Exceptional Entrainment of Circadian Activity Rhythms With Manipulations of Rhythm Waveform in Male Syrian Hamsters

The activity/rest rhythm of mammals reflects the output of an endogenous circadian oscillator entrained to the solar day by light. Despite detailed understanding of the neural and molecular bases of mammalian rhythms, we still lack practical tools for achieving rapid and flexible adjustment of clocks to accommodate shift-work, trans-meridian jet travel, or space exploration. Efforts to adapt clocks have focused on resetting the phase of an otherwise unaltered circadian clock. Departing from this tradition, recent work has demonstrated that bifurcation of circadian waveform in mice facilitates entrainment to extremely long and short zeitgeber periods. Here we evaluate the formal nature of entrainment to extreme non-24 h days in male Syrian hamsters. Wheel-running rhythms were first bifurcated into a 24 h rest/activity/rest/activity cycle according to established methods. Thereafter the 24 h lighting cycle was incrementally adjusted over several weeks to 30 h or to 18 h. Almost without exception, wheel-running rhythms of hamsters in gradually lengthened or shortened zeitgebers remained synchronized with the lighting cycle, with greater temporal precision observed in the former condition. Data from animals transferred abruptly from 24 h days to long or short cycles suggested that gradual adaptation facilitates but is not necessary for successful behavioral entrainment. The unprecedented behavioral adaptation following waveform bifurcation reveals a latent plasticity in mammalian circadian systems that can be realized in the absence of pharmacological or genetic manipulations. Oscillator interactions underlying circadian waveform manipulation, thus, represent a tractable target for understanding and enhancing circadian rhythm resetting.

[1]  Takako Noguchi,et al.  Circadian rhythm bifurcation induces flexible phase resetting by reducing circadian amplitude , 2018, The European journal of neuroscience.

[2]  Thijs J Walbeek,et al.  Simple Lighting Manipulations Facilitate Behavioral Entrainment of Mice to 18-h Days , 2017, Journal of biological rhythms.

[3]  M. Gorman,et al.  Circadian waveform bifurcation, but not phase-shifting, leaves cued fear memory intact , 2017, Physiology & Behavior.

[4]  E. Harrison,et al.  Extraordinary behavioral entrainment following circadian rhythm bifurcation in mice , 2016, Scientific Reports.

[5]  E. Harrison,et al.  Rapid Adjustment of Circadian Clocks to Simulated Travel to Time Zones across the Globe , 2015, Journal of biological rhythms.

[6]  E. Harrison,et al.  Increased photic sensitivity for phase resetting but not melatonin suppression in Siberian hamsters under short photoperiods , 2014, Hormones and Behavior.

[7]  G. Glickman,et al.  Twice Daily Melatonin Peaks in Siberian but not Syrian Hamsters under 24 h Light:Dark:Light:Dark Cycles , 2012, Chronobiology international.

[8]  Michael N Lehman,et al.  Photic Sensitivity for Circadian Response to Light Varies with Photoperiod , 2012, Journal of biological rhythms.

[9]  E. Harrison,et al.  Changing the Waveform of Circadian Rhythms: Considerations for Shift-Work , 2012, Front. Neur..

[10]  W. O. Friesen,et al.  Forced Desynchronization of Activity Rhythms in a Model of Chronic Jet Lag in Mice , 2012, Journal of biological rhythms.

[11]  M. Gorman,et al.  Dynamic interactions between coupled oscillators within the hamster circadian pacemaker. , 2010, Behavioral neuroscience.

[12]  R. Silver,et al.  Reorganization of Suprachiasmatic Nucleus Networks under 24-h LDLD Conditions , 2010, Journal of biological rhythms.

[13]  C. Eastman,et al.  Practical Interventions to Promote Circadian Adaptation to Permanent Night Shift Work: Study 4 , 2009, Journal of biological rhythms.

[14]  M. Gorman,et al.  Dim nighttime illumination accelerates adjustment to timezone travel in an animal model , 2009, Current Biology.

[15]  M. Harrington,et al.  NAN-190 potentiates the circadian response to light and speeds re-entrainment to advanced light cycles , 2008, Neuroscience.

[16]  C. Pittendrigh,et al.  The Circadian Component in Photoperiodic Induction , 2008 .

[17]  D. Golombek,et al.  Sildenafil accelerates reentrainment of circadian rhythms after advancing light schedules , 2007, Proceedings of the National Academy of Sciences.

[18]  H. Tei,et al.  Bimodal Clock Gene Expression in Mouse Suprachiasmatic Nucleus and Peripheral Tissues Under a 7-Hour Light and 5-Hour Dark Schedule , 2007, Journal of biological rhythms.

[19]  A. Díez-Noguera,et al.  Effects of Transient and Continuous Wheel Running Activity on the Upper and Lower Limits of Entrainment to Light‐Dark Cycles in Female Hamsters , 2007, Chronobiology international.

[20]  M. Gorman,et al.  Phase Angle Difference Alters Coupling Relations of Functionally Distinct Circadian Oscillators Revealed by Rhythm Splitting , 2006, Journal of biological rhythms.

[21]  A. Díez-Noguera,et al.  History-Dependent Changes in Entrainment of the Activity Rhythm in the Syrian Hamster (Mesocricetus auratus) , 2006, Journal of biological rhythms.

[22]  A. Díez-Noguera,et al.  Activity rhythm of golden hamster (Mesocricetus auratus) can be entrained to a 19-h light-dark cycle. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[23]  C. Eastman,et al.  Short nights attenuate light-induced circadian phase advances in humans. , 2005, The Journal of clinical endocrinology and metabolism.

[24]  M. Gorman,et al.  Influence of photoperiod and running wheel access on the entrainment of split circadian rhythms in hamsters , 2005, BMC Neuroscience.

[25]  M. Gorman,et al.  Scotopic Illumination Enhances Entrainment of Circadian Rhythms to Lengthening Light:Dark Cycles , 2005, Journal of biological rhythms.

[26]  C. Eastman,et al.  Complete or partial circadian re-entrainment improves performance, alertness, and mood during night-shift work. , 2004, Sleep.

[27]  A. Díez-Noguera,et al.  Effects of Photoperiod on Rat Motor Activity Rhythm at the Lower Limit of Entrainment , 2004, Journal of biological rhythms.

[28]  William J Schwartz,et al.  Forced Desynchronization of Dual Circadian Oscillators within the Rat Suprachiasmatic Nucleus , 2004, Current Biology.

[29]  M. Gorman,et al.  Photoperiod differentially modulates photic and nonphotic phase response curves of hamsters. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[30]  M. Gorman,et al.  Entrainment of 2 Subjective Nights by Daily Light:Dark:Light:Dark Cycles in 3 Rodent Species , 2003, Journal of biological rhythms.

[31]  C. Eastman,et al.  Combinations of Bright Light, Scheduled Dark, Sunglasses, and Melatonin to Facilitate Circadian Entrainment to Night Shift Work , 2003, Journal of biological rhythms.

[32]  R. Foster,et al.  Entrainment of Circadian Programs , 2003, Chronobiology international.

[33]  M. Gorman,et al.  Plasticity of Hamster Circadian Entrainment Patterns Depends on Light Intensity , 2003, Chronobiology international.

[34]  Diane B Boivin,et al.  Circadian Adaptation to Night-Shift Work by Judicious Light and Darkness Exposure , 2002, Journal of biological rhythms.

[35]  Z. Boulos,et al.  Twilights Widen the Range of Photic Entrainment in Hamsters , 2002, Journal of biological rhythms.

[36]  M. Gorman,et al.  Daily Novel Wheel Running Reorganizes and Splits Hamster Circadian Activity Rhythms , 2001, Journal of biological rhythms.

[37]  M. Gorman,et al.  Temporal Reorganization of the Suprachiasmatic Nuclei in Hamsters with Split Circadian Rhythms , 2001, Journal of biological rhythms.

[38]  Michael R. Gorman,et al.  Exotic photoperiods induce and entrain split circadian activity rhythms in hamsters , 2001, Journal of Comparative Physiology A.

[39]  J. Paquet,et al.  Profile of 24-h Light Exposure and Circadian Phase of Melatonin Secretion in Night Workers , 2001, Journal of biological rhythms.

[40]  W J Schwartz,et al.  Antiphase oscillation of the left and right suprachiasmatic nuclei. , 2000, Science.

[41]  S. Usui,et al.  Range of entrainment of rat circadian rhythms to sinusoidal light-intensity cycles. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[42]  N. Mrosovsky,et al.  Masking of locomotor activity in hamsters , 1999, Journal of Comparative Physiology A.

[43]  Jordi Vilaplana,et al.  Dissociation of the Rat Motor Activity Rhythm Under T Cycles Shorter Than 24 Hours , 1998, Physiology & Behavior.

[44]  M Terman,et al.  Light Treatment for Sleep Disorders: Consensus Report , 1995, Journal of biological rhythms.

[45]  D. Dijk,et al.  Light Treatment for Sleep Disorders: Consensus Report , 1995, Journal of biological rhythms.

[46]  Richard E. Kronauer,et al.  Light-induced suppression of endogenous circadian amplitude in humans , 1991, Nature.

[47]  R. Kronauer,et al.  Exposure to bright light and darkness to treat physiologic maladaptation to night work. , 1990, The New England journal of medicine.

[48]  G. Lynch,et al.  Characterization of circadian function in Djungarian hamsters insensitive to short day photoperiod , 1988, Journal of Comparative Physiology A.

[49]  J. Aschoff,et al.  Phase relations between a circadian rhythm and its zeitgeber within the range of entrainment , 1978, Naturwissenschaften.

[50]  Elliott Ja Circadian rhythms and photoperiodic time measurement in mammals. , 1976 .

[51]  C. Eastman,et al.  Short nights reduce light-induced circadian phase delays in humans. , 2006, Sleep.

[52]  Serge Daan,et al.  A functional analysis of circadian pacemakers in nocturnal rodents , 2005, Journal of comparative physiology.

[53]  F. Davis,et al.  Disruption of masking by hypothalamic lesions in Syrian hamsters , 2004, Journal of Comparative Physiology A.

[54]  S. Daan,et al.  University of Groningen A Functional Analysis of Circadian Pacemakers in Nocturnal Rodents. V. Pacemaker Structure Pittendrigh, , 2004 .

[55]  T. Wehr Seasonal Photoperiodic Responses of the Human Circadian System , 2001 .

[56]  A. Díez-Noguera,et al.  Simultaneous manifestation of free-running and entrained rhythms in the rat motor activity explained by a multioscillatory system. , 1997, Chronobiology international.

[57]  M. Stetson Processing of Environmental Information in Vertebrates , 1988, Proceedings in Life Sciences.

[58]  J. Aschoff Freerunning and Entrained Circadian Rhythms , 1981 .

[59]  J. Elliott Circadian rhythms and photoperiodic time measurement in mammals. , 1976, Federation proceedings.

[60]  V. Bruce Environmental Entrainment of Circadian Rhythms , 1960 .