The Interaction of Compliance and Activation on the Force-Length Operating Range and Force Generating Capacity of Skeletal Muscle: A Computational Study using a Guinea Fowl Musculoskeletal Model.

S M Cox,M Cromie Lear,K L Easton,J Rubenson,R L Marsh,S L Delp

doi:10.1093/iob/obz022

Abstract

SynopsisA muscle’s performance is influenced by where it operates on its force–length (F–L) curve. Here we explore how activation and tendon compliance interact to influence muscle operating lengths and force-generating capacity. To study this, we built a musculoskeletal model of the lower limb of the guinea fowl and simulated the F–L operating range during fixed-end fixed-posture contractions for 39 actuators under thousands of combinations of activation and posture using three different muscle models: Muscles with non-compliant tendons, muscles with compliant tendons but no activation-dependent shift in optimal fiber length (L0), and muscles with both compliant tendons and activation-dependent shifts in L0. We found that activation-dependent effects altered muscle fiber lengths up to 40% and increased or decreased force capacity by up to 50% during fixed-end contractions. Typically, activation-compliance effects reduce muscle force and are dominated by the effects of tendon compliance at high activations. At low activation, however, activation-dependent shifts in L0 are equally important and can result in relative force changes for low compliance muscles of up to 60%. There are regions of the F–L curve in which muscles are most sensitive to compliance and there are troughs of influence where these factors have little effect. These regions are hard to predict, though, because the magnitude and location of these areas of high and low sensitivity shift with compliance level. In this study we provide a map for when these effects will meaningfully influence force capacity and an example of their contributions to force production during a static task, namely standing.

Highlights

Where muscles operate on their force–length (F–L) relationship has important implications for muscle and locomotor performance
When models were re-run without including activation-dependent shifts in L0, we found third-order interaction terms between passive muscle length, activation level, and MTU compliance (Table 3)
These interaction terms imply that how muscle length changes with activation level differs between muscle of low and high compliance and that this relationship changes with the starting passive length of the muscle

Summary

Introduction

Where muscles operate on their force–length (F–L) relationship has important implications for muscle and locomotor performance. The result is that the operating ranges for muscles with compliant tendons shift to the left on the F–L curve with increasing activation. This theoretical prediction has been experimentally confirmed in several studies (Lakatta and Jewell 1977; Fukunaga et al 1997; Hawkins and Bey 1997; MacIntosh and MacNaughton 2005; Lemos et al 2008; Azizi and Roberts 2010; Arnold and Delp 2011; Sugisaki et al 2011; Rubenson et al 2012; Holt and Azizi 2016; Mayfield et al 2016). For instance: Is there a threshold of muscle–tendon compliance where the effect becomes functionally relevant? Does compliance have a consistent influence on the F–L operating range in all conditions (i.e., across different postures and muscle lengths) or are there conditions when it is more influential?

Objectives

Methods

Results

Conclusion