Motor-Unit Recruitment Plays an Important Role in Determining the Relationship Between Muscle Force and Force Variability

1. Subdivided portions of the cut ventral root innervation of the soleus muscle were electrically stimulated in 14 anesthetized cats. The stimulus trains imposed on these nerves simulated the recruitment and rate-modulation patterns of single motor units recorded during stretch-reflex responses in decerebrate preparations. Each activation pattern was evaluated for its ability to prevent muscle yield. 2. Three basic stimulus patterns, recruitment, step increases in stimulus rate, and doublets were imposed during the course of ramp stretches applied over a wide range of velocities. The effect of each stimulus pattern on muscle force was compared to the force output recorded without stretch-related recruitment or rate modulation. 3. Motor-unit recruitment was found to be most effective in preventing yield during muscle stretch. Newly recruited motor units showed no evidence of yielding for some 250 ms following activation, at which time muscle stiffness declined slightly. This time-dependent resistance to yield was observed regardless of whether the onset of the neural stimulus closely preceded or followed stretch onset. 4. Step increases in stimulus rate arising shortly after stretch onset did not prevent the occurrence of yield at most stretch velocities, but did augment muscle stiffness later in the stretch. Doublets in the stimulus train were found to augment muscle stiffness only when they occurred in newly recruited motor units. 5. These results suggest that at low or moderate initial forces, the prevention of yield in lengthening, reflexively intact muscle results primarily from rapid motor-unit recruitment. To a lesser extent, the spring-like character of the stretch-reflex response also derives from step increases in firing rate of motor units active before stretch onset and doublets in units recruited during the course of stretch. Smooth rate increases appear to augment muscle force later in the course of the reflex response.

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Activation of type-identified motor units during centrally evoked contractions in the cat medial gastrocnemius muscle. II. Motoneuron firing-rate modulation

Journal of Neurophysiology ◽

10.1152/jn.1996.75.1.38 ◽

1996 ◽

Vol 75 (1) ◽

pp. 38-50 ◽

Cited By ~ 31

Author(s):

K. E. Tansey ◽

B. R. Botterman

Keyword(s):

Firing Rate ◽

Motor Unit ◽

Muscle Force ◽

Motor Units ◽

Medial Gastrocnemius ◽

Firing Rates ◽

Rate Modulation ◽

The Mean ◽

Fast Twitch ◽

The Relationship

1. The aim of this study was to examine the nature of motoneuron firing-rate modulation in type-identified motor units during smoothly graded contractions of the cat medial gastrocnemius (MG) muscle evoked by stimulation of the mesencephalic locomotor region (MLR). Motoneuron discharge patterns, firing rates, and the extent of firing-rate modulation in individual units were studied, as was the extent of concomitant changes in firing rates within pairs of simultaneously active units. 2. In 21 pairs of simultaneously active motor units, studied during 41 evoked contractions, the motoneurons' discharge rates and patterns were measured by processing the cells' recorded action potentials through windowing devices and storing their timing in computer memory. Once recruited, most motoneurons increased their firing rates over a limited range of increasing muscle tension and then maintained a fairly constant firing rate as muscle force continued to rise. Most motoneurons also decreased their firing rates over a slightly larger, but still limited, range of declining muscle force before they were derecruited. Although this was the most common discharge pattern recorded, several other interesting patterns were also seen. 3. The mean firing rate for slow twitch (type S) motor units (27.8 imp/s, 5,092 activations) was found to be significantly different from the mean firing rate for fast twitch (type F) motor units (48.4 imp/s, 11,272 activations; Student's t-test, P < 0.001). There was no significant difference between the mean firing rates of fast twitch, fatigue-resistant (type FR) and fast twitch, fatigable (type FF) motor units. When the relationship between motoneuron firing rate and whole-muscle force was analyzed, it was noted that, in general, smaller, lower threshold motor units began firing at lower rates and reached lower peak firing rates than did larger, higher threshold motor units. These results confirm both earlier experimental observations and predictions made by other investigators on the basis of computer simulations of the cat MG motor pool, but are in contrast to motor-unit discharge behavior recorded in some human motor-unit studies. 4. The extent of concomitant changes in firing rate within pairs of simultaneously active motor units was examined to estimate the extent of simultaneous motoneuron firing-rate modulation across the motoneuron pool. A smoothed (5 point sliding average) version of the two motoneurons' instantaneous firing rates was plotted against each other, and the slope and statistical significance of the relationship was determined. In 16 motor-unit pairs, the slope of the motoneurons' firing-rate relationship was significantly distinct from 0. Parallel firing-rate modulation (< 10-fold difference in firing rate change reflected by a slope of > 0.1) was noted only in pairs containing motor units of like physiological type and then only if they were of similar recruitment threshold. 5. Other investigators have demonstrated that changes in a motoneuron's "steady-state" firing rate predictably reflect changes in the amount of effective synaptic current that cell is receiving. The finding in the present study of limited parallel firing-rate modulation between simultaneously active motoneurons would suggest that changes in the synaptic drive to the various motoneurons of the pool is unevenly distributed. This finding, in addition to the findings of orderly motor-unit recruitment and the relationship between motor-unit recruitment threshold and motoneuron firing rate, cannot be adequately accommodated for by the existing models of the synaptic organization in motoneuron pools. Therefore a new model of the synaptic organization within the motoneuron pool has been proposed.

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Model-Based Analysis of Muscle Strength and EMG-Force Relation with respect to Different Patterns of Motor Unit Loss

Neural Plasticity ◽

10.1155/2021/5513224 ◽

2021 ◽

Vol 2021 ◽

pp. 1-9

Author(s):

Chengjun Huang ◽

Maoqi Chen ◽

Yingchun Zhang ◽

Sheng Li ◽

Ping Zhou

Keyword(s):

Muscle Strength ◽

Motor Neuron ◽

Motor Unit ◽

Muscle Force ◽

Motor Units ◽

Force Variability ◽

Valuable Insight ◽

Model Based ◽

Force Relation ◽

Pool Model

This study presents a model-based sensitivity analysis of the strength of voluntary muscle contraction with respect to different patterns of motor unit loss. A motor unit pool model was implemented including simulation of a motor neuron pool, muscle force, and surface electromyogram (EMG) signals. Three different patterns of motor unit loss were simulated, including (1) motor unit loss restricted to the largest ones, (2) motor unit loss restricted to the smallest ones, and (3) motor unit loss without size restriction. The model outputs including muscle force amplitude, variability, and the resultant EMG-force relation were quantified under two different motor neuron firing strategies. It was found that motor unit loss restricted to the largest ones had the most dominant impact on muscle strength and significantly changed the EMG-force relation, while loss restricted to the smallest motor units had a pronounced effect on force variability. These findings provide valuable insight toward our understanding of the neurophysiological mechanisms underlying experimental observations of muscle strength, force control, and EMG-force relation in both normal and pathological conditions.

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Force variability is mostly not motor noise: Theoretical implications for motor control

PLoS Computational Biology ◽

10.1371/journal.pcbi.1008707 ◽

2021 ◽

Vol 17 (3) ◽

pp. e1008707

Author(s):

Akira Nagamori ◽

Christopher M. Laine ◽

Gerald E. Loeb ◽

Francisco J. Valero-Cuevas

Keyword(s):

Motor Unit ◽

Muscle Force ◽

Critical Path ◽

Control Strategies ◽

Discharge Rate ◽

Muscle Mechanics ◽

Sensorimotor Control ◽

Force Variability ◽

Motor Noise ◽

Signal Dependence

Variability in muscle force is a hallmark of healthy and pathological human behavior. Predominant theories of sensorimotor control assume ‘motor noise’ leads to force variability and its ‘signal dependence’ (variability in muscle force whose amplitude increases with intensity of neural drive). Here, we demonstrate that the two proposed mechanisms for motor noise (i.e. the stochastic nature of motor unit discharge and unfused tetanic contraction) cannot account for the majority of force variability nor for its signal dependence. We do so by considering three previously underappreciated but physiologically important features of a population of motor units: 1) fusion of motor unit twitches, 2) coupling among motoneuron discharge rate, cross-bridge dynamics, and muscle mechanics, and 3) a series-elastic element to account for the aponeurosis and tendon. These results argue strongly against the idea that force variability and the resulting kinematic variability are generated primarily by ‘motor noise.’ Rather, they underscore the importance of variability arising from properties of control strategies embodied through distributed sensorimotor systems. As such, our study provides a critical path toward developing theories and models of sensorimotor control that provide a physiologically valid and clinically useful understanding of healthy and pathologic force variability.

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Activation of type-identified motor units during centrally evoked contractions in the cat medial gastrocnemius muscle. I. Motor-unit recruitment

Journal of Neurophysiology ◽

10.1152/jn.1996.75.1.26 ◽

1996 ◽

Vol 75 (1) ◽

pp. 26-37 ◽

Cited By ~ 22

Author(s):

K. E. Tansey ◽

B. R. Botterman

Keyword(s):

Motor Unit ◽

Muscle Force ◽

Muscle Tension ◽

Motor Units ◽

Motor Unit Recruitment ◽

Medial Gastrocnemius ◽

Recruitment Order ◽

Fast Twitch ◽

Physiological Type ◽

Tetanic Tension

1. The recruitment order of 64 pairs of motor units, comprising 21 type-identified units, was studied during centrally evoked muscle contractions of the cat medial gastrocnemius (MG) muscle in an unanesthetized, high decerebrate preparation. Motor units were functionally isolated within the MG nerve by intra-axonal (or intramyelin) penetration with conventional glass microelectrodes. 2. Graded stimulation of the mesencephalic locomotor region (MLR) was used to evoke smoothly graded contractions, which under favorable conditions was estimated to reach 40% of maximum tetanic tension of the MG muscle. With this method of activation, 100% of slow twitch (type S) units, 95% of fast twitch, fatigue-resistant (type FR) units, 86% of fast twitch, fatigue-intermediate (type FI) units, and 49% of fast twitch, fatigable (type FF) units studied were recruited. 3. Motoneuron size as estimated by axonal conduction velocity (CV) was correlated with muscle-unit size as estimated by maximum tetanic tension (Po). Although the correlation between these properties was significant among type S and FR units, no significant correlation was found for these properties among type FI and FF units. 4. Motor-unit recruitment was ordered by physiological type (S > F, 100% of pairs; S > FR > FI > FF, 93% of pairs). Although none of the motor-unit properties studied predicted recruitment order perfectly, motor-unit recruitment was found to proceed by increasing Po (89% of pairs), decreasing contraction time (79% of pairs), decreasing fatigue index (80% of pairs), and increasing CV (76% of pairs). These percentages were significantly different from random (i.e., 50%). Statistically, all four motor-unit properties were equivalent in predicting recruitment order. These results are similar to those reported by other investigators for motor-unit recruitment order evoked from other supraspinal centers, as well as from peripheral sites. 5. When, however, motor-unit recruitment within pairs of motor units containing two fast-twitch (type F) units was examined, Po was a significantly better predictor of recruitment order than CV (85% vs. 52% of pairs). One explanation for this observation is that the correlation between Po and CV is high among type S, type FR units, and possibly among the lower-tension type FF units, but not among the remaining higher-tension type FF units. 6. The reproducibility of recruitment order in multiple contractions was investigated in 16 motor-unit pairs. Recruitment order was found to be variable in only three motor-unit pairs, all of which contained units of similar physiological type and recruitment threshold. 7. Analysis of recruitment order by pair-wise testing confirms the general conclusion reached in human studies that the muscle force level at recruitment for a motor unit is highly correlated with its strength. As an additional confirmation, the whole-muscle force level at recruitment for 41 units was measured in a series of contractions in which the rate of rise of muscle tension was limited to rates < 1,000 g/s. For these contractions, a significant correlation was found between muscle tension at recruitment and motor-unit Po.

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