A computational model of tissue movements during early heart assembly

Development of a contractile layer of the heart, the myocardium, involves the movement of bilateral progenitor fields to the embryonic midline in amniotes. The driving forces for this antero‐medial movement have been researched and debated for almost a century. Here we propose a novel, three dimensional mechanical model of embryonic tissue dynamics. Mechanically coupled adherent cells are represented as particles interconnected with elastic beams which can exert non‐central forces and torques. Tissue plasticity is modeled by a stochastic process consisting of changes in intercellular connections, followed by a relaxation to mechanical equilibrium. We demonstrate that the proposed model yields a realistic macroscopic elasto‐plastic behavior and we establish how microscopic model parameters determine material properties at the macroscopic scale. In addition to their mechanical role, model particles can also act as simulation agents and actively modulate their connectivity according to specific rules. Stochastic simulations yield fluctuating tissue movements exhibiting the same autocorrelation properties as data obtained from observing live avian embryos. Based on microincision experiments, we propose a set of autonomous shape changes that is characteristic for the early myocardium. In particular, we demonstrate that the observed tissue movements: the merging of the lateral heart fields and the subsequent assembly of a tubular heart can be well explained by computational simulations in which the early myocardium exerts an intrinsic bending moment (a tendency to curl spontaneously) which is mechanically constrained by adjacent tissues. According to our analysis, these forces contribute to shaping both the heart fields and the foregut.