Cell-type specific innervation of cortical pyramidal cells at their apical dendrites

  1. Ali Karimi
  2. Jan Odenthal
  3. Florian Drawitsch
  4. Kevin M Boergens
  5. Moritz Helmstaedter  Is a corresponding author
  1. Max Planck Institute for Brain Research, Germany

Abstract

We investigated the synaptic innervation of apical dendrites of cortical pyramidal cells in a region between layers (L) 1 and 2 using 3-D electron microscopy applied to four cortical regions in mouse. We found the relative inhibitory input at the apical dendrite's main bifurcation to be more than 2-fold larger for L2 than L3 and L5 thick-tufted pyramidal cells. Towards the distal tuft dendrites in upper L1, the relative inhibitory input was at least about 2-fold larger for L5 pyramidal cells than for all others. Only L3 pyramidal cells showed homogeneous inhibitory input fraction. The inhibitory-to-excitatory synaptic ratio is thus specific for the types of pyramidal cells. Inhibitory axons preferentially innervated either L2 or L3/5 apical dendrites, but not both. These findings describe connectomic principles for the control of pyramidal cells at their apical dendrites and support differential computational properties of L2,L3 and subtypes of L5 pyramidal cells in cortex.

Data availability

All 6 datasets are available for browsing at webknossos.org using the following links.S1: https://wklink.org/8732V2: https://wklink.org/9812PPC: https://wklink.org/1262ACC: https://wklink.org/6712LPtA: https://wklink.org/8912PPC2: https://wklink.org/6347All software used for analysis is available at (https://gitlab.mpcdf.mpg.de/connectomics/apicaltuftpaper) under the MIT license.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Ali Karimi

    Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6477-2523
  2. Jan Odenthal

    Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    No competing interests declared.
  3. Florian Drawitsch

    Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9543-1417
  4. Kevin M Boergens

    Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt, Germany
    Competing interests
    No competing interests declared.
  5. Moritz Helmstaedter

    Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt, Germany
    For correspondence
    mh@brain.mpg.de
    Competing interests
    Moritz Helmstaedter, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7973-0767

Funding

Max-Planck-Gesellschaft (Open-access funding)

  • Ali Karimi
  • Jan Odenthal
  • Florian Drawitsch
  • Kevin M Boergens
  • Moritz Helmstaedter

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

Ethics

Animal experimentation: All experimental procedures were performed according to the law of animal experimentation issued by the German Federal Government under the supervision of local ethics committees and according to the guidelines of the Max Planck Society. The experimental procedures were approved by Regierungspräsidium Darmstadt, under protocol ID V54 - 19c20/15 F126/1015 (LPtA, PPC2) or V54 - 19 c 20/15 - F126/1002 (V2, PPC, ACC). The S1 sample was prepared following experimental procedures approved by Regierung von Oberbayern, 55.2-1-54-2532.3-103-12.

Reviewing Editor

  1. Carol A Mason, Columbia University, United States

Publication history

  1. Received: March 14, 2019
  2. Accepted: February 26, 2020
  3. Accepted Manuscript published: February 28, 2020 (version 1)
  4. Version of Record published: June 16, 2020 (version 2)

Copyright

© 2020, Karimi 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. Ali Karimi
  2. Jan Odenthal
  3. Florian Drawitsch
  4. Kevin M Boergens
  5. Moritz Helmstaedter
(2020)
Cell-type specific innervation of cortical pyramidal cells at their apical dendrites
eLife 9:e46876.
https://doi.org/10.7554/eLife.46876

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