Temporal organization: reflections of a Darwinian clock-watcher.
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Animals↗
Biomedical subjects
C S Pittendrigh
Publications and source records attributed to C S Pittendrigh.
The amplitude of circadian oscillations: temperature dependence, latitudinal clines, and the photoperiodic time measurement.
This paper develops several propositions concerning the lability of the amplitude of Drosophila circadian pacemakers. The first is that the amplitude of the pacemaker's motion, unlike its period, is markedly temperature-dependent. The second is that latitudinal variation in pacemaker amplitude (higher in the north) is responsible for two very different sets of observations on Drosophila circadian systems at successively higher latitudes. One of these is a cline in D. auraria's phase-shifting response to light, which steadily weakens in a succession of more northerly strains. The other, concerning D. littoralis in the very far north, is a cline in the rate at which eclosion activity becomes arrhythmic (the circadian rhythm damps out) in constant darkness; damping is faster in the north. The third proposition concerns a plausible selection pressure for the cline in pacemaker amplitude that we propose underlies the two directly observed clines. Two points are emphasized: (1) The amplitude of the pacemaker's daily oscillation declines as the duration of the entraining light pulse (photoperiod) is increased; and (2) the duration of the daily photoperiods throughout the breeding season is steadily increased as one moves toward the poles. Selection for conservation of pacemaker amplitude (during the breeding season) would produce the latitudinal cline we propose. The fourth, and final proposition is that since the amplitude of the pacemaker's daily motion responds systematically to change in photoperiod, amplitude is clearly one way--and a temperature-dependent way--in which insect circadian systems may sense seasonal change. These propositions concerning the temperature and latitude dependence of pacemaker amplitude may be relevant to a wider array of circadian pacemakers than Drosophila.
Animals↗
Latitudinal clines in the properties of a circadian pacemaker.
The circadian rhythm of eclosion activity and its pacemaker were analyzed in a series of latitudinal races of Drosophila auraria ranging from 34.2 degrees to 42.9 degrees N in Japan. The phase of the rhythm (psi EL) to the daily photoperiod (PP) changes as daylength is increased, and the slope of psi EL (PP) changes with latitude. Is is sufficiently greater in the north to cause a phase reversal of northern and southern races on long versus short photoperiods. This reversal is found in assays of the pacemaker's phase (psi PL) as well as that of the rhythm (psi EL). Assay of the pacemaker shows that its period (tau) is longer in northern than in southern races, and that the amplitude of its phase response curve (PRC) is lower in the north. The period of the rhythm in all latitudinal races is longer than 24 hr in short photoperiods (LD 1:23), but is probably less than 24 hr (as an aftereffect of photoperiod) in longer days such as LD 14:10. The observed north-south differences in the phase relation of both pacemaker and rhythm to the light cycle are explained by the latitudinal clines in pacemaker properties and a postulated aftereffect of photoperiod on tau. It is suggested that the latitudinal cline in PRC amplitude has functional significance in conserving the amplitude of the pacemaker's signal to the rest of the system it times. Computer simulation shows that without such a reduction in the perceived light intensity, pacemaker amplitude will be lowered by the increase in duration of the daily light at higher latitudes.
Animals↗
The photoperiodic phenomena: seasonal modulation of the "day within".
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Humans↗
Temperature dependence and evolutionary adjustment of critical night length in insect photoperiodism.
The photoperiodic responses of Drosophila auraria are shown to involve its circadian system functioning as the "clock" that measures the duration of darkness at night. Attempts at further clarification of this finding were based on the widely held assumption that adaptive adjustment of critical night length is caused by change in the circadian system's entrainment behavior. Three different experimental programs yielded data that are incompatible with this starting premise. Collectively, the observations suggest a new interpretation of the lability (phenotypic and genetic) of critical night length based on change in the level of response to all night-length measurements-not on the measurements themselves. This proposition is found especially relevant to the temperature dependence of photoperiodic responses and its role in controlling the onset and termination of the breeding season at different latitudes.
Journal Article↗
Sleep and activity rhythms in mice: a description of circadian patterns and unexpected disruptions in sleep.
Studies on daily and circadian rhythms in wheel running and electrographically defined wakefulness, NREM sleep, and REM sleep in M. musculus were done to gather data on the temporal distribution of activity and sleep. Generally, peaks in NREM and sleep tended to coincide and to alternate with the coincident peaks of wakefulness and wheel running. However, during the active phase of the circadian wheel running cycle some NREM and REM sleep did occur; conversely, during its rest phase, wakefulness was often present. The most striking finding was that in mice with clearly entrained or free-running activity onsets, the circadian peak-through patterns in wakefulness, NREM, and REM sleep were not always distinct--they could be damped and/or polyphasic. Several explanations of these phenomena are considered.
Animals↗
Mutual entrainment of bilaterally distributed circadian pacemaker.
The interactions between the bilaterally distributed components of the circadin system that controls the locomotor activity rhythm of the cockroach Leucophaea maderae were investigated in a series of surgical lesion experiments. Complete excision of one optic lobe (either right or left) or its surgical isolation from the central nervous system had no effect on the animals' ability to free-run in constant darkness nor was there any indication, as judged by postoperative pi values of any difference between left and right lobe pacemakers. However, these surgical procedures consistently resulted in a significant increase in tau over preoperative value while optic nerve section had no effect on tau. The propostion is developed that the left and right pacemakers in the two optic lobes are mutally coupled and that the compound pacemaker's period is shorter than either of its constituent pacemakers. It was also found that the integrity of either compound eye is sufficient to assure entrainment of both left and right pacemakers.
Animals↗
An effect of castration and testosterone replacement on a circadian pacemaker in mice (Mus musculus).
Castration of mice in freerunning conditions (total darkness, DD) causes a reduction of running wheel activity in the beginning of the active period (alpha) and stimulates activity at the end of alpha. Simultaneously, the period (tau) of the freerunning rhythm is increased. Both effects are abolished by implantation of a Silastic capsule from which a physiological dose of testosterone is released at a constant rate. The results are tentatively explained by differential endocrine influences on two oscillating components in the pacemaker of the circadian activity rhythm.
Animals↗
Circadian oscillations in rodents: a systematic increase of their frequency with age.
The circadian activity rhythms of golden hamsters and two species of deermouse, when released from a light-dark cycle of 12 hours light and 12 hours of darkness into constant darkness, had progressively shorter periods as the animals became older. A possible bearing of this fact on the aging process is briefly outlined.
Aging↗
A test of the hypothesis that D2O affects circadian oscillations by diminishing the apparent temperature.
The period (tau) of a circadian pacemaker in the cockroach Leucophaea maderae is a nonmonotonic function of temperature. The slope of the curve (tau as a function of temperature) is negative at 20 degrees and positive at 30 degrees . When these insects are deuterated at 20 degrees and 30 degrees the period (tau) of the pacemaker lengthens in both cases, although there is a marked temperature dependence of D(2)O action. The increase in tau is nearly three times greater at 20 degrees than 30 degrees . This observation is a flat contradiction of a prediction made earlier that when D(2)O affects circadian pacemakers it does so by diminishing the apparent temperature of the cell. That prediction, however, involves an assumption that may well be unfounded. Unless D(2)O acts nonselectively on all the components in the system regulating tau, the prediction we sought to test is unfounded; and if D(2)O does not act nonselectively, the observed temperature dependence of D(2)O action is understandable in terms of simulating a lower temperature for those components it does affect.
Animals↗
On the very rapid enhancement by D2O of the temperature-tolerance of adult Drosophila.
Deuterium oxide, D(2)O, increases the temperature-tolerance of Drosophila pseudoobscura when it is administered to adult flies as a sucrose solution. The effect is very rapidly exerted; it is detected within 10 min after the flies have a brief (10 min) opportunity to drink. This increased resistance to heat-death surely implies an increased resistance of macromolecules to thermal denaturation. D(2)O is known to exert such an effect on in vitro protein solutions. The speed with which the increased stability develops clearly implicates a solvent action of D(2)O, and is most easily understood if the effect is traceable to enhancement of the hydrophobic interactions which contribute to conformational stability. The increased strength of deuterated hydrogen bonds cannot be excluded however. The possible bearing of these results on the hypothesis that D(2)O always increases the period of circadian oscillations by "diminishing the apparent temperature" is briefly considered.
Animals↗
A differential effect of heavy water on temperature-dependent and temperature-compensated aspects of circadian system of Drosophila pseudoobscura.
D(2)O is the only "chemical" agent that consistently affects the frequency of circadian oscillations: its effect is now known to be so widespread and predictable that its action merits closer study as a potential clue to the currently obscure concrete nature of circadian oscillators. The great diversity of D(2)O effects on biological systems in general is briefly reviewed and the need for rejectable hypotheses concerning the action of D(2)O on circadian clocks is stressed because current speculation on its action yields "predictions" expected from almost any hypothesis. We consider the hypothesis that it "diminishes the apparent temperature" of the cell and proceed to test this by examining the effect of D(2)O on temperature-dependent and temperature-compensated aspects of the circadian system in Drosophila. We find these components respond as differentially to D(2)O as they do to temperature; we conclude, however, with a warning that this result may be equivocal if, as we now suspect, the frequency of circadian oscillations is generally homeostatically conserved-not only in the face of temperature change, but change in any variable to which it is sensitive. More crucial tests of the temperature-equivalence hypothesis for D(2)O action are defined.
Animals↗
General homeostasis of the frequency of circadian oscillations.
Some well-defined statistical regularities characterize the change in period (tau) of cockroach circadian oscillations subjected to a large temperature step. These are explainable in terms of the well-known temperature-compensation (homeostasis) of tau of circadian oscillations. The same regularities are detectable in published data on the effect of several other variables affecting several other circadian oscillations. The proposition is then developed that the temperature-compensation of tau is only a special case of a general homeostatic conservation of the frequency of circadian oscillations in the face of all changes they are likely to encounter in the cell. Such a general homeostasis of tau is a functional prerequisite for an oscillator to function as a useful "clock."
Animals↗
Circadian systems: longevity as a function of circadian resonance in Drosophila melanogaster.
Drosophila melanogaster, which had been reared under standard conditions (25 degrees and a 24-hr light/dark cycle involving 12 hr of light) were exposed, on the first day of adult life, to four environments (all at 25 degrees ) as follows: (i) a 24-hr day consisting of 12 hr light and 12 hr dark; (ii) a 21-hr day (10.5 hr light, 10.5 hr dark); (iii) a 27-hr day (13.5 hr light, 13.5 hr dark); and (iv) constant light. The experiment was repeated four times. In all four experiments the flies on a 24-hr day lived significantly longer than the flies in the other environments. This result, comparable to other observations on plants, indicates that eukaryotic systems as oscillators perform most effectively when they are driven close to their natural "circadian" frequency.
Adaptation, Physiological↗
Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction.
It is an established fact that circadian rhythmicity is often somehow involved in the physiology of photoperiodic induction. It is shown, however, that there are three possible ways in which such rhythmicity could be involved. For the most part available data are inadequate to discriminate among these three roles, only one of which is covered by "Bünning's Hypothesis." Emphasis is given to a previously ignored possibility in which circadian organization is involved in photoperiodism"ut not as the clock responsible for the time-measurement. The meaning of circadian surfaces and their bearing on the interpretation of a widely used experimental protocol is developed.
Biological Clocks↗
Circadian systems. V. The driving oscillation and the temporal sequence of development.
A circadian oscillation (in the brain) of Drosophila spp. acts as a gating device restricting the emergence behavior of the adult to a limited fraction of each 24-hour cycle defined by that oscillator, but the oscillation does not gate intermediate steps of pupal development. Unlike the emergence act, such intermediate events in development occur at fixed times after prepupa formation and are totally independent of the phase of the ongoing oscillator that gates emergence behavior.
Animals↗
Circadian systems, VI. Photoperiodic time measurement in Pectinophora gossypiella.
Diapause (100% incidence) occurs in the moth Pectinophora gossypiella when it is exposed to 24-hour light/dark cycles involving 12 hours of red light (600 nm); only 2% occurs when the photoperiod is extended to 14 hours, again with 600-nm light. This wavelength fails to synchronize all the known circadian oscillations of the moth. These observations appear, therefore, to constitute positive evidence that the photoperiodic time measurement is not mediated by a circadian oscillation. However, it remains possible, even plausible, that the photoperiodic clock is a separate circadian oscillator coupled to light by a red-absorbing pigment. That possibility is testable. The nature of the clock-oscillator or not-remains open.
Animals↗
Circadian oscillation controlling hatching: its ontogeny during embryogenesis of a moth.
Populations of eggs of the moth Pectinophora gossypiella develop a circadian rhythm of hatching activity under certain circumstances. This rhythm derives from circadian oscillations in each egg, which can be initiated or made synchronous by steps or pulses of either light or temperature, but only if these signals are administered after the midpoint of embryogenesis. Correlations between the development of the oscillation, appearance of a pigment, sensitivity to photoperiodic induction, and a possible effect of light on growth rate are discussed.
Animals↗