Emergence of behavior in a self-organized living matter network

Abstract

What is the origin of behavior? Although typically associated with a nervous system, simple life forms also show complex behavior - thus serving as a model to study how behaviors emerge. Among them, the slime mold Physarum polycephalum, growing as a single giant cell, is renowned for its sophisticated behavior. Here, we show how locomotion and morphological adaptation behavior emerge from self-organized patterns of rhythmic contractions of the actomyosin lining of the tubes making up the network-shaped organism. We quantify the spatio-temporal contraction dynamics by decomposing experimentally recorded contraction patterns into spatial contraction modes. Surprisingly, we find a continuous spectrum of modes, as opposed to few dominant modes. Over time, activation of modes along this continuous spectrum is highly dynamic, resulting in contraction patterns of varying regularity. We show that regular patterns are associated with stereotyped behavior by triggering a behavioral response with a food stimulus. Furthermore, we demonstrate that the continuous spectrum of modes and the existence of irregular contraction patterns persist in specimens with a morphology as simple as a single tube. Our data suggests that the continuous spectrum of modes allows for dynamic transitions between a plethora of specific behaviors with transitions marked by highly irregular contraction states. By mapping specific behaviors to states of active contractions, we provide the basis to understand behaviors complexity as a function of biomechanical dynamics. This perspective will likely stimulate bio-inspired design of soft robots with a similarly rich behavioral repertoire as P. polycephalum.