Unique membrane properties and enhanced signal processing in human neocortical neurons
- The Hebrew University of Jerusalem, Israel
- VU University Amsterdam, Netherlands
- Interdisciplinary Center for Neural Computation, Israel
- VU University Amsterdam, Israel
- Instituto Cajal, Spain
- 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
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.
Reviewing Editor
- Michael Häusser, University College London, United Kingdom
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').
Version 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.
Metrics
-
- 6,298
- views
-
- 1,287
- downloads
-
- 146
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Unique membrane properties and enhanced signal processing in human neocortical neurons
eLife 5:e16553.
https://doi.org/10.7554/eLife.16553
Further reading
-
- Neuroscience
Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.
-
- Neuroscience
Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.
