An electrophysiological and kinematic model ofParamecium, the “swimming neuron”

Author:

Elices IreneORCID,Kulkarni AnirudhORCID,Escoubet Nicolas,Pontani Léa-LaetitiaORCID,Prevost Alexis MichelORCID,Brette RomainORCID

Abstract

AbstractParameciumis a large unicellular organism that swims in fresh water using cilia. When stimulated by various means (mechanically, chemically, optically, thermally), it often swims backward then turns and swims forward again in a new direction: this is called the avoiding reaction. This reaction is triggered by a calcium-based action potential. For this reason, several authors have calledParameciumthe “swimming neuron”. Here we present an empirically constrained model of its action potential based on electrophysiology experiments on live immobilized paramecia, together with simultaneous measurement of ciliary beating using particle image velocimetry. Using these measurements and additional behavioral measurements of free swimming, we extend the electrophysiological model by coupling calcium concentration to kinematic parameters, turning it into a swimming model. In this way, we obtain a model of autonomously behavingParamecium. Finally, we demonstrate how the modeled organism interacts with an environment, can follow gradients and display collective behavior. This work provides a modeling basis for investigating the physiological basis of autonomous behavior ofParameciumin ecological environments.Author SummaryBehavior depends on a complex interaction between a variety of physiological processes, the body and the environment. We propose to examine this complex interaction in an organism consisting of a single excitable and motile cell,Paramecium. The behavior ofParameciumis based on trial and error: when it encounters an undesirable situation, it backs up and changes direction. This avoiding reaction is triggered by an action potential. Here we developed an empirically constrained biophysical model ofParamecium’s action potential, which we then coupled to its kinematics. We then demonstrate the potential of this model in investigating various types of autonomous behavior, such as obstacle avoidance, gradient-following and collective behavior.

Publisher

Cold Spring Harbor Laboratory

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