Exploration of Circadian Rhythms in Patients with Bilateral Vestibular Loss

New insights have expanded the influence of the vestibular system to the regulation of circadian rhythmicity. Indeed, hypergravity or bilateral vestibular loss (BVL) in rodents causes a disruption in their daily rhythmicity for several days. The vestibular system thus influences hypothalamic regulat...

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Published inPloS one Vol. 11; no. 6; p. e0155067
Main Authors Martin, Tristan, Moussay, Sébastien, Bulla, Ingo, Bulla, Jan, Toupet, Michel, Etard, Olivier, Denise, Pierre, Davenne, Damien, Coquerel, Antoine, Quarck, Gaëlle
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 24.06.2016
Public Library of Science (PLoS)
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Summary:New insights have expanded the influence of the vestibular system to the regulation of circadian rhythmicity. Indeed, hypergravity or bilateral vestibular loss (BVL) in rodents causes a disruption in their daily rhythmicity for several days. The vestibular system thus influences hypothalamic regulation of circadian rhythms on Earth, which raises the question of whether daily rhythms might be altered due to vestibular pathology in humans. The aim of this study was to evaluate human circadian rhythmicity in people presenting a total bilateral vestibular loss (BVL) in comparison with control participants. Nine patients presenting a total idiopathic BVL and 8 healthy participants were compared. Their rest-activity cycle was recorded by actigraphy at home over 2 weeks. The daily rhythm of temperature was continuously recorded using a telemetric device and salivary cortisol was recorded every 3 hours from 6:00AM to 9:00PM over 24 hours. BVL patients displayed a similar rest activity cycle during the day to control participants but had higher nocturnal actigraphy, mainly during weekdays. Sleep efficiency was reduced in patients compared to control participants. Patients had a marked temperature rhythm but with a significant phase advance (73 min) and a higher variability of the acrophase (from 2:24 PM to 9:25 PM) with no correlation to rest-activity cycle, contrary to healthy participants. Salivary cortisol levels were higher in patients compared to healthy people at any time of day. We observed a marked circadian rhythmicity of temperature in patients with BVL, probably due to the influence of the light dark cycle. However, the lack of synchronization between the temperature and rest-activity cycle supports the hypothesis that the vestibular inputs are salient input to the circadian clock that enhance the stabilization and precision of both external and internal entrainment.
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PMCID: PMC4920359
AC52-06NA25396
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Competing Interests: The authors have declared that no competing interests exist.
Conceived and designed the experiments: GQ SM PD DD TM. Performed the experiments: TM. Analyzed the data: TM IB JB AC. Contributed reagents/materials/analysis tools: OE AC. Wrote the paper: TM GQ SM OE PD DD MT IB JB AC. Obtained permission to contact AFVBI: MT.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0155067