Decoding the Interplay Between Central and Peripheral Control for Versatile Locomotor Repertoire in Centipedes

Animals can generate versatile locomotor behaviors in response to the situation. For instance, they change gaits to increase locomotor speed and use different locomotor patterns like walking and swimming to traverse different environmental media. Such behavioral flexibility is realized through the coordinated motor outputs of the body parts. Extracting control principles underlying locomotor circuits contributes not only to neurobiological understanding but also to bio-inspired robotics aiming to establish the design methodology of locomotor intelligence. Neurobiological studies have shown that locomotor movements are controlled by higher centers (brain) and lower locomotor circuits (ventral nerve cord in invertebrates). Higher centers select locomotor modes and adjust speed and direction, while lower circuits generate motor patterns via central pattern generators (CPGs). Peripheral sensory feedback adjusts these rhythms in response to environmental changes. Understanding the integration of higher centers, lower locomotor circuits, and sensory feedback is crucial, but their interaction remains largely unclear. To address this issue, we use an amphibious centipede (Scolopendra subspinipes mutilans) as a model animal. This centipede exhibits versatile body coordination: it walks on land using leg movements, swims in water with body undulation, and combines both during fast walking. Its central nervous system, composed of the head and segmental ganglia, generates these movements. Since centipedes can walk without the head, the lower locomotor circuits are resilient. Due to their ability to endure neuronal lesions, these centipedes are suitable for studying interactions between higher centers and lower locomotor circuits in producing a versatile locomotor repertoire. Although we have previously proposed neuromechanical models of centipedes that replicate slow and fast walking patterns and transitions between walking and swimming, the influence of descending signals from higher centers on these behaviors remains unclear. In this study, we performed stepwise removal of the brain and subesophageal ganglion (SEG) in centipedes to identify the contributions of higher centers to locomotor control. In this presentation, we introduce new findings from behavioral experiments and our updated mathematical model, which reproduces versatile locomotor behaviors (transitions between slow walking, fast walking, and swimming) through simple descending control from higher centers interacting with lower locomotor circuits.