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Unique membrane properties and enhanced signal processing in human neocortical neurons

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 the human neocortex, the pyramidal neurons, possess unique biophysical properties that might impact on cortical computations. H...

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Autores principales: Eyal, Guy, Verhoog, Matthijs B, Testa-Silva, Guilherme, Deitcher, Yair, Lodder, Johannes C, Benavides-Piccione, Ruth, Morales, Juan, DeFelipe, Javier, de Kock, Christiaan PJ, Mansvelder, Huibert D, Segev, Idan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100995/
https://www.ncbi.nlm.nih.gov/pubmed/27710767
http://dx.doi.org/10.7554/eLife.16553
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author Eyal, Guy
Verhoog, Matthijs B
Testa-Silva, Guilherme
Deitcher, Yair
Lodder, Johannes C
Benavides-Piccione, Ruth
Morales, Juan
DeFelipe, Javier
de Kock, Christiaan PJ
Mansvelder, Huibert D
Segev, Idan
author_facet Eyal, Guy
Verhoog, Matthijs B
Testa-Silva, Guilherme
Deitcher, Yair
Lodder, Johannes C
Benavides-Piccione, Ruth
Morales, Juan
DeFelipe, Javier
de Kock, Christiaan PJ
Mansvelder, Huibert D
Segev, Idan
author_sort Eyal, Guy
collection PubMed
description 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 the 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 (C(m)) of ~0.5 µF/cm(2), half of the commonly accepted 'universal' value (~1 µF/cm(2)) for biological membranes. This finding was predicted by fitting in vitro voltage transients to theoretical transients then validated by direct measurement of C(m) in nucleated patch experiments. Models of 3D reconstructed HL2/3 PCs demonstrated that such low C(m) 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. DOI: http://dx.doi.org/10.7554/eLife.16553.001
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spelling pubmed-51009952016-11-10 Unique membrane properties and enhanced signal processing in human neocortical neurons Eyal, Guy Verhoog, Matthijs B Testa-Silva, Guilherme Deitcher, Yair Lodder, Johannes C Benavides-Piccione, Ruth Morales, Juan DeFelipe, Javier de Kock, Christiaan PJ Mansvelder, Huibert D Segev, Idan eLife Human Biology and Medicine 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 the 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 (C(m)) of ~0.5 µF/cm(2), half of the commonly accepted 'universal' value (~1 µF/cm(2)) for biological membranes. This finding was predicted by fitting in vitro voltage transients to theoretical transients then validated by direct measurement of C(m) in nucleated patch experiments. Models of 3D reconstructed HL2/3 PCs demonstrated that such low C(m) 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. DOI: http://dx.doi.org/10.7554/eLife.16553.001 eLife Sciences Publications, Ltd 2016-10-06 /pmc/articles/PMC5100995/ /pubmed/27710767 http://dx.doi.org/10.7554/eLife.16553 Text en © 2016, Eyal et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Human Biology and Medicine
Eyal, Guy
Verhoog, Matthijs B
Testa-Silva, Guilherme
Deitcher, Yair
Lodder, Johannes C
Benavides-Piccione, Ruth
Morales, Juan
DeFelipe, Javier
de Kock, Christiaan PJ
Mansvelder, Huibert D
Segev, Idan
Unique membrane properties and enhanced signal processing in human neocortical neurons
title Unique membrane properties and enhanced signal processing in human neocortical neurons
title_full Unique membrane properties and enhanced signal processing in human neocortical neurons
title_fullStr Unique membrane properties and enhanced signal processing in human neocortical neurons
title_full_unstemmed Unique membrane properties and enhanced signal processing in human neocortical neurons
title_short Unique membrane properties and enhanced signal processing in human neocortical neurons
title_sort unique membrane properties and enhanced signal processing in human neocortical neurons
topic Human Biology and Medicine
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100995/
https://www.ncbi.nlm.nih.gov/pubmed/27710767
http://dx.doi.org/10.7554/eLife.16553
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