Unique membrane properties and enhanced signal processing in human neocortical neurons

  1. Guy Eyal
  2. Matthijs B Verhoog
  3. Guilherme Testa-Silva
  4. Yair Deitcher
  5. Johannes C Lodder
  6. Ruth Benavides-Piccione
  7. Juan Morales
  8. Javier DeFelipe
  9. Christiaan PJ de Kock
  10. Huibert D Mansvelder
  11. Idan Segev  Is a corresponding author
  1. The Hebrew University of Jerusalem, Israel
  2. VU University Amsterdam, Netherlands
  3. Interdisciplinary Center for Neural Computation, Israel
  4. VU University Amsterdam, Israel
  5. Instituto Cajal, Spain
  6. Universidad Politécnica de Madrid, Spain

Abstract

The advanced cognitive capabilities of the human brain are often attributed to our recently evolved neocortex. However, it is not known whether the basic building blocks of human neocortex, the pyramidal neurons, possess unique biophysical properties that might impact on cortical computations. Here we show that layer 2/3 pyramidal neurons from human temporal cortex (HL2/3 PCs) have a specific membrane capacitance (Cm) of ~0.5 µF/cm2, half of the commonly accepted 'universal' value (~1 µF/cm2) for biological membranes. This finding was predicted by fitting in vitro voltage transients to theoretical transients then validated by direct measurement of Cm in nucleated patch experiments. Models of 3D reconstructed HL2/3 PCs demonstrated that such low Cm value significantly enhances both synaptic charge-transfer from dendrites to soma and spike propagation along the axon. This is the first demonstration that human cortical neurons have distinctive membrane properties, suggesting important implications for signal processing in human neocortex.

Article and author information

Author details

  1. Guy Eyal

    Department of Neurobiology, The Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9537-5571
  2. Matthijs B Verhoog

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Guilherme Testa-Silva

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Yair Deitcher

    The Hebrew University of Jerusalem, Interdisciplinary Center for Neural Computation, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Johannes C Lodder

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Ruth Benavides-Piccione

    Instituto Cajal, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Juan Morales

    Escuela Técnica Superior de Ingenieros Informáticos, Universidad Politécnica de Madrid, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Javier DeFelipe

    Instituto Cajal, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  9. Christiaan PJ de Kock

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Huibert D Mansvelder

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  11. Idan Segev

    Department of Neurobiology, The Hebrew University of Jerusalem, Jerusalem, Israel
    For correspondence
    idan@lobster.ls.huji.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7279-9630

Funding

Netherlands Organization for Scientific Research ((NWO; 917.76.360, 912.06.148 and a VICI grant) ERC StG)

  • Huibert D Mansvelder

Hersenstichting Nederland ((grant HSN 2010(1)-09)

  • Christiaan PJ de Kock

Spanish Ministry of Economy and Competitiveness (the Cajal Blue Brain (C080020-09; the Spanish partner of the Blue Brain initiative from EPFL))

  • Javier DeFelipe

Human Brain Project and the Gatsby Charitable Foundation (grant agreement no. 604102)

  • Idan Segev

European Union's Seventh Framework Programme ((FP7/2007-2013) under grant agreement mo. 604102 (Human Brain Project))

  • Javier DeFelipe

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 animal experimental procedures were approved by the VU University's AnimalExperimentation Ethics Committee and were in accordance with institutional and Dutch license procedures (approved protocol INF09-02A1V1).

Human subjects: All procedures on human tissue were performed with the approval of the Medical Ethical Committee (METc) of the VU University Medical Centre (VUmc), with written informed consent by patients involved to use brain tissue removed for treatment of their disease for scientific research, and in accordance with Dutch license procedures and the declaration of Helsinki (VUmc METc approval 'kenmerk 2012/362').

Reviewing Editor

  1. Michael Häusser, University College London, United Kingdom

Publication history

  1. Received: March 31, 2016
  2. Accepted: October 5, 2016
  3. Accepted Manuscript published: October 6, 2016 (version 1)
  4. Version of Record published: November 8, 2016 (version 2)

Copyright

© 2016, Eyal 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. Guy Eyal
  2. Matthijs B Verhoog
  3. Guilherme Testa-Silva
  4. Yair Deitcher
  5. Johannes C Lodder
  6. Ruth Benavides-Piccione
  7. Juan Morales
  8. Javier DeFelipe
  9. Christiaan PJ de Kock
  10. Huibert D Mansvelder
  11. Idan Segev
(2016)
Unique membrane properties and enhanced signal processing in human neocortical neurons
eLife 5:e16553.
https://doi.org/10.7554/eLife.16553

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