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.

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“…Interestingly, corresponding results have been found for crustacea (Clarac and Chasserat 1979;Sillar et al 1987). Furthermore, Knebel et al (2017) found in-phase coupling also between contralateral legs if all three thoracic ganglia were treated with pilocarpine, which again contrasts to normal walking behavior, but can be observed in swimming (Ikeda and Wiersma 1964, crayfish swimmerets) and flying (Pearson 1995, locust). These results raise questions concerning the functional properties of these oscillatory systems.…”

“…Here, the coordination of deafferented leg controllers is often quite different, eventually even opposite to that of normal walking (e.g. Büschges et al 1995;Knebel et al 2017;Borgmann et al 2007Borgmann et al , 2009Mantziaris et al 2017; we will deal with an interesting different case ; Johnston and Levine (2002) in the Discussion and Supplement).…”

“…This situation is highlighted by a detailed recent study on locusts (Knebel et al 2017), focusing on interleg coordination in deafferented locusts (recordings from motor neurons activating the depressor muscle). The authors argued that the temporal patterns observed in the different thoracic ganglia may provide the basis for that found in walking animals.…”

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“…Furthermore, we found no significant differences in coupling strengths in the case of 458 simultaneous recordings from all three ganglia, while it had previously been shown that 459 depressor activity in all segments seems to be weakly phase coupled in locusts [24]. 460 Comparison with a connectivity model of leg coordination in 461 the cockroach 462 David and colleagues (2016) reported CPG coupling strength in the meso-and 463 metathoracic ganglia of the cockroach by calculating the transition latencies and phase 464…”

“…June 17, 2019 22/33 ganglia after restricted activation, i.e. using a split bath preparation, of the prothoracic 438 ganglia in the locust [24]. Furthermore, it has been shown in cockroaches that 439 intrasegmental, i.e.…”