Clock Gene Daily Profiles and Their Phase Relationship in the Rat Suprachiasmatic Nucleus Are Affected by Photoperiod

Sumová, Alena; Jáč, Martin; Sládek, Martin; Šauman, Ivo; Illnerová, Helena

doi:10.1177/0748730403251801

Cited by 100 publications

(78 citation statements)

References 44 publications

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“…The increased width in multiunit activity patterns that we observed is consistent with the increased peak width in multiunit activity in the hamster (27), in patterns of c-fos and arginine vasopressin mRNA expression in the rat (28,29), in clock gene expression in the rat (30), and in patterns of Per expression in the hamster (31)(32)(33). The data on protein and mRNA expression are comparable with the multiunit data in that they represent responses of grouped neurons to different photoperiods.…”

Section: Discussionsupporting

confidence: 75%

Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding

Schaap

Albus

vanderLeest

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

191

176

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Circadian rhythms in neuronal ensemble, subpopulations, and single unit activity were recorded in the suprachiasmatic nuclei (SCN) of rat hypothalamic slices. Decomposition of the ensemble pattern revealed that neuronal subpopulations and single units within the SCN show surprisingly short periods of enhanced electrical activity of Ϸ5 h and show maximal activity at different phases of the circadian cycle. The summed activity accounts for the neuronal ensemble pattern of the SCN, indicating that circadian waveform of electrical activity is a composed tissue property. The recorded single unit activity pattern was used to simulate the responsiveness of SCN neurons to different photoperiods. We inferred predictions on changes in peak width, amplitude, and peak time in the multiunit activity pattern and confirmed these predictions with hypothalamic slices from animals that had been kept in a short or long photoperiod. We propose that the animals' ability to code for day length derives from plasticity in the neuronal network of oscillating SCN neurons.T he suprachiasmatic nuclei (SCN) contain a major pacemaker of circadian rhythms in mammals (1, 2). The SCN control circadian rhythms in the central nervous system and peripheral organs and as such ensures that organisms are able to anticipate and adjust to predictable changes in the environment that occur with the day-night cycle (3-5). The SCN is also involved in adaptation of the organism to the annual cycle by monitoring seasonal changes in day length (6). As an example, animals will accommodate their daily behavioral activity to the photoperiod. A multioscillator structure has been proposed to fulfill this dual task (7).At least nine candidate genes have been identified that play a role in rhythm generation on the basis of a transcriptionaltranslational feedback loop (8, 9). A number of additional genes may be involved to further refine or shape circadian rhythms (10). Although great progress has been made in understanding the molecular basis for circadian rhythm generation, it is unknown how individual neuronal activity rhythms are integrated to render a functioning pacemaker that is able to code for circadian and seasonal rhythms. The SCN each contain Ϸ10,000 neurons, which are small and densely packed (11). After dissociation, isolated SCN neurons express circadian rhythms in their firing patterns (12, 13). The freerunning periods of the individual neurons vary from 20 to 28 h. The average period matches the behavioral activity pattern of Ϸ24 h. In these cultured dispersals, synaptically coupled neurons can sometimes be observed with synchronized firing patterns (14). In SCN tissue explants cultured on multielectrode plates, the variation in free-running period is considerably smaller (15)(16)(17). In these explants, firing patterns can be observed which are in phase, or 6 -12 h out of phase. The range of phase relationships observed within the SCN in vitro suggests a level of temporal complexity that challenges our understanding of how a singular phase and perio...

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Section: Discussionsupporting

confidence: 75%

Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding

Schaap

Albus

vanderLeest

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

191

176

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“…In the SCN, rhythms of spontaneous neural firing and gene expression depend on prior entrainment conditions, as do various peripherally generated rhythms driven by the SCN (i.e., melatonin secretion and locomotor activity) (19,20,29,38,41). In all cases, markers of diurnal phase are expressed for longer after LD, whereas nocturnal functions lengthen under SD.…”

Section: Discussionmentioning

confidence: 99%

“…Several nocturnally expressed markers of circadian phase (e.g., elevated melatonin secretion and locomotor activity in nocturnal rodents) are expressed for a longer duration during short day (SD, e.g., 10 h light:14 h dark) than during long day entrainment (LD, e.g., 14 h light:10 h dark) (6,10). The converse is also true of the subjective day markers, SCN electrical activity and endogenous c-Fos and mper expression (19,20,29,38). Moreover, photoperiod alters the fraction of the circadian cycle during which c-Fos can be elicited by light pulses (41).…”

mentioning

confidence: 93%

Photoperiod differentially modulates photic and nonphotic phase response curves of hamsters

Evans¹,

Elliott²,

Gorman³

2004

American Journal of Physiology-Regulatory, Integrative and Comp

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Circadian pacemakers respond to light pulses with phase adjustments that allow for daily synchronization to 24-h light-dark cycles. In Syrian hamsters, Mesocricetus auratus, light-induced phase shifts are larger after entrainment to short daylengths (e.g., 10 h light:14 h dark) vs. long daylengths (e.g., 14 h light:10 h dark). The present study assessed whether photoperiodic modulation of phase resetting magnitude extends to nonphotic perturbations of the circadian rhythm and, if so, whether the relationship parallels that of photic responses. Male Syrian hamsters, entrained for 31 days to either short or long daylengths, were transferred to novel wheel running cages for 2 h at times spanning the entire circadian cycle. Phase shifts induced by this stimulus varied with the circadian time of exposure, but the amplitude of the resulting phase response curve was not markedly influenced by photoperiod. Previously reported photoperiodic effects on photic phase resetting were verified under the current paradigm using 15-min light pulses. Photoperiodic modulation of phase resetting magnitude is input specific and may reflect alterations in the transmission of photic stimuli.

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“…Jagota et al showed two distinct peaks of electrophysiological activity in the horizontally sectioned SCN culture in hamsters (10) but not in rats and mice (11), which responded differentially to photoperiods. In addition, the circadian rhythms in Per1 and Per2 expression were reported to change in different photoperiods (12)(13)(14)(15)(16)(17)(18)(19)23). The duration of gene expression was extended in long photoperiods, whereas the rhythm amplitudes were increased in short photoperiods, suggesting that the mutual coupling of individual cell oscillations was altered by photoperiods.…”

Section: Discussionmentioning

confidence: 99%

“…More recently, two distinct peaks of electrophysiological activity in the cultured SCN were observed in the Syrian hamster (10,11), and the peaks responded differentially to photoperiods (10). In addition, circadian rhythms in clock gene expression and their protein products were reported to change in different photoperiods (12)(13)(14)(15)(16)(17). Generally, the interval of high Per1 and Per2 expression is extended in long photoperiods, whereas the rhythm amplitudes are increased in short photoperiods.…”

mentioning

confidence: 98%

Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity

Inagaki

Honma

Ono

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

251

248

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The pattern of circadian behavioral rhythms is photoperioddependent, highlighted by the conservation of a phase relation between the behavioral rhythm and photoperiod. A model of two separate, but mutually coupled, circadian oscillators has been proposed to explain photoperiodic responses of behavioral rhythm in nocturnal rodents: an evening oscillator, which drives the activity onset and entrains to dusk, and a morning oscillator, which drives the end of activity and entrains to dawn. Continuous measurement of circadian rhythms in clock gene Per1 expression by a bioluminescence reporter enabled us to identify the separate oscillating cell groups in the mouse suprachiasmatic nucleus (SCN), which composed circadian oscillations of different phases and responded to photoperiods differentially. The circadian oscillation in the posterior SCN was phase-locked to the end of activity under three photoperiods examined. On the other hand, the oscillation in the anterior SCN was phase-locked to the onset of activity but showed a bimodal pattern under a long photoperiod [light-dark cycle (LD)18:6]. The bimodality in the anterior SCN reflected two circadian oscillatory cell groups of early and late phases. The anterior oscillation was unimodal under intermediate (LD12:12) and short (LD6:18) photoperiods, which was always phase-lagged behind the posterior oscillation when the late phase in LD18:6 was taken. The phase difference was largest in LD18:6 and smallest in LD6:18. These findings indicate that three oscillating cell groups in the SCN constitute regionally specific circadian oscillations, and at least two of them are involved in photoperiodic response of behavioral rhythm.bioluminescence reporter ͉ circadian rhythm ͉ clock gene ͉ photoperiod ͉ behavioral rhythm A daptation to seasonal changes in environment is critical to the survival of many organisms. Photoperiodic time measurement by the circadian clock is one of the strategies by which they conserve the phase relation between behavioral events such as the activity onset and dawn or dusk (1). A dramatic change induced by photoperiod is in the length of an activity band, the duration of activity in behavioral rhythms. Nocturnal rodents such as rats and mice exhibit compressed activity bands in long photoperiods and decompressed bands in short photoperiods. A long-standing hypothesis for the photoperiodic time measurement assumes two separate, but mutually coupled, circadian oscillators that drive the activity onset and end of activity, respectively, and respond to dawn and dusk differentially. Therefore, their phase-relationship encodes day lengths and changes the length of an activity band (1).The circadian clock in mammals is located in the suprachiasmatic nucleus (SCN) of the hypothalamus; it entrains to a light-dark cycle (LD) and determines the phases of overt circadian rhythms in behavior and physiology (2). Over the last decade, our understanding of the circadian clock in the SCN has advanced tremendously (3-5). The SCN consists of a number of oscillating cel...

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Clock Gene Daily Profiles and Their Phase Relationship in the Rat Suprachiasmatic Nucleus Are Affected by Photoperiod

Cited by 100 publications

References 44 publications

Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding

Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding

Photoperiod differentially modulates photic and nonphotic phase response curves of hamsters

Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity

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