing analysis on synthetic populations of grid cells, where we have complete control over the amount heterogeneity in grid properties, we demonstrate that grid property variability of a similar magnitude to the analyzed data leads to significantly decreased decoding error. This holds even when restricted to activity from a single module. Our results highlight how the heterogeneity of the neural response properties may benefit coding and opens new directions for theoretical and experimental analysis of grid cells.

    1. Neuroscience
    Maren Klingelhöfer-Jens, Katharina Hutterer ... Tina B Lonsdorf
    Research Article

    Childhood adversity is a strong predictor of developing psychopathological conditions. Multiple theories on the mechanisms underlying this association have been suggested which, however, differ in the operationalization of ‘exposure.’ Altered (threat) learning mechanisms represent central mechanisms by which environmental inputs shape emotional and cognitive processes and ultimately behavior. 1402 healthy participants underwent a fear conditioning paradigm (acquisition training, generalization), while acquiring skin conductance responses (SCRs) and ratings (arousal, valence, and contingency). Childhood adversity was operationalized as (1) dichotomization, and following (2) the specificity model, (3) the cumulative risk model, and (4) the dimensional model. Individuals exposed to childhood adversity showed blunted physiological reactivity in SCRs, but not ratings, and reduced CS+/CS- discrimination during both phases, mainly driven by attenuated CS+ responding. The latter was evident across different operationalizations of ‘exposure’ following the different theories. None of the theories tested showed clear explanatory superiority. Notably, a remarkably different pattern of increased responding to the CS- is reported in the literature for anxiety patients, suggesting that individuals exposed to childhood adversity may represent a specific sub-sample. We highlight that theories linking childhood adversity to (vulnerability to) psychopathology need refinement.