Self-organization of modular network architecture by activity-dependent neuronal migration and outgrowth

  1. Samora Okujeni  Is a corresponding author
  2. Ulrich Egert
  1. University of Freiburg, Germany

Abstract

The spatial distribution of neurons and activity-dependent neurite outgrowth shape long-range interaction, recurrent local connectivity and the modularity in neuronal networks. We investigated how this mesoscale architecture develops by interaction of neurite outgrowth, cell migration and activity in cultured networks of rat cortical neurons and show that simple rules can explain variations of network modularity. In contrast to theoretical studies on activity-dependent outgrowth but consistent with predictions for modular networks, spontaneous activity and the rate of synchronized bursts increased with clustering, whereas peak firing rates in bursts increased in highly interconnected homogeneous networks. As Ca2+ influx increased exponentially with increasing network recruitment during bursts, its modulation was highly correlated to peak firing rates. During network maturation, long-term estimates of Ca2+ influx showed convergence, even for highly different mesoscale architectures, neurite extent, connectivity, modularity and average activity levels, indicating homeostatic regulation towards a common set-point of Ca2+ influx.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Matlab code and source data files have been provided for Figures 3-6.

Article and author information

Author details

  1. Samora Okujeni

    Department of Microsystems Engineering, Faculty of Engineering, University of Freiburg, Freiburg, Germany
    For correspondence
    samora.okujeni@biologie.uni-freiburg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7924-3651
  2. Ulrich Egert

    Department of Microsystems Engineering, Faculty of Engineering, University of Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4583-0425

Funding

Deutsche Forschungsgemeinschaft (EXC 1086)

  • Ulrich Egert

Bundesministerium für Bildung und Forschung (FKZ 01GQ0420)

  • Ulrich Egert

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

Reviewing Editor

  1. Timothy O'Leary, University of Cambridge, United Kingdom

Ethics

Animal experimentation: Animal handling and tissue preparation were done in accordance with the guidelines for animal research at the University of Freiburg and approved by the Regierungspräsidium Freiburg (permits X-12/08D, X-16/07A, X-15/01H, X-18/04K).

Version history

  1. Received: April 26, 2019
  2. Accepted: September 16, 2019
  3. Accepted Manuscript published: September 17, 2019 (version 1)
  4. Version of Record published: October 8, 2019 (version 2)
  5. Version of Record updated: October 11, 2019 (version 3)

Copyright

© 2019, Okujeni & Egert

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

  • 2,798
    views
  • 364
    downloads
  • 16
    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. Samora Okujeni
  2. Ulrich Egert
(2019)
Self-organization of modular network architecture by activity-dependent neuronal migration and outgrowth
eLife 8:e47996.
https://doi.org/10.7554/eLife.47996

Share this article

https://doi.org/10.7554/eLife.47996

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.