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Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus

Different neuronal types within brain motor areas contribute to the generation of complex motor behaviors. A widely studied songbird forebrain nucleus (HVC) has been recognized as fundamental in shaping the precise timing characteristics of birdsong. This is based, among other evidence, on the stret...

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Autores principales: Goldin, Matías A., Mindlin, Gabriel B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5568752/
https://www.ncbi.nlm.nih.gov/pubmed/28829769
http://dx.doi.org/10.1371/journal.pcbi.1005699
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author Goldin, Matías A.
Mindlin, Gabriel B.
author_facet Goldin, Matías A.
Mindlin, Gabriel B.
author_sort Goldin, Matías A.
collection PubMed
description Different neuronal types within brain motor areas contribute to the generation of complex motor behaviors. A widely studied songbird forebrain nucleus (HVC) has been recognized as fundamental in shaping the precise timing characteristics of birdsong. This is based, among other evidence, on the stretching and the “breaking” of song structure when HVC is cooled. However, little is known about the temperature effects that take place in its neurons. To address this, we investigated the dynamics of HVC both experimentally and computationally. We developed a technique where simultaneous electrophysiological recordings were performed during temperature manipulation of HVC. We recorded spontaneous activity and found three effects: widening of the spike shape, decrease of the firing rate and change in the interspike interval distribution. All these effects could be explained with a detailed conductance based model of all the neurons present in HVC. Temperature dependence of the ionic channel time constants explained the first effect, while the second was based in the changes of the maximal conductance using single synaptic excitatory inputs. The last phenomenon, only emerged after introducing a more realistic synaptic input to the inhibitory interneurons. Two timescales were present in the interspike distributions. The behavior of one timescale was reproduced with different input balances received form the excitatory neurons, whereas the other, which disappears with cooling, could not be found assuming poissonian synaptic inputs. Furthermore, the computational model shows that the bursting of the excitatory neurons arises naturally at normal brain temperature and that they have an intrinsic delay at low temperatures. The same effect occurs at single synapses, which may explain song stretching. These findings shed light on the temperature dependence of neuronal dynamics and present a comprehensive framework to study neuronal connectivity. This study, which is based on intrinsic neuronal characteristics, may help to understand emergent behavioral changes.
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spelling pubmed-55687522017-09-09 Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus Goldin, Matías A. Mindlin, Gabriel B. PLoS Comput Biol Research Article Different neuronal types within brain motor areas contribute to the generation of complex motor behaviors. A widely studied songbird forebrain nucleus (HVC) has been recognized as fundamental in shaping the precise timing characteristics of birdsong. This is based, among other evidence, on the stretching and the “breaking” of song structure when HVC is cooled. However, little is known about the temperature effects that take place in its neurons. To address this, we investigated the dynamics of HVC both experimentally and computationally. We developed a technique where simultaneous electrophysiological recordings were performed during temperature manipulation of HVC. We recorded spontaneous activity and found three effects: widening of the spike shape, decrease of the firing rate and change in the interspike interval distribution. All these effects could be explained with a detailed conductance based model of all the neurons present in HVC. Temperature dependence of the ionic channel time constants explained the first effect, while the second was based in the changes of the maximal conductance using single synaptic excitatory inputs. The last phenomenon, only emerged after introducing a more realistic synaptic input to the inhibitory interneurons. Two timescales were present in the interspike distributions. The behavior of one timescale was reproduced with different input balances received form the excitatory neurons, whereas the other, which disappears with cooling, could not be found assuming poissonian synaptic inputs. Furthermore, the computational model shows that the bursting of the excitatory neurons arises naturally at normal brain temperature and that they have an intrinsic delay at low temperatures. The same effect occurs at single synapses, which may explain song stretching. These findings shed light on the temperature dependence of neuronal dynamics and present a comprehensive framework to study neuronal connectivity. This study, which is based on intrinsic neuronal characteristics, may help to understand emergent behavioral changes. Public Library of Science 2017-08-22 /pmc/articles/PMC5568752/ /pubmed/28829769 http://dx.doi.org/10.1371/journal.pcbi.1005699 Text en © 2017 Goldin, Mindlin http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Goldin, Matías A.
Mindlin, Gabriel B.
Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
title Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
title_full Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
title_fullStr Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
title_full_unstemmed Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
title_short Temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
title_sort temperature manipulation of neuronal dynamics in a forebrain motor control nucleus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5568752/
https://www.ncbi.nlm.nih.gov/pubmed/28829769
http://dx.doi.org/10.1371/journal.pcbi.1005699
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