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Title: Exploration of Circadian Rhythms in Patients with Bilateral Vestibular Loss

Journal Article · · PLoS ONE
 [1];  [1];  [2];  [3];  [4];  [5];  [6];  [1];  [7];  [1];
  1. UNICAEN, COMETE, Caen (France); INSERM, Caen, (France); Normandie Universite, Caen (France)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; Universität Greifswald (Germany). 8 Institut für Mathematik und Informatik
  3. Bergen Univ. (Norway). Dept. of Mathematics
  4. Centre d’explorations fonctionnelles oto-neurologiques, Paris (France)
  5. Normandie Universite, Caen (France); CHU de Caen, Service des Explorations Fonctionnelles, Caen (France)
  6. UNICAEN, COMETE, Caen (France); INSERM, Caen, (France); Normandie Universite, Caen (France); CHU de Caen, Service des Explorations Fonctionnelles, Caen (France)
  7. UNICAEN, COMETE, Caen (France); INSERM, Caen, (France); Normandie Universite, Caen (France); CHU de Caen, Laboratoire de pharmacologie-toxicologie, Caen (France)

Background 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. Methodology and Principal Findings 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. Conclusion 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.

Research Organization:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC52-06NA25396
OSTI ID:
1627788
Journal Information:
PLoS ONE, Vol. 11, Issue 6; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (77)

Aging and selective sensorimotor strategies in the regulation of upright balance journal June 2007
Attentional demands for postural control: the effects of aging and sensory reintegration journal December 2001
Posture and Gaze during Circular Locomotion journal October 2001
The vestibulo-ocular reflex in three dimensions journal May 2002
Changes in the human vestibulo-ocular reflex after loss of peripheral sensitivity journal August 1984
Rotational Responses in Patients with Bilateral Caloric Reduction journal January 1989
Idiopathic bilateral vestibular loss journal February 1997
Gait initiation characteristics in elderly patients with unilateral vestibular impairment journal April 2011
Bilateral loss of vestibular function: clinical findings in 53 patients journal May 1998
Postural Compensation for Vestibular Loss journal May 2009
Vestibular syndrome: A change in internal spatial representation journal December 2008
Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors journal April 2011
Spatial and non-spatial performance in mutant mice devoid of otoliths journal July 2012
Vestibular Influences on the Autonomic Nervous System journal June 1996
Evaluation of the chemical model of vestibular lesions induced by arsanilate in rats journal January 2012
Bone remodeling is regulated by inner ear vestibular signals: BONE REMODELING IS REGULATED BY INNER EAR VESTIBULAR SIGNALS journal September 2013
Genetic Evidence for a Neurovestibular Influence on the Mammalian Circadian Pacemaker journal June 2006
Nonlinear partial differential equations and applications: Neurovestibular modulation of circadian and homeostatic regulation: Vestibulohypothalamic connection? journal November 2002
Chronic centrifugation (hypergravity) disrupts the circadian system of the rat journal September 2003
Evidence for vestibular regulation of autonomic functions in a mouse genetic model journal December 2002
Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. journal November 1979
Circadian Rhythms in Drinking Behavior and Locomotor Activity of Rats Are Eliminated by Hypothalamic Lesions journal June 1972
Exposure to Bright Light and Darkness to Treat Physiologic Maladaptation to Night Work journal May 1990
Entrainment of the Human Circadian System by Light journal August 2005
A comparison of circadian rhythms in work performance between physically active and inactive subjects journal January 1993
Intergeniculate leaflet and ventral lateral geniculate nucleus afferent connections: An anatomical substrate for functional input from the vestibulo-visuomotor system journal January 2004
Ocular and cervical VEMPs: A study of 74 patients suffering from peripheral vestibular disorders journal August 2011
Interference between walking and a cognitive task is increased in patients with bilateral vestibular loss journal June 2012
The Role of Actigraphy in the Study of Sleep and Circadian Rhythms journal May 2003
Circadian adjustment of men and women to night work journal April 1996
Ageing, physical function, and the diurnal rhythms of cortisol and dehydroepiandrosterone journal March 2012
Effects of Waking Time and Breakfast Intake Prior to Evaluation of Psychomotor Performance in the Early Morning journal January 2009
Effects of Waking Time and Breakfast Intake Prior to Evaluation of Physical Performance in the Early Morning journal January 2009
Influence of time of day on all-out swimming. journal June 1983
Sleep disturbances are correlated with decreased morning awakening salivary cortisol journal October 2004
Validation of a new telemetric core temperature monitor journal October 2004
Bright Light Therapy: Improved Sensitivity to Its Effects on Rest-Activity Rhythms in Alzheimer Patients by Application of Nonparametric Methods journal January 1999
Validation of an innovative method, based on tilt sensing, for the assessment of activity and body position journal April 2015
The role of actigraphy in the assessment of primary insomnia: a retrospective study journal January 2014
Comparison of actigraphic, polysomnographic, and subjective assessment of sleep parameters in sleep-disordered patients journal September 2001
Diurnal Rhythm of the Muscular Performance of Elbow Flexors During Isometric Contractions journal January 1996
Diurnal evolution of cycling biomechanical parameters during a 60-s Wingate test: Diurnal variation in cycling patterns journal August 2010
Individual differences in the phase and amplitude of the human circadian temperature rhythm: with an emphasis on morningness-eveningness: Phase and amplitude of the temperature rhythm journal June 2000
Comparing the Morningness-Eveningness Questionnaire and Munich ChronoType Questionnaire to the Dim Light Melatonin Onset journal August 2015
Circadian rhythms of activity in healthy young and elderly humans journal May 1989
Screening methods for delirium: early diagnosis by means of objective quantification of motor activity patterns using wrist-actigraphy journal December 2008
Disturbed circadian motor activity patterns in postcardiotomy delirium journal February 2009
Comparison of actigraphy and polysomnography to assess effects of zolpidem in a clinical research unit journal April 2012
Wake Detection Capacity of Actigraphy During Sleep journal October 2007
The role and validity of actigraphy in sleep medicine: An update journal August 2011
Circadian Preference and Sleep-Wake Regularity: Associations With Self-Report Sleep Parameters in Daytime-Working Adults journal November 2011
The Sleep of Healthy People—A Diary Study journal January 2000
Morningness/eveningness and the need for sleep: Morningness/eveningness and the need for sleep journal December 1999
Compensation Following Bilateral Vestibular Damage journal January 2011
Personality changes in patients with vestibular dysfunction journal January 2013
Disagreement between subjective and actigraphic measures of sleep duration in a population-based study of elderly persons* journal September 2008
Sleep, vigilance, and thermosensitivity journal November 2011
Adaptive plasticity in vestibular influences on cardiovascular control journal September 2000
Dose-response relationships for resetting of human circadian clock by light journal February 1996
Phase-shifting human circadian rhythms: influence of sleep timing, social contact and light exposure. journal August 1996
Sleep, performance, circadian rhythms, and light-dark cycles during two space shuttle flights journal November 2001
Individual differences in human circadian rhythms journal September 1977
Body temperature, activity and melatonin profiles in adults with attention-deficit/hyperactivity disorder and delayed sleep: a case-control study journal August 2013
Efficacy of a single sequence of intermittent bright light pulses for delaying circadian phase in humans journal July 2004
Aspects du sommeil normal journal October 2004
Current and Future Management of Bilateral Loss of Vestibular Sensation — An Update on the Johns Hopkins Multichannel Vestibular Prosthesis Project journal September 2010
Effect of Light on Human Circadian Physiology journal June 2009
Mixed-Effects Models in Sand S-PLUS book January 2000
Postural strategies associated with somatosensory and vestibular loss journal August 1990
Visual motion detection in patients with absent vestibular function journal June 2003
Phase advance of sleep and temperature circadian rhythms in the middle years of life in humans journal March 2002
Gait intiation in bilateral vestibular loss journal November 2001
Circadian Clues to Sleep Onset Mechanisms journal November 2001
Postural responses to vibration of neck muscles in patients with uni- and bilateral vestibular loss journal May 1998
Circadian Rhythms During Cycling Exercise and Finger-Tapping task journal January 2002
Otolithic and tonic neck receptors control of limb blood flow in humans journal June 1997
A relationship between heat loss and sleepiness: effects of postural change and melatonin administration journal July 1997

Cited By (3)

Relationship between sleep quality and dizziness journal March 2018
Full Spectrum of Reported Symptoms of Bilateral Vestibulopathy Needs Further Investigation—A Systematic Review journal June 2018
Circadian Rhythms, Exercise, and Cardiovascular Health journal July 2018

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