Elsevier

Journal of Biomechanics

Volume 48, Issue 2, 21 January 2015, Pages 195-203
Journal of Biomechanics

Biomechanical benefits of the onion-skin motor unit control scheme

https://doi.org/10.1016/j.jbiomech.2014.12.003Get rights and content

Abstract

Muscle force is modulated by varying the number of active motor units and their firing rates. For the past five decades, the notion that the magnitude of the firing rates is directly related to motor unit size and recruitment threshold has been widely accepted. This construct, here named the After-hyperpolarization scheme evolved from observations in electrically stimulated cat motoneurons and from reported observations in voluntary contractions in humans. It supports the assumption that the firing rates of motor units match their mechanical properties to “optimize” force production, so that the firing rate range corresponds to that required for force-twitch fusion (tetanization) and effective graduation of muscle force. In contrast, we have shown that, at any time and force during isometric voluntary constant-force contractions in humans, the relationship between firing rate and recruitment threshold is inversely related. We refer to this construct as the Onion-Skin scheme because earlier-recruited motor units always have greater firing rates than latter-recruited ones. By applying a novel mathematical model that calculates the force produced by a muscle for the two schemes we found that the Onion-Skin scheme is more energy efficient, provides smoother muscle force at low to moderate force levels, and appears to be more conducive to evolutionary survival than the After-hyperpolarization scheme.

Introduction

Muscle force is modulated by varying the number of active motor units and their firing rates. The manner in which motor units are controlled determines the characteristics of the force generated by the muscle that in turn determines the manner in which we interact with our environment and each other.

There is general agreement that, as the excitation to the motoneuron pool increases to produce more force, motor units are recruited in order of increasing size, as described by the “Size Principle” (Henneman, 1957, Hu et al., 2013). As for the firing rate, over the past five decades there has been a common acceptance of the notion promulgated dominantly by Eccles et al. in 1958 that higher-threshold motoneurons have greater firing rates than lower-threshold ones. This notion stems from the observation that, when the nerves of anesthetized cats are electrically stimulated, the larger-diameter (higher-threshold) motoneurons exhibit a shorter after-hyperpolarization (AHP) and greater firing rates than the smaller-diameter (lower-threshold) ones. The lower-threshold motor units have wider and smaller amplitude force twitches than the higher-threshold motor units and require lower firing rates to tetanize (produce twitch fusion). By inference, this arrangement would “optimize” the force generating capacity of the muscle since each motor unit would fire at rates producing twitch fusion and thus contributing its greatest individual force. This hypothesis, which we will refer to as the AHP scheme, was supported by Kernell, 1965, Kernell, 2003 and has been tacitly accepted by many thereafter and adopted in support of their observations in humans (Grimby et al., 1979, Moritz et al., 2005, Oya et al., 2009, among others). However, the empirical studies that reported a linear relation between recruitment threshold and firing rates grouped motor unit data from different subjects and contractions performed on different days or at different force levels (Gydikov and Kosarov, 1974, Grimby et al., 1979, Moritz et al., 2005, Tracy et al., 2005, Barry et al., 2007, Oya et al., 2009, Jesunathas et al., 2012). But, we make note that this approach is known to introduce inter-subject variability and errors in the analysis (De Luca and Hostage, 2010, De Luca and Contessa, 2012, Hu et al., 2013, Hu et al., 2014b).

We (De Luca et al., 1982, De Luca and Hostage, 2010, De Luca and Contessa, 2012) and others Seyffarth, 1940; Person and Kudina, 1972; Masakado et al., 1995; Stock et al., 2012; Hu et al., 2013, 2014b; De Luca et al., 2014; among others) have shown that, at any time and force during voluntary constant-force contractions in humans, earlier-recruited motor units maintain higher firing rates than later-recruited ones, providing an inverse orderly hierarchy of nested firing rate curves resembling the layers of the skin of an onion. We refer to this construct as the Onion-Skin scheme (De Luca and Erim, 1994).

In this work, we applied a novel model of muscle force generation (Contessa and De Luca, 2013) to compare the force characteristics produced by the two schemes during constant-force contractions. We did so for two muscles: the first dorsal interosseous (FDI) of the hand and the vastus lateralis (VL) of the thigh. These muscles were chosen because they have different properties: the FDI is a smaller muscle commonly involved in precise low-force level activities, and the VL is one of the largest muscles in the body that generates large forces.

Section snippets

Methods

The model used for the simulation of the firing rate and force behavior of motor units is a modified version of that developed by Contessa and De Luca (2013) for the FDI and VL muscles. The input–output relationship at the motoneuron level, describing the firing behavior of motor units, and the firing rate to force transduction at the muscle fiber level, describing the mechanical properties of motor units, are modeled separately. The model is based on the concept of Common Drive (De Luca et

Results

We mathematically modeled the firing rate characteristics of motor units as a function of increasing input excitation to the motoneuron pool of the FDI and VL muscles for the Onion-Skin (Fig. 1A1 and B1) and for the AHP schemes (Fig. 1A2 and B2), as described by Eqs. (2), (3), (8) in Section 2. The Onion-Skin scheme describes an inverse hierarchical relationship between the recruitment threshold and the firing rate of motoneurons at any time and input excitation value. The AHP-scheme describes

Discussion

Our analysis revealed a clear distinction between the force generating capacities of the two schemes. The Onion-Skin scheme presented clear evolutionary benefits.

The low-threshold motor units produce more force at lower input excitation levels in the Onion-Skin scheme than in the AHP scheme. Consequently, a fewer number of motor units, with lower recruitment threshold and fatigue-resistant characteristics, are needed in the Onion-Skin scheme to produce a given force at low levels. For example,

Conclusion

In summary, the Onion-Skin scheme is not designed to maximize muscle force, as the AHP scheme has been inferred to do by Kernell (2003). Instead the Onion-Skin scheme provides means to generate force more quickly and more smoothly when force is initiated, and it provides a lower maximal force with the capacity to sustain it over longer time. Also, the higher-threshold motor units maintain a reserve capacity that could be accessible in extreme situations by increasing their firing rates. These

Conflict of interest statement

Carlo J. De Luca is the President of Delsys, the company that developed the technology for decomposing the surface electromyographic signals, and the President of the Neuromuscular Research Foundation.

Acknowledgements

This work was supported by the National Center for Medical Rehabilitation Research (NCMRR)/National Institute of Child Health and Human Development (NICHD) Grant HD-050111, and by a grant from the Neuromuscular Research Foundation.

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