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Integration of Biological Clocks and Rhythms

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Abstract

Animals, plants, and microorganisms exhibit numerous biological rhythms that are generated by numerous biological clocks. This article summarizes experimental data pertinent to the often‐ignored issue of integration of multiple rhythms. Five contexts of integration are discussed: (i) integration of circadian rhythms of multiple processes within an individual organism, (ii) integration of biological rhythms operating in different time scales (such as tidal, daily, and seasonal), (iii) integration of rhythms across multiple species, (iv) integration of rhythms of different members of a species, and (v) integration of rhythmicity and physiological homeostasis. Understanding of these multiple rhythmic interactions is an important first step in the eventual thorough understanding of how organisms arrange their vital functions temporally within and without their bodies. © 2012 American Physiological Society. Compr Physiol 2:1213‐1239, 2012.

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Figure 1. Figure 1.

Ten‐day segments of simultaneous records of rectal temperature, plasma urea concentration, and plasma cholesterol concentration of a female goat (Capra hircus). The horizontal bars at the top indicate the timing of the light‐dark cycle. Notice that the rhythms of rectal temperature and urea concentration have similar phases (peaking in the middle of the night) but the rhythm of cholesterol concentration has the opposite phase (peaking in the middle of the day). Data from reference 395.

Figure 2. Figure 2.

Acrophases of the rhythms of 21 variables in the horse (Equus caballus). Circles indicate the means for five horses over 2 days. Horizontal lines indicate the 95% confidence intervals of the means. The rhythms of 13 variables peak during the light phase of the light‐dark cycle. Data from reference 399.

Figure 3. Figure 3.

Five‐day segments of the records of body temperature and locomotor activity (recorded by telemetry with 6‐min resolution) of a tree shrew (Tupaia belangeri). The horizontal black and white bars indicate the duration of the dark and light phases of the prevailing light‐dark cycle. Notice that both body temperature and activity level are high during the day and low at night. Data from reference 433.

Figure 4. Figure 4.

Daily variation in three psychological functions (as well as body temperature) of human subjects studied under a constant routine protocol (in continuous bed rest, receiving equally spaced meals, and not allowed to sleep) for 60 consecutive hours. The data points are the means (± SE) of five subjects. Notice that the rhythm of body temperature is very robust but that the rhythms of the psychological functions (especially short‐term memory) are rather sloppy. Data from reference 245.

Figure 5. Figure 5.

Double‐plotted actograms of the rhythms of feeding activity and egg laying of quails (Coturnix coturnix) maintained under a light‐dark cycle (A) or in constant darkness (B). The white ovals indicate the time of oviposition. Notice that entrainment of both rhythms is apparent under the light‐dark cycle (A) but that the feeding rhythm free runs with a period shorter than 24 h whereas the egg‐laying rhythm free runs with a period longer than 24 h in constant darkness (B). Data from reference 221.

Figure 6. Figure 6.

Distributions of the times of entry into and arousal from hibernation of eight European hamsters (Cricetus cricetus) maintained in the laboratory under simulated winter conditions (8°C, 8L:16D). The data are plotted separately for shallow and deep torpor bouts. Notice that, for entry into shallow or deep torpor, the distributions are more or less clustered around the late evening and early morning. Data from reference 565.

Figure 7. Figure 7.

Seven‐day segments (with 2‐h resolution) of the records of body core temperature of representative individuals of four mammalian species. The white and dark horizontal bars at the top of each graph indicate the duration of the light and dark phases of the prevailing light‐dark cycles. Interspecies differences in waveform and acrophase are evident in the temperature records. Data from reference 449.

Figure 8. Figure 8.

Frequency distributions of free‐running periods and durations of the active phase of 51 nocturnal and diurnal species as reported in the literature. Organisms included are vertebrate and invertebrate animals, as well as non‐animals. Data from references 1, 2, 8,17, 25, 26, 34,36,40,55,56,63,65,67,70,75,94,96,99,109,125,128,131,133,143,145,156,160,177,179,181,193,196,201,205,213,216,221,224, 226, 227, 231,253,257,259,262,267,275,284,290,299,301,303,304,307,310,322, 327, 328, 347,373,374,375,378,389,390,406,409, 411, 412, 435, 436, 443,446,447,450,453,467,468,474,477,482, 493, 494, 496,501, 517, 518, 525, 526, 529,540,545,548,550,552,554,562,569,573,586,587, and 593.

Figure 9. Figure 9.

Intra‐ and interindividual variabilities of four parameters of the body‐temperature rhythm of laboratory rats, 13‐lined ground squirrels, Beagle dogs, and British Thoroughbred horses. All computations of variability (standard deviation of the mean) are based on measurements conducted on 7 individuals for 7 consecutive days with 2‐h resolution. The bars show the mean variability (± SE) for each condition. All animals were maintained under 24‐h light‐dark cycles. For each parameter, means sharing the same letter (a or b) are not significantly different from each other. Data from reference 449.

Figure 10. Figure 10.

Daily variation in alertness of morning types, intermediate types, and evening types. Subjective self‐evaluation of alertness was conducted by 1800 university students from six countries. Mean values for each of the three types are shown. Notice that, for intermediate types, alertness reaches a daily maximum at noon and stays elevated until 2000 h. For morning types and evening types, alertness rises a few hours earlier or later. Data from reference 512.

Figure 11. Figure 11.

Mean number of wheel revolutions of tau‐mutant and wild‐type golden hamsters (Mesocricetus auratus) maintained in constant darkness. The bars correspond to the means (± SE) of 32 mutants (period = 20.4 h) and 32 wild types (period = 24.1 h). The two groups are significantly different when activity is expressed per circadian cycle but statistically indistinguishable when activity is expressed per 24 h. Data from reference 446.



Figure 1.

Ten‐day segments of simultaneous records of rectal temperature, plasma urea concentration, and plasma cholesterol concentration of a female goat (Capra hircus). The horizontal bars at the top indicate the timing of the light‐dark cycle. Notice that the rhythms of rectal temperature and urea concentration have similar phases (peaking in the middle of the night) but the rhythm of cholesterol concentration has the opposite phase (peaking in the middle of the day). Data from reference 395.



Figure 2.

Acrophases of the rhythms of 21 variables in the horse (Equus caballus). Circles indicate the means for five horses over 2 days. Horizontal lines indicate the 95% confidence intervals of the means. The rhythms of 13 variables peak during the light phase of the light‐dark cycle. Data from reference 399.



Figure 3.

Five‐day segments of the records of body temperature and locomotor activity (recorded by telemetry with 6‐min resolution) of a tree shrew (Tupaia belangeri). The horizontal black and white bars indicate the duration of the dark and light phases of the prevailing light‐dark cycle. Notice that both body temperature and activity level are high during the day and low at night. Data from reference 433.



Figure 4.

Daily variation in three psychological functions (as well as body temperature) of human subjects studied under a constant routine protocol (in continuous bed rest, receiving equally spaced meals, and not allowed to sleep) for 60 consecutive hours. The data points are the means (± SE) of five subjects. Notice that the rhythm of body temperature is very robust but that the rhythms of the psychological functions (especially short‐term memory) are rather sloppy. Data from reference 245.



Figure 5.

Double‐plotted actograms of the rhythms of feeding activity and egg laying of quails (Coturnix coturnix) maintained under a light‐dark cycle (A) or in constant darkness (B). The white ovals indicate the time of oviposition. Notice that entrainment of both rhythms is apparent under the light‐dark cycle (A) but that the feeding rhythm free runs with a period shorter than 24 h whereas the egg‐laying rhythm free runs with a period longer than 24 h in constant darkness (B). Data from reference 221.



Figure 6.

Distributions of the times of entry into and arousal from hibernation of eight European hamsters (Cricetus cricetus) maintained in the laboratory under simulated winter conditions (8°C, 8L:16D). The data are plotted separately for shallow and deep torpor bouts. Notice that, for entry into shallow or deep torpor, the distributions are more or less clustered around the late evening and early morning. Data from reference 565.



Figure 7.

Seven‐day segments (with 2‐h resolution) of the records of body core temperature of representative individuals of four mammalian species. The white and dark horizontal bars at the top of each graph indicate the duration of the light and dark phases of the prevailing light‐dark cycles. Interspecies differences in waveform and acrophase are evident in the temperature records. Data from reference 449.



Figure 8.

Frequency distributions of free‐running periods and durations of the active phase of 51 nocturnal and diurnal species as reported in the literature. Organisms included are vertebrate and invertebrate animals, as well as non‐animals. Data from references 1, 2, 8,17, 25, 26, 34,36,40,55,56,63,65,67,70,75,94,96,99,109,125,128,131,133,143,145,156,160,177,179,181,193,196,201,205,213,216,221,224, 226, 227, 231,253,257,259,262,267,275,284,290,299,301,303,304,307,310,322, 327, 328, 347,373,374,375,378,389,390,406,409, 411, 412, 435, 436, 443,446,447,450,453,467,468,474,477,482, 493, 494, 496,501, 517, 518, 525, 526, 529,540,545,548,550,552,554,562,569,573,586,587, and 593.



Figure 9.

Intra‐ and interindividual variabilities of four parameters of the body‐temperature rhythm of laboratory rats, 13‐lined ground squirrels, Beagle dogs, and British Thoroughbred horses. All computations of variability (standard deviation of the mean) are based on measurements conducted on 7 individuals for 7 consecutive days with 2‐h resolution. The bars show the mean variability (± SE) for each condition. All animals were maintained under 24‐h light‐dark cycles. For each parameter, means sharing the same letter (a or b) are not significantly different from each other. Data from reference 449.



Figure 10.

Daily variation in alertness of morning types, intermediate types, and evening types. Subjective self‐evaluation of alertness was conducted by 1800 university students from six countries. Mean values for each of the three types are shown. Notice that, for intermediate types, alertness reaches a daily maximum at noon and stays elevated until 2000 h. For morning types and evening types, alertness rises a few hours earlier or later. Data from reference 512.



Figure 11.

Mean number of wheel revolutions of tau‐mutant and wild‐type golden hamsters (Mesocricetus auratus) maintained in constant darkness. The bars correspond to the means (± SE) of 32 mutants (period = 20.4 h) and 32 wild types (period = 24.1 h). The two groups are significantly different when activity is expressed per circadian cycle but statistically indistinguishable when activity is expressed per 24 h. Data from reference 446.

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Further Reading
 1.Dunlap JC, Loros JJ, DeCoursey PJ, editors. Chronobiology: Biological Timekeeping. Sunderland, Mass.: Sinauer, 2004.
 2. Koukkari WL, Sothern RB. Introducing Biological Rhythms. New York: Springer, 2006.
 3. Refinetti R. Circadian Physiology (2nd ed). Boca Raton, Fla.: CRC Press, 2006.
 4.Rosato E, editor. Circadian Rhythms: Methods and Protocols. Totowa, NJ: Humana Press, 2007.
 5.Stillman B, Stewart D, Grodzicker T, editors. Clocks and Rhythms. Woodbury, NY: Cold Spring Harbor Laboratory Press, 2007.
 6.Young MW, editor. Circadian Rhythms. New York: Elsevier, 2005.

Further Reading

Dunlap JC, Loros JJ, DeCoursey PJ, eds. Chronobiology: Biological Timekeeping. Sunderland, Mass.: Sinauer, 2004.

Koukkari WL, Sothern RB. Introducing Biological Rhythms. New York: Springer, 2006.

Refinetti R. Circadian Physiology, 2nd edition. Boca Raton, Fla.: CRC Press, 2006.

Rosato E, ed. Circadian Rhythms: Methods and Protocols. Totowa, NJ: Humana Press, 2007.

Stillman B, Stewart D, Grodzicker T, eds. Clocks and Rhythms. Woodbury, NY: Cold Spring Harbor Laboratory Press.

Young MW, ed. Circadian Rhythms. New York: Elsevier, 2005.


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Roberto Refinetti. Integration of Biological Clocks and Rhythms. Compr Physiol 2012, 2: 1213-1239. doi: 10.1002/cphy.c100088