A design principle underlying the synchronization of oscillations in cellular systems (original) (raw)
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Synchronization in coupled cells with activator-inhibitor pathways
Physical Review E, 2007
The functional dynamics exhibited by cell collectives are fascinating examples of robust, synchronized, collective behavior in spatially extended biological systems. To investigate the roles of local cellular dynamics and interaction strength in the spatiotemporal dynamics of cell collectives of different sizes, we study a model system consisting of a ring of coupled cells incorporating a three-step biochemical pathway of regulated activator-inhibitor reactions. The isolated individual cells display very complex dynamics as a result of the nonlinear interactions common in cellular processes. On coupling the cells to nearest neighbors, through diffusion of the pathway end product, the ring of cells yields a host of interesting and unusual dynamical features such as, suppression of chaos, phase synchronization, traveling waves, and intermittency, for varying interaction strengths and system sizes. But robust complete synchronization can be induced in these coupled cells with a small degree of random coupling among them even where regular coupling yielded only intermittent synchronization. Our studies indicate that robustness in synchronized functional dynamics in tissues and cell populations in nature can be ensured by a few transient random connections among the cells. Such connections are being discovered only recently in real cellular systems.
Stability of synchronization in a multi-cellular system
EPL (Europhysics Letters), 2010
Networks of biochemical reactions regulated by positive-and negative-feedback processes underlie functional dynamics in single cells. Synchronization of dynamics in the constituent cells is a hallmark of collective behavior in multi-cellular biological systems. Stability of the synchronized state is required for robust functioning of the multi-cell system in the face of noise and perturbation. Yet, the ability to respond to signals and change functional dynamics are also important features during development, disease, and evolution in living systems. In this paper, using a coupled multi-cell system model, we investigate the role of system size, coupling strength and its topology on the synchronization of the collective dynamics and its stability. Even though different coupling topologies lead to synchronization of collective dynamics, diffusive coupling through the end product of the pathway does not confer stability to the synchronized state. The results are discussed with a view to their prevalence in biological systems.
Output synchronization in networks of cyclic biochemical oscillators
American Control Conference, 2007
This paper is concerned with the global analysis of asymptotic synchronization of outputs in networks of identical oscillators. The oscillator models are assumed to possess a cyclic feedback structure. Such networks of oscillators abound in biochemistry, and are exemplified by circadian rhythm and cardiac cell networks. The main result exploits an incremental output feedback passivity property of cyclic feedback systems to prove global asymptotic output synchronization in a network composed of identical cyclic feedback systems. This result is illustrated on a network of Goodwin oscillators.
Collective Cell Movement Promotes Synchronization of Coupled Genetic Oscillators
Biophysical Journal, 2014
Collective cell movement is a crucial component of embryonic development. Intercellular interactions regulate collective cell movement by allowing cells to transfer information. A key question is how collective cell movement itself influences information flow produced in tissues by intercellular interactions. Here, we study the effect of collective cell movement on the synchronization of locally coupled genetic oscillators. This study is motivated by the segmentation clock in zebrafish somitogenesis, where short-range correlated movement of cells has been observed. We describe the segmentation clock tissue by a Voronoi diagram, cell movement by the force balance of self-propelled and repulsive forces between cells, the dynamics of the direction of self-propelled motion, and the synchronization of genetic oscillators by locally coupled phase oscillators. We find that movement with a correlation length of about 2~3 cell diameters is optimal for the synchronization of coupled oscillators. Quantification of cell mixing reveals that this short-range correlation of cell movement allows cells to exchange neighbors most efficiently. Moreover, short-range correlated movement strongly destabilizes nonuniform spatial phase patterns, further promoting global synchronization. Our theoretical results suggest that collective cell movement may enhance the synchronization of the segmentation clock in zebrafish somitogenesis. More generally, collective cell movement may promote information flow in tissues by enhancing cell mixing and destabilizing spurious patterns.
Spontaneous synchronization of coupled circadian oscillators
2005
In mammals, the circadian pacemaker, which controls daily rhythms, is located in the suprachiasmatic nucleus (SCN). Circadian oscillations are generated in individual SCN neurons by a molecular regulatory network. Cells oscillate with periods ranging from 20 to 28 h, but at the tissue level, SCN neurons display significant synchrony, suggesting a robust intercellular coupling in which neurotransmitters are assumed to play a crucial role. We present a dynamical model for the coupling of a population of circadian oscillators in the SCN. The cellular oscillator, a three-variable model, describes the core negative feedback loop of the circadian clock. The coupling mechanism is incorporated through the global level of neurotransmitter concentration. Global coupling is efficient to synchronize a population of 10,000 cells. Synchronized cells can be entrained by a 24-h light-dark cycle. Simulations of the interaction between two populations representing two regions of the SCN show that the driven population can be phase-leading. Experimentally testable predictions are: 1), phases of individual cells are governed by their intrinsic periods; and 2), efficient synchronization is achieved when the average neurotransmitter concentration would dampen individual oscillators. However, due to the global neurotransmitter oscillation, cells are effectively synchronized.
Self-sustained collective oscillation generated in an array of nonoscillatory cells
Physical Review E, 2009
Oscillations are ubiquitous phenomena in biological systems. Conventional models of biological periodic oscillations usually invoke interconnecting transcriptional feedback loops. Some specific proteins function as transcription factors, which in turn negatively regulate the expression of the genes that encode these "clock proteins". These loops may lead to rhythmic changes in gene expression in a cell. In the case of multi-cellular tissue, collective oscillation is often due to synchronization of these cells, which manifest themselves as autonomous oscillators. In contrast, we propose here a different scenario for the occurrence of collective oscillation in a group of non-oscillatory cells. Neither periodic external stimulation nor pacemaker cells with intrinsically oscillator are included in present system. By adopting a spatially inhomogeneous active factor, we observe and analyze a coupling-induced oscillation, inherent to the phenomenon of wave propagation due to intracellular communication.
The generation of oscillations in networks of electrically coupled cells
Proceedings of the National Academy of Sciences, 2001
In several biological systems, the electrical coupling of nonoscillating cells generates synchronized membrane potential oscillations. Because the isolated cell is nonoscillating and electrical coupling tends to equalize the membrane potentials of the coupled cells, the mechanism underlying these oscillations is unclear. Here we present a dynamic mechanism by which the electrical coupling of identical nonoscillating cells can generate synchronous membrane potential oscillations. We demonstrate this mechanism by constructing a biologically feasible model of electrically coupled cells, characterized by an excitable membrane and calcium dynamics. We show that strong electrical coupling in this network generates multiple oscillatory states with different spatio-temporal patterns and discuss their possible role in the cooperative computations performed by the system.
Physical Biology, 2012
Cell movement and intercellular signaling occur simultaneously during the development of tissues, but little is known about how movement affects signaling. Previous theoretical studies have shown that faster moving cells favor synchronization across a population of locally coupled genetic oscillators. An important assumption in these studies is that cells can immediately interact with their new neighbors after arriving at a new location. However, intercellular interactions in cellular systems may need some time to become fully established. How movement affects synchronization in this situation has not been examined. Here we develop a coupled phase oscillator model in which we consider cell movement and the gradual recovery of intercellular coupling experienced by a cell after movement, characterized by a moving rate and a coupling recovery rate respectively. We find (1) an optimal moving rate for synchronization, and (2) a critical moving rate above which achieving synchronization is not possible. These results indicate that the extent to which movement enhances synchrony is limited by a gradual recovery of coupling. These findings suggest that the ratio of time scales of movement and signaling recovery is critical for information transfer between moving cells.
Synchronization in multicell systems exhibiting dynamic plasticity
Pramana, 2008
Collective behaviour in multicell systems arises from exchange of chemicals/signals between cells and may be different from their intrinsic behaviour. These chemicals are products of regulated networks of biochemical pathways that underlie cellular functions, and can exhibit a variety of dynamics arising from the non-linearity of the reaction processes. We have addressed the emergent synchronization properties of a ring of cells, diffusively coupled by the end product of an intracellular model biochemical pathway exhibiting non-robust birhythmic behaviour. The aim is to examine the role of intercellular interaction in stabilizing the non-robust dynamics in the emergent collective behaviour in the ring of cells. We show that, irrespective of the inherent frequencies of individual cells, depending on the coupling strength, the collective behaviour does synchronize to only one type of oscillations above a threshold number of cells. Using two perturbation analyses, we also show that this emergent synchronized dynamical state is fairly robust under external perturbations. Thus, the inherent plasticity in the oscillatory phenotypes in these model cells may get suppressed to exhibit collective dynamics of a single type in a multicell system, but environmental influences can sometimes expose this underlying plasticity in its collective dynamics.