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

Abstract

Paramecium is 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 called Paramecium the "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 behaving Paramecium. 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 of Paramecium in ecological environments.

Interaction of the mechanosensitive microswimmerParameciumwith obstacles

“…Raw images were directly recorded to a hard drive and compressed by first removing the background then applying a threshold [11]. Automatic tracking was performed on compressed images using FastTrack [35].…”

“…First, given that most contacts do not trigger an avoiding reaction, we postulate that the current triggered upon contact is smaller than in typical mechanical stimulations of immobilized cells. To trigger an action potential, the charge Q transmitted at contact must exceed a threshold Q * ≈ CV * , where C ≈ 300 pF is the membrane capacitance [11] and V * ≈ 3 mV is the threshold potential to trigger an action potential relative to the initial potential, which quantifies cell excitability [25]. Thus, Q * ≈ 1 pC.…”

“…At the cellular level, it is known that a mechanical stimulation opens mechanosensitive channels located in the plasma membrane, which are specifically permeable to calcium [7–9]. The resulting inward calcium current depolarizes the membrane, which then opens voltagegated calcium channels in the cilia, triggering an action potential and the reversal of the cilia [10, 11]. Mechanotransduction has been previously studied using electrophysiology experiments [2, 3].…”