Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation

1987 ◽  
Vol 58 (3) ◽  
pp. 525-542 ◽  
Author(s):  
C. J. De Luca ◽  
B. Mambrito

1. Myoelectric (ME) activity of several motor units was detected simultaneously from the human flexor pollicis longus and extensor pollicis longus muscles, the only two muscles that control the interphalangeal joint of the thumb. The ME signals were detected while the subjects produced isometric force outputs to track three different paradigms: triangular trajectories, random-force trajectories requiring both flexion and extension contractions, and net zero force resulting from stiffening the joint by voluntarily coactivating both muscles. 2. The ME signals were decomposed into their constituent motor-unit action potential trains. The firing rate behavior of the concurrently active motor units was studied using cross-correlation techniques. 3. During isometric contractions, the firing rates of motor units within a muscle were greatly cross-correlated with essentially zero time shift with respect to each other. This observation confirms our previous report of this behavior, which has been called common drive. Common drive was also found among the motor units of the agonist and antagonist muscles during voluntary coactivation to stiffen the interphalangeal joint. This observation suggests two interesting points: 1) that the common drive mechanism has a component of central origin, and 2) that the central nervous system may control the motoneuron pools of an agonist-antagonist muscle pair as if they were one pool when both are performing the same task. 4. During force reversals, the firing rates of motor units reverse in an orderly manner: earlier recruited motor units decrease their firing rate before later recruited motor units. This orderly reversal of firing rates is consistent with the concept of orderly recruitment and derecruitment. 5. A control scheme is suggested to explain the behavior of the motor units in both muscles during force reversal. It consists of centrally mediated reciprocally organized flexion and extension commands along with a common coactivation command to both muscles. This control scheme allows for coactivation and reciprocal activation of an agonist-antagonist set. 6. The agonist-antagonist pair was observed to generate a net force in two control modalities: proportional activation and reciprocal activation. In proportional activation, the agonist-antagonist set is coactivated during either of two states: when uncertainty exists in the required task or when a compensatory force contraction is perceived to be required.(ABSTRACT TRUNCATED AT 400 WORDS)

2012 ◽  
Vol 107 (1) ◽  
pp. 178-195 ◽  
Author(s):  
Carlo J. De Luca ◽  
Paola Contessa

For the past five decades there has been wide acceptance of a relationship between the firing rate of motor units and the afterhyperpolarization of motoneurons. It has been promulgated that the higher-threshold, larger-soma, motoneurons fire faster than the lower-threshold, smaller-soma, motor units. This relationship was based on studies on anesthetized cats with electrically stimulated motoneurons. We questioned its applicability to motor unit control during voluntary contractions in humans. We found that during linearly force-increasing contractions, firing rates increased as exponential functions. At any time and force level, including at recruitment, the firing rate values were inversely related to the recruitment threshold of the motor unit. The time constants of the exponential functions were directly related to the recruitment threshold. From the Henneman size principle it follows that the characteristics of the firing rates are also related to the size of the soma. The “firing rate spectrum” presents a beautifully simple control scheme in which, at any given time or force, the firing rate value of earlier-recruited motor units is greater than that of later-recruited motor units. This hierarchical control scheme describes a mechanism that provides an effective economy of force generation for the earlier-recruited lower force-twitch motor units, and reduces the fatigue of later-recruited higher force-twitch motor units—both characteristics being well suited for generating and sustaining force during the fight-or-flight response.


2002 ◽  
Vol 88 (4) ◽  
pp. 1867-1879 ◽  
Author(s):  
J. F. Prather ◽  
B. D. Clark ◽  
T. C. Cope

The aim of this study was to investigate whether activation of spinal motoneurons by sensory afferents of the caudal cutaneous sural (CCS) nerve evokes an atypical motor control scheme. In this scheme, motor units that contract fast and forcefully are driven by CCS afferents to fire faster than motor units that contract more slowly and weakly. This is the opposite of the scheme described by the size principle. Earlier studies from this lab do not support the atypical scheme and instead demonstrate that both CCS and muscle stretch recruit motor units according to the size principle. The latter finding may indicate that CCS and muscle-stretch inputs have similar functional organizations or that comparison of recruitment sequence was simply unable to resolve a difference. In the present experiments, we examine this issue using rate modulation as a more sensitive index of motoneuron activation than recruitment. Quantification of the firing output generated by these two inputs in the same pairs of motoneurons enabled direct comparison of the functional arrangements of CCS versus muscle-stretch inputs across the pool of medial gastrocnemius (MG) motoneurons. No systematic difference was observed in the rate modulation produced by CCS versus muscle-stretch inputs for 35 pairs of MG motoneurons. For the subset of 24 motoneuron pairs exhibiting linear co-modulation of firing rate ( r > 0.5) in response to both CCS and muscle inputs, the slopes of the regression lines were statistically indistinguishable between the two inputs. For individual motoneuron pairs, small differences in slope between inputs were not related to differences in conduction velocity (CV), recruitment order, or, for a small sample, differences in motor unit force. We conclude that an atypical motor control scheme involving selective activation of typically less excitable motoneurons, if it does occur during normal movement, is not an obligatory consequence of activation by sural nerve afferents. On average and for both muscle-stretch and skin-pinch inputs, the motoneuron with the faster CV in the pair tended to be driven to fire at slightly but significantly faster firing rates. Computer simulations based in part on frequency-current relations measured directly from motoneurons revealed that properties intrinsic to motoneurons are sufficient to account for the higher firing rates of the faster CV motoneuron in a pair.


2002 ◽  
Vol 88 (2) ◽  
pp. 751-760 ◽  
Author(s):  
I. Phanachet ◽  
T. Whittle ◽  
K. Wanigaratne ◽  
G. M. Murray

The precise function of the inferior head of the human lateral pterygoid muscle (IHLP) is unclear. The aim of this study was to clarify the normal function of the IHLP. The hypothesis was that an important function of the IHLP is the generation and fine control of horizontal (i.e., anteroposterior and mediolateral) jaw movements. The activities of 50 single motor units (SMUs) were recorded from IHLP (14 subjects) during two- or three-step contralateral movement ( n = 36) and/or protrusion ( n = 33). Most recording sites were identified by computer tomography. There was a statistically significant overall increase in firing rate as the magnitude of jaw displacement increased between the holding phases (range of increments: 0.3–1.6 mm). The firing rates during the dynamic phases for each unit were significantly greater than those during the previous holding phases but less than those during the subsequent holding phases. For the contralateral step task at the intermediate rate, the cross-correlation coefficients between jaw displacement in the mediolateral axis and the mean firing rate of each unit ranged from r = 0.29 to 0.77; mean ± SD; r = 0.49 ± 0.13 (protrusive step task: r = 0.12–0.74, r = 0.44 ± 0.14 for correlation with anterior–posterior axis). The correlation coefficients at the fast rate during the contralateral step task and the protrusive step task were significantly higher than those at the slow rate. The firing rate change of the SMUs per unit displacement between holding phases was significantly greater for the lower-threshold than for the higher-threshold units during contralateral movement and protrusion. After dividing IHLP into four regions, the SMUs recorded in the superior part exhibited significantly greater mean firing rate changes per unit displacement during protrusion than for the SMUs recorded in the inferior part. Significantly fewer units were related to the protrusive task in the superior–medial part. These data support previously proposed notions of functional heterogeneity within IHLP. The present findings provide further evidence for an involvement of the IHLP in the generation and fine control of horizontal jaw movements.


1993 ◽  
Vol 69 (3) ◽  
pp. 943-952 ◽  
Author(s):  
R. R. Carter ◽  
P. E. Crago ◽  
P. H. Gorman

1. We investigated the role of stretch reflexes in controlling two antagonist muscles acting at the interphalangeal joint in the normal human thumb. Reflex action was compared when either muscle contracted alone and during cocontraction. 2. The total torque of the flexor pollicis longus (FPL) and extensor pollicis longus (EPL) muscles was measured in response to an externally imposed extension of the interphalangeal joint. The initial joint angle and the amplitude of the extension were constant in all experiments, and the preload of the active muscle(s) was varied. Joint torque was measured at the peak of short-latency stretch reflex action during contraction of the FPL alone, contraction of the EPL alone, and during cocontraction. Incremental joint stiffness was calculated as the change in torque divided by the change in angle. 3. Incremental stiffness increased in proportion to the preload torque during single muscle contractions of either the FPL (lengthening disturbances) or the EPL (shortening disturbances). Thus stiffness was not regulated to a constant value in the face of varying loads for either single muscle stretch or release. 4. Incremental stiffness varied across the range of cocontraction levels while the net torque was maintained at approximately 0. Thus net torque alone did not determine the stiffness during cocontraction. 5. The contributions of each muscle to the net intrinsic torque during cocontraction were estimated by scaling the individual muscles' responses so that their sum gave the best fit (in a least-squares sense) to the cocontraction torque before reflex action. The solution is unique because the individual torques have opposite signs, but the stiffnesses add. This gave estimates of the initial torques of both muscles during cocontraction. 6. The contributions of the two muscles during cocontraction were used to estimate the active joint stiffness that would be expected if the two muscles were activated independently to the same levels as in the cocontraction trials. The stiffness measured at the peak of stretch reflex action during cocontraction trials differed from the sum of the stiffnesses of the two muscles when they were contracting alone. At low cocontraction levels, the measured stiffness was less than expected on the basis of summation of the action of the two muscles, whereas at high cocontraction levels, the measured stiffness was greater than expected. This demonstrates that there is nonlinear stretch reflex interaction. That is, reflex action for a pair of antagonists is not simply the linear sum of the reflex actions of the two muscles acting independently.(ABSTRACT TRUNCATED AT 400 WORDS)


2011 ◽  
Vol 105 (1) ◽  
pp. 380-387 ◽  
Author(s):  
Christopher M. Laine ◽  
E. Fiona Bailey

The tongue plays a key role in various volitional and automatic functions such as swallowing, maintenance of airway patency, and speech. Precisely how hypoglossal motor neurons, which control the tongue, receive and process their often concurrent input drives is a subject of ongoing research. We investigated common synaptic input to the hypoglossal motor nucleus by measuring the coordination of spike timing, firing rate, and oscillatory activity across motor units recorded from unilateral (i.e., within a belly) or bilateral (i.e., across both bellies) locations within the genioglossus (GG), the primary protruder muscle of the tongue. Simultaneously recorded pairs of motor units were obtained from 14 healthy adult volunteers using tungsten microelectrodes inserted percutaneously into the GG while the subjects were engaged in volitional tongue protrusion or rest breathing. Bilateral motor unit pairs showed concurrent low frequency alterations in firing rate (common drive) with no significant difference between tasks. Unilateral motor unit pairs showed significantly stronger common drive in the protrusion task compared with rest breathing, as well as higher indices of synchronous spiking (short-term synchrony). Common oscillatory input was assessed using coherence analysis and was observed in all conditions for frequencies up to ∼5 Hz. Coherence at frequencies up to ∼10 Hz was strongest in motor unit pairs recorded from the same GG belly in tongue protrusion. Taken together, our results suggest that cortical drive increases motor unit coordination within but not across GG bellies, while input drive during rest breathing is distributed uniformly to both bellies of the muscle.


2019 ◽  
Vol 40 (09) ◽  
pp. 555-562 ◽  
Author(s):  
Pedro Fatela ◽  
Goncalo V. Mendonca ◽  
António Prieto Veloso ◽  
Janne Avela ◽  
Pedro Mil-Homens

AbstractWe aimed to determine whether blood flow restriction (BFR) alters the characteristics of individual motor units during low-intensity (LI) exercise. Eight men (26.0±3.8 yrs) performed 5 sets of 15 knee extensions at 20% of one-repetition maximum (with and without BFR). Maximal isometric voluntary contractions (MVC) were performed before and after exercise to quantify force decrement. Submaximal isometric voluntary contractions were additionally performed for 18 s, matching trapezoidal target-force trajectories at 40% pre-MVC. EMG activity was recorded from the vastus lateralis muscle. Then, signals were decomposed to extract motor unit recruitment threshold, firing rates and action potential amplitudes (MUAP). Force decrement was only seen after LI BFR exercise (–20.5%; p<0.05). LI BFR exercise also induced greater decrements in the linear slope coefficient of the regression lines between motor unit recruitment threshold and firing rate (BFR: –165.1±120.4 vs. non-BFR: –44.4±33.1%, p<0.05). Finally, there was a notable shift towards higher values of firing rate and MUAP amplitude post-LI BFR exercise. Taken together, our data indicate that LI BFR exercise increases the activity of motor units with higher MUAP amplitude. They also indicate that motor units with similar MUAP amplitudes become activated at higher firing rates post-LI BFR exercise.


1996 ◽  
Vol 75 (1) ◽  
pp. 38-50 ◽  
Author(s):  
K. E. Tansey ◽  
B. R. Botterman

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.


2005 ◽  
Vol 94 (2) ◽  
pp. 919-927 ◽  
Author(s):  
Mary Kay Floeter ◽  
Ping Zhai ◽  
Rajiv Saigal ◽  
Yongkyun Kim ◽  
Jeffrey Statland

Patients with corticospinal tract dysfunction have slow voluntary movements with brisk stretch reflexes and spasticity. Previous studies reported reduced firing rates of motor units during voluntary contraction. To assess whether this firing behavior occurs because motor neurons do not respond normally to excitatory inputs, we studied motor units in patients with primary lateral sclerosis, a degenerative syndrome of progressive spasticity. Firing rates were measured from motor units in the wrist extensor muscles at varying levels of voluntary contraction ≤10% maximal force. At each force level, the firing rate was measured with and without added muscle vibration, a maneuver that repetitively activates muscle spindles. In motor units from age-matched control subjects, the firing rate increased with successively stronger contractions as well as with the addition of vibration at each force level. In patients with primary lateral sclerosis, motor-unit firing rates remained stable, or in some cases declined, with progressively stronger contractions or with muscle vibration. We conclude that excitatory inputs produce a blunted response in motor neurons in patients with primary lateral sclerosis compared with age-matched controls. The potential explanations include abnormal activation of voltage-activated channels that produce stable membrane plateaus at low voltages, abnormal recruitment of the motor pool, or tonic inhibition of motor neurons.


2001 ◽  
Vol 85 (4) ◽  
pp. 1777-1781 ◽  
Author(s):  
R. H. Westgaard ◽  
C. J. De Luca

The firing pattern of low-threshold motor units was examined in the human trapezius and first dorsal interosseous (FDI) muscles during slowly augmenting, low-amplitude contractions that were intended to mimic contractile activity in postural muscles. The motor unit activity was detected with a special needle electrode and was analyzed with the assistance of computer algorithms. The surface electromyographic (EMG) signal was recorded. Its root-mean-square (RMS) value was calculated and presented to the subject who used it to regulate the muscle force level. In the trapezius, there was minimal, if any, firing rate modulation of early recruited motor units during slow contractions (≤1% EMGmax/s), and later recruited motor units consistently presented higher peak firing rates. As the force rate of the contraction increased (3% EMGmax/s), the firing rates of the motor units in the trapezius approached an orderly hierarchical pattern with the earliest recruited motor units having the greatest firing rate. In contrast, and as reported previously, the firing rates of all motor units in the FDI always presented the previously reported hierarchical “onion-skin” pattern. We conclude that the low-threshold motor units in the postural trapezius muscle, that is the motor units that are most often called on to activate the muscle in postural activities, have different control features in slow and fast contractions. More detailed analysis revealed that, in the low force-rate contractions of the trapezius, recruitment of new motor units inhibited the firing rate of active motor units, providing an explanation for the depressed firing rate of the low-threshold motor units. We speculate that Renshaw cell inhibition contributes to the observed deviation of the low-threshold motor units from the hierarchical onion-skin pattern.


Author(s):  
Tanner Micah Reece ◽  
Trent J Herda

The primary purpose of the present study is to determine if an organized control scheme exists for the antagonist muscle during steady isometric torque. A secondary focus is to better understand how firing rates of the antagonist muscle changes from a moderate- to higher-contraction intensity. Fourteen subjects performed two submaximal isometric trapezoid muscle actions of the forearm flexors that included a linearly increasing, steady force at both 40% and 70% maximum voluntary contraction, and linearly decreasing segments. Surface electromyographic signals of the biceps and triceps brachii were collected and decomposed into constituent motor unit action potential trains. Motor unit firing rate vs. recruitment threshold, motor unit action potential amplitude vs. recruitment threshold, and motor unit firing rate vs. action potential amplitude relationships of the biceps brachii (agonist) and triceps brachii (antagonist) muscles were analyzed. Moderate- to-strong relationships (|r| ³ 0.69) were present for the agonist and antagonist muscles for each relationship with no differences between muscles (p = 0.716, 0.428, 0.182). The y-intercepts of the motor unit firing rate vs. recruitment threshold relationship of the antagonist did not increase from 40% to 70% maximal voluntary contractions (p = 0.96), unlike for the agonist (p = 0.009). The antagonist muscle exhibits a similar motor unit control scheme to the agonist. Unlike the agonist, however, the firing rates of the antagonist did not increase with increasing intensity. Future research should investigate how antagonist firing rates adapt to resistance training and changes in antagonist firing rates in the absence of peripheral feedback.


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