Characterization of Electromechanical Delay Based on a Biophysical Multi-Scale Skeletal Muscle Model

Abstract

Skeletal muscles can be voluntary controlled by the somatic nervous system yielding an active contractile stress response. Thereby, the active muscle stresses are transmitted to the skeleton by a cascade of connective tissue and thus enable motion. In the context of joint perturbations as well as the assessment of the complexity of neural control, the initial phase of the muscle-tendon system's stress response has a particular importance and is analyzed by means of electromechanical delay (EMD). EMD is defined as the time lag between the stimulation of a muscle and a measurable change in force output. While EMD is believed to depend on multiple structures / phenomena, it is hard to separate their contributions experimentally. We employ a physiologically detailed, three-dimensional, multi-scale model of an idealized muscle-tendon system to analyze the influence of (i) muscle and tendon length, (ii) the material behavior of skeletal muscle and tendon tissue, (iii) the chemo-electro-mechanical behavior of the muscle fibers and (iv) neural control on EMD. Comparisons with experimental data show that simulated EMD values are within the physiological range, i.e., between 6.1 and 68.6 ms, and that the model is able to reproduce the characteristic EMD-stretch curve, yielding the minimum EMD at optimal length. Simulating consecutive recruitment of motor units increases EMD by more than 20 ms, indicating that during voluntary contractions neural control is the dominant factor determining EMD. In contrast, the muscle fiber action potential conduction velocity is found to influence EMD even of a 27 cm long muscle by not more than 3.7 ms. We further demonstrate that in conditions where only little pre-stretch is applied to a muscle-tendon system, the mechanical behavior of both muscle and tendon tissue considerably impacts EMD. Predicting EMD for different muscle and tendon lengths indicates that the anatomy of a specific muscle-tendon system is optimized for its function, i.e., shorter tendon lengths are beneficial to minimize the neural control effort for muscles primary acting as motor in concentric contractions.

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