Weak synchronization can alter circadian period length: implications for aging and disease conditions

The synchronization of multiple oscillators serves as the central mechanism for maintaining stable circadian rhythms in physiology and behavior. Aging and disease can disrupt synchronization, leading to changes in the periodicity of circadian activities. While our understanding of the circadian cloc...

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Main Authors: Jihwan Myung, Sungho Hong, Christoph Schmal, Hélène Vitet, Mei-Yi Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1242800/full
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author Jihwan Myung
Jihwan Myung
Jihwan Myung
Sungho Hong
Christoph Schmal
Hélène Vitet
Hélène Vitet
Hélène Vitet
Mei-Yi Wu
Mei-Yi Wu
Mei-Yi Wu
Mei-Yi Wu
author_facet Jihwan Myung
Jihwan Myung
Jihwan Myung
Sungho Hong
Christoph Schmal
Hélène Vitet
Hélène Vitet
Hélène Vitet
Mei-Yi Wu
Mei-Yi Wu
Mei-Yi Wu
Mei-Yi Wu
author_sort Jihwan Myung
collection DOAJ
description The synchronization of multiple oscillators serves as the central mechanism for maintaining stable circadian rhythms in physiology and behavior. Aging and disease can disrupt synchronization, leading to changes in the periodicity of circadian activities. While our understanding of the circadian clock under synchronization has advanced significantly, less is known about its behavior outside synchronization, which can also fall within a predictable domain. These states not only impact the stability of the rhythms but also modulate the period length. In C57BL/6 mice, aging, diseases, and removal of peripheral circadian oscillators often result in lengthened behavioral circadian periods. Here, we show that these changes can be explained by a surprisingly simple mathematical relationship: the frequency is the reciprocal of the period, and its distribution becomes skewed when the period distribution is symmetric. The synchronized frequency of a population in the skewed distribution and the macroscopic frequency of combined oscillators differ, accounting for some of the atypical circadian period outputs observed in networks without synchronization. Building on this finding, we investigate the dynamics of circadian outputs in the context of aging and disease, where synchronization is weakened.
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spelling doaj.art-c816f6b9619743ea954e1dc73b2563d82023-09-28T04:23:38ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-09-011710.3389/fnins.2023.12428001242800Weak synchronization can alter circadian period length: implications for aging and disease conditionsJihwan Myung0Jihwan Myung1Jihwan Myung2Sungho Hong3Christoph Schmal4Hélène Vitet5Hélène Vitet6Hélène Vitet7Mei-Yi Wu8Mei-Yi Wu9Mei-Yi Wu10Mei-Yi Wu11Graduate Institute of Mind, Brain and Consciousness (GIMBC), Taipei Medical University, Taipei City, TaiwanBrain and Consciousness Research Centre (BCRC), TMU-Shuang Ho Hospital, New Taipei City, TaiwanComputational Neuroscience Unit, Okinawa Institute of Science and Technology, Okinawa, JapanComputational Neuroscience Unit, Okinawa Institute of Science and Technology, Okinawa, JapanInstitute for Theoretical Biology, Humboldt-Universität zu Berlin, Berlin, GermanyGraduate Institute of Mind, Brain and Consciousness (GIMBC), Taipei Medical University, Taipei City, TaiwanBrain and Consciousness Research Centre (BCRC), TMU-Shuang Ho Hospital, New Taipei City, TaiwanDepartment of Pediatrics, College of Medicine, National Cheng Kung University, Tainan City, TaiwanDivision of Nephrology, Department of Internal Medicine, Taipei Medical University-Shuang Ho Hospital, New Taipei City, TaiwanDivision of Nephrology, Department of Internal Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, TaiwanInstitute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, TaiwanTMU Research Center of Urology and Kidney, Taipei Medical University, Taipei, TaiwanThe synchronization of multiple oscillators serves as the central mechanism for maintaining stable circadian rhythms in physiology and behavior. Aging and disease can disrupt synchronization, leading to changes in the periodicity of circadian activities. While our understanding of the circadian clock under synchronization has advanced significantly, less is known about its behavior outside synchronization, which can also fall within a predictable domain. These states not only impact the stability of the rhythms but also modulate the period length. In C57BL/6 mice, aging, diseases, and removal of peripheral circadian oscillators often result in lengthened behavioral circadian periods. Here, we show that these changes can be explained by a surprisingly simple mathematical relationship: the frequency is the reciprocal of the period, and its distribution becomes skewed when the period distribution is symmetric. The synchronized frequency of a population in the skewed distribution and the macroscopic frequency of combined oscillators differ, accounting for some of the atypical circadian period outputs observed in networks without synchronization. Building on this finding, we investigate the dynamics of circadian outputs in the context of aging and disease, where synchronization is weakened.https://www.frontiersin.org/articles/10.3389/fnins.2023.1242800/fullunsynchronized statesperiod-frequency relationcircadian rhythmsfrequency synchronizationKuramoto modelperiod distribution
spellingShingle Jihwan Myung
Jihwan Myung
Jihwan Myung
Sungho Hong
Christoph Schmal
Hélène Vitet
Hélène Vitet
Hélène Vitet
Mei-Yi Wu
Mei-Yi Wu
Mei-Yi Wu
Mei-Yi Wu
Weak synchronization can alter circadian period length: implications for aging and disease conditions
Frontiers in Neuroscience
unsynchronized states
period-frequency relation
circadian rhythms
frequency synchronization
Kuramoto model
period distribution
title Weak synchronization can alter circadian period length: implications for aging and disease conditions
title_full Weak synchronization can alter circadian period length: implications for aging and disease conditions
title_fullStr Weak synchronization can alter circadian period length: implications for aging and disease conditions
title_full_unstemmed Weak synchronization can alter circadian period length: implications for aging and disease conditions
title_short Weak synchronization can alter circadian period length: implications for aging and disease conditions
title_sort weak synchronization can alter circadian period length implications for aging and disease conditions
topic unsynchronized states
period-frequency relation
circadian rhythms
frequency synchronization
Kuramoto model
period distribution
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1242800/full
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