Biomechanical benefits of the onion-skin motor unit control 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.
References (37)
- et al.
Common drive of motor units in regulation of muscle force
Trends Neurosci.
(1994) Rhythmic properties of motoneurones innervating muscle fibres of different speed in m. gastrocnemius medialis of the cat
Brain Res.
(1979)- et al.
Motor unit firing behavior in slow and fast contractions of the first dorsal interosseous muscle of healthy men
Electroencephalogr. Clin. Neurophysiol.
(1995) - et al.
Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle
Electroencephalogr. Clin. Neurophysiol.
(1972) - et al.
Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults
J. Neurophysiol.
(2007) - et al.
Frequency response of human soleus muscle
J. Neurophysiol.
(1976) Motor units: anatomy, physiology, and functional organization
Handbook of Physiology, Sec I. The Nervous System, V.ol. II. Motor System VB Brooks
(1981)Topography of terminal motor innervation in striated muscles from stillborn infants
Am. J. Phys. Med.
(1959)- et al.
Neural control of muscle force: indications from a simulation model
J. Neurophysiol.
(2013) - et al.
Relationship between firing rate and recruitment threshold of motoneurons in voluntary isometric contractions
J. Neurophysiol.
(2010)
Hierarchical control of motor units in voluntary contractions
J. Neurophysiol.
Influence of proprioceptive feedback on the firing rate and recruitment of motoneurons
J. Neural Eng.
Transposed firing activation of motor units
J. Neurophysiol.
Control scheme governing concurrently active human motor units during voluntary contractions
J. Physiol.
An integrative model of motor unit activity during sustained submaximal contractions
J. Appl. Physiol.
The action potentials of the alpha motoneurones supplying fast and slow muscles
J. Physiol.
Morphologic studies of motor units in normal human muscles
Models of recruitment and rate coding organization in motor-unit pools
J. Neurophysiol.
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