Cargando…

Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus

The dynamics of circadian rhythms needs to be adapted to day length changes between summer and winter. It has been observed experimentally, however, that the dynamics of individual neurons of the suprachiasmatic nucleus (SCN) does not change as the seasons change. Rather, the seasonal adaptation of...

Descripción completa

Detalles Bibliográficos
Autores principales: Bodenstein, Christian, Gosak, Marko, Schuster, Stefan, Marhl, Marko, Perc, Matjaž
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3447953/
https://www.ncbi.nlm.nih.gov/pubmed/23028293
http://dx.doi.org/10.1371/journal.pcbi.1002697
_version_ 1782244203306156032
author Bodenstein, Christian
Gosak, Marko
Schuster, Stefan
Marhl, Marko
Perc, Matjaž
author_facet Bodenstein, Christian
Gosak, Marko
Schuster, Stefan
Marhl, Marko
Perc, Matjaž
author_sort Bodenstein, Christian
collection PubMed
description The dynamics of circadian rhythms needs to be adapted to day length changes between summer and winter. It has been observed experimentally, however, that the dynamics of individual neurons of the suprachiasmatic nucleus (SCN) does not change as the seasons change. Rather, the seasonal adaptation of the circadian clock is hypothesized to be a consequence of changes in the intercellular dynamics, which leads to a phase distribution of electrical activity of SCN neurons that is narrower in winter and broader during summer. Yet to understand this complex intercellular dynamics, a more thorough understanding of the impact of the network structure formed by the SCN neurons is needed. To that effect, we propose a mathematical model for the dynamics of the SCN neuronal architecture in which the structure of the network plays a pivotal role. Using our model we show that the fraction of long-range cell-to-cell connections and the seasonal changes in the daily rhythms may be tightly related. In particular, simulations of the proposed mathematical model indicate that the fraction of long-range connections between the cells adjusts the phase distribution and consequently the length of the behavioral activity as follows: dense long-range connections during winter lead to a narrow activity phase, while rare long-range connections during summer lead to a broad activity phase. Our model is also able to account for the experimental observations indicating a larger light-induced phase-shift of the circadian clock during winter, which we show to be a consequence of higher synchronization between neurons. Our model thus provides evidence that the variations in the seasonal dynamics of circadian clocks can in part also be understood and regulated by the plasticity of the SCN network structure.
format Online
Article
Text
id pubmed-3447953
institution National Center for Biotechnology Information
language English
publishDate 2012
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-34479532012-10-01 Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus Bodenstein, Christian Gosak, Marko Schuster, Stefan Marhl, Marko Perc, Matjaž PLoS Comput Biol Research Article The dynamics of circadian rhythms needs to be adapted to day length changes between summer and winter. It has been observed experimentally, however, that the dynamics of individual neurons of the suprachiasmatic nucleus (SCN) does not change as the seasons change. Rather, the seasonal adaptation of the circadian clock is hypothesized to be a consequence of changes in the intercellular dynamics, which leads to a phase distribution of electrical activity of SCN neurons that is narrower in winter and broader during summer. Yet to understand this complex intercellular dynamics, a more thorough understanding of the impact of the network structure formed by the SCN neurons is needed. To that effect, we propose a mathematical model for the dynamics of the SCN neuronal architecture in which the structure of the network plays a pivotal role. Using our model we show that the fraction of long-range cell-to-cell connections and the seasonal changes in the daily rhythms may be tightly related. In particular, simulations of the proposed mathematical model indicate that the fraction of long-range connections between the cells adjusts the phase distribution and consequently the length of the behavioral activity as follows: dense long-range connections during winter lead to a narrow activity phase, while rare long-range connections during summer lead to a broad activity phase. Our model is also able to account for the experimental observations indicating a larger light-induced phase-shift of the circadian clock during winter, which we show to be a consequence of higher synchronization between neurons. Our model thus provides evidence that the variations in the seasonal dynamics of circadian clocks can in part also be understood and regulated by the plasticity of the SCN network structure. Public Library of Science 2012-09-20 /pmc/articles/PMC3447953/ /pubmed/23028293 http://dx.doi.org/10.1371/journal.pcbi.1002697 Text en © 2012 Bodenstein et al 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
Bodenstein, Christian
Gosak, Marko
Schuster, Stefan
Marhl, Marko
Perc, Matjaž
Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus
title Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus
title_full Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus
title_fullStr Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus
title_full_unstemmed Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus
title_short Modeling the Seasonal Adaptation of Circadian Clocks by Changes in the Network Structure of the Suprachiasmatic Nucleus
title_sort modeling the seasonal adaptation of circadian clocks by changes in the network structure of the suprachiasmatic nucleus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3447953/
https://www.ncbi.nlm.nih.gov/pubmed/23028293
http://dx.doi.org/10.1371/journal.pcbi.1002697
work_keys_str_mv AT bodensteinchristian modelingtheseasonaladaptationofcircadianclocksbychangesinthenetworkstructureofthesuprachiasmaticnucleus
AT gosakmarko modelingtheseasonaladaptationofcircadianclocksbychangesinthenetworkstructureofthesuprachiasmaticnucleus
AT schusterstefan modelingtheseasonaladaptationofcircadianclocksbychangesinthenetworkstructureofthesuprachiasmaticnucleus
AT marhlmarko modelingtheseasonaladaptationofcircadianclocksbychangesinthenetworkstructureofthesuprachiasmaticnucleus
AT percmatjaz modelingtheseasonaladaptationofcircadianclocksbychangesinthenetworkstructureofthesuprachiasmaticnucleus