Unique membrane properties and enhanced signal processing in human neocortical neurons

Author:

Eyal Guy1ORCID,Verhoog Matthijs B2,Testa-Silva Guilherme2,Deitcher Yair3,Lodder Johannes C2,Benavides-Piccione Ruth45,Morales Juan6,DeFelipe Javier45,de Kock Christiaan PJ2,Mansvelder Huibert D2,Segev Idan13ORCID

Affiliation:

1. Department of Neurobiology, The Hebrew University of Jerusalem, Jerusalem, Israel

2. Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, VU University Amsterdam, Amsterdam, The Netherlands

3. Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel

4. Instituto Cajal, Madrid, Spain

5. Laboratorio Cajal de Circuitos Corticales, Universidad Politécnica de Madrid, Madrid, Spain

6. Escuela Técnica Superior de Ingenieros Informáticos, Universidad Politécnica de Madrid, 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 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 (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.

Funder

Ministerio de Economía y Competitividad

European Union's Seventh Framework Programme

Hersenstichting Nederland

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

European Research Council

Human Brain Project

Gatsby Charitable Foundation

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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