The basis of sharp spike onset in standard biophysical models
| Autor: | Bertrand Fontaine, Maria Teleńczuk, Romain Brette |
|---|---|
| Přispěvatelé: | HAL UPMC, Gestionnaire, Institut de la Vision, Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratory of Auditory Neurophysiology, Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven) |
| Jazyk: | angličtina |
| Rok vydání: | 2017 |
| Předmět: |
Physiology
[SDV.NEU.NB]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology Action Potentials lcsh:Medicine Pharmacokinetic Analysis Compartment Models Sodium Channels Nerve Fibers 0302 clinical medicine Animal Cells Medicine and Health Sciences Axon Resistive coupling lcsh:Science Neurons 0303 health sciences Basis (linear algebra) [PHYS.PHYS.PHYS-BIO-PH] Physics [physics]/Physics [physics]/Biological Physics [physics.bio-ph] Physics Pyramidal Cells Anatomy Electrophysiology medicine.anatomical_structure Physical Sciences Spike (software development) Cellular Types Current loop Research Article Two-Compartment Models Ganglion Cells [PHYS.PHYS.PHYS-BIO-PH]Physics [physics]/Physics [physics]/Biological Physics [physics.bio-ph] Models Neurological Materials Science Material Properties Biophysics Neurophysiology Capacitance Biology Membrane Potential 03 medical and health sciences medicine Animals Humans 030304 developmental biology Pharmacology lcsh:R [SDV.NEU.NB] Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Neurobiology Biology and Life Sciences Dendrites Cell Biology Axons Pharmacologic Analysis nervous system Cellular Neuroscience Soma lcsh:Q Orthodromic Neuroscience 030217 neurology & neurosurgery Initial segment |
| Zdroj: | PLoS ONE PLoS ONE, 2017, 12 (4), pp.e0175362. ⟨10.1371/journal.pone.0175362⟩ PLoS ONE, Public Library of Science, 2017, 12 (4), pp.e0175362. ⟨10.1371/journal.pone.0175362⟩ PLoS ONE, Vol 12, Iss 4, p e0175362 (2017) |
| ISSN: | 1932-6203 |
| Popis: | In most vertebrate neurons, spikes initiate in the axonal initial segment (AIS). When recorded in the soma, they have a surprisingly sharp onset, as if sodium (Na) channels opened abruptly. The main view stipulates that spikes initiate in a conventional manner at the distal end of the AIS, then progressively sharpen as they backpropagate to the soma. We examined the biophysical models used to substantiate this view, and we found that orthodromic spikes do no initiate through a local axonal current loop that propagates along the axon, but through a global current loop encompassing the AIS and soma, which forms an electrical dipole. Therefore, the phenomenon is not adequately modeled as the backpropagation of an electrical wave along the axon, since the wavelength would be as large as the entire system. Instead, in these models, we found that spike initiation rather follows the critical resistive coupling model proposed recently, where the Na current entering the AIS is matched by the axial resistive current flowing to the soma. Besides demonstrating it by examining the balance of currents at spike initiation, we show that the observed increase in spike sharpness along the axon is artifactual and disappears when an appropriate measure of rapidness is used; instead, somatic onset rapidness can be predicted from spike shape at initiation site. Finally, we reproduce the phenomenon in a two-compartment model, showing that it does not rely on propagation. In these models, the sharp onset of somatic spikes is therefore not an artifact of observing spikes at the incorrect location, but rather the signature that spikes are initiated through a global soma-AIS current loop forming an electrical dipole.Author summaryIn most vertebrate neurons, spikes are initiated in the axonal initial segment, next to the soma. When recorded at the soma, action potentials appear to suddenly rise as if all sodium channels opened at once. This has been previously attributed to the backpropagation of spikes from the initial segment to the soma. Here we demonstrate with biophysical models that backpropagation does not contribute to the sharpness of spike onset. Instead, we show that the phenomenon is due to the resistive coupling between the large somatodendritic compartment and the small axonal compartment, a geometrical discontinuity that leads to an abrupt variation in voltage. |
| Databáze: | OpenAIRE |
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