Rigidity and flexibility: The central basis of inter-leg coordination in the locust

Abstract

Many motor behaviors, and specifically locomotion, are the product of an intricate interplay between neuronal oscillators known as central pattern generators (CPGs), descending central commands, and sensory feedback loops. The relative contribution of each of these components to the final behavior determines the trade-off between fixed movements and those that are carefully adapted to the environment. Here we sought to decipher the endogenous, default, motor output of the CPG network controlling the locust legs, in the absence of any sensory or descending influences. We induced rhythmic activity in the leg CPGs in isolated nervous system preparations, using different application procedures of the muscarinic agonist pilocarpine. We found that the three thoracic ganglia, each controlling a pair of legs, have different inherent bilateral coupling. Furthermore, we found that the pharmacological activation of one ganglion is sufficient to induce activity in the other, untreated, ganglia. Each ganglion was thus capable to impart its own bilateral inherent pattern onto the other ganglia via a tight synchrony among the ipsilateral CPGs. By cutting a connective and severing the lateral-longitudinal connections, we were able to uncouple the oscillators’ activity. While the bilateral connections demonstrated a high modularity, the ipsilateral CPGs maintained a strict synchronized activity. These findings suggest that the central infrastructure behind locust walking features both rigid elements, which presumably support the generation of stereotypic orchestrated leg movements, and flexible elements, which might provide the central basis for adaptations to the environment and to higher motor commands.