Exploration of Circadian Rhythms in Patients with Bilateral Vestibular Loss

Martin, Tristan; Moussay, Sébastien; Bulla, Ingo; Bulla, Jan; Toupet, Michel; Etard, Olivier; Denise, Pierre; Davenne, Damien; Coquerel, Antoine; Quarck, Gaëlle; Challet, Etienne

doi:10.1371/journal.pone.0155067

Exploration of Circadian Rhythms in Patients with Bilateral Vestibular Loss

Journal Article · Fri Jun 24 00:00:00 EDT 2016 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0155067· OSTI ID:1627788

Martin, Tristan ^[1]; Moussay, Sébastien ^[2]; Bulla, Ingo ^[3]; Bulla, Jan ^[4]; Toupet, Michel ^[5]; Etard, Olivier ^[6]; Denise, Pierre ^[7]; Davenne, Damien ^[2]; Coquerel, Antoine ^[8]; Quarck, Gaëlle ^[2]; Challet, Etienne

UNICAEN, COMETE, Caen (France); INSERM, Caen, (France); Normandie Universite, Caen (France); DOE/OSTI
UNICAEN, COMETE, Caen (France); INSERM, Caen, (France); Normandie Universite, Caen (France)
Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Theoretical Biology and Biophysics; Universität Greifswald (Germany). 8 Institut für Mathematik und Informatik
Bergen Univ. (Norway). Dept. of Mathematics
Centre d’explorations fonctionnelles oto-neurologiques, Paris (France)
Normandie Universite, Caen (France); CHU de Caen, Service des Explorations Fonctionnelles, Caen (France)
UNICAEN, COMETE, Caen (France); INSERM, Caen, (France); Normandie Universite, Caen (France); CHU de Caen, Service des Explorations Fonctionnelles, Caen (France)
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.

View Accepted Manuscript (DOE)

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, Journal Name: PLoS ONE Journal Issue: 6 Vol. 11; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (83)

Intergeniculate leaflet and ventral lateral geniculate nucleus afferent connections: An anatomical substrate for functional input from the vestibulo-visuomotor system Horowitz, Seth S.; Blanchard, Jane H.; Morin, Lawrence P. The Journal of Comparative Neurology, Vol. 474, Issue 2 https://doi.org/10.1002/cne.20125	journal	January 2004
Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors Besnard, S.; Machado, M. L.; Vignaux, G. Hippocampus, Vol. 22, Issue 4 https://doi.org/10.1002/hipo.20942	journal	April 2011
Postural strategies associated with somatosensory and vestibular loss Horak, F. B.; Nashner, L. M.; Diener, H. C. Experimental Brain Research, Vol. 82, Issue 1 https://doi.org/10.1007/bf00230848	journal	August 1990
The vestibulo-ocular reflex in three dimensions Raphan, Theodore; Cohen, Bernard Experimental Brain Research, Vol. 145, Issue 1 https://doi.org/10.1007/s00221-002-1067-z	journal	May 2002
Circadian rhythms of activity in healthy young and elderly humans Lieberman, Harris R.; Wurtman, Judith J.; Teicher, Martin H. Neurobiology of Aging, Vol. 10, Issue 3 https://doi.org/10.1016/0197-4580(89)90060-2	journal	May 1989
Individual differences in human circadian rhythms Horne, James A.; Östberg, Olov Biological Psychology, Vol. 5, Issue 3 https://doi.org/10.1016/0301-0511(77)90001-1	journal	September 1977
Ocular and cervical VEMPs: A study of 74 patients suffering from peripheral vestibular disorders Chiarovano, Elodie; Zamith, Franck; Vidal, Pierre-Paul Clinical Neurophysiology, Vol. 122, Issue 8 https://doi.org/10.1016/j.clinph.2011.01.006	journal	August 2011
Gait initiation characteristics in elderly patients with unilateral vestibular impairment Henriksson, Marketta; Henriksson, Jan; Bergenius, Johan Gait & Posture, Vol. 33, Issue 4 https://doi.org/10.1016/j.gaitpost.2011.02.018	journal	April 2011
Effect of Light on Human Circadian Physiology Duffy, Jeanne F.; Czeisler, Charles A. Sleep Medicine Clinics, Vol. 4, Issue 2 https://doi.org/10.1016/j.jsmc.2009.01.004	journal	June 2009
Spatial and non-spatial performance in mutant mice devoid of otoliths Machado, M. L.; Kroichvili, N.; Freret, T. Neuroscience Letters, Vol. 522, Issue 1 https://doi.org/10.1016/j.neulet.2012.06.016	journal	July 2012
Ageing, physical function, and the diurnal rhythms of cortisol and dehydroepiandrosterone Heaney, Jennifer L. J.; Phillips, Anna C.; Carroll, Douglas Psychoneuroendocrinology, Vol. 37, Issue 3 https://doi.org/10.1016/j.psyneuen.2011.07.001	journal	March 2012
Comparison of actigraphy and polysomnography to assess effects of zolpidem in a clinical research unit Peterson, Barry T.; Chiao, Ping; Pickering, Eve Sleep Medicine, Vol. 13, Issue 4 https://doi.org/10.1016/j.sleep.2011.12.003	journal	April 2012
The role of actigraphy in the assessment of primary insomnia: a retrospective study Natale, Vincenzo; Léger, Damien; Martoni, Monica Sleep Medicine, Vol. 15, Issue 1 https://doi.org/10.1016/j.sleep.2013.08.792	journal	January 2014
The role and validity of actigraphy in sleep medicine: An update Sadeh, Avi Sleep Medicine Reviews, Vol. 15, Issue 4 https://doi.org/10.1016/j.smrv.2010.10.001	journal	August 2011
Visual motion detection in patients with absent vestibular function Shallo-Hoffmann, Josephine; Bronstein, Adolfo M. Vision Research, Vol. 43, Issue 14 https://doi.org/10.1016/s0042-6989(03)00218-9	journal	June 2003
Phase advance of sleep and temperature circadian rhythms in the middle years of life in humans Carrier, Julie; Paquet, Jean; Morettini, Jocelyn Neuroscience Letters, Vol. 320, Issue 1-2 https://doi.org/10.1016/s0304-3940(02)00038-1	journal	March 2002
Gait intiation in bilateral vestibular loss Sasaki, Osamu; Asawa, Shiro; Katsuno, Satoshi Auris Nasus Larynx, Vol. 28, Issue 4 https://doi.org/10.1016/s0385-8146(01)00094-3	journal	November 2001
Circadian Clues to Sleep Onset Mechanisms Kräuchi, K. Neuropsychopharmacology, Vol. 25, Issue 5 https://doi.org/10.1016/s0893-133x(01)00315-3	journal	November 2001
Postural responses to vibration of neck muscles in patients with uni- and bilateral vestibular loss Lekhel, Hamid; Popov, Konstantin; Bronstein, Adolfo Gait & Posture, Vol. 7, Issue 3 https://doi.org/10.1016/s0966-6362(98)00012-5	journal	May 1998
Nonlinear partial differential equations and applications: Neurovestibular modulation of circadian and homeostatic regulation: Vestibulohypothalamic connection? Fuller, P. M.; Jones, T. A.; Jones, S. M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 24 https://doi.org/10.1073/pnas.242251499	journal	November 2002
Circadian Rhythms in Drinking Behavior and Locomotor Activity of Rats Are Eliminated by Hypothalamic Lesions Stephan, F. K.; Zucker, I. Proceedings of the National Academy of Sciences, Vol. 69, Issue 6 https://doi.org/10.1073/pnas.69.6.1583	journal	June 1972
Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Inouye, S. T.; Kawamura, H. Proceedings of the National Academy of Sciences, Vol. 76, Issue 11 https://doi.org/10.1073/pnas.76.11.5962	journal	November 1979
Effects of Waking Time and Breakfast Intake Prior to Evaluation of Physical Performance in the Early Morning Bougard, Clément; Bessot, Nicolas; Moussay, Sébastien Chronobiology International, Vol. 26, Issue 2 https://doi.org/10.1080/07420520902774532	journal	January 2009
Effects of Waking Time and Breakfast Intake Prior to Evaluation of Psychomotor Performance in the Early Morning Bougard, Clément; Moussay, Sébastien; Gauthier, Antoine Chronobiology International, Vol. 26, Issue 2 https://doi.org/10.1080/07420520902774540	journal	January 2009
Circadian Rhythms During Cycling Exercise and Finger-Tapping task Moussay, S.; Dosseville, F.; Gauthier, A. Chronobiology International, Vol. 19, Issue 6 https://doi.org/10.1081/cbi-120015966	journal	January 2002
Wake Detection Capacity of Actigraphy During Sleep Paquet, Jean; Kawinska, Anna; Carrier, Julie Sleep, Vol. 30, Issue 10 https://doi.org/10.1093/sleep/30.10.1362	journal	October 2007
Disagreement between subjective and actigraphic measures of sleep duration in a population-based study of elderly persons* Van Den Berg, Julia F.; Van Rooij, Frank J. A.; Vos, Henk Journal of Sleep Research, Vol. 17, Issue 3 https://doi.org/10.1111/j.1365-2869.2008.00638.x	journal	September 2008
Disturbed circadian motor activity patterns in postcardiotomy delirium Osse, Robert Jan; Tulen, Joke H. M.; Bogers, Ad J. J. C. Psychiatry and Clinical Neurosciences, Vol. 63, Issue 1 https://doi.org/10.1111/j.1440-1819.2008.01888.x	journal	February 2009
Diurnal evolution of cycling biomechanical parameters during a 60-s Wingate test: Diurnal variation in cycling patterns Lericollais, R.; Gauthier, A.; Bessot, N. Scandinavian Journal of Medicine & Science in Sports, Vol. 21, Issue 6 https://doi.org/10.1111/j.1600-0838.2010.01172.x	journal	August 2010
Vestibular Influences on the Autonomic Nervous System Yates, Bill J. Annals of the New York Academy of Sciences, Vol. 781, Issue 1 Lipids and Sy https://doi.org/10.1111/j.1749-6632.1996.tb15720.x	journal	June 1996
Posture and Gaze during Circular Locomotion Imai, Takao; Moore, Steven T.; Raphan, Theodore Annals of the New York Academy of Sciences, Vol. 942, Issue 1 https://doi.org/10.1111/j.1749-6632.2001.tb03770.x	journal	October 2001
Body temperature, activity and melatonin profiles in adults with attention-deficit/hyperactivity disorder and delayed sleep: a case-control study Bijlenga, Denise; Van Someren, Eus J. W.; Gruber, Reut Journal of Sleep Research, Vol. 22, Issue 6 https://doi.org/10.1111/jsr.12075	journal	August 2013
Phase-shifting human circadian rhythms: influence of sleep timing, social contact and light exposure. Duffy, J. F.; Kronauer, R. E.; Czeisler, C. A. The Journal of Physiology, Vol. 495, Issue 1 https://doi.org/10.1113/jphysiol.1996.sp021593	journal	August 1996
Influence of time of day on all-out swimming. Baxter, C.; Reilly, T. British Journal of Sports Medicine, Vol. 17, Issue 2 https://doi.org/10.1136/bjsm.17.2.122	journal	June 1983
Otolithic and tonic neck receptors control of limb blood flow in humans Normand, Hervé; Etard, Olivier; Denise, Pierre Journal of Applied Physiology, Vol. 82, Issue 6 https://doi.org/10.1152/jappl.1997.82.6.1734	journal	June 1997
A relationship between heat loss and sleepiness: effects of postural change and melatonin administration Kräuchi, Kurt; Cajochen, Christian; Wirz-Justice, Anna Journal of Applied Physiology, Vol. 83, Issue 1 https://doi.org/10.1152/jappl.1997.83.1.134	journal	July 1997
Chronic centrifugation (hypergravity) disrupts the circadian system of the rat Holley, D. C.; DeRoshia, C. W.; Moran, M. M. Journal of Applied Physiology, Vol. 95, Issue 3 https://doi.org/10.1152/japplphysiol.00707.2002	journal	September 2003
Entrainment of the Human Circadian System by Light Duffy, Jeanne F.; Wright, Kenneth P. Journal of Biological Rhythms, Vol. 20, Issue 4 https://doi.org/10.1177/0748730405277983	journal	August 2005
Comparing the Morningness-Eveningness Questionnaire and Munich ChronoType Questionnaire to the Dim Light Melatonin Onset Kantermann, Thomas; Sung, Haein; Burgess, Helen J. Journal of Biological Rhythms, Vol. 30, Issue 5 https://doi.org/10.1177/0748730415597520	journal	August 2015
Screening methods for delirium: early diagnosis by means of objective quantification of motor activity patterns using wrist-actigraphy Osse, R. J.; Tulen, J. H. M.; Hengeveld, M. W. Interactive CardioVascular and Thoracic Surgery, Vol. 8, Issue 3 https://doi.org/10.1510/icvts.2008.192278	journal	December 2008
Rotational Responses in Patients with Bilateral Caloric Reduction Furman, Joseph M. R.; Kamerer, Donald B. Acta Oto-Laryngologica, Vol. 108, Issue 5-6 https://doi.org/10.3109/00016488909125539	journal	January 1989
Circadian Preference and Sleep-Wake Regularity: Associations With Self-Report Sleep Parameters in Daytime-Working Adults Soehner, Adriane M.; Kennedy, Kathy S.; Monk, Timothy H. Chronobiology International, Vol. 28, Issue 9 https://doi.org/10.3109/07420528.2011.613137	journal	November 2011
Validation of an innovative method, based on tilt sensing, for the assessment of activity and body position Bonmati-Carrion, M. A.; Middleton, B.; Revell, V. L. Chronobiology International, Vol. 32, Issue 5 https://doi.org/10.3109/07420528.2015.1016613	journal	April 2015
Compensation Following Bilateral Vestibular Damage McCall, Andrew A.; Yates, Bill J. Frontiers in Neurology, Vol. 2 https://doi.org/10.3389/fneur.2011.00088	journal	January 2011
Circadian adjustment of men and women to night work Hakola, T.; Härmä, Mi; Laitinen, Jt Scandinavian Journal of Work, Environment & Health, Vol. 22, Issue 2 https://doi.org/10.5271/sjweh.121	journal	April 1996
Changes in the human vestibulo-ocular reflex after loss of peripheral sensitivity Baloh, R. W.; Honrubia, V.; Yee, R. D. Annals of Neurology, Vol. 16, Issue 2 https://doi.org/10.1002/ana.410160209	journal	August 1984
Bone remodeling is regulated by inner ear vestibular signals: BONE REMODELING IS REGULATED BY INNER EAR VESTIBULAR SIGNALS Vignaux, Guillaume; Besnard, Stéphane; Ndong, Jean Journal of Bone and Mineral Research, Vol. 28, Issue 10 https://doi.org/10.1002/jbmr.1940	journal	September 2013
Mixed-Effects Models in Sand S-PLUS Pinheiro, José C.; Bates, Douglas M. Statistics and Computing https://doi.org/10.1007/978-1-4419-0318-1	book	January 2000
Bilateral loss of vestibular function: clinical findings in 53 patients Rinne, T.; Bronstein, A. M.; Rudge, P. Journal of Neurology, Vol. 245, Issue 6-7 https://doi.org/10.1007/s004150050225	journal	May 1998
Sleep, vigilance, and thermosensitivity Romeijn, Nico; Raymann, Roy J. E. M.; Møst, Els Pflügers Archiv - European Journal of Physiology, Vol. 463, Issue 1 https://doi.org/10.1007/s00424-011-1042-2	journal	November 2011
Visual motion detection in patients with absent vestibular function Shallo-Hoffmann, Josephine; Bronstein, Adolfo M. Vision Research, Vol. 43, Issue 14 https://doi.org/10.1016/S0042-6989(03)00218-9	journal	June 2003
Idiopathic bilateral vestibular loss Sargent, E.; Goebel, J.; Hanson, J. Otolaryngology - Head and Neck Surgery, Vol. 116, Issue 2 https://doi.org/10.1016/S0194-5998(97)70318-8	journal	February 1997
Phase advance of sleep and temperature circadian rhythms in the middle years of life in humans Carrier, Julie; Paquet, Jean; Morettini, Jocelyn Neuroscience Letters, Vol. 320, Issue 1-2 https://doi.org/10.1016/S0304-3940(02)00038-1	journal	March 2002
Adaptive plasticity in vestibular influences on cardiovascular control Yates, B. J.; Holmes, M. J.; Jian, B. J. Brain Research Bulletin, Vol. 53, Issue 1 https://doi.org/10.1016/S0361-9230(00)00302-6	journal	September 2000
Gait intiation in bilateral vestibular loss Sasaki, Osamu; Asawa, Shiro; Katsuno, Satoshi Auris Nasus Larynx, Vol. 28, Issue 4 https://doi.org/10.1016/S0385-8146(01)00094-3	journal	November 2001
Circadian Clues to Sleep Onset Mechanisms Kräuchi, K. Neuropsychopharmacology, Vol. 25, Issue 5 https://doi.org/10.1016/S0893-133X(01)00315-3	journal	November 2001
Attentional demands for postural control: the effects of aging and sensory reintegration Teasdale, N.; Simoneau, M. Gait & Posture, Vol. 14, Issue 3 https://doi.org/10.1016/S0966-6362(01)00134-5	journal	December 2001
Postural responses to vibration of neck muscles in patients with uni- and bilateral vestibular loss Lekhel, Hamid; Popov, Konstantin; Bronstein, Adolfo Gait & Posture, Vol. 7, Issue 3 https://doi.org/10.1016/S0966-6362(98)00012-5	journal	May 1998
Comparison of actigraphic, polysomnographic, and subjective assessment of sleep parameters in sleep-disordered patients Kushida, Clete A.; Chang, Arthur; Gadkary, Chirag Sleep Medicine, Vol. 2, Issue 5 https://doi.org/10.1016/S1389-9457(00)00098-8	journal	September 2001
Aspects du sommeil normal Dauvilliers, Y.; Billiard, M. EMC - Neurologie, Vol. 1, Issue 4 https://doi.org/10.1016/j.emcn.2004.05.001	journal	October 2004
Interference between walking and a cognitive task is increased in patients with bilateral vestibular loss Bessot, Nicolas; Denise, Pierre; Toupet, Michel Gait & Posture, Vol. 36, Issue 2 https://doi.org/10.1016/j.gaitpost.2012.02.021	journal	June 2012
Validation of a new telemetric core temperature monitor McKenzie, J. E.; Osgood, D. W. Journal of Thermal Biology, Vol. 29, Issue 7-8 https://doi.org/10.1016/j.jtherbio.2004.08.020	journal	October 2004
Vestibular syndrome: A change in internal spatial representation Borel, L.; Lopez, C.; Péruch, P. Neurophysiologie Clinique/Clinical Neurophysiology, Vol. 38, Issue 6 https://doi.org/10.1016/j.neucli.2008.09.002	journal	December 2008
Sleep disturbances are correlated with decreased morning awakening salivary cortisol Backhaus, Jutta; Junghanns, Klaus; Hohagen, Fritz Psychoneuroendocrinology, Vol. 29, Issue 9 https://doi.org/10.1016/j.psyneuen.2004.01.010	journal	October 2004
Evaluation of the chemical model of vestibular lesions induced by arsanilate in rats Vignaux, G.; Chabbert, C.; Gaboyard-Niay, S. Toxicology and Applied Pharmacology, Vol. 258, Issue 1 https://doi.org/10.1016/j.taap.2011.10.008	journal	January 2012
Dose-response relationships for resetting of human circadian clock by light Boivin, Diane B.; Duffy, Jeanne F.; Kronauer, Richard E. Nature, Vol. 379, Issue 6565 https://doi.org/10.1038/379540a0	journal	February 1996
Morningness/eveningness and the need for sleep: Morningness/eveningness and the need for sleep Taillard, Jacques; Philip, Pierre; Bioulac, Bernard Journal of Sleep Research, Vol. 8, Issue 4 https://doi.org/10.1046/j.1365-2869.1999.00176.x	journal	December 1999
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 Baehr, Erin K.; Revelle, William; Eastman, Charmane I. Journal of Sleep Research, Vol. 9, Issue 2 https://doi.org/10.1046/j.1365-2869.2000.00196.x	journal	June 2000
Exposure to Bright Light and Darkness to Treat Physiologic Maladaptation to Night Work Czeisler, Charles A.; Johnson, Michael P.; Duffy, Jeanne F. New England Journal of Medicine, Vol. 322, Issue 18 https://doi.org/10.1056/NEJM199005033221801	journal	May 1990
Evidence for vestibular regulation of autonomic functions in a mouse genetic model Murakami, D. M.; Erkman, L.; Hermanson, O. Proceedings of the National Academy of Sciences, Vol. 99, Issue 26 https://doi.org/10.1073/pnas.252652299	journal	December 2002
A comparison of circadian rhythms in work performance between physically active and inactive subjects Atkinson, G.; Coldwells, A.; Reilly, T. Ergonomics, Vol. 36, Issue 1-3 https://doi.org/10.1080/00140139308967882	journal	January 1993
The Sleep of Healthy People—A Diary Study Monk, Timothy H.; Buysse, Daniel J.; Rose, Lynda R. Chronobiology International, Vol. 17, Issue 1 https://doi.org/10.1081/CBI-100101031	journal	January 2000
Circadian Rhythms During Cycling Exercise and Finger-Tapping task Moussay, S.; Dosseville, F.; Gauthier, A. Chronobiology International, Vol. 19, Issue 6 https://doi.org/10.1081/CBI-120015966	journal	January 2002
The Role of Actigraphy in the Study of Sleep and Circadian Rhythms Ancoli-Israel, Sonia; Cole, Roger; Alessi, Cathy Sleep, Vol. 26, Issue 3 https://doi.org/10.1093/sleep/26.3.342	journal	May 2003
Postural Compensation for Vestibular Loss Horak, Fay B. Annals of the New York Academy of Sciences, Vol. 1164, Issue 1 https://doi.org/10.1111/j.1749-6632.2008.03708.x	journal	May 2009
Efficacy of a single sequence of intermittent bright light pulses for delaying circadian phase in humans Gronfier, Claude; Wright, Kenneth P.; Kronauer, Richard E. American Journal of Physiology-Endocrinology and Metabolism, Vol. 287, Issue 1 https://doi.org/10.1152/ajpendo.00385.2003	journal	July 2004
Sleep, performance, circadian rhythms, and light-dark cycles during two space shuttle flights Dijk, Derk-Jan; Neri, David F.; Wyatt, James K. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 281, Issue 5 https://doi.org/10.1152/ajpregu.2001.281.5.R1647	journal	November 2001
Genetic Evidence for a Neurovestibular Influence on the Mammalian Circadian Pacemaker Fuller, Patrick M.; Fuller, Charles A. Journal of Biological Rhythms, Vol. 21, Issue 3 https://doi.org/10.1177/0748730406288148	journal	June 2006
Current and Future Management of Bilateral Loss of Vestibular Sensation — An Update on the Johns Hopkins Multichannel Vestibular Prosthesis Project Santina, Charles Della C.; Migliaccio, Americo A.; Hayden, Russell Cochlear Implants International, Vol. 11, Issue sup2 https://doi.org/10.1179/146701010X12726366068454	journal	September 2010
Aging and selective sensorimotor strategies in the regulation of upright balance Bugnariu, Nicoleta; Fung, Joyce Journal of NeuroEngineering and Rehabilitation, Vol. 4, Issue 1 https://doi.org/10.1186/1743-0003-4-19	journal	June 2007
Diurnal Rhythm of the Muscular Performance of Elbow Flexors During Isometric Contractions Gauthier, Antoine; Davenne, Damien; Martin, Alain Chronobiology International, Vol. 13, Issue 2 https://doi.org/10.3109/07420529609037077	journal	January 1996
Bright Light Therapy: Improved Sensitivity to Its Effects on Rest-Activity Rhythms in Alzheimer Patients by Application of Nonparametric Methods Van Someren, Eus J. W.; Swaab, Dick F.; Colenda, Christopher C. Chronobiology International, Vol. 16, Issue 4 https://doi.org/10.3109/07420529908998724	journal	January 1999
Personality changes in patients with vestibular dysfunction Smith, Paul F.; Darlington, Cynthia L. Frontiers in Human Neuroscience, Vol. 7 https://doi.org/10.3389/fnhum.2013.00678	journal	January 2013

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