Unravelling intra- and intersegmental neuronal connectivity between central pattern generating networks in a multi-legged locomotor system

Abstract

Animal walking results from a complex interplay of central pattern generating networks (CPGs), local sensory signals expressing position, velocity and forces generated in the legs, and coordinating signals between neighboring ones. In the stick insect intra-and intersegmental coordination is conveyed by these sensory signals. The CPGs control the activity of motoneuron pools and are thereby responsible for the generation of rhythmic leg movements. The rhythmic activity of the CPGs can be modified by the aforementioned sensory signals. However, the precise nature of the interaction between the CPGs and these sensory signals has remained largely unknown. Experimental methods aiming at finding out details of these interactions often apply the muscarinic acetylcholine receptor agonist, pilocarpine in order to induce rhythmic activity in the CPGs. Using this general approach, we removed the influence of sensory signals and investigated the putative connections between CPGs associated with the June 17, 2019 1/33 coxa-trochanter (CTr)-joint in the different segments (legs) in more detail. The experimental data underwent connectivity analysis using Dynamic Causal Modelling (DCM). This method can uncover the underlying coupling structure and strength between pairs of segmental ganglia (CPGs). For the analysis we set up different coupling schemes (models) for DCM and compared them using Bayesian Model Selection (BMS). Models with contralateral connections in each segment and ipsilateral connections on both sides, as well as the coupling from the meta-to the ipsilateral prothoracic ganglion were preferred by BMS to all other types of models tested.Moreover, the intrasegmental coupling strength in the mesothoracic ganglion was the strongest and most stable in all three ganglia.Various experiments on vertebrates and invertebrates confirm the existence of central 2 pattern generating networks (CPGs). These networks are responsible for the generation 3 of periodic muscle activity in a given leg [14,29]. The movement of each leg has to be 4 coordinated with that of the other legs in order to produce walking. In the stick insect 5 Carausius morosus, each leg is individually controlled by its own CPGs located in the 6 pro-(front legs), meso-(middle legs) and metathoracic ganglion (hind legs) [15,46]. 7 Each leg consists of three main leg joints about which leg segments execute coordinated 8 movements during walking and climbing. The thorax-coxa (ThC) joint is responsible for 9 forward and backward movements, the coxa-trochanter (CTr) joint enables the femur to 10 move in upward and downward direction. The femur-tibia (FTi) joint brings about 11 flexing and stretching of the leg by moving the tibia relative to the femur. Each of the 12 leg joints is associated with an antagonistic muscle pair: the protractor-retractor (ThC), 13 the levator-depressor (CTr) and the flexor-extensor (FTi) muscle pair [19]. The 14 rhythmic (periodic) activation of the muscles originates in the corresponding CPGs [5] 15 and sensory signals play a signifi...