Unique membrane properties and enhanced signal processing in human neocortical neurons
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
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
- Michael Häusser, University College London, United Kingdom
Publication history
- Received: March 31, 2016
- Accepted: October 5, 2016
- Accepted Manuscript published: October 6, 2016 (version 1)
- 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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