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A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits

Computational models of neural circuits with varying levels of biophysical detail have been generated in pursuit of an underlying mechanism explaining the ubiquitous hippocampal theta rhythm. However, within the theta rhythm are at least two types with distinct frequencies associated with different...

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Autores principales: Skinner, Frances K., Rich, Scott, Lunyov, Anton R., Lefebvre, Jeremie, Chatzikalymniou, Alexandra P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097141/
https://www.ncbi.nlm.nih.gov/pubmed/33967702
http://dx.doi.org/10.3389/fncir.2021.643360
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author Skinner, Frances K.
Rich, Scott
Lunyov, Anton R.
Lefebvre, Jeremie
Chatzikalymniou, Alexandra P.
author_facet Skinner, Frances K.
Rich, Scott
Lunyov, Anton R.
Lefebvre, Jeremie
Chatzikalymniou, Alexandra P.
author_sort Skinner, Frances K.
collection PubMed
description Computational models of neural circuits with varying levels of biophysical detail have been generated in pursuit of an underlying mechanism explaining the ubiquitous hippocampal theta rhythm. However, within the theta rhythm are at least two types with distinct frequencies associated with different behavioral states, an aspect that must be considered in pursuit of these mechanistic explanations. Here, using our previously developed excitatory-inhibitory network models that generate theta rhythms, we investigate the robustness of theta generation to intrinsic neuronal variability by building a database of heterogeneous excitatory cells and implementing them in our microcircuit model. We specifically investigate the impact of three key “building block” features of the excitatory cell model that underlie our model design: these cells' rheobase, their capacity for post-inhibitory rebound, and their spike-frequency adaptation. We show that theta rhythms at various frequencies can arise dependent upon the combination of these building block features, and we find that the speed of these oscillations are dependent upon the excitatory cells' response to inhibitory drive, as encapsulated by their phase response curves. Taken together, these findings support a hypothesis for theta frequency control that includes two aspects: (i) an internal mechanism that stems from the building block features of excitatory cell dynamics; (ii) an external mechanism that we describe as “inhibition-based tuning” of excitatory cell firing. We propose that these mechanisms control theta rhythm frequencies and underlie their robustness.
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spelling pubmed-80971412021-05-06 A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits Skinner, Frances K. Rich, Scott Lunyov, Anton R. Lefebvre, Jeremie Chatzikalymniou, Alexandra P. Front Neural Circuits Neuroscience Computational models of neural circuits with varying levels of biophysical detail have been generated in pursuit of an underlying mechanism explaining the ubiquitous hippocampal theta rhythm. However, within the theta rhythm are at least two types with distinct frequencies associated with different behavioral states, an aspect that must be considered in pursuit of these mechanistic explanations. Here, using our previously developed excitatory-inhibitory network models that generate theta rhythms, we investigate the robustness of theta generation to intrinsic neuronal variability by building a database of heterogeneous excitatory cells and implementing them in our microcircuit model. We specifically investigate the impact of three key “building block” features of the excitatory cell model that underlie our model design: these cells' rheobase, their capacity for post-inhibitory rebound, and their spike-frequency adaptation. We show that theta rhythms at various frequencies can arise dependent upon the combination of these building block features, and we find that the speed of these oscillations are dependent upon the excitatory cells' response to inhibitory drive, as encapsulated by their phase response curves. Taken together, these findings support a hypothesis for theta frequency control that includes two aspects: (i) an internal mechanism that stems from the building block features of excitatory cell dynamics; (ii) an external mechanism that we describe as “inhibition-based tuning” of excitatory cell firing. We propose that these mechanisms control theta rhythm frequencies and underlie their robustness. Frontiers Media S.A. 2021-04-21 /pmc/articles/PMC8097141/ /pubmed/33967702 http://dx.doi.org/10.3389/fncir.2021.643360 Text en Copyright © 2021 Skinner, Rich, Lunyov, Lefebvre and Chatzikalymniou. https://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
Skinner, Frances K.
Rich, Scott
Lunyov, Anton R.
Lefebvre, Jeremie
Chatzikalymniou, Alexandra P.
A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits
title A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits
title_full A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits
title_fullStr A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits
title_full_unstemmed A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits
title_short A Hypothesis for Theta Rhythm Frequency Control in CA1 Microcircuits
title_sort hypothesis for theta rhythm frequency control in ca1 microcircuits
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097141/
https://www.ncbi.nlm.nih.gov/pubmed/33967702
http://dx.doi.org/10.3389/fncir.2021.643360
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