Uniting functional network topology and oscillations in the fronto-parietal single unit network of behaving primates

  1. Benjamin Dann
  2. Jonathan A Michaels
  3. Stefan Schaffelhofer
  4. Hansjörg Scherberger  Is a corresponding author
  1. German Primate Center, Germany
  2. German Primate Center GmbH, Germany

Abstract

The functional communication of neurons in cortical networks underlies higher cognitive processes. Yet, little is known about the organization of the single neuron network or its relationship to the synchronization processes that are essential for its formation. Here, we show that the functional single neuron network of three fronto-parietal areas during active behavior of macaque monkeys is highly complex. The network was closely connected (small-world) and consisted of functional modules spanning these areas. Surprisingly, the importance of different neurons to the network was highly heterogeneous with a small number of neurons contributing strongly to the network function (hubs), which were in turn strongly inter-connected (rich-club). Examination of the network synchronization revealed that the identified rich-club consisted of neurons that were synchronized in the beta or low frequency range, whereas other neurons were mostly non-oscillatory synchronized. Therefore, oscillatory synchrony may be a central communication mechanism for highly organized functional spiking networks.

Article and author information

Author details

  1. Benjamin Dann

    Neurobiology Laboratory, German Primate Center, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Jonathan A Michaels

    Neurobiology Laboratory, German Primate Center, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5179-3181
  3. Stefan Schaffelhofer

    Neurobiology Lab, German Primate Center GmbH, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1006-971X
  4. Hansjörg Scherberger

    Neurobiology Lab, German Primate Center GmbH, Göttingen, Germany
    For correspondence
    hscherb@gwdg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6593-2800

Funding

Deutsche Forschungsgemeinschaft (SCHE 1575/1-1 & 3-1 and SFB889, C9)

  • Hansjörg Scherberger

European Commission (FP7-611687, NEBIAS)

  • Hansjörg Scherberger

Bundesministerium für Bildung und Forschung (BCCN-II, 01GQ1005C)

  • Hansjörg Scherberger

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

Reviewing Editor

  1. Klaas Enno Stephan, University of Zurich and ETH Zurich, Switzerland

Ethics

Animal experimentation: All procedures and animal care were conducted in accordance with the guidelines for the care and use of mammals in neuroscience and behavioral research (National Research Council, 2003), and were in agreement with German and European laws governing animal care. Authorization for conducting this study has been granted by the regional government office, the Animal Welfare Division of the Office for Consumer Protection and Food Safety of the State of Lower Saxony, Germany (permit no. 032/09). Monkey handling also followed the recommendations of the Weatherall Report of good animal practice. Animals were pairhoused in a spacious cage (well exceeding legal requirements) and were maintained on a 12-hour on/off lighting schedule. Housing procedures included an environmental enrichment program with access to toys, swings, and hidden treats (e.g., seeds in sawdust). Monkeys had visual and auditory contact to other monkeys. They were fed on a diet of enriched biscuits and fruits. Daily access to fluids was controlled during training and experimental periods to promote behavioral motivation. All surgical procedures were performed under anesthesia, and all efforts were made to minimize post-surgical pain or suffering. Institutional veterinarians continually monitored animal health and well-being.

Version history

  1. Received: March 2, 2016
  2. Accepted: August 14, 2016
  3. Accepted Manuscript published: August 15, 2016 (version 1)
  4. Version of Record published: September 12, 2016 (version 2)

Copyright

© 2016, Dann 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. Benjamin Dann
  2. Jonathan A Michaels
  3. Stefan Schaffelhofer
  4. Hansjörg Scherberger
(2016)
Uniting functional network topology and oscillations in the fronto-parietal single unit network of behaving primates
eLife 5:e15719.
https://doi.org/10.7554/eLife.15719

Share this article

https://doi.org/10.7554/eLife.15719

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