The clock in the dorsal suprachiasmatic nucleus runs faster than that in the ventral

Noguchi, Takaaki; Watanabe, Kazuto; Ogura, Akihiko; Yamaoka, Sadao

doi:10.1111/j.1460-9568.2004.03784.x

Cited by 61 publications

(58 citation statements)

References 20 publications

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“…Instead, the appearance of the circadian peak at different times of the day may result from differences in the intrinsic circadian period among subregions under mutually synchronized condition. The circadian period was reported to be shorter in the dorsal region than that in the ventral one (24)(25)(26). These results are well consistent with the present findings.…”

Section: Resultssupporting

confidence: 93%

Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus

Enoki

Kuroda

Ono³

et al. 2012

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

102

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The circadian pacemaker in the hypothalamic suprachiasmatic nucleus (SCN) is a hierarchical multioscillator system in which neuronal networks play crucial roles in expressing coherent rhythms in physiology and behavior. However, our understanding of the neuronal network is still incomplete. Intracellular calcium mediates the input signals, such as phase-resetting stimuli, to the core molecular loop involving clock genes for circadian rhythm generation and the output signals from the loop to various cellular functions, including changes in neurotransmitter release. Using a unique large-scale calcium imaging method with genetically encoded calcium sensors, we visualized intracellular calcium from the entire surface of SCN slice in culture including the regions where autonomous clock gene expression was undetectable. We found circadian calcium rhythms at a single-cell level in the SCN, which were topologically specific with a larger amplitude and more delayed phase in the ventral region than the dorsal. The robustness of the rhythm was reduced but persisted even after blocking the neuronal firing with tetrodotoxin (TTX). Notably, TTX dissociated the circadian calcium rhythms between the dorsal and ventral SCN. In contrast, a blocker of gap junctions, carbenoxolone, had only a minor effect on the calcium rhythms at both the single-cell and network levels. These results reveal the topological specificity of the circadian calcium rhythm in the SCN and the presence of coupled regional pacemakers in the dorsal and ventral regions. Neuronal firings are not necessary for the persistence of the calcium rhythms but indispensable for the hierarchical organization of rhythmicity in the SCN. yellow cameleon 3.60 | Nipkow-spinning disk confocal | adeno-associated virus | time-lapse imaging | acrophase map

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Section: Resultssupporting

confidence: 93%

Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus

Enoki

Kuroda

Ono³

et al. 2012

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

102

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“…A similar pattern and time course is observed with Period gene expression quantified with in situ hybridization (Hamada et al, 2004) or with a luminescent reporter (Yamaguchi et al, 2003). Evidence from an in vitro organotypic SCN slice culture where the coronal SCN slice is bisected horizontally suggests that oscillator cells in the dorsal SCN oscillate with shorter periods than those in the ventral SCN (Noguchi et al, 2004). These findings suggest that the dorsal cells may initiate the rhythmic response among the oscillators, and it is possible that gate cells may directly contact these cells.…”

Section: Target Of the Signalmentioning

confidence: 56%

Gates and Oscillators II: Zeitgebers and the Network Model of the Brain Clock

Antle

Foley

et al. 2007

J Biol Rhythms

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Circadian rhythms in physiology and behavior are regulated by the SCN. When assessed by expression of clock genes, at least 2 distinct functional cell types are discernible within the SCN: nonrhythmic, light-inducible, retinorecipient cells and rhythmic autonomous oscillator cells that are not directly retinorecipient. To predict the responses of the circadian system, the authors have proposed a model based on these biological properties. In this model, output of rhythmic oscillator cells regulates the activity of the gate cells. The gate cells provide a daily organizing signal that maintains phase coherence among the oscillator cells. In the absence of external stimuli, this arrangement yields a multicomponent system capable of producing a self-sustained consensus rhythm. This follow-up study considers how the system responds when the gate cells are activated by an external stimulus, simulating a response to an entraining (or phase-setting) signal. In this model, the authors find that the system can be entrained to periods within the circadian range, that the free-running system can be phase shifted by timed activation of the gate, and that the phase response curve for activation is similar to that observed when animals are exposed to a light pulse. Finally, exogenous triggering of the gate over a number of days can organize an arrhythmic system, simulating the light-dependent reappearance of rhythmicity in a population of disorganized, independent oscillators. The model demonstrates that a single mechanism (i.e., the output of gate cells) can account for not only free-running and entrained rhythmicity but also other circadian phenomena, including limits of entrainment, a PRC with both delay and advance zones, and the light-dependent reappearance of rhythmicity in an arrhythmic animal. Keywords zeitgeber; zeitnehmer; coupling; oscillator; synchronization The circadian system has evolved to adapt organisms to temporally recurrent events in their environment. While it is known that circadian rhythms can be generated within individual cells by autoregulatory transcription-translation feedback loops (Reppert and Weaver, 2001),

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“…Because AVP and VIP release can have different circadian periods in the same organotypic SCN slice, it was hypothesized that these 2 groups of neurons are separate oscillators (12). Subsequent in vivo (13) and in vitro (8,14) results continue to support the idea that neurons from the dorsal and ventral SCN maintain daily rhythms. We sought to identify intrinsically circadian neurons within the SCN as AVPor VIP-ergic.…”

mentioning

confidence: 50%

Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons

Webb

Angelo

Huettner

et al. 2009

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

205

216

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Circadian rhythms are modeled as reliable and self-sustained oscillations generated by single cells. The mammalian suprachiasmatic nucleus (SCN) keeps near 24-h time in vivo and in vitro, but the identity of the individual cellular pacemakers is unknown. We tested the hypothesis that circadian cycling is intrinsic to a unique class of SCN neurons by measuring firing rate or Period2 gene expression in single neurons. We found that fully isolated SCN neurons can sustain circadian cycling for at least 1 week. Plating SCN neurons at <100 cells/mm 2 eliminated synaptic inputs and revealed circadian neurons that contained arginine vasopressin (AVP) or vasoactive intestinal polypeptide (VIP) or neither. Surprisingly, arrhythmic neurons (nearly 80% of recorded neurons) also expressed these neuropeptides. Furthermore, neurons were observed to lose or gain circadian rhythmicity in these dispersed cell cultures, both spontaneously and in response to forskolin stimulation. In SCN explants treated with tetrodotoxin to block spike-dependent signaling, neurons gained or lost circadian cycling over many days. The rate of PERIOD2 protein accumulation on the previous cycle reliably predicted the spontaneous onset of arrhythmicity. We conclude that individual SCN neurons can generate circadian oscillations; however, there is no evidence for a specialized or anatomically localized class of cell-autonomous pacemakers. Instead, these results indicate that AVP, VIP, and other SCN neurons are intrinsic but unstable circadian oscillators that rely on network interactions to stabilize their otherwise noisy cycling.luciferase ͉ pacemaker ͉ Period gene ͉ suprachiasmatic nucleus ͉ vasoactive intestinal polypeptide C ircadian pacemakers are schematized as intracellular transcription-translation negative feedback loops (1). In mammals, transcription factors including CLOCK and BMAL1 promote the expression of clock genes, including Period 1 (Per1) and 2 (Per2). The protein products of these genes return to the nucleus after a delay of many hours to repress their own transcription. Genetic deletion of these repressors abolishes circadian rhythms in behavior and physiology (2). The strongest evidence for cell-autonomous, circadian rhythm generation in mammals comes from transcriptional rhythms measured from primary and immortalized fibroblasts (3, 4).The mammalian suprachiasmatic nucleus (SCN) of the anterior hypothalamus coordinates daily rhythms including sleep-wake and hormone release (5). Multielectrode array (MEA) recordings of neuronal firing and luciferase-based reporters of Per1 and Per2 expression showed dissociated SCN neurons in the same culture with different circadian periods (6, 7). Furthermore, Na ϩ -dependent action potentials, vasoactive intestinal polypeptide (VIP), and its receptor, VPAC2, are required for cellular synchrony and maintaining daily oscillations across the SCN (8, 9). Taken together, these results suggest that single SCN neurons are competent circadian oscillators. However, which, if any, SCN neurons are capable ...

show abstract

The clock in the dorsal suprachiasmatic nucleus runs faster than that in the ventral

Cited by 61 publications

References 20 publications

Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus

Topological specificity and hierarchical network of the circadian calcium rhythm in the suprachiasmatic nucleus

Gates and Oscillators II: Zeitgebers and the Network Model of the Brain Clock

Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons

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