SUMMARYThe analysis of inter-leg coordination in insect walking is generally a study of six-legged locomotion. For decades, the stick insect Carausius morosus has been instrumental for unravelling the rules and mechanisms that control leg coordination in hexapeds. We analysed inter-leg coordination in C. morosus that freely walked on straight paths on plane surfaces with different slopes. Consecutive 1.7s sections were assigned inter-leg coordination patterns (which we call gaits) based on footfall patterns. Regular gaits, i.e. wave, tetrapod or tripod gaits, occurred in different proportions depending on surface slopes. Tetrapod gaits were observed most frequently, wave gaits only occurred on 90deg inclining slopes and tripod gaits occurred most often on 15deg declining slopes, i.e. in 40% of the sections. Depending on the slope, 36-66% of the sections were assigned irregular gaits. Irregular gaits were mostly due to multiple stepping by the front legs, which is perhaps probing behaviour, not phase coupled to the middle legsʼ cycles. In irregular gaits, middle leg and hindleg coordination was regular, related to quadrupedal walk and wave gaits. Apparently, front legs uncouple from and couple to the walking system without compromising middle leg and hindleg coordination. In front leg amputees, the remaining legs were strictly coordinated. In hindleg and middle leg amputees, the front legs continued multiple stepping. The coordination of middle leg amputees was maladapted, with front legs and hindlegs performing multiple steps or ipsilateral legs being in simultaneous swing. Thus, afferent information from middle legs might be necessary for a regular hindleg stepping pattern. Supplementary material available online at

The biomechanical conditions for walking in the stick insect require a modeling approach that is based on the control of pairs of antagonistic motoneuron (MN) pools for each leg joint by independent central pattern generators (CPGs). Each CPG controls a pair of antagonistic MN pools. Furthermore, specific sensory feedback signals play an important role in the control of single leg movement and in the generation of inter-leg coordination or the interplay between both tasks. Currently, however, no mathematical model exists that provides a theoretical approach to understanding the generation of coordinated locomotion in such a multi-legged locomotor system. In the present study, I created such a theoretical model for the stick insect walking system, which describes the MN activity of a single forward stepping middle leg and helps to explain the neuronal mechanisms underlying coordinating information transfer between ipsilateral legs. In this model, CPGs that belong to the same leg, as well as those belonging to different legs, are connected by specific sensory feedback pathways that convey information about movements and forces generated during locomotion. The model emphasizes the importance of sensory feedback, which is used by the central nervous system to enhance weak excitatory and inhibitory synaptic connections from front to rear between the three thorax-coxa-joint CPGs. Thereby the sensory feedback activates caudal pattern generation networks and helps to coordinate leg movements by generating in-phase and out-of-phase thoracic MN activity.

The mechanism underlying the generation of stepping has been the object of intensive studies. Stepping involves the coordinated movement of different leg joints and is, in the case of insects, produced by antagonistic muscle pairs. In the stick insect, the coordinated actions of three such antagonistic muscle pairs produce leg movements and determine the stepping pattern of the limb. The activity of the muscles is controlled by the nervous system as a whole and more specifically by local neuronal networks for each muscle pair. While many basic properties of these control mechanisms have been uncovered, some important details of their interactions in various physiological conditions have so far remained unknown. In this study, we present a neuromechanical model of the coupled protractor-retractor and levator-depressor neuromuscular systems and use it to elucidate details of their coordinated actions during forward and backward walking. The switch from protraction to retraction is evoked at a critical angle of the femur during downward movement. This angle represents a sensory input that integrates load, motion, and ground contact. Using the model, we can make detailed suggestions as to how rhythmic stepping might be generated by the central pattern generators of the local neuronal networks, how this activity might be transmitted to the corresponding motoneurons, and how the latter might control the activity of the related muscles. The entirety of these processes yields the coordinated interaction between neuronal and mechanical parts of the system. Moreover, we put forward a mechanism by which motoneuron activity could be modified by a premotor network and suggest that this mechanism might serve as a basis for fast adaptive behavior, like switches between forward and backward stepping, which occur, for example, during curve walking, and especially sharp turning, of insects.

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