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Twilight Times: Light and the Circadian System

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Twilight Times: Light and the Circadian System Photochemistry and Photobiology, 1997, 66(5): 549-561 Invited Review Twilight Times: Light and the Circadian System Till Roenneberg*’ and Russell G. Foster2 ’Institute for Medical Psychology, Ludwig-Maximilian University, Munich, Germany and 2Department of Biology, Imperial College, London, UK Received 21 May 1997; accepted 31 July 1997 Whose twilights were more clear, than our mid-day. even if it is isolated from the rest of the brain (1). Long John Donne (1571-1631) before the primary circadian clock of mammals was identi- Of the progress of the soul fied in the SCN, the endogenous nature of circadian rhythms was recognized, first in plants (2-5) and then in many dif- ferent animal species (6). Identification has been based upon THE CIRCADIAN CLOCK the critical observation that when organisms are kept in iso- The spatial and temporal features of the environment have lation, void of any temporal cues, their daily routine contin- provided the abiotic selection pressures that have shaped the ues unabated, although the endogenous daily period (7)may evolution of life on earth. We are accustomed to accept that deviate from the external 24 h cycle (T), hence the term the spatial world offers specialized niches. However, we circadian (about 1 day). Such drifting rhythms are often rarely consider that the temporal structure of our planet of- termed “free-running’’ rhythms, and depending on the or- fers similar opportunities. Most organisms have evolved spe- ganism and on the nature of the constant conditions (e.g. cializations that allow them to exploit their environment in constant light or constant darkness), the endogenous period terms of both space and time, and this demands that indi- of the free-running rhythm can range from about 19 to 28 h. viduals have an endogenous representation of these environ- The circadian period not only depends on the quality of mental features. We know surprisingly little about the en- environmental conditions, as will be discussed below, but is dogenous representation of space, but in recent years an un- also under tight genetic control as shown by classic as well derstanding of how organisms build a representation of their as by molecular genetics (7). Single genes or gene complex- temporal world has begun to emerge. es have been isolated in the fruit fly Drosophila (8), the Organisms do not merely respond to their environment, fungus Neurospora (9,10), in Chlamydomonas (11) and in they also have the capacity to adjust physiology and behav- the cyanobacterium Synechococcus (12), as well as in the ior in anticipation of changing environmental conditions. In hamster (13) and the mouse (14), that profoundly influence a competitive world, “being prepared” offers a great selec- the length of the circadian period and are likely to be mo- tive advantage. It takes considerable time to bring about the lecular components of the clock itself. The current models complex realignments of physiological systems that permit for molecular pacemakers will be briefly described in a sep- an optimal expression of different behavioral states (e.g. ac- arate section. Considerable research has shown that the tivity and rest or exploitation of temporally restricted re- mechanisms of the circadian pacemaker (the endogenous sources). By fine-tuning physiology in advance of the chang- rhythm generator) are part of the biochemistry of single cells ing conditions, an organism can be ready to exploit the (15-19). This has been known for decades because the me- changed conditions to its best advantage. tabolism of single cell organisms, such as Euglena (20,21), At the heart of the biological machinery that “creates” a Chlamydomonas (22), Acetabularia (23), Gonyaulax (24), day within us is a biological or Circadian clock. In mammals, Pyrocystis (25), Tetrahymena (26) and Paramecium (27) is for example, this resides within a small paired nucleus in also controlled by a circadian system (for an extensive re- the brain located above the crossing of the optic nerves, the view of circadian rhythms in unicellular organisms see Ed- suprachiasmatic nuclei or SCN.? The neuronal activity of munds (28)). this nucleus continues to oscillate with a 24 h rhythmicity In addition to the free-running nature of circadian rhythms, two other universal properties have been identified: *To whom correspondence should be addresed at: Institute for Med- (a) The period of circadian rhythms is not greatly affected ical Psychology, Chronobiology Group, Ludwig-Maximilian Uni- by changes in environmental temperature. The rates of most versity, Goethestr. 31, 80336 Munich, Germany. Fax: 49 89 5996- biochemical reactions approximately double with a 10°C rise 615; e-mail: [email protected] in temperature (Qlo 2 2). By contrast, circadian rhythms jAhhreviations: CT, circadian time; PRC, phase response curve; RGC, retinal ganglion cells; RHT, retino-hypothalamic tract; show temperature compensation so that period length SCN, suprachiasmatic nuclei. changes very little over larger temperature fluctuations (29). Q 1997 American Society for Photobiology 003 I -8655/97 $5.00+0.00 As a result, those circadian rhythms studied have a Ql0that 549 550 Till Roenneberg and Russell G. Foster is very close to 1. (b) Circadian rhythms can be adjusted so can greatly alter the amount of light detected by an organ- that internal and environmental time are synchronized. It is ism. As a result, the sensory system needs to smooth out this process of entrainment that forms the central focus of these local fluctuations to obtain a reliable measure of light our discussion below. levels, and hence time of day. One way to achieve this would be to use a long sampling or integration time to gather pho- ENTRAINMENT OF CIRCADIAN RHYTHMS tons. In addition, the system would need to measure overall light levels in the environment (irradiance) and ignore The function of the circadian system is to regulate the phases brightness in particular areas of the sky (radiance). at which biological events occur, either in relation to specific The spectral composition of the light. In addition to pro- features of the 24 h environmental cycle or in relation to found changes in irradiance at twilight (approx. 6 log units), periodic events within the organism. To fulfill its function, there are very precise spectral changes; twilight is primarily the circadian system must remain synchronized with the so- characterized by relative enrichment of the shorter wave- lar day. This entrainment is accomplished by resetting mech- lengths (<500 nm) compared to the mid-long wavelengths anisms that correct for the deviations of the endogenous pe- (500-650 nm). If circadian systems used two photoreceptors riod from 24 h (T - T). These consist of an input pathway (with different spectral sensitivities) to sample the relative (receptor and transduction elements) for specific environ- amounts of short- and longwave radiation, then this could mental signals (zeitgeber) and of elements within the circa- provide a very reliable marker of the phase of twilight. dian pacemaker, capable of transforming the incoming sig- The position of the sun. The position of the sun relative nals to appropriate changes of the rhythm’s phase. When to the horizon, could also provide a very accurate measure entrained, the circadian clock adopts a distinct phase rela- of the phase of twilight. Of course, the sensory requirements tionship with the astronomical day, and each of the different for plotting the sun are very different from the requirements expressed rhythms adopts its own phase relationships with for measuring the overall levels of light in the sky. Mapping the clock. the position of the sun would require an elaborate radiance Circadian systems respond, depending on’the species and detector, possibly with a lens, and the maintenance of to- its spatial and temporal niches, to a variety of different zeit- pographic order between the photoreceptors and the site of geber. For example, many microorganisms, plants and photic integration. heterothermic animals can be entrained by regular changes The extent to which all the features of twilight are en- in the ambient temperature (28). Social signals like species- countered by an organism will depend upon its ecology and specific songs in birds (30) or sound signals in humans (31) strategy for sampling light. can act as zeitgeber, and in some species regular feeding schedules can also result in entrainment (32,33). However, the stable and systematic daily change in the quality of light The ecology of photoentrainment at dawn or dusk provides the most reliable .indicator of the Organisms are often highly adapted to both a spatial and phase of the day. As a result, most organisms have evolved temporal niche (34). The most obvious example for temporal to use the twilight transition as their primary zeitgeber to specialization is the timing of activity to portions of the light adjust circadian phase (photoentrainment). Note that most of (day active), dark (night active) or twilight zones (crepus- the regular daily changes in other physical properties (tem- cular). Occupation of these temporal niches has resulted in perature, humidity, etc.) or biological changes (availability distinctive specializations. For example, night-active animals of resources or the danger by predators) are in some way rely more on their olfactory, acoustic or mechanosensory linked to the solar day and can thus be predicted by using systems, while day-active ones primarily use the visual light as the zeitgeber. Regardless how short or long the cir- sense. The opening of flowers, the eclosion of insects or the cadian period may be in constant experimental conditions, time of birth are other examples of functions that are re- in nature the discrepancy between T and T will be relatively stricted to unique times of the day characterized by specific srnall and will be corrected for in the twilight zones, either environmental properties (light intensity, humidity, wind, the at dawn (if T > T) or at dusk (if T < T), by advancing or presence of other organisms such as predators or pollen- delaying respectively.
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