Living systems exhibit complex yet organized behavior on multiple spatiotemporal scales. To investigate the nature of multiscale coordination in living systems, one needs a meaningful and systematic way to quantify the complex dynamics, a challenge in both theoretical and empirical realms. The present work shows how integrating approaches from computational algebraic topology and dynamical systems may help us meet this challenge. In particular, we focus on the application of multiscale topological analysis to coordinated rhythmic processes. First, theoretical arguments are introduced as to why certain topological features and their scale-dependency are highly relevant to understanding complex collective dynamics. Second, we propose a method to capture such dynamically relevant topological information using persistent homology, which allows us to effectively construct a multiscale topological portrait of rhythmic coordination. Finally, the method is put to test in detecting transitions in real data from an experiment of rhythmic coordination in ensembles of interacting humans. The recurrence plots of topological portraits highlight collective transitions in coordination patterns that were elusive to more traditional methods. This sensitivity to collective transitions would be lost if the behavioral dynamics of individuals were treated as separate degrees of freedom instead of constituents of the topology that they collectively forge. Such multiscale topological portraits highlight collective aspects of coordination patterns that are irreducible to properties of individual parts. The present work demonstrates how the analysis of multiscale coordination dynamics can benefit from topological methods, thereby paving the way for further systematic quantification of complex, high-dimensional dynamics in living systems.
Topological portraits of multiscale coordination dynamics
Mengsen Zhang, William D. Kalies, J. A. Scott Kelso, Emmanuelle Tognoli
Coordination in living systems—from cells to people—must be understood at multiple levels of description. Analyses and modelling of empirically observed patterns of biological coordination often focus either on ensemble-level statistics in large-scale systems with many components, or on detailed dynamics in small-scale systems with few components. The two approaches have proceeded largely independent of each other. To bridge this gap between levels and scales, we have recently conducted a human experiment of mid-scale social coordination specifically designed to reveal coordination at multiple levels (ensemble, subgroups and dyads) simultaneously. Based on this experiment, the present work shows that, surprisingly, a single system of equations captures key observations at all relevant levels. It also connects empirically validated models of large- and small-scale biological coordination—the Kuramoto and extended Haken–Kelso–Bunz (HKB) models—and the hallmark phenomena that each is known to capture. For example, it exhibits both multistability and metastability observed in small-scale empirical research (via the second-order coupling and symmetry breaking in extended HKB) and the growth of biological complexity as a function of scale (via the scalability of the Kuramoto model). Only by incorporating both of these features simultaneously can we reproduce the essential coordination behaviour observed in our experiment.
Connecting empirical phenomena and theoretical models of biological coordination across scales
Mengsen Zhang , Christopher Beetle , J. A. Scott Kelso and Emmanuelle Tognoli
Systems Biology is a young and rapidly evolving research field, which combines experimental techniques and mathematical modeling in order to achieve a mechanistic understanding of processes underlying the regulation and evolution of living systems. Systems Biology is often associated with an Engineering approach: The purpose is to formulate a data-rich, detailed simulation model that allows to perform numerical (‘in silico’) experiments and then draw conclusions about the biological system. While methods from Engineering may be an appropriate approach to extending the scope of biological investigations to experimentally inaccessible realms and to supporting data-rich experimental work, it may not be the best strategy in a search for design principles of biological systems and the fundamental laws underlying Biology. Physics has a long tradition of characterizing and understanding emergent collective behaviors in systems of interacting units and searching for universal laws. Therefore, it is natural that many concepts used in Systems Biology have their roots in Physics. With an emphasis on Theoretical Physics, we will here review the ‘Physics core’ of Systems Biology, show how some success stories in Systems Biology can be traced back to concepts developed in Physics, and discuss how Systems Biology can further benefit from its Theoretical Physics foundation.