scholarly journals Interfacing Spinal Motor Units in Non-Human Primates Identifies a Principal Neural Component for Force Control Constrained by the Size Principle

2021 ◽  
Author(s):  
Alessandro Del Vecchio ◽  
Rachael H. A. Jones ◽  
Ian S. Schofield ◽  
Thomas M Kinfe ◽  
Jaime Ibáñez ◽  
...  
Keyword(s):  
Motor Unit ◽  
Discharge Rate ◽  
Motor Units ◽  
Rate Of Force Development ◽  
High Rate ◽  
Common Input ◽  
Size Principle ◽  
Flexible Control ◽  
Force Development ◽  
Orderly Fashion

ABSTRACTMotor units convert the last neural code of movement into muscle forces. The classic view of motor unit control is that the central nervous system sends common synaptic inputs to motoneuron pools and that motoneurons respond in an orderly fashion dictated by the size principle. This view however is in contrast with the large number of dimensions observed in motor cortex which may allow individual and flexible control of motor units. Evidence for flexible control of motor units may be obtained by tracking motor units longitudinally during the performance of tasks with some level of behavioural variability. Here we identified and tracked populations of motor units in the brachioradialis muscle of two macaque monkeys during ten sessions spanning over one month during high force isometric contractions with a broad range of rate of force development (1.8 – 38.6 N·m·s-1). During the same sessions we recorded intramuscular EMG signals from 16 arm muscles of both limbs and elicited the full recruitment through neural stimulation of the median and deep radial nerves. We found a very stable recruitment order and discharge characteristics of the motor units over sessions and contraction trials. The small deviations from orderly recruitment were observed between motor units with close recruitment thresholds, and only during high rate of force development. Moreover, we also found that one component explained more than ~50% of the motor unit discharge rate variance, and that the remaining components could be described as a time-shifted version of the first, as it could be predicted from the interplay between the size principle of recruitment and one common input. In conclusion, our results show that motoneurons recruitment is determined by the interplay of the size principle and common input and that this recruitment scheme is not violated over time nor by the speed of the contractions.

scholarly journals Lack of increased rate of force development after strength training is explained by specific neural, not muscular, motor unit adaptations

2021 ◽  
Author(s):  
Alessandro Del Vecchio ◽  
Andrea Casolo ◽  
Jakob Lund Dideriksen ◽  
Per Aagaard ◽  
Francesco Felici ◽  
...  
Keyword(s):  
Strength Training ◽  
Motor Unit ◽  
Discharge Rate ◽  
Force Production ◽  
Population Data ◽  
Motor Units ◽  
Rate Of Force Development ◽  
Force Development ◽  
Maximal Force ◽  
Contraction Speed

While maximal force increases following short-term isometric strength training, the rate of force development (RFD) may remain relatively unaffected. The underlying neural and muscular mechanisms during rapid contractions after strength training are largely unknown. Since strength training increases the neural drive to muscles, it may be hypothesized that there are distinct neural or muscular adaptations determining the change in RFD independently of an increase in maximal force. Therefore, we examined motor unit population data acquired from surface electromyography during the rapid generation of force before and after four weeks of strength training. We observed that strength training did not change the RFD because it did not influence the number of motor units recruited per second or their initial discharge rate during rapid contractions. While strength training did not change motoneuron behaviour in the force increase phase of rapid contractions, it increased the discharge rate of motoneurons (by ~4 spikes/s) when reaching the plateau phase (~150 ms) of the rapid contractions, determining an increase in maximal force production. Computer simulations with a motor unit model that included neural and muscular properties, closely matched the experimental observations and demonstrated that the lack of change in RFD following training is primarily mediated by an unchanged maximal recruitment speed of motoneurons. These results demonstrate that maximal force and contraction speed are determined by different adaptations in motoneuron behaviour following strength training and indicate that increases in the recruitment speed of motoneurons are required to evoke training-induced increases in RFD.

scholarly journals Neural and muscular determinants of maximal rate of force development

2020 ◽  
Vol 123 (1) ◽  
pp. 149-157 ◽  
Author(s):  
Jakob L. Dideriksen ◽  
Alessandro Del Vecchio ◽  
Dario Farina
Keyword(s):  
Motor Unit ◽  
Maximum Rate ◽  
Rapid Development ◽  
Motor Units ◽  
Rate Of Force Development ◽  
Time Range ◽  
Limiting Factor ◽  
Force Development ◽  
Twitch Contraction ◽  
Discharge Rates

The ability to produce rapid forces requires quick motor unit recruitment, high motor unit discharge rates, and fast motor unit force twitches. The relative importance of these parameters for maximum rate of force development (RFD), however, is poorly understood. In this study, we systematically investigated these relationships using a computational model of motor unit pool activity and force. Across simulations, neural and muscular properties were systematically varied in experimentally observed ranges. Motor units were recruited over an interval starting from contraction onset (range: 22–233 ms). Upon recruitment, discharge rates declined from an initial rate (range: 89–212 pulses per second), with varying likelihood of doublet (interspike interval of 3 ms; range: 0–50%). Finally, muscular adaptations were modeled by changing average twitch contraction time (range: 42–78 ms). Spectral analysis showed that the effective neural drive to the simulated muscle had smaller bandwidths than the average motor unit twitch, indicating that the bandwidth of the motor output, and thus the capacity for explosive force, was limited mainly by neural properties. The simulated RFD increased by 1,050 ± 281% maximal voluntary contraction force per second from the longest to the shortest recruitment interval. This effect was more than fourfold higher than the effect of increasing the initial discharge rate, more than fivefold higher than the effect of increasing the chance of doublets, and more than sixfold higher than the effect of decreasing twitch contraction times. The simulated results suggest that the physiological variation of the rate by which motor units are recruited during ballistic contractions is the main determinant for the variability in RFD across individuals. NEW & NOTEWORTHY An important limitation of human performance is the ability to generate explosive movements by means of rapid development of muscle force. The physiological determinants of this ability, however, are poorly understood. In this study, we show using extensive simulations that the rate by which motor units are recruited is the main limiting factor for maximum rate of force development.

scholarly journals Recruitment of motor units in two fascicles of the semispinalis cervicis muscle

2012 ◽  
Vol 107 (11) ◽  
pp. 3078-3085 ◽  
Author(s):  
Jochen Schomacher ◽  
Jakob Lund Dideriksen ◽  
Dario Farina ◽  
Deborah Falla
Keyword(s):  
Motor Unit ◽  
Discharge Rate ◽  
Maximum Voluntary Contraction ◽  
Motor Units ◽  
Voluntary Contraction ◽  
Common Input ◽  
Motor Unit Synchronization ◽  
Motor Unit Action ◽  
Input Strength ◽  
Individual Motor

This study investigated the behavior of motor units in the semispinalis cervicis muscle. Intramuscular EMG recordings were obtained unilaterally at levels C2 and C5 in 15 healthy volunteers (8 men, 7 women) who performed isometric neck extensions at 5%, 10%, and 20% of the maximal force [maximum voluntary contraction (MVC)] for 2 min each and linearly increasing force contractions from 0 to 30% MVC over 3 s. Individual motor unit action potentials were identified. The discharge rate and interspike interval variability of the motor units in the two locations did not differ. However, the recruitment threshold of motor units detected at C2 ( n = 16, mean ± SD: 10.3 ± 6.0% MVC) was greater than that of motor units detected at C5 ( n = 92, 6.9 ± 4.3% MVC) ( P < 0.01). A significant level of short-term synchronization was identified in 246 of 307 motor unit pairs when computed within one spinal level but only in 28 of 110 pairs of motor units between the two levels. The common input strength, which quantifies motor unit synchronization, was greater for pairs within one level (0.47 ± 0.32) compared with pairs between levels (0.09 ± 0.07) ( P < 0.05). In a second experiment on eight healthy subjects, interference EMG was recorded from the same locations during a linearly increasing force contraction from 0 to 40% MVC and showed significantly greater EMG amplitude at C5 than at C2. In conclusion, synaptic input is distributed partly independently and nonuniformly to different fascicles of the semispinalis cervicis muscle.

scholarly journals The relative strength of common synaptic input to motor neurons is not a determinant of the maximal rate of force development in humans

2019 ◽  
Vol 127 (1) ◽  
pp. 205-214 ◽  
Author(s):  
Alessandro Del Vecchio ◽  
Deborah Falla ◽  
Francesco Felici ◽  
Dario Farina
Keyword(s):  
Motor Unit ◽  
Motor Neurons ◽  
Synaptic Input ◽  
Discharge Rate ◽  
Rate Of Force Development ◽  
Force Generation ◽  
Unit Discharge ◽  
Force Development ◽  
Motor Unit Synchronization ◽  
Motor Unit Discharge

Correlation between motor unit discharge times, often referred to as motor unit synchronization, is determined by common synaptic input to motor neurons. Although it has been largely speculated that synchronization should influence the rate of force development, the association between the degree of motor unit synchronization and rapid force generation has not been determined. In this study, we examined this association with both simulations and experimental motor unit recordings. The analysis of experimental motor unit discharges from the tibialis anterior muscle of 20 healthy individuals during rapid isometric contractions revealed that the average motor unit discharge rate was associated with the rate of force development. Moreover, the extent of motor unit synchronization was entirely determined by the average motor unit discharge rate ( R > 0.7, P < 0.0001). The simulation model demonstrated that the relative proportion of common synaptic input received by motor neurons, which determines motor unit synchronization, does not influence the rate of force development ( R = 0.03, P > 0.05). Nonetheless, the estimates of correlation between motor unit spike trains were significantly correlated with the rate of force generation ( R > 0.8, P < 0.0001). These results indicate that the average motor unit discharge rate, but not the degree of motor unit synchronization, contributes to most of the variance of human contractile speed among individuals. In addition, estimates of correlation between motor unit discharge times depend strongly on the number of identified motor units and therefore are not indicative of the strength of common input. NEW & NOTEWORTHY It is commonly assumed that motor unit synchronization has an impact on the rate of force development of a muscle. Here we present computer simulations and experimental data of human tibialis anterior motor units during rapid contractions that show that motor unit synchronization is not a determinant of the rate of force production. This conclusion clarifies the neural determinants of rapid force generation.

scholarly journals Motor unit contributions to activation reduction and torque steadiness following active lengthening: a study of residual torque enhancement

2020 ◽  
Vol 123 (6) ◽  
pp. 2209-2216 ◽  
Author(s):  
Jennifer M. Jakobi ◽  
Samantha L. Kuzyk ◽  
Chris J. McNeil ◽  
Brian H. Dalton ◽  
Geoffrey A. Power
Keyword(s):  
Motor Unit ◽  
Discharge Rate ◽  
Motor Units ◽  
Electromyographic Activity ◽  
Torque Capacity ◽  
Active Motor ◽  
Motor Neuron Pool ◽  
Acute Condition ◽  
The Impact ◽  
Neuron Pool

Our findings indicate that lower electromyographic activity during the torque-enhanced condition following active lengthening compared with a purely isometric contraction arises from fewer active motor units and a lower discharge rate of those that are active. We used an acute condition of increased torque capacity to induce a decrease in net output of the motor neuron pool during a submaximal task to demonstrate, in humans, the impact of motor unit activity on torque steadiness.

Change in Muscle Fascicle Length Influences the Recruitment and Discharge Rate of Motor Units During Isometric Contractions

2005 ◽  
Vol 94 (5) ◽  
pp. 3126-3133 ◽  
Author(s):  
Benjamin Pasquet ◽  
Alain Carpentier ◽  
Jacques Duchateau
Keyword(s):  
Motor Unit ◽  
Ankle Joint ◽  
Discharge Rate ◽  
Motor Units ◽  
Motor Unit Recruitment ◽  
Isometric Contractions ◽  
Neutral Position ◽  
Proprioceptive Information ◽  
Fascicle Length ◽  
Muscle Fascicle

This study examines the effect of fascicle length change on motor-unit recruitment and discharge rate in the human tibialis anterior (TA) during isometric contractions of various intensities. The torque produced during dorsiflexion and the surface and intramuscular electromyograms (EMGs) from the TA were recorded in eight subjects. The behavior of the same motor unit ( n = 59) was compared at two ankle joint angles (+10 and −10° around the ankle neutral position). Muscle fascicle length of the TA was measured noninvasively using ultrasonography recordings. When the ankle angle was moved from 10° plantarflexion to 10° dorsiflexion, the torque produced during maximal voluntary contraction (MVC) was significantly reduced [35.2 ± 3.3 vs. 44.3 ± 4.2 (SD) Nm; P < 0.001] and the average surface EMG increased (0.47 ± 0.08 vs. 0.43 ± 0.06 mV; P < 0.05). At reduced ankle joint angle, muscle fascicle length declined by 12.7% ( P < 0.01) at rest and by 18.9% ( P < 0.001) during MVC. Motor units were activated at a lower recruitment threshold for short compared with long muscle fascicle length, either when expressed in absolute values (2.1 ± 2.5 vs. 3.6 ± 3.7 Nm; P < 0.001) or relative to their respective MVC (5.2 ± 6.1 vs. 8.8 ± 9.0%). Higher discharge rate and additional motor-unit recruitment were observed at a given absolute or relative torque when muscle fascicles were shortened. However, the data indicate that increased rate coding was mainly present at low torque level (<10% MVC), when the muscle-tendon complex was compliant, whereas recruitment of additional motor units played a dominant role at higher torque level and decreased compliance (10–35% MVC). Taken together, the results suggest that the central command is modulated by the afferent proprioceptive information during submaximal contractions performed at different muscle fascicle lengths.

Spike-triggered average torque and muscle fiber conduction velocity of low-threshold motor units following submaximal endurance contractions

2005 ◽  
Vol 98 (4) ◽  
pp. 1495-1502 ◽  
Author(s):  
Dario Farina ◽  
Lars Arendt-Nielsen ◽  
Thomas Graven-Nielsen
Keyword(s):  
Action Potential ◽  
Motor Unit ◽  
Conduction Velocity ◽  
Surface Potential ◽  
Muscle Fiber ◽  
Discharge Rate ◽  
Motor Units ◽  
Muscle Fiber Conduction Velocity ◽  
Sustained Contraction ◽  
Low Threshold

The motor unit twitch torque is modified by sustained contraction, but the association to changes in muscle fiber electrophysiological properties is not fully known. Thus twitch torque, muscle fiber conduction velocity, and action potential properties of single motor units were assessed in 11 subjects following an isometric submaximal contraction of the tibialis anterior muscle until endurance. The volunteers activated a target motor unit at the minimum discharge rate in eight 3-min-long contractions, three before and five after an isometric contraction at 40% of the maximal torque, sustained until endurance. Multichannel surface electromyogram signals and joint torque were averaged with the target motor unit potential as trigger. Discharge rate (mean ± SE, 6.6 ± 0.2 pulses/s) and interpulse interval variability (33.3 ± 7.0%) were not different in the eight contractions. Peak twitch torque and recruitment threshold increased significantly (93 ± 29 and 12 ± 5%, P < 0.05) in the contraction immediately after the endurance task with respect to the preendurance values (0.94 ± 0.26 mN·m and 3.7 ± 0.5% of the maximal torque), whereas time to peak of the twitch torque did not change (74.4 ± 10.1 ms). Muscle fiber conduction velocity decreased and action potential duration increased in the contraction after the endurance (6.3 ± 1.8 and 9.8 ± 1.8%, respectively, P < 0.05; preendurance values, 3.9 ± 0.2 m/s and 11.1 ± 0.8 ms), whereas the surface potential peak-to-peak amplitude did not change (27.1 ± 3.1 μV). There was no significant correlation between the relative changes in muscle fiber conduction velocity or surface potential duration and in peak twitch torque ( R2 = 0.04 and 0.10, respectively). In conclusion, modifications in peak twitch torque of low-threshold motor units with sustained contraction are mainly determined by mechanisms not related to changes in action potential shape and in its propagation velocity.

Motor-unit recruitment in the decerebrate cat: several unit properties are equally good predictors of order

1991 ◽  
Vol 66 (4) ◽  
pp. 1127-1138 ◽  
Author(s):  
T. C. Cope ◽  
B. D. Clark
Keyword(s):  
Motor Unit ◽  
Rank Order ◽  
Motor Units ◽  
Afferent Input ◽  
Medial Gastrocnemius ◽  
Size Principle ◽  
Recruitment Pattern ◽  
Decerebrate Cat ◽  
Recruitment Order ◽  
Stimulation Of

1. Recruitment order was studied in pairs of motor units of the medial gastrocnemius (MG) muscle of decerebrate cats with the use of dual microelectrode recording from intact ventral root filaments. Excitation was provided by stretch of MG, stretch of synergists [lateral gastrocnemius (LG), plantaris (PL), and soleus (SOL) muscles] or electrical stimulation of the caudal cutaneous sural (CCS) nerve. Motor units were characterized by axonal conduction velocity (CV), tetanic tension (Pmax), twitch contraction time (CT), and fatigue index (FI). 2. Consistent with the recruitment pattern described by others, most often in relation to either CV or Pmax, the first unit of a pair to be recruited by MG stretch was typically the one with the lower CV and Pmax, and the higher FI and CT. The proportion of pairs that agreed in rank order of each property and recruitment order was as follows: for CT, 94%; for CV, 87%; for Pmax, 84%; and for FI, 75%. With a single marginal exception (CT vs. FI), no motor-unit property proved to be significantly better than the others at predicting recruitment (G test; P greater than 0.05). 3. In all 11 tested pairs containing one slow (type S) and one fast (type F) unit, the S was more easily recruited by stretch. Type F units divided into groups with high (type FR), low (type FF), and intermediate (type FInt) values for FI were recruited in order from FR to FInt to FF in 8/11 pairs. Thus our findings were similar to earlier demonstrations that recruitment proceeds in order by type. 4. Stretch of MG synergists usually recruited units in the same order as MG stretch. In two S-S pairs, recruitment order was switched with synergist stretch. 5. Stimulation of the CCS nerve was generally excitatory to the MG units sampled. Most unit pairs were recruited by CCS stimulation in the same order as by MG stretch, but, for 6 of 39 pairs, CCS stimulation switched the order produced by stretch. Thus, whereas sural afferent input can preferentially excite some units over others as suggested by Kanda et al., that effect is not widespread or selective for unit type under these conditions. 6. Assuming that all MG motor units cooperate as a single functional pool in homonymous stretch reflexes, we support others in concluding that a motoneuron's recruitment threshold is not strictly determined by its size. However, our data do not distinguish other schemes that predict recruitment order more accurately than the size principle.(ABSTRACT TRUNCATED AT 400 WORDS)

Cutaneous stimulation fails to alter motor unit recruitment in the decerebrate cat

1993 ◽  
Vol 70 (4) ◽  
pp. 1433-1439 ◽  
Author(s):  
B. D. Clark ◽  
S. M. Dacko ◽  
T. C. Cope
Keyword(s):  
Motor Unit ◽  
Conduction Velocity ◽  
Motor Units ◽  
Firing Frequency ◽  
Medial Gastrocnemius ◽  
Electromyographic Activity ◽  
Size Principle ◽  
Decerebrate Cat ◽  
Slow Twitch ◽  
Recruitment Order

1. An attempt was made to repeat the observation that cutaneous input to the cat medial gastrocnemius (MG) muscle sometimes had the differential effect of inhibiting motoneurons with slow axonal conduction velocity while simultaneously exciting others with fast conduction velocity. Dual microelectrode recording from intact ventral root filaments was used to study the effects of cutaneous inputs on recruitment order and on firing frequency of physiologically characterized MG motor units in decerebrate cats. Motor responses to pinch of the skin over the lateral surface of the ankle as well as electrical stimulation of the caudal cutaneous sural (CCS) nerve were contrasted with the responses to static muscle stretch as well as muscle vibration. 2. In contrast to the prediction, recruitment order in pairwise tests was the same for skin pinch or CCS stimulation as it was for MG stretch or vibration in all 32 tested pairs of motor units. This sample included seven pairs comprising one slow-twitch (S) and one fast-twitch motor unit, where the predicted reversal of recruitment should have been most apparent. Regardless of the source of excitation, recruitment of motor units of the MG was consistent with Henneman's size principle in approximately 90% of trials. 3. Skin pinch increased the firing rate of 30 of 32 individual motor units previously activated by stretch or vibration, including 7 slow-twitch units. In the remaining two units, skin pinch transiently (100-400 ms) slowed the firing of an S unit in 11 of 13 vibration + pinch trials. The other unit (type unknown) showed one or two retarded spikes in each of four vibration + pinch trials. In three S units, including the lone inhibitable unit and two others that were only excited by skin pinch, there was a significant positive rank correlation between change in unit firing frequency and change in soleus integrated electromyographic activity.(ABSTRACT TRUNCATED AT 400 WORDS)

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