A Neuro-Mechanical Model of a Single Leg Joint Highlighting the Basic Physiological Role of Fast and Slow Muscle Fibres of an Insect Muscle System

Abstract

In legged animals, the muscle system has a dual function: to produce forces and torques necessary to move the limbs in a systematic way, and to maintain the body in a static position. These two functions are performed by the contribution of specialized motor units, i.e. motoneurons driving sets of specialized muscle fibres. With reference to their overall contraction and metabolic properties they are called fast and slow muscle fibres and can be found ubiquitously in skeletal muscles. Both fibre types are active during stepping, but only the slow ones maintain the posture of the body. From these findings, the general hypothesis on a functional segregation between both fibre types and their neuronal control has arisen. Earlier muscle models did not fully take this aspect into account. They either focused on certain aspects of muscular function or were developed to describe specific behaviours only. By contrast, our neuro-mechanical model is more general as it allows functionally to differentiate between static and dynamic aspects of movement control. It does so by including both muscle fibre types and separate motoneuron drives. Our model helps to gain a deeper insight into how the nervous system might combine neuronal control of locomotion and posture. It predicts that (1) positioning the leg at a specific retraction angle in steady state is most likely due to the extent of recruitment of slow muscle fibres and not to the force developed in the individual fibres of the antagonistic muscles; (2) the fast muscle fibres of antagonistic muscles contract alternately during stepping, while co-contraction of the slow muscle fibres takes place during steady state; (3) there are several possible ways of transition between movement and steady state of the leg achieved by varying the time course of recruitment of the fibres in the participating muscles.

Effects of force detecting sense organs on muscle synergies are correlated with their response properties

“…9). In both stick insect and cockroach legs, there is a proximal to distal gradient in the size of intrinsic leg muscles: muscles acting at the coxo-trochanteral joints produce the largest forces (torques) generated in support and propulsion (Pearson and Iles, 1971; Schmitz, 1986; Toth et al, 2013). In both species, groups of trochanteral campaniform (Groups 3, 4) detect the net forces at the CTr and more proximal body coxa joints (Zill et al, 1999, 2012).…”

The comparative investigation of the stick insect and cockroach models in the study of insect locomotion

“…Their variable walking patterns [14] suggest independent control of leg joints, and subgroups of INs and MNs that can achieve this have been identified [7,18,43]. Current models therefore contain three joint CPGs for each leg [44][45][46]47 ], and such leg CPGs can be connected to produce inter-leg coordination. These models use biophysically based ion-channel (Hodgkin-Huxley-type) models of INs and MNs (see Box 1) to describe cellular mechanisms that generate rhythmic motor activity and neural circuits responsible for adaptive behaviors like backward and sideward stepping.…”

“…Models such as those of Kukillaya et al [31] and Tó th et al [46,47 ] span the space of central-decentralized and feedforward-feedback control (cf. [58]), but their complexity makes analyses of such models difficult.…”

Effects of functional decoupling of a leg in a model of stick insect walking incorporating three ipsilateral legs

“…It was shown earlier (Tóth et al. ,b) that the premotor INs can completely inhibit the MN activity if they themselves are disinhibited (Fig. D).…”