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Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics

The response of a neuronal population over a space of inputs depends on the intrinsic properties of its constituent neurons. Two main modes of single neuron dynamics–integration and resonance–have been distinguished. While resonator cell types exist in a variety of brain areas, few models incorporat...

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Autores principales: Puelma Touzel, Maximilian, Wolf, Fred
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4697854/
https://www.ncbi.nlm.nih.gov/pubmed/26720924
http://dx.doi.org/10.1371/journal.pcbi.1004636
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author Puelma Touzel, Maximilian
Wolf, Fred
author_facet Puelma Touzel, Maximilian
Wolf, Fred
author_sort Puelma Touzel, Maximilian
collection PubMed
description The response of a neuronal population over a space of inputs depends on the intrinsic properties of its constituent neurons. Two main modes of single neuron dynamics–integration and resonance–have been distinguished. While resonator cell types exist in a variety of brain areas, few models incorporate this feature and fewer have investigated its effects. To understand better how a resonator’s frequency preference emerges from its intrinsic dynamics and contributes to its local area’s population firing rate dynamics, we analyze the dynamic gain of an analytically solvable two-degree of freedom neuron model. In the Fokker-Planck approach, the dynamic gain is intractable. The alternative Gauss-Rice approach lifts the resetting of the voltage after a spike. This allows us to derive a complete expression for the dynamic gain of a resonator neuron model in terms of a cascade of filters on the input. We find six distinct response types and use them to fully characterize the routes to resonance across all values of the relevant timescales. We find that resonance arises primarily due to slow adaptation with an intrinsic frequency acting to sharpen and adjust the location of the resonant peak. We determine the parameter regions for the existence of an intrinsic frequency and for subthreshold and spiking resonance, finding all possible intersections of the three. The expressions and analysis presented here provide an account of how intrinsic neuron dynamics shape dynamic population response properties and can facilitate the construction of an exact theory of correlations and stability of population activity in networks containing populations of resonator neurons.
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spelling pubmed-46978542016-01-13 Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics Puelma Touzel, Maximilian Wolf, Fred PLoS Comput Biol Research Article The response of a neuronal population over a space of inputs depends on the intrinsic properties of its constituent neurons. Two main modes of single neuron dynamics–integration and resonance–have been distinguished. While resonator cell types exist in a variety of brain areas, few models incorporate this feature and fewer have investigated its effects. To understand better how a resonator’s frequency preference emerges from its intrinsic dynamics and contributes to its local area’s population firing rate dynamics, we analyze the dynamic gain of an analytically solvable two-degree of freedom neuron model. In the Fokker-Planck approach, the dynamic gain is intractable. The alternative Gauss-Rice approach lifts the resetting of the voltage after a spike. This allows us to derive a complete expression for the dynamic gain of a resonator neuron model in terms of a cascade of filters on the input. We find six distinct response types and use them to fully characterize the routes to resonance across all values of the relevant timescales. We find that resonance arises primarily due to slow adaptation with an intrinsic frequency acting to sharpen and adjust the location of the resonant peak. We determine the parameter regions for the existence of an intrinsic frequency and for subthreshold and spiking resonance, finding all possible intersections of the three. The expressions and analysis presented here provide an account of how intrinsic neuron dynamics shape dynamic population response properties and can facilitate the construction of an exact theory of correlations and stability of population activity in networks containing populations of resonator neurons. Public Library of Science 2015-12-31 /pmc/articles/PMC4697854/ /pubmed/26720924 http://dx.doi.org/10.1371/journal.pcbi.1004636 Text en © 2015 Puelma Touzel, Wolf http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Puelma Touzel, Maximilian
Wolf, Fred
Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics
title Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics
title_full Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics
title_fullStr Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics
title_full_unstemmed Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics
title_short Complete Firing-Rate Response of Neurons with Complex Intrinsic Dynamics
title_sort complete firing-rate response of neurons with complex intrinsic dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4697854/
https://www.ncbi.nlm.nih.gov/pubmed/26720924
http://dx.doi.org/10.1371/journal.pcbi.1004636
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