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Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness

Brain neurons exhibit complex electroresponsive properties – including intrinsic subthreshold oscillations and pacemaking, resonance and phase-reset – which are thought to play a critical role in controlling neural network dynamics. Although these properties emerge from detailed representations of m...

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Autores principales: Geminiani, Alice, Casellato, Claudia, Locatelli, Francesca, Prestori, Francesca, Pedrocchi, Alessandra, D'Angelo, Egidio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6287018/
https://www.ncbi.nlm.nih.gov/pubmed/30559658
http://dx.doi.org/10.3389/fninf.2018.00088
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author Geminiani, Alice
Casellato, Claudia
Locatelli, Francesca
Prestori, Francesca
Pedrocchi, Alessandra
D'Angelo, Egidio
author_facet Geminiani, Alice
Casellato, Claudia
Locatelli, Francesca
Prestori, Francesca
Pedrocchi, Alessandra
D'Angelo, Egidio
author_sort Geminiani, Alice
collection PubMed
description Brain neurons exhibit complex electroresponsive properties – including intrinsic subthreshold oscillations and pacemaking, resonance and phase-reset – which are thought to play a critical role in controlling neural network dynamics. Although these properties emerge from detailed representations of molecular-level mechanisms in “realistic” models, they cannot usually be generated by simplified neuronal models (although these may show spike-frequency adaptation and bursting). We report here that this whole set of properties can be generated by the extended generalized leaky integrate-and-fire (E-GLIF) neuron model. E-GLIF derives from the GLIF model family and is therefore mono-compartmental, keeps the limited computational load typical of a linear low-dimensional system, admits analytical solutions and can be tuned through gradient-descent algorithms. Importantly, E-GLIF is designed to maintain a correspondence between model parameters and neuronal membrane mechanisms through a minimum set of equations. In order to test its potential, E-GLIF was used to model a specific neuron showing rich and complex electroresponsiveness, the cerebellar Golgi cell, and was validated against experimental electrophysiological data recorded from Golgi cells in acute cerebellar slices. During simulations, E-GLIF was activated by stimulus patterns, including current steps and synaptic inputs, identical to those used for the experiments. The results demonstrate that E-GLIF can reproduce the whole set of complex neuronal dynamics typical of these neurons – including intensity-frequency curves, spike-frequency adaptation, post-inhibitory rebound bursting, spontaneous subthreshold oscillations, resonance, and phase-reset – providing a new effective tool to investigate brain dynamics in large-scale simulations.
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spelling pubmed-62870182018-12-17 Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness Geminiani, Alice Casellato, Claudia Locatelli, Francesca Prestori, Francesca Pedrocchi, Alessandra D'Angelo, Egidio Front Neuroinform Neuroscience Brain neurons exhibit complex electroresponsive properties – including intrinsic subthreshold oscillations and pacemaking, resonance and phase-reset – which are thought to play a critical role in controlling neural network dynamics. Although these properties emerge from detailed representations of molecular-level mechanisms in “realistic” models, they cannot usually be generated by simplified neuronal models (although these may show spike-frequency adaptation and bursting). We report here that this whole set of properties can be generated by the extended generalized leaky integrate-and-fire (E-GLIF) neuron model. E-GLIF derives from the GLIF model family and is therefore mono-compartmental, keeps the limited computational load typical of a linear low-dimensional system, admits analytical solutions and can be tuned through gradient-descent algorithms. Importantly, E-GLIF is designed to maintain a correspondence between model parameters and neuronal membrane mechanisms through a minimum set of equations. In order to test its potential, E-GLIF was used to model a specific neuron showing rich and complex electroresponsiveness, the cerebellar Golgi cell, and was validated against experimental electrophysiological data recorded from Golgi cells in acute cerebellar slices. During simulations, E-GLIF was activated by stimulus patterns, including current steps and synaptic inputs, identical to those used for the experiments. The results demonstrate that E-GLIF can reproduce the whole set of complex neuronal dynamics typical of these neurons – including intensity-frequency curves, spike-frequency adaptation, post-inhibitory rebound bursting, spontaneous subthreshold oscillations, resonance, and phase-reset – providing a new effective tool to investigate brain dynamics in large-scale simulations. Frontiers Media S.A. 2018-12-03 /pmc/articles/PMC6287018/ /pubmed/30559658 http://dx.doi.org/10.3389/fninf.2018.00088 Text en Copyright © 2018 Geminiani, Casellato, Locatelli, Prestori, Pedrocchi and D'Angelo. 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 Neuroscience
Geminiani, Alice
Casellato, Claudia
Locatelli, Francesca
Prestori, Francesca
Pedrocchi, Alessandra
D'Angelo, Egidio
Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness
title Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness
title_full Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness
title_fullStr Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness
title_full_unstemmed Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness
title_short Complex Dynamics in Simplified Neuronal Models: Reproducing Golgi Cell Electroresponsiveness
title_sort complex dynamics in simplified neuronal models: reproducing golgi cell electroresponsiveness
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6287018/
https://www.ncbi.nlm.nih.gov/pubmed/30559658
http://dx.doi.org/10.3389/fninf.2018.00088
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