Decoding the essential interplay between central and peripheral control in adaptive locomotion of amphibious centipedes

Kotaro Yasui,Auke J. Ijspeert,Akio Ishiguro,Hitoshi Aonuma,Takeshi Kano,Emily M. Standen

doi:10.1038/s41598-019-53258-3

Abstract

Amphibious animals adapt their body coordination to compensate for changing substrate properties as they transition between terrestrial and aquatic environments. Using behavioural experiments and mathematical modelling of the amphibious centipede Scolopendra subspinipes mutilans, we reveal an interplay between descending command (brain), local pattern generation, and sensory feedback that controls the leg and body motion during swimming and walking. The elongated and segmented centipede body exhibits a gradual transition in the locomotor patterns as the animal crosses between land and water. Changing environmental conditions elicit a mechano-sensory feedback mechanism, inducing a gait change at the local segment level. The body segments operating downstream of a severed nerve cord (no descending control) can generate walking with mechano-sensory inputs alone while swimming behaviour is not recovered. Integrating the descending control for swimming initiation with the sensory feedback control for walking in a mathematical model successfully generates the adaptive behaviour of centipede locomotion, capturing the possible mechanism for flexible motor control in animals.

Highlights

Amphibious animals adapt their body coordination to compensate for changing substrate properties as they transition between terrestrial and aquatic environments
Amphibian salamanders swim in water by propagating axial bending waves with their limbs folded along the body trunk, whereas on land they show a quadrupedal gait with a standing wave of body undulation[1]. Such an adaptive behaviour is achieved by changing the coordination patterns of many degrees of freedom in the body depending on the substrates, and this strategy is widely observed in various amphibious animals, e.g. fish[2,3,4], turtles[5], and insects[6,7]
The homogeneous and segmented body structure of the centipede provides a great opportunity to investigate the role of local sensory feedback in switching motor coordination since the elongate, legged body segments of the centipede facilitate the visualization of kinematic changes in the body as the animal crosses between terrestrial and aquatic environments

Summary

Introduction

Amphibious animals adapt their body coordination to compensate for changing substrate properties as they transition between terrestrial and aquatic environments. Using behavioural experiments and mathematical modelling of the amphibious centipede Scolopendra subspinipes mutilans, we reveal an interplay between descending command (brain), local pattern generation, and sensory feedback that controls the leg and body motion during swimming and walking. *email: circuit was modelled and validated by physical robot experiments[13] These studies, though pivotal, did not address how amphibious animals sense environmental changes, and it is still unclear to what extent local sensory feedback mechanisms are responsible for switching between different locomotor patterns. These findings suggest that centipedes might possess decentralized control mechanisms for generating locomotion patterns

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