Walking with Salamanders: From Molecules to Biorobotics

Abstract

How do four-legged animals adapt their locomotion to the environment? How do central and peripheral mechanisms interact within the spinal cord to produce adaptive locomotion and how is locomotion recovered when spinal circuits are perturbed? Salamanders are the only tetrapods that regenerate voluntary locomotion after full spinal transection. Given their evolutionary position, they provide a unique opportunity to bridge discoveries made in fish and mammalian models. Genetic dissection of salamander neural circuits is becoming feasible with new methods for precise manipulation, elimination, and visualisation of cells. These approaches can be combined with classical tools in neuroscience and with modelling and a robotic environment. We propose that salamanders provide a blueprint of the function, evolution, and regeneration of tetrapod locomotor circuits. Salamanders as a Model Organism for Studying Locomotion Two major challenges in neuroscience are to decipher how the interplay between central and peripheral mechanisms controls locomotion in four-legged animals (tetrapods) and to delineate the reorganisation of motor circuits after spinal lesion. In this review, we outline the reasons why salamanders are ideally suited to address these two problems. First, salamanders are the only tetrapods capable of regenerating their locomotor circuits after full transection at adult stage [1-3]. Second, they are the closest extant representatives of the first tetrapods that transitioned from aquatic to terrestrial life [4]. This key evolutionary position makes salamanders ideal to provide a bridge between discoveries in fish (such as zebrafish) and mammals (such as mouse). Salamanders swim underwater and walk on ground [4], allowing researchers to investigate to what extent body dynamics and sensory feedback shape these locomotor patterns. Third, high precision dissection of their neural circuits is becoming possible thanks to new tools that will allow visualisation and optogenetic and chemogenetic manipulations that can be combined with classical neuroscience tools and advanced modelling and robotic environments. It is thus timely to highlight the recent advances in salamander research at the intersection of genomics, systems neuroscience, modelling, and robotics, which altogether provide a unique opportunity to decode locomotor control in the intact and regenerated tetrapod nervous system. In this review, we systematically place these approaches and recent results into a cross-species comparative setting, with a special focus on zebrafish and mouse as comparative models for which most data on the genetic identity of locomotor circuits are available. For closer examination of the locomotor circuitries of other related animal models such as lamprey, cat, and Xenopus embryo, we refer readers to prior reviews (lamprey: [5], cat: [6], Xenopus embryo: [7]). The Salamander Nervous System: A Bridge between Fish and Mammalian Models Salamander locomotor circuits include the main features found in all vertebrates (Figure 1A,C). Their...

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“…Robots are thus useful to validate simulation results in the real world, with real physics. Here, we used numerical simulations and robotics to investigate the generation of different behaviors in the salamander, an interesting animal model as it can move underwater and on ground (Ryczko et al, 2020). In particular, we addressed the following questions:…”