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Synchronization-induced rhythmicity of circadian oscillators in the suprachiasmatic nucleus.

Bernard S, Gonze D, Cajavec B, Herzel H, Kramer A - PLoS Comput. Biol. (2007)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece. samubernard@gmail.com

ABSTRACT
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.

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Effect of the Number of Oscillators as Well as the Connectivity on Synchronization(A) Synchronization properties of randomly coupled networks with respect to the number of neurons n (c0 = 0.10). Each dot represents the order parameter R for one realization of a random network and a simulation. Ten simulations were performed for each value of cell number n. The total length of the simulations was 312 h after starting with random initial conditions, and the order parameter was calculated over the last 240 h.(B) Three examples of average output for n = 12, 24, and 101.(C) Synchronization properties of randomly coupled networks with respect to the connectivity c0 (n = 12). Ten simulations were performed for each value of nominal connectivity c0. Other parameters as in (A).(D) Three examples of average Per/Cry mRNA concentration for c0 = 0.05, 0.10, and 0.15.
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pcbi-0030068-g005: Effect of the Number of Oscillators as Well as the Connectivity on Synchronization(A) Synchronization properties of randomly coupled networks with respect to the number of neurons n (c0 = 0.10). Each dot represents the order parameter R for one realization of a random network and a simulation. Ten simulations were performed for each value of cell number n. The total length of the simulations was 312 h after starting with random initial conditions, and the order parameter was calculated over the last 240 h.(B) Three examples of average output for n = 12, 24, and 101.(C) Synchronization properties of randomly coupled networks with respect to the connectivity c0 (n = 12). Ten simulations were performed for each value of nominal connectivity c0. Other parameters as in (A).(D) Three examples of average Per/Cry mRNA concentration for c0 = 0.05, 0.10, and 0.15.

Mentions: So far, we have looked at a large number of oscillators and found that robust synchronization is achieved when oscillators are appropriately coupled. To analyze the influence of the number of oscillators as well as the connectivity on synchronization dynamics, we used a uniform, random coupling (type 1), and we varied either the number of oscillators or the nominal connectivity (Figure 5) and measured the R values.


Synchronization-induced rhythmicity of circadian oscillators in the suprachiasmatic nucleus.

Bernard S, Gonze D, Cajavec B, Herzel H, Kramer A - PLoS Comput. Biol. (2007)

Effect of the Number of Oscillators as Well as the Connectivity on Synchronization(A) Synchronization properties of randomly coupled networks with respect to the number of neurons n (c0 = 0.10). Each dot represents the order parameter R for one realization of a random network and a simulation. Ten simulations were performed for each value of cell number n. The total length of the simulations was 312 h after starting with random initial conditions, and the order parameter was calculated over the last 240 h.(B) Three examples of average output for n = 12, 24, and 101.(C) Synchronization properties of randomly coupled networks with respect to the connectivity c0 (n = 12). Ten simulations were performed for each value of nominal connectivity c0. Other parameters as in (A).(D) Three examples of average Per/Cry mRNA concentration for c0 = 0.05, 0.10, and 0.15.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1851983&req=5

pcbi-0030068-g005: Effect of the Number of Oscillators as Well as the Connectivity on Synchronization(A) Synchronization properties of randomly coupled networks with respect to the number of neurons n (c0 = 0.10). Each dot represents the order parameter R for one realization of a random network and a simulation. Ten simulations were performed for each value of cell number n. The total length of the simulations was 312 h after starting with random initial conditions, and the order parameter was calculated over the last 240 h.(B) Three examples of average output for n = 12, 24, and 101.(C) Synchronization properties of randomly coupled networks with respect to the connectivity c0 (n = 12). Ten simulations were performed for each value of nominal connectivity c0. Other parameters as in (A).(D) Three examples of average Per/Cry mRNA concentration for c0 = 0.05, 0.10, and 0.15.
Mentions: So far, we have looked at a large number of oscillators and found that robust synchronization is achieved when oscillators are appropriately coupled. To analyze the influence of the number of oscillators as well as the connectivity on synchronization dynamics, we used a uniform, random coupling (type 1), and we varied either the number of oscillators or the nominal connectivity (Figure 5) and measured the R values.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Applied and Computational Mathematics, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece. samubernard@gmail.com

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus