Long-Range population dynamics of anatomically defined neocortical networks

  1. Jerry L Chen  Is a corresponding author
  2. Fabian F Voigt
  3. Mitra Javadzadeh
  4. Roland Krueppel
  5. Fritjof Helmchen  Is a corresponding author
  1. Boston University, United States
  2. University of Zurich, Switzerland
  3. Federal Ministry of Education and Research, Germany

Abstract

The coordination of activity across neocortical areas is essential for mammalian brain function. Understanding this process requires simultaneous functional measurements across the cortex. However, it has not been possible to dissociate direct cortico-cortical interactions from other sources of neuronal correlations by targeting recordings to neuronal subpopulations that anatomically project between areas. Here, we combined anatomical tracers with a novel multi-area two-photon microscope to perform simultaneous calcium imaging across mouse primary (S1) and secondary (S2) somatosensory whisker cortex during texture discrimination behavior, specifically identifying feedforward and feedback neurons. We observed coordinated S1-S2 activity that is related to motor behaviors such as goal-directed whisking and licking but is not specific to identified projection neurons. However, feedforward and feedback neurons especially participated in inter-areal coordination when motor behavior was paired with whisker-texture touches, suggesting that direct S1-S2 interactions are sensory-dependent. Our results demonstrate specific functional coordination of anatomically-identified projection neurons across sensory cortices.

Article and author information

Author details

  1. Jerry L Chen

    Department of Biology, Boston University, Boston, United States
    For correspondence
    jerry@chen-lab.org
    Competing interests
    The authors declare that no competing interests exist.
  2. Fabian F Voigt

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Mitra Javadzadeh

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Roland Krueppel

    Federal Ministry of Education and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Fritjof Helmchen

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    For correspondence
    helmchen@hifo.uzh.ch
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

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

Ethics

Animal experimentation: Experimental procedures followed the guidelines of the Veterinary Office of Switzerland and were approved by the Cantonal Veterinary Office in Zurich. Experiments were carried out under the approved licenses 62/2011 and 285/2014.

Version history

  1. Received: January 25, 2016
  2. Accepted: May 21, 2016
  3. Accepted Manuscript published: May 24, 2016 (version 1)
  4. Accepted Manuscript updated: May 25, 2016 (version 2)
  5. Version of Record published: June 17, 2016 (version 3)

Copyright

© 2016, Chen 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

  • 5,630
    Page views
  • 1,411
    Downloads
  • 89
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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. Jerry L Chen
  2. Fabian F Voigt
  3. Mitra Javadzadeh
  4. Roland Krueppel
  5. Fritjof Helmchen
(2016)
Long-Range population dynamics of anatomically defined neocortical networks
eLife 5:e14679.
https://doi.org/10.7554/eLife.14679

Share this article

https://doi.org/10.7554/eLife.14679

Further reading

    1. Neuroscience
    Sydney Trask, Nicole C Ferrara
    Insight

    Gradually reducing a source of fear during extinction treatments may weaken negative memories in the long term.

    1. Cell Biology
    2. Neuroscience
    Haibin Yu, Dandan Liu ... Kai Yuan
    Research Article

    O-GlcNAcylation is a dynamic post-translational modification that diversifies the proteome. Its dysregulation is associated with neurological disorders that impair cognitive function, and yet identification of phenotype-relevant candidate substrates in a brain-region specific manner remains unfeasible. By combining an O-GlcNAc binding activity derived from Clostridium perfringens OGA (CpOGA) with TurboID proximity labeling in Drosophila, we developed an O-GlcNAcylation profiling tool that translates O-GlcNAc modification into biotin conjugation for tissue-specific candidate substrates enrichment. We mapped the O-GlcNAc interactome in major brain regions of Drosophila and found that components of the translational machinery, particularly ribosomal subunits, were abundantly O-GlcNAcylated in the mushroom body of Drosophila brain. Hypo-O-GlcNAcylation induced by ectopic expression of active CpOGA in the mushroom body decreased local translational activity, leading to olfactory learning deficits that could be rescued by dMyc overexpression-induced increase of protein synthesis. Our study provides a useful tool for future dissection of tissue-specific functions of O-GlcNAcylation in Drosophila, and suggests a possibility that O-GlcNAcylation impacts cognitive function via regulating regional translational activity in the brain.