Mechanosensation Mediates Long-Range Spatial Decision-Making in an Aneural Organism

Abstract

Running title:Mechanical force sensing underlies Physarum aneural cognition AbstractThe unicellular protist Physarum polycephalum is an important emerging model for understanding how aneural organisms process information toward adaptive behavior. Here, we reveal that Physarum can use mechanosensation to reliably make decisions about distant objects its environment, preferentially growing in the direction of heavier, substrate-deforming but chemically-inert masses. This long-range mass-sensing is abolished by gentle rhythmic mechanical disruption, changing substrate stiffness, or addition of a mechanosensitive transient receptor potential channel inhibitor. Computational modeling revealed that Physarum may perform this calculation by sensing the fraction of its growth perimeter that is distorted above a threshold straina fundamentally novel method of mechanosensation. Together, these data identify a surprising behavioral preference relying on biomechanical features and not nutritional content, and characterize a new example of an aneural organism that exploits physics to make decisions about growth and form. Highlights The aneural Physarum makes behavioral decisions by control of its morphology  It has a preference for larger masses, which it can detect at long range  This effect is mediated by mechanosensing, not requiring chemical attractants  Machine learning reveals that it surveys environment and makes decision in < 4 hours  A biophysical model reveals how its pulsations enable long-distance mapping of environmental features A defining feature of any living organism is its ability to select actions that maximize utility in diverse environments (Barandiaran and Moreno, 2006). Decision-making is a process that is well-characterized in behavioral studies of human and other vertebrate species possessing nervous systems. Increasingly, it is also recognized as a fundamental capability whose evolutionary roots extend to the most basal forms on the tree of life (Baluška and Levin, 2016;Lyon, 2006Lyon, , 2015. Even unicellular organisms, including bacteria, have been studied as computational systems that collect information from their environment and use it to guide subsequent behaviors (Balazsi et al.

Adaptive behaviour and learning in slime moulds: the role of oscillations

“…For instance, higher frequencies are observed in response to attractive, high-quality resources [41], whereas lower frequencies are recorded when P. polycephalum encounters repulsive stimuli such as chemical repellents [40]. As a result, slime moulds migrate towards or away from a variety of external stimuli such as chemicals [38], light [42], temperature [43], humidity [44], gravity [45] or substrate distortion [46].…”

“…Physarum polycephalum demonstrates key aspects of complex decision-making [24–27,47,48] (figure 1). It can find its way in a maze [49], construct efficient transport networks [50], distinguish how different masses distort the substrate [46], avoid obstacles [51] and risky environments [52], optimize its nutrient intake [53,54], and use conspecifics' cues to choose what substrate to exploit [55,56]. All these feats rely on the abilities of P. polycephalum to sense and respond simultaneously to a wide range of biotic and abiotic stimuli [38–45].…”

The nervous system as a solution for implementing closed negative feedback control loops

“…As stated above, coupling sensory and motor functions allows for reciprocal influence between inputs and outputs; behavior thus becomes an emergent property of agents capable of it. It is worth noting that this emergent capacity of behaving (sometimes referred to as cognizing ; see Corcoran et al, 2020) is not restricted to organisms with nervous systems (e.g., Brette, 2021; Murugan et al, 2021). However, nervous systems seem to be a solution for efficiently accomplishing said function.…”

Studying Protista WBR and Repair Using Physarum polycephalum

“…That intracellular communication method, known as shuttle streaming, acts as an intrinsic cellular oscillator that drives synchronization across the cell and allows for collective behavior of the organism (Table 1) [1]. The coordination of activities over short and long distances gives rise to more complex mechanosensing, problem solving, and decision-making capabilities that optimize the slime mould's ability to find food and avoid danger [2][3][4][5][6]. The coordinated oscillations also seem necessary for regeneration and repair capacities [7], however, the prior use of Physarum to study regeneration is limited.…”