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Institute of Physiology, Academy of Sciences of the Czech Republic, 142 20 Prague 4, Czech Republic
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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To date, photic entrainment of the mammalian circadian system has been studied by following phase shifts of overt rhythms in the periphery governed by a circadian pacemaker located in the suprachiasmatic nucleus (SCN). The present study follows for the first time photic resetting of intrinsic rhythmicity of the SCN itself. Rats maintained under either a shorter photoperiod, with 12 h of light and 12 h of darkness per day, or under a long, 18:6-h light-dark photoperiod were exposed to a light stimulus during the dark period and then released into darkness, and the next day the SCN rhythm in the light-stimulated c-Fos protein immunoreactivity was followed as a marker of the SCN endogenous rhythmicity. After a light stimulus in the early night, the evening rise in the photic elevation of Fos protein photoinduction as well as the morning decline were phase delayed within one cycle. After a light stimulus in the late night, only the morning decline in the photic elevation of Fos was phase advanced the next night, not the evening rise; consequently, the interval enabling high photic elevation of Fos was reduced. After a light stimulus was administered around the middle of the night, the next night the evening rise in the light-stimulated Fos was eventually phase delayed, the morning decline was phase advanced, and the rhythm amplitude was reduced significantly; under 18:6-h light-dark, a mere 5-min light exposure exhibited such effects. The data indicate that resetting of the SCN rhythmicity in the light-elevated c-Fos 1 day after a resetting stimulus administration, i.e., during transient cycles, may proceed via nonparallel phase shifts of the evening rise and of the morning decline of the light-stimulated Fos, and via amplitude lowering and suggest a complex circadian pacemaking system in the rat SCN.
immediate early gene; light-stimulated c-Fos; circadian pacemaker
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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DIURNAL OSCILLATIONS of behavioral, physiological, and endocrine functions in mammals are controlled by a circadian pacemaker located in the suprachiasmatic nuclei (SCN) of the hypothalamus (18). The phase and period of the pacemaker are entrained to the natural 24-h day-night cycle by the alternation of environmental light and darkness, namely by the light part of the day (27). Photic information is conveyed to the SCN by way of a direct retinal projection, the retinohypothalamic tract, and to a lesser extent also by other pathways, namely by the geniculohypothalamic tract (6, 24, 25). After a light stimulus, in addition to other processes, immediate early genes (IEGs), namely c-fos and jun-B genes, are transcriptionally activated in the retinorecipient, i.e., ventrolateral part of the SCN (1, 20, 28, 30); these genes are believed to function in coupling short-term signals elicited by extracellular events to long-term changes in cellular phenotype by mediating subsequent changes in gene expression (7, 26). When a cell is stimulated, the first wave of gene transcription involves IEG activation. Once translated, the protein products of fos and jun, i.e., c-Fos and Jun-B, reenter the nucleus and may form various complexes, collectively termed activator protein 1, which bind in a sequence-specific manner to recognition sites on many different genes, thereby regulating the transcription of "late response" target genes (19, 21, 29). Presence of c-Fos in the cell may thus serve as a marker of neuronal activation. Importantly, light induces c-fos and jun-B expression and elevates c-Fos and Jun-B in the mammalian SCN only during the subjective night, when it also phase shifts circadian rhythmicity (20, 30, 35). The rhythm in the light-elevated c-fos and jun-B mRNA and c-Fos and Jun-B protein thus also represents the endogenous rhythm of the SCN sensitivity to light.
Formal properties of the photic entrainment of circadian rhythmicity have been widely studied (2, 27, 36). Mostly overt rhythms, namely the locomotor activity rhythm or the rhythm in pineal melatonin production, have been used as hands of the circadian clock (2, 9, 10, 36). Recently, resetting of the intrinsic rhythmicity of the SCN itself has been studied as well, mostly resetting of the rhythm in the SCN electrical activity (3, 5, 32) or, to a lesser extent, in the SCN arginine vasopressin level (31). The former rhythm has a well-defined phase marker, i.e., the time of the electrical activity maximum that occurs during the subjective day. Although the first simple study on resetting of the SCN rhythm in electrical activity was done under in vivo conditions (16), latter studies have been mostly performed in the SCN containing brain slices maintained in vitro (5). Such an approach enables the study of resetting properties of various drugs and processes involved; however, it does not allow the study of photic entrainment of the SCN circadian rhythmicity in its complexity.
The present study was undertaken to find out how photic resetting of SCN intrinsic rhythmicity proceeds in vivo. As a marker of the SCN rhythmicity, the circadian rhythm in photic elevation of c-Fos was used. This rhythm was already successfully used as a marker in studies following nonphotic resetting of the SCN circadian pacemaking system, either by arousal in hamsters (23) or by melatonin in rats (33). The rhythm exhibits two well-defined phase markers, i.e., the time of the evening rise in the SCN photic elevation of c-Fos and the time of the morning decline. The waveform of the rhythm, which may reflect neuronal activation and the functional state of the ventrolateral SCN pacemaking system, depends on the photoperiod (35). To find out whether and how the photoperiod affects entrainment of the intrinsic SCN rhythmicity, the photic resetting of the rhythm in c-Fos response to light was followed in animals maintained under a short photoperiod as well as in those maintained under a long photoperiod.
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METHODS |
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Abstract
Introduction
Methods
Results
Discussion
References
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Animals. Sixty-day-old male Wistar rats (Velaz, Prague, Czech Republic) were housed at a temperature of 23 ± 2°C with free access to food and water. Animals were maintained under either a shorter photoperiod [12:12-h light-dark cycle (12:12 LD), lights on from 0600 to 1800] or a long photoperiod [18:6-h light-dark cycle (18:6 LD), lights on from 0300 to 2100] for at least 3 wk before experiments; the regime 12:12 LD is recognized by rats sensitized to the effects of photoperiod as an already short photoperiod (38). Illumination intensity provided by overhead 40-W fluorescent tubes was between 50 and 200 lx, depending on cage position.
Experimental paradigm. On the day of the experiment (night 1), rats were either exposed to a 200-lx light stimulus or left untreated (control animals), and then they were released into constant darkness. The next day (night 2), rats were exposed to a single 30-min light pulse at various times to get the whole nighttime profile of the photic c-Fos elevation, and then they were returned to darkness and killed 30 min later. For determination of c-Fos, c-Fos immunoreactivity as an indicator of c-Fos protein level was used; Fos immunoreactivity in the ventrolateral area of the SCN closely correlates with c-fos mRNA determined by in situ hybridization method (35).
Immunohistochemistry.
Rats were deeply anesthetized with pentobarbital sodium (50 mg ip) and
perfused through the ascending aorta with heparinized saline followed
by phospate-buffered saline (PBS; 0.01 M sodium phosphate/0.15 M NaCl,
pH 7.2) and then freshly prepared 4% paraformaldehyde in PBS. Brains
were removed, postfixed for 12 h at 4°C, and cryoprotected in 20%
sucrose in PBS overnight at 4°C. Thirty-micrometer-thick coronal
sections were cut and processed for immunohistochemistry using the
avidin-biotin method, with diaminobenzidine as the chromogen as
described (4). The primary Fos antiserum (1:8,000) was generated against the NH2-terminal peptide
sequence (kindly provided by D. Hancock; Imperial Cancer Research Fund,
London, UK, and generously supplied by Michael Hastings, University of
Cambridge, UK). Labeled cell nuclei in the ventrolateral SCN
(irrespective of the intensity of staining) were counted in the most
heavily stained section by two independent observers without knowledge
of the experimental procedure. With the above-mentioned Fos antiserum,
Fos immunoreactivity was barely detectable in the SCN of rats killed in
darkness in the early and late night without a prior light exposure
(mean number of labeled cells per nucleus ± SE was 4.4 ± 1.4;
n = 25), although our recent findings
with a highly sensitive antiserum (Z. Trávní
ková, A. Sumová, and H. Illnerová, unpublished observations) as well as
those of others (39) indicate presence of an endogenous rhythm in c-Fos
protein and c-fos mRNA in darkness in
the dorsomedial area of the SCN.
Data analysis. Data were analyzed by one-way analysis of variance and subsequent pairwise comparisons by the Student-Newman-Keuls multiple-range test (time differences) or the Bonferroni t-statistic (amplitude differences).
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Resetting of rhythm in photic elevation of Fos protein in 12:12 LD. In control rats released into darkness and exposed to a 30-min light pulse at various time points the next night, the light-stimulated Fos immunoreactivity began to increase around 1900, but only at 2000 was the rise significant (P < 0.05 compared with 1600, 1700, and 1800) (Figs. 1 and 2). In the morning, the light-stimulated Fos protein declined significantly at 0600 (P < 0.05 compared with 0300, 0400, and 0500), and at 0700 the Fos level returned to basal levels.
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Resetting of rhythm in photic elevation of c-Fos protein in 18:6 LD. In control rats released into darkness, the light-stimulated Fos immunoreactivity increased significantly at 2200 (P < 0.01 compared with 1900, 2000, and 2100; Figs. 3 and 4). In the morning, a significant decline occurred at 0400 (P < 0.05 compared with 0200 and 0300) and the light-stimulated Fos returned to basal levels between 0600 and 0700. The interval enabling high photic elevation of c-Fos was shorter by ~4 h than that in 12:12 LD (Figs. 1 and 2).
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Changes of amplitude during resetting of SCN rhythm in 12:12 and 18:6 LD. Under a shorter, 12:12 LD photoperiod and after a 1-h light pulse administered either in the first or in the second half of the night, the maximum of the light-stimulated Fos immunoreactivity, calculated as the mean of the three highest nighttime points, was surprisingly significantly lower than that in control rats, although eventually, at individual time points, the values were comparable to those in control rats (Fig. 1 and Table 1). After a 4-h and a 9-h light pulse encompassing the middle of the night, the next day the maximum of the light-stimulated Fos was reduced dramatically to just 57 and 53%, respectively, of the control value (Fig. 2 and Table 1).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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In agreement with our recent data (35), the interval enabling high photic elevation of c-Fos in the SCN is wider under a shorter, 12:12 LD photoperiod than under a long, 18:6 LD photoperiod. After a light pulse in the first half of the night, the SCN rhythm in the photic elevation of c-Fos protein is phase delayed within one cycle; under 12:12 LD, the evening rise in the light-stimulated Fos immunoreactivity is slightly more delayed than the morning decline, whereas under 18:6 LD the opposite appears to be true. Similarly, after a light stimulus in the first half of the night, the evening rise in the pineal melatonin production, i.e., in the N-acetyltransferase (NAT) activity driving the melatonin rhythm, is more phase delayed than the morning decline under a short photoperiod, whereas under a long photoperiod the morning NAT decline is more delayed than the evening rise (8, 14, 15). After a light pulse administered in the late night, under both photoperiods, only the morning decline in the light-stimulated c-Fos protein, and not the evening rise, is phase advanced the next night, as it is similarly the case with the pineal NAT rise and decline (8, 12, 14, 15). It takes 4 days before the evening NAT rise starts to be phase advanced as well (14). By analogy, it may take more transient cycles before the evening rise in the light-stimulated Fos in the SCN becomes phase advanced as well, i.e., before the whole circadian pacemaking system attains a new steady state.
Under a short photoperiod, a long light stimulus encompassing the middle of the night has a dual effect on the SCN rhythm in the light-stimulated c-Fos immunoreactivity the next night, i.e., a phase-delaying effect on the evening rise in the photostimulated c-Fos and a phase-advancing effect on the morning decline; due to the dual effect of such a light stimulus, the interval enabling high c-Fos protein photoelevation is temporarily reduced, as it is similarly the case with the duration of the nocturnal pineal melatonin production (10, 11, 15). Under a long photoperiod, when the interval enabling high photic elevation of c-Fos is compressed, even a light pulse of only a 5-min duration administered close to midnight may have a dual effect on the SCN rhythm in the light-stimulated c-Fos immunoreactivity; consequently, the interval enabling high photic elevation of c-Fos becomes temporarily even more compressed. Similarly, under 18:6 LD, a pulse of even a 1-min duration administered close to midnight phase delays the evening NAT rise and at the same time phase advances the morning decline (10, 13).
The above data indicate that the photic resetting of the SCN intrinsic rhythmicity in the light-stimulated c-Fos immunoreactivity is similar to the resetting of the overt rhythm in the pineal NAT activity driven by the SCN pacemaker. The similarity suggests that changes in the pineal rhythm reflect mostly changes in the functional state of the SCN pacemaking system, as it may be the case after transition of animals from a long to a short photoperiod and vice-versa (34).
Slight dissimilarities between the resetting of the SCN rhythm and the resetting of the pineal rhythm may, however, exist. Under 12:12 LD, the amplitude of the pineal NAT rhythm is reduced only after a long light stimulus encompassing the middle of the night (9, 10, 15), whereas resetting of the SCN rhythm in the photic elevation of c-Fos appears to proceed via lowering of the amplitude after all photic stimuli, although most markedly after a stimulus administered around the middle of the night. Similarly, under 18:6 LD, a light stimulus administered close to the middle of the night does not reduce the pineal NAT rhythm amplitude so markedly as it lowers the amplitude of the SCN rhythm in the light-induced c-Fos (8). It appears therefore that the amplitude of the SCN intrinsic rhythmicity may not necessarily closely control the amplitude of overt rhythms. Resetting of the overt circadian rhythmicity in humans after a light exposure around the time of the temperature minimum proceeds also via lowering of the rhythmicity amplitude (17).
The present study follows for the first time in detail the photic resetting of the SCN intrinsic rhythmicity in vivo, using the evening rise and the morning decline in the photic elevation of Fos protein as markers of the phase of the SCN pacemaking system. The data show that the next day after a light stimulus administration, i.e., during transient cycles, the markers do not necessarily phase shift in parallel, and under certain conditions they may even shift in opposite direction. Consequently, their phase relationship representing the interval enabling high photic elevation of c-Fos may be temporarily markedly reduced. Similarly, the phase relationship is markedly reduced under a long photoperiod (34, 35). Such a reduced state may not allow larger phase delays of the evening rise in the light-stimulated c-Fos, as it is similarly the case with the NAT rhythm (37). Importantly, resetting of the SCN intrinsic rhythmicity may proceed via lowering of its amplitude, as it has been predicted (22).
In conclusion, photic resetting of the SCN intrinsic rhythmicity in the light-stimulated c-Fos immunoreactivity depends on the photoperiod. During transient cycles, it may proceed via lowering of the amplitude of the SCN rhythmicity, and nonparallel phase shifting of the evening rise and of the morning decline in the light-stimulated c-Fos protein. Altogether, the data suggest complexity of the SCN circadian pacemaking system and its resetting.
Perspectives
The present study follows for the first time in detail photic resetting of the intrinsic rhythmicity of the circadian pacemaking system in the SCN and changes of the rhythmicity amplitude during the resetting. This approach also enables the study of the question of whether there is a correlation between magnitude of the amplitude of the intrinsic SCN rhythmicity and that of overt rhythms driven by the SCN pacemaker. The rhythm in the photic elevation of c-Fos used in this study as a marker of the SCN intrinsic rhythmicity is specific for the ventrolateral SCN. To learn more about the photic entrainment of the circadian pacemaking system in the whole SCN, resetting of a rhythm specific for the dorsomedial SCN should be studied as well. At present it becomes increasingly clear that even the human circadian system is entrained to the 24-h day mostly by photic stimuli. Hence knowledge of the mechanism of photic resetting of the circadian pacemaking system may be important for treatment of chronobiological disorders such as jet lag, maladaption to shift work, or a sleep-delayed syndrome.| |
ACKNOWLEDGEMENTS |
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The excellent technical assistance of Ms. Michaela Maisnerova is greatly acknowledged.
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FOOTNOTES |
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This work was supported by the Grant Agency of the Academy of Sciences of the Czech Republic Grant A-7011508 and by the Grant Agency of the Czech Republic Grant 309970512.
Address for reprint requests: A. Sumová, Institute of Physiology,
Academy of Sciences of the Czech Republic, Víde
ská
1083, 142 20 Prague 4, Czech Republic.
Received 15 August 1997; accepted in final form 2 December 1997.
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Introduction
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References
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) or exposed
to a 1-h light pulse (
) from 2300 to 2400 (A) or from 0200 to 0300 (B)
(night 1), and then they were released into
darkness and exposed to a single 30-min light pulse the next night
(night 2). Each point represents mean ± SE from 2 animals. Filled bars indicate dark periods.
