Chaotic internal dynamics coexist with a stable temporal scaffold in a mesoscale sarcomere model informed by high-resolution recordings

Cardiomyocytes maintain a coherent mechanical rhythm despite fluctuations in myosin motors and local contractile units. To examine the intervening mesoscale, we used a reversible state in neonatal rat cardiomyocytes: local warming evokes slow Ca2+-associated sarcomere-length changes together with faster oscillations near the neonatal beat rate, termed hyperthermal sarcomeric oscillations (HSOs). High-speed sarcomere-length nanometry followed five consecutive sarcomeres simultaneously in seven cells. Local amplitudes varied much more than fast-cycle periods, and adjacent sarcomeres displayed both co-directed and opposed motion. These observations motivated a compact chain model with interacting local amplitude-phase states and a common fast phase. The prescribed common phase allowed the model to focus on internal organization under stable timing. A parameter set selected in an exploratory screen was used throughout the subsequent dynamical analyses. Complete ten-dimensional Lyapunov spectra from 360 runs identified a reproducible positive-largest-exponent regime at intermediate coupling. In the same regime, an identical perturbation accessed more independent response directions across initial states, and a simple linear rule transferred less well between trajectories. Small harmonic terms in the observation map improved HSO-like waveform asymmetry in held-out cells while leaving the internal dynamics unchanged. The model also reproduced the experimentally observed predominance of one-link phase updates (95.4% versus 93.9%), although its length redistribution remained more local. Thus, stable beat-like timing can coexist with sensitive, nonrepeating redistribution among coupled local contractile elements, providing a concrete mesoscale representation of robust temporal order with flexible internal organization.