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. 2014 Oct;11(5):056022.
doi: 10.1088/1741-2560/11/5/056022. Epub 2014 Sep 22.

Contributions to muscle force and EMG by combined neural excitation and electrical stimulation

Patrick E Crago  1 , Nathaniel S Makowski, Natalie M Cole
Affiliations

Contributions to muscle force and EMG by combined neural excitation and electrical stimulation

Patrick E Crago et al. J Neural Eng. 2014 Oct.

Abstract

Objective: Stimulation of muscle for research or clinical interventions is often superimposed on ongoing physiological activity without a quantitative understanding of the impact of the stimulation on the net muscle activity and the physiological response. Experimental studies show that total force during stimulation is less than the sum of the isolated voluntary and stimulated forces, but the occlusion mechanism is not understood.

Approach: We develop a model of efferent motor activity elicited by superimposing stimulation during a physiologically activated contraction. The model combines action potential interactions due to collision block, source resetting, and refractory periods with previously published models of physiological motor unit recruitment, rate modulation, force production, and EMG generation in human first dorsal interosseous muscle to investigate the mechanisms and effectiveness of stimulation on the net muscle force and EMG.

Main results: Stimulation during a physiological contraction demonstrates partial occlusion of force and the neural component of the EMG, due to action potential interactions in motor units activated by both sources. Depending on neural and stimulation firing rates as well as on force-frequency properties, individual motor unit forces can be greater, smaller, or unchanged by the stimulation. In contrast, voluntary motor unit EMG potentials in simultaneously stimulated motor units show progressive occlusion with increasing stimulus rate. The simulations predict that occlusion would be decreased by a reverse stimulation recruitment order.

Significance: The results are consistent with and provide a mechanistic interpretation of previously published experimental evidence of force occlusion. The models also predict two effects that have not been reported previously--voluntary EMG occlusion and the advantages of a proximal stimulation site. This study provides a basis for the rational design of both future experiments and clinical neuroprosthetic interventions involving either motor or sensory stimulation.

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Figures

Figure 1
Figure 1
Block diagram of simulation model, with references to the sections where they are described. The inputs to the system include 1) the level of voluntary excitation, which determines the recruitment and firing rate of the N motor neurons, and 2) the stimulation level, which determines the recruitment order and stimulus rate on each of the N axons. The action potential interactions model determines the action potential trains arriving at the endpoint of each of the N axons. The motor unit force model calculates the force produced by each motor unit as well as the summed total force. The motor unit action potential model calculates the composite EMG and separates the voluntary EMG and M-waves.
Figure 2
Figure 2
Example of simulated whole muscle force, EMG, and M-waves. Force and EMG are in arbitrary units. (a) A stimulated contraction at 30% MVC is achieved by stimulating 29 motor units at 20 s−1. (b) A neurally generated 40% MVC contraction achieved by recruiting 98 motor units is maintained for a full 3 s period, and the same stimulation as shown in (a) is superimposed beginning at time 1.5 s. The total EMG (c) is separated into the M-wave (d) and voluntary EMG (e) components.
Figure 3
Figure 3
Force and EMG occlusion as a function of voluntary and stimulated contraction levels and stimulus rate during motor point stimulation with random recruitment order. (a,b) The increment in force produced by stimulation at 10 s−1 and 30 s−1 respectively is plotted as a function of the initial voluntary force for stimulation levels producing 0% - 100% of MVC in the absence of any voluntary force. In each panel, the dotted line is unity slope, i.e. without any stimulation. (c) Normalized stimulated force increments at each stimulus rate as a function of the initial voluntary force for both motor neuron pool models. The forces (mean +/− sd) at each stimulation level were normalized to the stimulated force without any background voluntary contraction and then averaged. Each symbol represents a different stimulus rate. (d) The voluntary component of the combined EMG during stimulation is plotted versus the voluntary EMG prior to stimulation onset for stimulation at 20 s−1 for different levels of stimulation. A thin unity slope line is shown for visual reference. (e, f) Voluntary force as a function of the voluntary EMG during stimulation at 20 and 45 s−1 respectively at various stimulated contraction levels given by the legend in (f).
Figure 4
Figure 4
. (a) Force and (b) EMG occlusion during simultaneous voluntary (De Luca and Contessa model) and 15 s−1 stimulated contractions applied at the wrist with the reverse recruitment order. Each line shows increasing voluntary contractions at one level of stimulation as indicated in the legend. Stimulated forces greater than 70% MVC could not be generated by stimulation at 15 s−1.
Figure 5
Figure 5
The alterations in firing rate and the contributions of single motor units to the incremental force and voluntary EMG for motor point stimulation. The voluntary level was 50%MVC and the stimulation level was 30%MVC. a) Cumulative incremental force of motor units across the motor unit pool. b) Incremental force produced by stimulation of each motor unit. c) Motor unit rates determined by neural drive and stimulation. Also shown are the net rates arriving at the endpoint (endpoint APs), and the rates of endpoint APs originating at the neuron. d) Probability distribution of endpoint action potential periods driven by neural activation alone. e) Probability distribution of endpoint action potential periods of all stimulated units. The motor unit contraction time τc of individual motor units is superimposed. For d) and e), the color scales give the probabilities of an action potential occurring in 5 ms bins estimated over a 50 s simulation time period. The area of each point is also scaled by the probability to facilitate comparisons.
Figure 6
Figure 6
Voluntary contributions to the total combined force as a function of stimulation force level. Each line is for a constant level of combined force.
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