Intra- and intersegmental influences among central pattern generating networks in the walking system of the stick insect

Abstract

To efficiently move around, animals need to coordinate their limbs. Proper, context-dependent coupling among the neural networks underlying leg movement is necessary for generating intersegmental coordination. In the slow-walking stick insect, local sensory information is very important for shaping coordination. However, central coupling mechanisms among segmental central pattern generators (CPGs) may also contribute to this. Here, we analyzed the interactions between contralateral networks that drive the depressor trochanteris muscle of the legs in both isolated and interconnected deafferented thoracic ganglia of the stick insect on application of pilocarpine, a muscarinic acetylcholine receptor agonist. Our results show that depressor CPG activity is only weakly coupled between all segments. Intrasegmental phase relationships differ between the three isolated ganglia, and they are modified and stabilized when ganglia are interconnected. However, the coordination patterns that emerge do not resemble those observed during walking. Our findings are in line with recent studies and highlight the influence of sensory input on coordination in slowly walking insects. Finally, as a direct interaction between depressor CPG networks and contralateral motoneurons could not be observed, we hypothesize that coupling is based on interactions at the level of CPG interneurons. Maintaining functional interleg coordination is vitally important as animals locomote through changing environments. The relative importance of central mechanisms vs. sensory feedback in this process is not well understood. We analyzed coordination among the neural networks generating leg movements in stick insect preparations lacking phasic sensory feedback. Under these conditions, the networks governing different legs were only weakly coupled. In stick insect, central connections alone are thus insufficient to produce the leg coordination observed behaviorally.

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

“…In addition to 245 the intersegmental decrease, there was a strong increase in the intrasegmental coupling 246 in the mesothoracic ganglion (by factors of 2-20) and a decrease in connectivity in the 247 metathoracic ganglion (by a factor of 2). This is in agreement with [28] where the 248 authors could demonstrate that the mesothoracic ganglion showed intrasegmental 249 phase-coupling even in the isolated state, while the connection of the metathoracic 250 ganglion to the mesothoracic ganglion had to be present in order to detect robust 251 in-phase coupling in the metathoracic ganglion. The connectivity strengths were calculated for intervals that were pre-identified as phase-coupled by the PC approach.…”

Decentralized Control of Insect Walking – a simple neural network explains a wide range of behavioral and neurophysiological results

“…In general, in fully or partly deafferented insects ipislateral neighboring legs fire in-phase, whereas in walking these legs typically show about anti-phase coupling. Supporting results for Carausius are presented by Mantziaris et al (2017), and Borgmann et al (2007, who recorded from the motor neurons activating the retractor muscles, and by Büschges et al (1995), who recorded from motor neurons of all three joints. Interestingly, corresponding results have been found for crustacea (Clarac and Chasserat 1979;Sillar et al 1987).…”

“…However, as the behavioral data proposes that we deal with a continuous behavioral spectrum, this concept does not support a view of distinct motor schemas on the neuronal level (Graham (1972) for Carausius; Wosnitza et al (2013) for Drosophila; see also Mantziaris et al (2017) for discussion). Regular "gaits" only appear in the eye of the observer and it might therefore be misleading to assume that a controller has been evolved to produce separate gaits.…”

“…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).…”

A Synthetic Nervous System Controls a Simulated Cockroach

“…Behavioral experiments have revealed correlations between the positions of different legs in arthropods [29,45], but the underlying networks remain largely unknown. Work in locusts suggests that some direct neural connections between the legs may contribute to coordination during walking [3,46]. Therefore, in SimRoach2, the levator-depressor (CTr) CPGs between legs are connected and neural pathways were engineered to produce the observed behavior.…”