Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.

Robust synchronization is a critical feature of several systems including the mammalian circadian clock. The master circadian clock in mammals consists of about 20000 'sloppy' neuronal oscillators within the hypothalamus that keep robust time by synchronization driven by inter-neuronal cou...

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Autores principales:	Bharath Ananthasubramaniam, Erik D Herzog, Hanspeter Herzel
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/2380d0d04b3c40b0adf3c2ed47dfcecc
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spelling	oai:doaj.org-article:2380d0d04b3c40b0adf3c2ed47dfcecc2021-11-18T05:52:57ZTiming of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.1553-734X1553-735810.1371/journal.pcbi.1003565https://doaj.org/article/2380d0d04b3c40b0adf3c2ed47dfcecc2014-04-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24743470/pdf/?tool=EBIhttps://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Robust synchronization is a critical feature of several systems including the mammalian circadian clock. The master circadian clock in mammals consists of about 20000 'sloppy' neuronal oscillators within the hypothalamus that keep robust time by synchronization driven by inter-neuronal coupling. The complete understanding of this synchronization in the mammalian circadian clock and the mechanisms underlying it remain an open question. Experiments and computational studies have shown that coupling individual oscillators can achieve robust synchrony, despite heterogeneity and different network topologies. But, much less is known regarding the mechanisms and circuits involved in achieving this coupling, due to both system complexity and experimental limitations. Here, we computationally study the coupling mediated by the primary coupling neuropeptide, vasoactive intestinal peptide (VIP) and its canonical receptor, VPAC2R, using the transcriptional elements and generic mode of VIP-VPAC2R signaling. We find that synchrony is only possible if VIP (an inducer of Per expression) is released in-phase with activators of Per expression. Moreover, anti-phasic VIP release suppresses coherent rhythms by moving the network into a desynchronous state. Importantly, experimentally observed rhythms in VPAC2R have little effect on network synchronization, but can improve the amplitude of the SCN network rhythms while narrowing the network entrainment range. We further show that these findings are valid across several computational network models. Thus, we identified a general design principle to achieve robust synchronization: An activating coupling agent, such as VIP, must act in-phase with the activity of core-clock promoters. More generally, the phase of coupling is as critical as the strength of coupling from the viewpoint of synchrony and entrainment.Bharath AnanthasubramaniamErik D HerzogHanspeter HerzelPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 10, Iss 4, p e1003565 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Bharath Ananthasubramaniam Erik D Herzog Hanspeter Herzel Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
description	Robust synchronization is a critical feature of several systems including the mammalian circadian clock. The master circadian clock in mammals consists of about 20000 'sloppy' neuronal oscillators within the hypothalamus that keep robust time by synchronization driven by inter-neuronal coupling. The complete understanding of this synchronization in the mammalian circadian clock and the mechanisms underlying it remain an open question. Experiments and computational studies have shown that coupling individual oscillators can achieve robust synchrony, despite heterogeneity and different network topologies. But, much less is known regarding the mechanisms and circuits involved in achieving this coupling, due to both system complexity and experimental limitations. Here, we computationally study the coupling mediated by the primary coupling neuropeptide, vasoactive intestinal peptide (VIP) and its canonical receptor, VPAC2R, using the transcriptional elements and generic mode of VIP-VPAC2R signaling. We find that synchrony is only possible if VIP (an inducer of Per expression) is released in-phase with activators of Per expression. Moreover, anti-phasic VIP release suppresses coherent rhythms by moving the network into a desynchronous state. Importantly, experimentally observed rhythms in VPAC2R have little effect on network synchronization, but can improve the amplitude of the SCN network rhythms while narrowing the network entrainment range. We further show that these findings are valid across several computational network models. Thus, we identified a general design principle to achieve robust synchronization: An activating coupling agent, such as VIP, must act in-phase with the activity of core-clock promoters. More generally, the phase of coupling is as critical as the strength of coupling from the viewpoint of synchrony and entrainment.
format	article
author	Bharath Ananthasubramaniam Erik D Herzog Hanspeter Herzel
author_facet	Bharath Ananthasubramaniam Erik D Herzog Hanspeter Herzel
author_sort	Bharath Ananthasubramaniam
title	Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
title_short	Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
title_full	Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
title_fullStr	Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
title_full_unstemmed	Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
title_sort	timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/2380d0d04b3c40b0adf3c2ed47dfcecc
work_keys_str_mv	AT bharathananthasubramaniam timingofneuropeptidecouplingdeterminessynchronyandentrainmentinthemammaliancircadianclock AT erikdherzog timingofneuropeptidecouplingdeterminessynchronyandentrainmentinthemammaliancircadianclock AT hanspeterherzel timingofneuropeptidecouplingdeterminessynchronyandentrainmentinthemammaliancircadianclock
_version_	1718424654064910336

Timing of neuropeptide coupling determines synchrony and entrainment in the mammalian circadian clock.

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