Synchronization-induced rhythmicity of circadian oscillators in the suprachiasmatic nucleus.
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The authors simulated different experimental conditions and found that: (1) in normal, constant conditions, coupled circadian oscillators quickly synchronize and produce a coherent output; (2) in large populations, such oscillators either synchronize or gradually lose rhythmicity, but do not run out of phase, demonstrating that rhythmicity and synchrony are codependent; (3) the number of oscillators and connectivity are important for these synchronization properties; (4) slow oscillators have a higher impact on the period in mixed populations; and (5) coupled circadian oscillators can be efficiently entrained by light-dark cycles.Based on these results, it is predicted that: (1) a majority of SCN neurons needs periodic synchronization signal to be rhythmic; (2) a small number of neurons or a low connectivity results in desynchrony; and (3) amplitudes and phases of neurons are negatively correlated.The authors conclude that to understand the orchestration of timekeeping in the SCN, intracellular circadian clocks cannot be isolated from their intercellular communication components.
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Affiliation: Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece. samubernard@gmail.com
ABSTRACT
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The suprachiasmatic nuclei (SCN) host a robust, self-sustained circadian pacemaker that coordinates physiological rhythms with the daily changes in the environment. Neuronal clocks within the SCN form a heterogeneous network that must synchronize to maintain timekeeping activity. Coherent circadian output of the SCN tissue is established by intercellular signaling factors, such as vasointestinal polypeptide. It was recently shown that besides coordinating cells, the synchronization factors play a crucial role in the sustenance of intrinsic cellular rhythmicity. Disruption of intercellular signaling abolishes sustained rhythmicity in a majority of neurons and desynchronizes the remaining rhythmic neurons. Based on these observations, the authors propose a model for the synchronization of circadian oscillators that combines intracellular and intercellular dynamics at the single-cell level. The model is a heterogeneous network of circadian neuronal oscillators where individual oscillators are damped rather than self-sustained. The authors simulated different experimental conditions and found that: (1) in normal, constant conditions, coupled circadian oscillators quickly synchronize and produce a coherent output; (2) in large populations, such oscillators either synchronize or gradually lose rhythmicity, but do not run out of phase, demonstrating that rhythmicity and synchrony are codependent; (3) the number of oscillators and connectivity are important for these synchronization properties; (4) slow oscillators have a higher impact on the period in mixed populations; and (5) coupled circadian oscillators can be efficiently entrained by light-dark cycles. Based on these results, it is predicted that: (1) a majority of SCN neurons needs periodic synchronization signal to be rhythmic; (2) a small number of neurons or a low connectivity results in desynchrony; and (3) amplitudes and phases of neurons are negatively correlated. The authors conclude that to understand the orchestration of timekeeping in the SCN, intracellular circadian clocks cannot be isolated from their intercellular communication components. Related in: MedlinePlus |
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Mentions: With this experimental observation in mind, we tested whether our model might be able to explain this nonintuitive result. We randomly mixed and connected a 24 h–period population with a 20 h–period population (total, n = 100; standard deviations of the periods, 0.1 h) in various ratios. The resulting period of the synchronized population was compared with the period that would have been expected from averaging the individual oscillator periods. For ratios between 0.2 and 0.8 (i.e., 20% and 80% wild-type cells), the resulting population period was systematically longer than expected (five runs per ratio, R > 0.8; Figure 6A and 6B). Thus, in mixed population, slow oscillators seem to have a higher impact on the period than the faster ones. |
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Affiliation: Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece. samubernard@gmail.com