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

2007 ◽  
Vol 104 (18) ◽  
pp. 7664-7669 ◽  
Author(s):  
Natsuko Inagaki ◽  
Sato Honma ◽  
Daisuke Ono ◽  
Yusuke Tanahashi ◽  
Ken-ichi Honma
Keyword(s):  
Suprachiasmatic Nucleus ◽  
Late Phase ◽  
Photoperiodic Response ◽  
Circadian Oscillation ◽  
Behavioral Rhythms ◽  
Circadian Oscillators ◽  
Behavioral Rhythm ◽  
Cell Groups ◽  
Photoperiodic Responses ◽  
Activity Onset

The pattern of circadian behavioral rhythms is photoperiod-dependent, 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.

Two Coupled Circadian Oscillators Are Involved in Nonphotic Acceleration of Reentrainment to Shifted Light Cycles in Mice

2018 ◽  
Vol 33 (6) ◽  
pp. 614-625 ◽  
Author(s):  
Yujiro Yamanaka ◽  
Sato Honma ◽  
Ken-ichi Honma
Keyword(s):  
Behavioral Interventions ◽  
Wheel Running ◽  
Dark Period ◽  
Phase Shifts ◽  
Constant Darkness ◽  
Circadian Oscillators ◽  
Behavioral Rhythm ◽  
Activity Onset ◽  
Activity Band ◽  
The Relationship

The onset and offset of an activity band in the circadian behavioral rhythm are known to differentially reentrain to shifted light-dark cycles (LD). Differential reentrainment could be explained by different light responsivities of circadian oscillators underlying these phase-markers. In contrast, reentrainment is accelerated by exposure to nonphotic time cues such as timed wheel-running. However, the relationship between the 2 oscillators and nonphotic acceleration of reentrainment is largely unknown. We examined phase-shifts of the mouse behavioral rhythm in response to an 8-h phase-advanced shift of LD and effects of behavioral interventions: maintained in a home cage (HC), exposed to a running wheel (RW) in HC (HC+RW), transferred to a new cage (NC), and exposed to RW in NC (NC+RW). Each intervention was given for 3h from the beginning of the shifted dark period and repeated for 4 days. Following the last dark period, the mice were released into constant darkness (DD). As a result, activity onset and offset were differentially phase-shifted. The activity onset on the first day of DD (DD1) was phase-advanced from the baseline slightly in HC and HC+RW, substantially in NC+RW, but not significantly in NC. The amount of phase-shift was significantly larger in the NC+RW than in the other groups. In contrast, the activity offset was significantly advanced in all groups by 6 to 8 h. The differential phase-shifts resulted in shortening of the activity band (α compression). The α compression was gradually relieved upon exposure to DD (α decompression), and the activity band finally became stable. Interestingly, the magnitude of phase-shifts of activity offset, but not of activity onset, in the following DD was negatively correlated with the extent of α compression in DD1. These findings indicate that the 2 circadian oscillators underlying activity onset and offset are involved in asymmetric phase-shifts and nonphotic acceleration of reentrainment.

scholarly journals Dissociation of Per1 and Bmal1 circadian rhythms in the suprachiasmatic nucleus in parallel with behavioral outputs

2017 ◽  
Vol 114 (18) ◽  
pp. E3699-E3708 ◽  
Author(s):  
Daisuke Ono ◽  
Sato Honma ◽  
Yoshihiro Nakajima ◽  
Shigeru Kuroda ◽  
Ryosuke Enoki ◽  
...  
Keyword(s):  
Circadian Rhythms ◽  
Suprachiasmatic Nucleus ◽  
Clock Genes ◽  
Behavioral Rhythm ◽  
Calcium Indicator ◽  
Intracellular Ca ◽  
Regional Specificity ◽  
Free Running ◽  
Activity Onset ◽  
And Behavior

The temporal order of physiology and behavior in mammals is primarily regulated by the circadian pacemaker located in the hypothalamic suprachiasmatic nucleus (SCN). Taking advantage of bioluminescence reporters, we monitored the circadian rhythms of the expression of clock genes Per1 and Bmal1 in the SCN of freely moving mice and found that the rate of phase shifts induced by a single light pulse was different in the two rhythms. The Per1-luc rhythm was phase-delayed instantaneously by the light presented at the subjective evening in parallel with the activity onset of behavioral rhythm, whereas the Bmal1-ELuc rhythm was phase-delayed gradually, similar to the activity offset. The dissociation was confirmed in cultured SCN slices of mice carrying both Per1-luc and Bmal1-ELuc reporters. The two rhythms in a single SCN slice showed significantly different periods in a long-term (3 wk) culture and were internally desynchronized. Regional specificity in the SCN was not detected for the period of Per1-luc and Bmal1-ELuc rhythms. Furthermore, neither is synchronized with circadian intracellular Ca2+ rhythms monitored by a calcium indicator, GCaMP6s, or with firing rhythms monitored on a multielectrode array dish, although the coupling between the circadian firing and Ca2+ rhythms persisted during culture. These findings indicate that the expressions of two key clock genes, Per1 and Bmal1, in the SCN are regulated in such a way that they may adopt different phases and free-running periods relative to each other and are respectively associated with the expression of activity onset and offset.

scholarly journals Divergent Roles of Clock Genes in Retinal and Suprachiasmatic Nucleus Circadian Oscillators

PLoS ONE ◽  
2012 ◽  
Vol 7 (6) ◽  
pp. e38985 ◽  
Author(s):  
Guo-Xiang Ruan ◽  
Karen L. Gamble ◽  
Michael L. Risner ◽  
Laurel A. Young ◽  
Douglas G. McMahon
Keyword(s):  
Suprachiasmatic Nucleus ◽  
Clock Genes ◽  
Circadian Oscillators

Photoperiod alters phase difference between activity onset in vivo and mPer2::luc peak in vitro

2008 ◽  
Vol 295 (5) ◽  
pp. R1688-R1694 ◽  
Author(s):  
Carl T. Mickman ◽  
Jeremy S. Stubblefield ◽  
Mary E. Harrington ◽  
Dwight E. Nelson
Keyword(s):  
Phase Relationship ◽  
Stable Phase ◽  
Light Cycle ◽  
Behavioral Rhythms ◽  
Activity Onset ◽  
Long Photoperiod ◽  
Initial Cycle ◽  
Phase Relationships

Photoperiod is a significant modulator of behavior and physiology for many organisms. In rodents changes in photoperiod are associated with changes in circadian period and photic resetting of circadian pacemakers. Utilizing rhythms of in vivo behavior and in vitro mPer2::luc expression, we investigated whether different entrainment photoperiods [light:dark (L:D) 16:8 and L:D 8:16] alter the period or phase relationships between these rhythms and the entraining light cycle in Per2::luc C57BL/6J mice. We also tested whether mPer2::luc rhythms differs in anterior and posterior suprachiasmatic nucleus (SCN) slices. Our results demonstrate that photoperiod significantly changes the timing of the mPer2::luc peak relative to the time of light offset and the activity onset in vivo. In both L:D 8:16 and L:D 16:8 the mPer2::luc peak maintained a more stable phase relationship to activity offset, while altering the phase relationship to activity onset. After the initial cycle in culture, the period, phase, and peaks per cycle were not significantly different for anterior vs. posterior SCN slices taken from animals within one photoperiod. After short-photoperiod treatment, anterior SCN slices showed increased-amplitude Per2::luc waveforms and posterior SCN slices showed shorter-duration peak width. Finally, the SCN tissue in vitro did not demonstrate differences in period attributable to photoperiod pretreatment, indicating that period aftereffects observed in behavioral rhythms after long- and short-day photoperiods are not sustained in Per2::luc rhythms in vitro. The change in phase relationship to activity onset suggests that Per2::luc rhythms in the SCN may track activity offset rather than activity onset. The reduced amplitude rhythms following long-photoperiod treatment may represent a loss of coupling of component oscillators.

scholarly journals Astrocytic Modulation of Neuronal Activity in the Suprachiasmatic Nucleus: Insights from Mathematical Modeling

2020 ◽  
Vol 35 (3) ◽  
pp. 287-301
Author(s):  
Natthapong Sueviriyapan ◽  
Chak Foon Tso ◽  
Erik D. Herzog ◽  
Michael A. Henson
Keyword(s):  
Circadian Rhythm ◽  
Suprachiasmatic Nucleus ◽  
Neuronal Activity ◽  
Clock Genes ◽  
Rhythmic Activity ◽  
Neuronal Population ◽  
Circadian Period ◽  
Circadian Oscillators ◽  
Bidirectional Interactions ◽  
The Impact

The suprachiasmatic nucleus (SCN) of the hypothalamus consists of a highly heterogeneous neuronal population networked together to allow precise and robust circadian timekeeping in mammals. While the critical importance of SCN neurons in regulating circadian rhythms has been extensively studied, the roles of SCN astrocytes in circadian system function are not well understood. Recent experiments have demonstrated that SCN astrocytes are circadian oscillators with the same functional clock genes as SCN neurons. Astrocytes generate rhythmic outputs that are thought to modulate neuronal activity through pre- and postsynaptic interactions. In this study, we developed an in silico multicellular model of the SCN clock to investigate the impact of astrocytes in modulating neuronal activity and affecting key clock properties such as circadian rhythmicity, period, and synchronization. The model predicted that astrocytes could alter the rhythmic activity of neurons via bidirectional interactions at tripartite synapses. Specifically, astrocyte-regulated extracellular glutamate was predicted to increase neuropeptide signaling from neurons. Consistent with experimental results, we found that astrocytes could increase the circadian period and enhance neural synchronization according to their endogenous circadian period. The impact of astrocytic modulation of circadian rhythm amplitude, period, and synchronization was predicted to be strongest when astrocytes had periods between 0 and 2 h longer than neurons. Increasing the number of neurons coupled to the astrocyte also increased its impact on period modulation and synchrony. These computational results suggest that signals that modulate astrocytic rhythms or signaling (e.g., as a function of season, age, or treatment) could cause disruptions in circadian rhythm or serve as putative therapeutic targets.

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