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Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons

The cortical layer 1 (L1) contains a population of GABAergic interneurons, considered a key component of information integration, processing, and relaying in neocortical networks. In fact, L1 interneurons combine top–down information with feed-forward sensory inputs in layer 2/3 and 5 pyramidal cell...

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Autores principales: Borda Bossana, Stefano, Verbist, Christophe, Giugliano, Michele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7313227/
https://www.ncbi.nlm.nih.gov/pubmed/32625063
http://dx.doi.org/10.3389/fncel.2020.00118
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author Borda Bossana, Stefano
Verbist, Christophe
Giugliano, Michele
author_facet Borda Bossana, Stefano
Verbist, Christophe
Giugliano, Michele
author_sort Borda Bossana, Stefano
collection PubMed
description The cortical layer 1 (L1) contains a population of GABAergic interneurons, considered a key component of information integration, processing, and relaying in neocortical networks. In fact, L1 interneurons combine top–down information with feed-forward sensory inputs in layer 2/3 and 5 pyramidal cells (PCs), while filtering their incoming signals. Despite the importance of L1 for network emerging phenomena, little is known on the dynamics of the spike initiation and the encoding properties of its neurons. Using acute brain tissue slices from the rat neocortex, combined with the analysis of an existing database of model neurons, we investigated the dynamical transfer properties of these cells by sampling an entire population of known “electrical classes” and comparing experiments and model predictions. We found the bandwidth of spike initiation to be significantly narrower than in L2/3 and 5 PCs, with values below 100 cycle/s, but without significant heterogeneity in the cell response properties across distinct electrical types. The upper limit of the neuronal bandwidth was significantly correlated to the mean firing rate, as anticipated from theoretical studies but not reported for PCs. At high spectral frequencies, the magnitude of the neuronal response attenuated as a power-law, with an exponent significantly smaller than what was reported for pyramidal neurons and reminiscent of the dynamics of a “leaky” integrate-and-fire model of spike initiation. Finally, most of our in vitro results matched quantitatively the numerical simulations of the models as a further contribution to independently validate the models against novel experimental data.
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spelling pubmed-73132272020-07-02 Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons Borda Bossana, Stefano Verbist, Christophe Giugliano, Michele Front Cell Neurosci Cellular Neuroscience The cortical layer 1 (L1) contains a population of GABAergic interneurons, considered a key component of information integration, processing, and relaying in neocortical networks. In fact, L1 interneurons combine top–down information with feed-forward sensory inputs in layer 2/3 and 5 pyramidal cells (PCs), while filtering their incoming signals. Despite the importance of L1 for network emerging phenomena, little is known on the dynamics of the spike initiation and the encoding properties of its neurons. Using acute brain tissue slices from the rat neocortex, combined with the analysis of an existing database of model neurons, we investigated the dynamical transfer properties of these cells by sampling an entire population of known “electrical classes” and comparing experiments and model predictions. We found the bandwidth of spike initiation to be significantly narrower than in L2/3 and 5 PCs, with values below 100 cycle/s, but without significant heterogeneity in the cell response properties across distinct electrical types. The upper limit of the neuronal bandwidth was significantly correlated to the mean firing rate, as anticipated from theoretical studies but not reported for PCs. At high spectral frequencies, the magnitude of the neuronal response attenuated as a power-law, with an exponent significantly smaller than what was reported for pyramidal neurons and reminiscent of the dynamics of a “leaky” integrate-and-fire model of spike initiation. Finally, most of our in vitro results matched quantitatively the numerical simulations of the models as a further contribution to independently validate the models against novel experimental data. Frontiers Media S.A. 2020-06-17 /pmc/articles/PMC7313227/ /pubmed/32625063 http://dx.doi.org/10.3389/fncel.2020.00118 Text en Copyright © 2020 Borda Bossana, Verbist and Giugliano. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular Neuroscience
Borda Bossana, Stefano
Verbist, Christophe
Giugliano, Michele
Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons
title Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons
title_full Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons
title_fullStr Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons
title_full_unstemmed Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons
title_short Homogeneous and Narrow Bandwidth of Spike Initiation in Rat L1 Cortical Interneurons
title_sort homogeneous and narrow bandwidth of spike initiation in rat l1 cortical interneurons
topic Cellular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7313227/
https://www.ncbi.nlm.nih.gov/pubmed/32625063
http://dx.doi.org/10.3389/fncel.2020.00118
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