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Circadian Rhythms

Fred W. Turek, Olivier Van Reeth

10.1002/cphy.cp040258

Source: Supplement 14: Handbook of Physiology, Environmental Physiology

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Generation and Entrainment of Circadian Rhythms
1.1 Endogenous Self‐Sustained Clocks Drive Circadian Rhythms
1.2 Entrainment of Circadian Clocks: Control of Period and Phase
2 Circadian Pacemakers: The Executive Clock in the Suprachiasmatic Nucleus
2.1 The Suprachiasmatic Nucleus of the Hypothalamus
2.2 The Multioscillatory Nature of the Mammalian Circadian Clock System
2.3 Nature of Circadian Code from SCN
3 Genetic Basis
3.1 Inbred Strains
3.2 Twin Studies
3.3 A Mammalian Clock Mutation
4 Ontogeny of Circadian Rhythms
4.1 Development of Clock and Expression of Circadian Rhythms
4.2 Aging of the Circadian Clock System
5 Adaptive Significance
5.1 External Synchronization
5.2 Internal Synchronization
6 Role of Circadian Clock in Expression of Other Biological Rhythms
6.1 Ultradian Rhythms
6.2 Infradian Rhythms
6.3 Annual Rhythms
7 Summary
8 Note Added in Proof
Figure 1. Figure 1.

Continuous record of the circadian rhythm of wheel‐running behavior in a golden hamster maintained in constant darkness for 100 days. Each revolution of the running wheel was recorded on‐line via a personal computer. Black bars represent periods of activity. Successive days are plotted from top to bottom, and the activity record has been double‐mounted on a 48 h time interval to aid in the visualization of data. This record shows the remarkable precision of the activity rhythm under free‐running conditions devoid of any timing cues. The onset of activity shows a period slightly greater than 24 h throughout the 100 days, with deviations from the mean period being only a few minutes between any 2 days. The decrease in testicular size (and its associated decrease in serum testosterone levels), due to exposure to constant darkness, leads to a decrease in the total amount of activity per day during the latter half of this record.
Figure 2. Figure 2.

Daily rhythm of wheel‐running behavior in a golden hamster exposed to a 14:10 light‐dark cycle, which was phase‐advanced by 8 h on day 8 of this record. Timing of light‐dark cycles before and after the advance in the light cycle is diagrammed at the top of the record. The animal was entrained to the initial cycle such that the onset of activity occurred within a few minutes of lights‐off each day. Following the shift in the cycle, it took about 10 days for the animal to become reentrained to the new lighting schedule.
Figure 3. Figure 3.

Schematic representation of two generalized phase response curves (PRC) for the phase‐shifting effects on the circadian clock regulating the rhythm of locomotor activity following the presentation of either single pulses of light (5—60 min in duration) or stimuli which induce an acute increase in activity (for example, exposure to a novel running wheel or injection of a short‐acting benzodiazepine) in golden hamsters free‐running in constant darkness. Closed circles: light pulse PRC; open circles: activity‐induced PRC. Circadian time 12 refers to the time of activity onset in this nocturnal species. While exposure to light during the subjective daytime has little or no effect on the phase of the activity rhythm, exposure to light near the time of activity onset (that is, near the time of sunset) induces a delay in the rhythm, while an equivalent light pulse given near the end of the subjective night (that is, near the time of sunrise) induces an advance in the rhythm. While the amplitudes of the phase advances and phase delays that occur in response to the presentation of activity‐inducing stimuli are similar to those observed in response to light pulses, the circadian time for the phase delay, phase advance, and unresponsive regions of the two PRCs are dramatically different.
Figure 4. Figure 4.

Period of circadian rhythm of locomotor activity before the destruction of the SCN (host rhythm) and following the transplantation of fetal SCN tissue (restored rhythm) in wild‐type hamsters and in hamsters homozygous or heterozygous for the tau mutation, which shortens the endogenous free‐running period of the activity rhythm. A: Reciprocal transplants between homozygous mutant and wild‐type animals. B: Reciprocal transplants between heterozygous mutant and wild‐type hamsters. Closed circles: periods of the intact hosts; open circles: period of rhythm following transplantation of wild‐type tissue; triangles: period of rhythm following transplantation of homozygous mutant tissue; stars: period of rhythm following transplantation of heterozygous mutant tissue.

Reproduced with permission from reference 141
Figure 5. Figure 5.

Representative patterns of vasopressin (VP) release from two individual SCN explants studied in constant conditions using a perifusion culture technique. Both explants were obtained from rats maintained on an 12:12 light‐dark cycle, but preparation of the cultures occurred at two different times. The top panel shows the VP rhythm from an explant prepared at the onset of the 12 h light phase, while the bottom panel shows the rhythm from an explant prepared near the end of the light phase. Open and closed bars denote determinations of the amount of VP released into the medium over 2 h sampling intervals during the subjective day (that is, the portion of the circadian cycle coinciding with the projected light phase of the cycle) and the subjective night, respectively.

Reproduced with permission from reference 40
Figure 6. Figure 6.

Effects of pulses of light with varying radiance on c‐fos mRNA in the SCN region and the phase of the activity rhythm in hamsters maintained in constant darkness. All light pulses were 5 min in duration and were presented at circadian time 19. Left panels: Following exposure to the light pulse, animals were returned to constant darkness for 25 min before the brains were prepared for c‐fos analysis by in situ hybridization procedures. Panel 1 shows c‐fos levels in an animal receiving no light pulse, while panels 2‐5 show levels in animals exposed to increasing levels of illumination. Right panels: Representative activity records of hamsters exposed to light stimuli of similar irradiance to the corresponding left panels. Asterisks mark the time of the light pulse, after which the animals continued to free‐run in constant darkness.

Reproduced with permission from reference 83
Figure 7. Figure 7.

Dependence of light‐induced behavioral phase‐shifting and jun‐B and c‐fos mRNA levels in the SCN region as a function of circadian phase. Hamsters were maintained in darkness before being exposed to a 5 min pulse of light. A: Asterisks superimposed on the phase response curve to light pulses in hamsters denote the time of the light pulses in B and C. B: jun‐B mRNA in the SCN after light pulses of 5 min duration at circadian time 3, 9, 14, 19, and 21. Animals were returned to darkness for 25 min and brains were prepared for in situ hybridization. Values represent the mean signal in the SCN of light‐pulsed hamsters relative to the mean signal at the same circadian time in animals receiving no light. Hamsters receiving no light exhibited no significant jun‐B mRNA hybridization in the SCN at all circadian times examined. C: c‐fos mRNA in the SCN region induced by light following the procedures described in B.

Reproduced with permission from reference 84
Figure 8. Figure 8.

Schematic representation of a putative model for the organization of the circadian system in complex organisms. See text for further details.

Reproduced with permission from reference 203
Figure 9. Figure 9.

Top: Mean (± S.E.M.) phase shifts in the activity rhythm of young and old hamsters maintained in constant light that were subjected, beginning at either circadian time 6 (left panel) or circadian time 18 (right panel) to a 6 h dark pulse. A value above the solid line indicates an advance in the onset of locomotor activity; a value below indicates a delay. Values in parentheses indicate the number of trials for each group of animals. The mean phase shift in the activity rhythm in response to the dark pulse was significantly greater (P < 0.001) in young than in old hamsters at both circadian times tested. Bottom: Representative sections from the wheel‐running activity records of two young (left panels) and two old (right panels) hamsters housed in constant light before and after they were subjected to a 6 h dark pulse beginning at circadian time 6 (top panels) or circadian time 18 (bottom panels). The day of the dark pulse is designated by DP at the left of each record with the exact beginning and end of the dark pulse designated by two stars.

Reproduced with permission from reference 219
Figure 10. Figure 10.

Running wheel activity records from two Djungarian hamsters (left) and the mean paired testes weight (right) of groups of nine to ten hamsters exposed for 28 days to two 10 min pulses of light per 24 h. The bar at the top of each activity record indicates the light‐dark 6:18 photoperiod (unfilled bar represents lights‐on) to which the hamsters were exposed for about 21 days prior to transfer to the “skeleton” photoperiods. The second bar at the top of each activity record indicates the time at which the animals were exposed to the two 10 min pulses of light. Depending on the initial placement of the 10 min pulse of light relative to the previous 6:18 light‐dark cycle, the activity rhythm of some of the animals was advanced for a few cycles until an 8:16 light‐dark entrainment pattern was established (that is, activity confined to the 16 h interval of darkness) (top left panel), whereas in other animals the activity rhythm was delayed for a few cycles until a 16L: 8D entrainment pattern was established (that is, activity confined to the 8 h interval of darkness) (lower left panel). Testes weight for control animals maintained on 6:18 light‐dark are shown for comparative purposes.

Reproduced with permission from reference 99


Figure 1.

Continuous record of the circadian rhythm of wheel‐running behavior in a golden hamster maintained in constant darkness for 100 days. Each revolution of the running wheel was recorded on‐line via a personal computer. Black bars represent periods of activity. Successive days are plotted from top to bottom, and the activity record has been double‐mounted on a 48 h time interval to aid in the visualization of data. This record shows the remarkable precision of the activity rhythm under free‐running conditions devoid of any timing cues. The onset of activity shows a period slightly greater than 24 h throughout the 100 days, with deviations from the mean period being only a few minutes between any 2 days. The decrease in testicular size (and its associated decrease in serum testosterone levels), due to exposure to constant darkness, leads to a decrease in the total amount of activity per day during the latter half of this record.



Figure 2.

Daily rhythm of wheel‐running behavior in a golden hamster exposed to a 14:10 light‐dark cycle, which was phase‐advanced by 8 h on day 8 of this record. Timing of light‐dark cycles before and after the advance in the light cycle is diagrammed at the top of the record. The animal was entrained to the initial cycle such that the onset of activity occurred within a few minutes of lights‐off each day. Following the shift in the cycle, it took about 10 days for the animal to become reentrained to the new lighting schedule.



Figure 3.

Schematic representation of two generalized phase response curves (PRC) for the phase‐shifting effects on the circadian clock regulating the rhythm of locomotor activity following the presentation of either single pulses of light (5—60 min in duration) or stimuli which induce an acute increase in activity (for example, exposure to a novel running wheel or injection of a short‐acting benzodiazepine) in golden hamsters free‐running in constant darkness. Closed circles: light pulse PRC; open circles: activity‐induced PRC. Circadian time 12 refers to the time of activity onset in this nocturnal species. While exposure to light during the subjective daytime has little or no effect on the phase of the activity rhythm, exposure to light near the time of activity onset (that is, near the time of sunset) induces a delay in the rhythm, while an equivalent light pulse given near the end of the subjective night (that is, near the time of sunrise) induces an advance in the rhythm. While the amplitudes of the phase advances and phase delays that occur in response to the presentation of activity‐inducing stimuli are similar to those observed in response to light pulses, the circadian time for the phase delay, phase advance, and unresponsive regions of the two PRCs are dramatically different.



Figure 4.

Period of circadian rhythm of locomotor activity before the destruction of the SCN (host rhythm) and following the transplantation of fetal SCN tissue (restored rhythm) in wild‐type hamsters and in hamsters homozygous or heterozygous for the tau mutation, which shortens the endogenous free‐running period of the activity rhythm. A: Reciprocal transplants between homozygous mutant and wild‐type animals. B: Reciprocal transplants between heterozygous mutant and wild‐type hamsters. Closed circles: periods of the intact hosts; open circles: period of rhythm following transplantation of wild‐type tissue; triangles: period of rhythm following transplantation of homozygous mutant tissue; stars: period of rhythm following transplantation of heterozygous mutant tissue.

Reproduced with permission from reference 141


Figure 5.

Representative patterns of vasopressin (VP) release from two individual SCN explants studied in constant conditions using a perifusion culture technique. Both explants were obtained from rats maintained on an 12:12 light‐dark cycle, but preparation of the cultures occurred at two different times. The top panel shows the VP rhythm from an explant prepared at the onset of the 12 h light phase, while the bottom panel shows the rhythm from an explant prepared near the end of the light phase. Open and closed bars denote determinations of the amount of VP released into the medium over 2 h sampling intervals during the subjective day (that is, the portion of the circadian cycle coinciding with the projected light phase of the cycle) and the subjective night, respectively.

Reproduced with permission from reference 40


Figure 6.

Effects of pulses of light with varying radiance on c‐fos mRNA in the SCN region and the phase of the activity rhythm in hamsters maintained in constant darkness. All light pulses were 5 min in duration and were presented at circadian time 19. Left panels: Following exposure to the light pulse, animals were returned to constant darkness for 25 min before the brains were prepared for c‐fos analysis by in situ hybridization procedures. Panel 1 shows c‐fos levels in an animal receiving no light pulse, while panels 2‐5 show levels in animals exposed to increasing levels of illumination. Right panels: Representative activity records of hamsters exposed to light stimuli of similar irradiance to the corresponding left panels. Asterisks mark the time of the light pulse, after which the animals continued to free‐run in constant darkness.

Reproduced with permission from reference 83


Figure 7.

Dependence of light‐induced behavioral phase‐shifting and jun‐B and c‐fos mRNA levels in the SCN region as a function of circadian phase. Hamsters were maintained in darkness before being exposed to a 5 min pulse of light. A: Asterisks superimposed on the phase response curve to light pulses in hamsters denote the time of the light pulses in B and C. B: jun‐B mRNA in the SCN after light pulses of 5 min duration at circadian time 3, 9, 14, 19, and 21. Animals were returned to darkness for 25 min and brains were prepared for in situ hybridization. Values represent the mean signal in the SCN of light‐pulsed hamsters relative to the mean signal at the same circadian time in animals receiving no light. Hamsters receiving no light exhibited no significant jun‐B mRNA hybridization in the SCN at all circadian times examined. C: c‐fos mRNA in the SCN region induced by light following the procedures described in B.

Reproduced with permission from reference 84


Figure 8.

Schematic representation of a putative model for the organization of the circadian system in complex organisms. See text for further details.

Reproduced with permission from reference 203


Figure 9.

Top: Mean (± S.E.M.) phase shifts in the activity rhythm of young and old hamsters maintained in constant light that were subjected, beginning at either circadian time 6 (left panel) or circadian time 18 (right panel) to a 6 h dark pulse. A value above the solid line indicates an advance in the onset of locomotor activity; a value below indicates a delay. Values in parentheses indicate the number of trials for each group of animals. The mean phase shift in the activity rhythm in response to the dark pulse was significantly greater (P < 0.001) in young than in old hamsters at both circadian times tested. Bottom: Representative sections from the wheel‐running activity records of two young (left panels) and two old (right panels) hamsters housed in constant light before and after they were subjected to a 6 h dark pulse beginning at circadian time 6 (top panels) or circadian time 18 (bottom panels). The day of the dark pulse is designated by DP at the left of each record with the exact beginning and end of the dark pulse designated by two stars.

Reproduced with permission from reference 219


Figure 10.

Running wheel activity records from two Djungarian hamsters (left) and the mean paired testes weight (right) of groups of nine to ten hamsters exposed for 28 days to two 10 min pulses of light per 24 h. The bar at the top of each activity record indicates the light‐dark 6:18 photoperiod (unfilled bar represents lights‐on) to which the hamsters were exposed for about 21 days prior to transfer to the “skeleton” photoperiods. The second bar at the top of each activity record indicates the time at which the animals were exposed to the two 10 min pulses of light. Depending on the initial placement of the 10 min pulse of light relative to the previous 6:18 light‐dark cycle, the activity rhythm of some of the animals was advanced for a few cycles until an 8:16 light‐dark entrainment pattern was established (that is, activity confined to the 16 h interval of darkness) (top left panel), whereas in other animals the activity rhythm was delayed for a few cycles until a 16L: 8D entrainment pattern was established (that is, activity confined to the 8 h interval of darkness) (lower left panel). Testes weight for control animals maintained on 6:18 light‐dark are shown for comparative purposes.

Reproduced with permission from reference 99
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Article Title: Circadian Rhythms
 

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Fred W. Turek, Olivier Van Reeth. Circadian Rhythms. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 1329-1359. First published in print 1996. doi: 10.1002/cphy.cp040258