Neocortical pyramidal neurons with axons emerging from dendrites are frequent in non-primates, but rare in monkey and human

  1. Petra Wahle  Is a corresponding author
  2. Eric Sobierajski
  3. Ina Gasterstädt
  4. Nadja Lehmann
  5. Susanna Weber
  6. Joachim HR Lübke
  7. Maren Engelhardt
  8. Claudia Distler
  9. Gundela Meyer
  1. Ruhr University Bochum, Germany
  2. Heidelberg University, Germany
  3. Research Centre Jülich GmbH, Germany
  4. Johannes Kepler University, Austria
  5. University of La Laguna, Spain

Abstract

The canonical view of neuronal function is that inputs are received by dendrites and somata, become integrated in the somatodendritic compartment and upon reaching a sufficient threshold, generate axonal output with axons emerging from the cell body. The latter is not necessarily the case. Instead, axons may originate from dendrites. The terms 'axon carrying dendrite' (AcD) and 'AcD neurons' have been coined to describe this feature. In rodent hippocampus, AcD cells are shown to be functionally 'privileged', since inputs here can circumvent somatic integration and lead to immediate action potential initiation in the axon. Here, we report on the diversity of axon origins in neocortical pyramidal cells of rodent, ungulate, carnivore, and primate. Detection methods were Thy-1-EGFP labeling in mouse, retrograde biocytin tracing in rat, cat, ferret, and macaque, SMI-32/βIV-spectrin immunofluorescence in pig, cat, and macaque, and Golgi staining in macaque and human. We found that in non-primate mammals, 10-21% of pyramidal cells of layers II-VI had an AcD. In marked contrast, in macaque and human, this proportion was lower, and was particularly low for supragranular neurons. A comparison of six cortical areas (sensory, association, limbic) in three macaques yielded percentages of AcD cells which varied by a factor of 2 between the areas and between the individuals. Unexpectedly, pyramidal cells in the white matter of postnatal cat and aged human cortex exhibit AcDs to much higher percentages. In addition, interneurons assessed in developing cat and adult human cortex had AcDs at type-specific proportions and for some types at much higher percentages than pyramidal cells. Our findings expand the current knowledge regarding the distribution and proportion of AcD cells in neocortex of non-primate taxa, which strikingly differ from primates where these cells are mainly found in deeper layers and white matter.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 3 , 4, 5, 6, 7

Article and author information

Author details

  1. Petra Wahle

    Developmental Neurobiology, Ruhr University Bochum, Bochum, Germany
    For correspondence
    petra.wahle@rub.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8710-0375
  2. Eric Sobierajski

    Developmental Neurobiology, Ruhr University Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ina Gasterstädt

    Developmental Neurobiology, Ruhr University Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Nadja Lehmann

    Mannheim Center for Translational Neuroscience, Heidelberg University, Mannheim, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4801-3057
  5. Susanna Weber

    Mannheim Center for Translational Neuroscience, Heidelberg University, Mannheim, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Joachim HR Lübke

    Research Centre Jülich GmbH, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4086-3199
  7. Maren Engelhardt

    Faculty of Medicine, Johannes Kepler University, Linz, Austria
    Competing interests
    The authors declare that no competing interests exist.
  8. Claudia Distler

    Faculty of Biology and Biotechnology, Ruhr University Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Gundela Meyer

    Department of Basic Medical Science, University of La Laguna, Santa Cruz de Tenerife, Spain
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (WA 541/13-1)

  • Petra Wahle

Deutsche Forschungsgemeinschaft (WA 541/15-1)

  • Petra Wahle

Deutsche Forschungsgemeinschaft (EN 1240/2-1)

  • Maren Engelhardt

Deutsche Forschungsgemeinschaft (Ho-450/25-1)

  • Claudia Distler

Deutsche Forschungsgemeinschaft (SFB 509/A11)

  • Claudia Distler

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

Ethics

Human subjects: The data presented in this paper were collected via tissue sharing and from material that had originally been processed for projects not related to the present topic, i.e. no animals were sacrificed specifically for the present study. Human material was provided by Prof. Meyer and Prof. Lübke from previously published studies.

Reviewing Editor

  1. Kristine Krug, Otto-von-Guericke University Magdeburg, Germany

Publication history

  1. Received: December 3, 2021
  2. Preprint posted: December 27, 2021 (view preprint)
  3. Accepted: April 19, 2022
  4. Accepted Manuscript published: April 20, 2022 (version 1)
  5. Version of Record published: June 1, 2022 (version 2)

Copyright

© 2022, Wahle 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. Petra Wahle
  2. Eric Sobierajski
  3. Ina Gasterstädt
  4. Nadja Lehmann
  5. Susanna Weber
  6. Joachim HR Lübke
  7. Maren Engelhardt
  8. Claudia Distler
  9. Gundela Meyer
(2022)
Neocortical pyramidal neurons with axons emerging from dendrites are frequent in non-primates, but rare in monkey and human
eLife 11:e76101.
https://doi.org/10.7554/eLife.76101

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