Abstract

Rhythmic limb movements during locomotion are controlled by central pattern generator (CPG) circuits located in the spinal cord. It is considered that these circuits are composed of individual rhythm generators (RGs) for each limb interacting with each other through multiple commissural and long propriospinal circuits. The organization and operation of each RG are not fully understood, and different competing theories exist about interactions between its flexor and extensor components, as well as about left–right commissural interactions between the RGs. The central idea of circuit organization proposed in this study is that with an increase of excitatory input to each RG (or an increase in locomotor speed) the rhythmogenic mechanism of the RGs changes from “flexor-driven” rhythmicity to a “classical half-center” mechanism. We test this hypothesis using our experimental data on changes in duration of stance and swing phases in the intact and spinal cats walking on the ground or tied-belt treadmills (symmetric conditions) or split-belt treadmills with different left and right belt speeds (asymmetric conditions). We compare these experimental data with the results of mathematical modeling, in which simulated CPG circuits operate in similar symmetric and asymmetric conditions with matching or differing control drives to the left and right RGs. The obtained results support the proposed concept of state-dependent changes in RG operation and specific commissural interactions between the RGs. The performed simulations and mathematical analysis of model operation under different conditions provide new insights into CPG network organization and limb coordination during locomotion.

Highlights

  • It is commonly accepted that the spinal locomotor central pattern generator (CPG) circuits include separate rhythm generators (RGs) that each control a single limb and interact with each other via multiple commissural and long propriospinal pathways

  • Each RG is thought to contain two excitatory neuron populations representing flexor and extensor half-centers connected by reciprocal inhibition, whose activity defines the flexor and extensor phases of limb movements, respectively

  • We focused on the analysis of speeddependent changes in the durations of the main locomotor phases using data from previous experiments during tied-belt and split-belt treadmill locomotion in intact and spinal cats (Frigon et al, 2015, 2017) and new experiments performed during overground locomotion in an intact cat

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Summary

Introduction

It is commonly accepted that the spinal locomotor central pattern generator (CPG) circuits include separate rhythm generators (RGs) that each control a single limb and interact with each other via multiple commissural and long propriospinal pathways. According to the classical half-center concept (Brown, 1914), switching between the flexor and extensor activity phases (for review see McCrea and Rybak, 2008; Stuart and Hultborn, 2008) occurs through a so-called release mechanism (Wang and Rinzel, 1992) based on an adapting (decrementing) activity of each half-center and mutual inhibition between them This mechanism does not necessarily require the ability of each half-center to intrinsically generate rhythmic activity, and the resultant RG pattern is usually flexor– extensor balanced, so that the durations of both phases are approximately equal. Optogenetic studies in the isolated spinal cord have demonstrated that rhythmic flexor and extensor activities can be evoked in certain conditions independent of each other (Hägglund et al, 2013), confirming that both flexor and extensor half-centers are conditional intrinsic oscillators, i.e., capable of endogenous generation of rhythmic bursting activity. Pearson and Duysens (1976) and Duysens (2006) have previously proposed a flexor-driven concept (so called swing generator model (for review see Duysens et al, 2013), in which only the flexor half-center is intrinsically rhythmic, representing a true RG, while the extensor half-center shows sustained activity if uncoupled and exhibits anti-phase oscillations due to rhythmic inhibition from the flexor half-center

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