Integrative Neuroscience of<i>Paramecium</i>, a “Swimming Neuron”

Brette, Romain

doi:10.1523/eneuro.0018-21.2021

Cited by 40 publications

(35 citation statements)

References 253 publications

(367 reference statements)

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“…We have addressed only the avoiding reaction of Paramecium . The modeling effort could be completed by addressing other behavioral aspects, such as the escape reaction (increased ciliary beating speed upon hyperpolarization), which involves distinct hyperpolarization-activated channels (Brette, 2021). Paramecium is sensitive to many sensory modalities, including temperature, various chemical substances, mechanical stimulation, light.…”

Section: Discussionmentioning

confidence: 99%

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

Elices

Kulkarni

Escoubet

et al. 2022

Preprint

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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.

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Section: Discussionmentioning

confidence: 99%

“…Paramecium electrophysiology is reviewed in (Eckert and Brehm, 1979) and updated in (Brette, 2021; Valentine and Van Houten, 2022). Paramecium in an isopotential cell (Eckert and Naitoh, 1970; Satow and Kung, 1979).…”

Section: Methodsmentioning

confidence: 99%

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

Elices

Kulkarni

Escoubet

et al. 2022

Preprint

Self Cite

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“…By studying an organism without a neuromuscular system, we build our intuition slowly toward more general principles mapping the collective behavior of complicated construction onto an organism-scale emergent simplicity. In doing so, we complement existing and ongoing work on more traditional model organisms § 1 Introduction and hope to lend support to a tantalizing link between emergent animal behavior [7], a growing field in cellular cognition [22][23][24] and the physics of active matter [25][26][27][28][29].…”

Section: Partmentioning

confidence: 95%

Mobile defects born from an energy cascade shape the locomotive behavior of a headless animal

Bull,

Prakash

2021

Preprint

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The physics of behavior seeks simple descriptions of animal behavior. The field has advanced rapidly by using techniques in low dimensional dynamics distilled from computer vision. Yet, we still do not generally understand the rules which shape these emergent behavioral manifolds in the face of complicated neuro-construction -even in the simplest of animals. In this work, we introduce a non-neuromuscular model system which is complex enough to teach us something new but also simple enough for us to understand. In this simple animal, the manifolds underlying the governing dynamics are shaped and stabilized by a physical mechanism: an active-elastic, inverse-energy cascade. Building upon pioneering work in the field, we explore the formulation of the governing dynamics of a polarized active elastic sheet in terms of the normal modes of an elastic structure decorated by a polarized activity at every node. By incorporating a torque mediated coupling physics, we show that the power is pumped from the shortest length scale up to longer length scale modes via a combination of direct mode coupling and preferential dissipation of higher frequency modes. We use this result to motivate the study of organismal locomotion as an emergent simplicity governing organism-scale behavior. To master the low dimensional dynamics on this manifold, we present a zero-transients limit study of the dynamics of +1 or vortex-like defects in the ciliary field (which is experimentally supported for small organisms). We show, experimentally, numerically and analytically that these defects arise from this energy cascade to generate long-lived, stable modes of locomotive behavior. Using a geometric model, we show how the defect undergoes unbinding. We extend this framework as a tool for studying larger organisms with non-circular shape and introduce local activity modulation for defect steering. We expect this work to inform the foundations of organismal control of distributed actuation without muscles or neurons.

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“…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.…”

Section: Behavior As a Loop Rather Than An Arc And How Neural Tissue ...mentioning

confidence: 99%

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

Sosa

Alcalá

2022

J Exper Analysis Behavior

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Behavior can be regarded as the output of a system (action), as a function linking stimulus to response (reaction), or as an abstraction of the bidirectional relationship between the environment and the organism (interaction). When considering the latter possibility, a relevant question arises concerning how an organism can materially and continuously implement such a relationship during its lifetime in order to perpetuate itself. The feedback control approach has taken up the task of answering just that question. During the last several decades, said approach has been progressing and has started to be recognized as a paradigm shift, superseding certain canonical notions in mainstream behavior analysis, cognitive psychology, and even neuroscience. In this paper, we describe the main features of feedback control theory and its associated techniques, concentrating on its critiques of behavior analysis, as well as the commonalities they share. While some of feedback control theory's major critiques of behavior analysis arise from the fact that they focus on different levels of organization, we believe that some are legitimate and meaningful. Moreover, feedback control theory seems to blend with neurobiology more smoothly as compared to canonical behavior analysis, which only subsists in a scattered handful of fields. If this paradigm shift truly takes place, behavior analysts—whether they accept or reject this new currency—should be mindful of the basics of the feedback control approach.

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Integrative Neuroscience ofParamecium, a “Swimming Neuron”

Cited by 40 publications

References 253 publications

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

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

Mobile defects born from an energy cascade shape the locomotive behavior of a headless animal

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

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