Motor unit recruitment during vertebrate locomotion

AbstractVertebrate skeletal muscles act across joints and produce segmental accelerations and therefore animal movement when they contract. Different muscles and different motor units vary in their mechanical contractile properties. Early studies on motor unit recruitment demonstrated orderly recruitment of motor units from the slowest to the fastest during a graded contraction. However, many subsequent studies illustrate conditions when alternative recruitment strategies may exist. Motor unit recruitment during locomotion is thus multifactorial and more complex than typically thought.Different types of motor unit vary in their mechanical properties, including rates of force activation and deactivation, maximum unloaded shortening velocities and the shortening velocities at which maximum mechanical power output and maximum mechanical efficiency occur. In short, it would make mechanical sense to perform fast activities with the faster motor units and slow activities with the slower motor units. However, determining patterns of motor unit recruitment during locomotion has presented experimental challenges.Comparisons between distinct muscles have shown that fast fish swimming and the cat paw shake are activities which employ predominantly the fast and not the slower muscle. Glycogen depletion studies have showed that jumping in the bushbaby uses fast without slow motor units within the vastus lateralis and gastrocnemius muscles. Studies in man show that differential recruitment of the different types of muscle fibre occurs at different times within each running stride. It is suggested that vertebrates may have a strategy of recruiting the motor units that are most mechanically suited for the different locomotor demands. However, we have much to learn about motor recruitment patterns during locomotion.

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Task-dependent recruitment across ankle extensor muscles and between mechanical demands is driven by the metabolic cost of muscle contraction

Journal of The Royal Society Interface ◽

10.1098/rsif.2020.0765 ◽

2021 ◽

Vol 18 (174) ◽

pp. 20200765

Author(s):

Adrian K. M. Lai ◽

Taylor J. M. Dick ◽

Andrew A. Biewener ◽

James M. Wakeling

Keyword(s):

Muscle Contraction ◽

Motor Unit ◽

Body Movement ◽

Metabolic Cost ◽

Motor Units ◽

Mechanical Efficiency ◽

Motor Unit Recruitment ◽

Medial Gastrocnemius ◽

Range Of Movement ◽

Wide Range

The nervous system is faced with numerous strategies for recruiting a large number of motor units within and among muscle synergists to produce and control body movement. This is challenging, considering multiple combinations of motor unit recruitment may result in the same movement. Yet vertebrates are capable of performing a wide range of movement tasks with different mechanical demands. In this study, we used an experimental human cycling paradigm and musculoskeletal simulations to test the theory that a strategy of prioritizing the minimization of the metabolic cost of muscle contraction, which improves mechanical efficiency, governs the recruitment of motor units within a muscle and the coordination among synergist muscles within the limb. Our results support our hypothesis, for which measured muscle activity and model-predicted muscle forces in soleus—the slower but stronger ankle plantarflexor—is favoured over the weaker but faster medial gastrocnemius (MG) to produce plantarflexor force to meet increased load demands. However, for faster-contracting speeds induced by faster-pedalling cadence, the faster MG is favoured. Similar recruitment patterns were observed for the slow and fast fibres within each muscle. By contrast, a commonly used modelling strategy that minimizes muscle excitations failed to predict force sharing and known physiological recruitment strategies, such as orderly motor unit recruitment. Our findings illustrate that this common strategy for recruiting motor units within muscles and coordination between muscles can explain the control of the plantarflexor muscles across a range of mechanical demands.

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Motor unit territories supplied by primary branches of the phrenic nerve

Journal of Applied Physiology ◽

10.1152/jappl.1989.66.1.61 ◽

1989 ◽

Vol 66 (1) ◽

pp. 61-71 ◽

Cited By ~ 30

Author(s):

C. G. Hammond ◽

D. C. Gordon ◽

J. T. Fisher ◽

F. J. Richmond

Keyword(s):

Motor Unit ◽

Phrenic Nerve ◽

Motor Units ◽

Glycogen Depletion ◽

Precise Analysis ◽

The Central Nervous System ◽

Evoked Activity ◽

Crural Diaphragm ◽

Emg Electrodes ◽

Stimulation Of

Recent studies have demonstrated that, under certain circumstances, the diaphragm does not contract as a homogeneous unit. These observations suggest that motor units may not be randomly distributed throughout the muscle but confined to localized subvolumes. In the present study, electromyographic (EMG) and glycogen depletion methods were combined to investigate the organization of motor units supplied by the primary branches of the phrenic nerve in the cat. Four primary branches are generally present, one branch to the crus and three branches to the sternocostal region. The gross motor-unit territory of each of the four phrenic primary branches was determined by stimulating each nerve separately, while recording from nine EMG electrodes distributed over the hemidiaphragm. Stimulation of the crural branch evoked activity in the ipsilateral crus, whereas stimulation of each of the remaining branches evoked activity in discrete but overlapping areas of the sternocostal diaphragm. A more precise analysis of the distribution and borders of the motor territories was obtained by mapping regions depleted of muscle glycogen due to stimulation of each primary branch for 90 min. Glycogen depletion results closely matched the EMG findings of a localized distribution of motor units served by single primary branches. Stimulation of the crural branch typically caused depletion of the ipsilateral crus, whereas the sternocostal branches each served a striplike compartment. In the majority of cases, the borders of the sternocostal compartments were relatively abrupt and consisted of a 1- to 2-mm transition zone of depleted and nondepleted fibers. These studies demonstrate that motor unit territories of the primary branches of the phrenic nerve are highly delineated. This compartmentalization provides the central nervous system with the potential for a more precise regional motor control of costal and crural diaphragm than previously suspected.

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Determining patterns of motor recruitment during locomotion

Journal of Experimental Biology ◽

10.1242/jeb.205.3.359 ◽

2002 ◽

Vol 205 (3) ◽

pp. 359-369 ◽

Cited By ~ 1

Author(s):

James M. Wakeling ◽

Motoshi Kaya ◽

Genevieve K. Temple ◽

Ian A. Johnston ◽

Walter Herzog

Keyword(s):

Motor Unit ◽

Frequency Band ◽

Fibre Type ◽

Low Frequency ◽

Motor Units ◽

Motor Unit Recruitment ◽

Medial Gastrocnemius ◽

Fibre Types ◽

Myoelectric Signals ◽

Frequency Bands

SUMMARY Motor units are the functional units of muscle contraction in vertebrates. Each motor unit comprises muscle fibres of a particular fibre type and can be considered as fast or slow depending on its fibre-type composition. Motor units are typically recruited in a set order, from slow to fast, in response to the force requirements from the muscle. The anatomical separation of fast and slow muscle in fish permits direct recordings from these two fibre types. The frequency spectra from different slow and fast myotomal muscles were measured in the rainbow trout Oncorhynchus mykiss. These two muscle fibre types generated distinct low and high myoelectric frequency bands. The cat paw-shake is an activity that recruits mainly fast muscle. This study showed that the myoelectric signal from the medial gastrocnemius of the cat was concentrated in a high frequency band during paw-shake behaviour. During slow walking, the slow motor units of the medial gastrocnemius are also recruited, and this appeared as increased muscle activity within a low frequency band. Therefore, high and low frequency bands could be distinguished in the myoelectric signals from the cat medial gastrocnemius and probably corresponded, respectively, to fast and slow motor unit recruitment. Myoelectric signals are resolved into time/frequency space using wavelets to demonstrate how patterns of motor unit recruitment can be determined for a range of locomotor activities.

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Contributions of motor-unit recruitment and rate modulation of compensation for muscle yielding

Journal of Neurophysiology ◽

10.1152/jn.1982.47.5.797 ◽

1982 ◽

Vol 47 (5) ◽

pp. 797-809 ◽

Cited By ~ 13

Author(s):

P. J. Cordo ◽

W. Z. Rymer

Keyword(s):

Motor Unit ◽

Stretch Reflex ◽

Muscle Force ◽

Motor Units ◽

Muscle Stiffness ◽

Motor Unit Recruitment ◽

Reflex Response ◽

Rate Modulation ◽

Stimulus Rate ◽

Wide Range

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

Journal of Neurophysiology ◽

10.1152/jn.00537.2005 ◽

2005 ◽

Vol 94 (5) ◽

pp. 3126-3133 ◽

Cited By ~ 37

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.

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Blood Flow Restriction Alters Motor Unit Behavior During Resistance Exercise

International Journal of Sports Medicine ◽

10.1055/a-0888-8816 ◽

2019 ◽

Vol 40 (09) ◽

pp. 555-562 ◽

Cited By ~ 1

Author(s):

Pedro Fatela ◽

Goncalo V. Mendonca ◽

António Prieto Veloso ◽

Janne Avela ◽

Pedro Mil-Homens

Keyword(s):

Blood Flow ◽

Firing Rate ◽

Motor Unit ◽

Motor Units ◽

Blood Flow Restriction ◽

Motor Unit Recruitment ◽

Recruitment Threshold ◽

Firing Rates ◽

Flow Restriction ◽

Voluntary Contractions

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.

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Hip position and sex differences in motor unit firing patterns of the vastus medialis and vastus medialis oblique in healthy individuals

Journal of Applied Physiology ◽

10.1152/japplphysiol.00702.2017 ◽

2018 ◽

Vol 124 (6) ◽

pp. 1438-1446 ◽

Cited By ~ 8

Author(s):

Yi-Ling Peng ◽

Matthew S. Tenan ◽

Lisa Griffin

Keyword(s):

Sex Differences ◽

Motor Unit ◽

Knee Pain ◽

Motor Units ◽

Motor Unit Recruitment ◽

Vastus Medialis ◽

Firing Patterns ◽

Fine Wire ◽

Motor Unit Firing ◽

Hip Rotation

Weakness of the vastus medialis oblique (VMO) has been proposed to explain the high prevalence of knee pain in female subjects. Clinicians commonly use exercises in an attempt to preferentially activate the VMO. Recently, our group found evidence to support clinical theory that the VMO is neurologically distinct from the vastus medialis (VM). However, the ability to voluntarily activate these muscle subsections is still disputed. The aim of this study was to determine if VM and VMO activation varies between sexes and if control of the two muscles is different between rehabilitation exercises. Thirteen men and 13 women performed isometric straight leg raises in two hip positions, neutral hip rotation and 30 degrees lateral hip rotation. Bipolar intramuscular fine-wire electrodes were inserted into the VM and VMO to obtain motor unit recruitment thresholds and initial firing rates at recruitment. Linear mixed models and Tukey post hoc tests were used to assess significant differences in 654 motor units. Women demonstrated faster motor unit firing rate at recruitment, 1.18 ± 0.56 Hz higher than men. Motor units fired 0.47 ± 0.19 Hz faster during neutral hip rotation compared with lateral hip rotation. The VMO motor units were recruited 2.92 ± 1.28% earlier than the VM. All motor units were recruited 3.74 ± 1.27% earlier during neutral hip rotation than lateral hip rotation. Thus the VM and the VMO can be activated differentially, and their motor unit recruitment properties are affected by sex and hip position. NEW & NOTEWORTHY This is the first study to reveal differential activation of the vastus medialis oblique from the vastus medialis in clinical exercise protocols. Our research group used fine-wire electrodes to examine EMG signals of the vastus medialis oblique and vastus medialis to avoid possible cross talk. We also consider the effect of sex on motor unit firing patterns because of higher prevalence of knee pain in women, and yet few studies evaluating the sex differences in neuromuscular control.

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Probabilities Associated With Counting Average Motor Unit Firing Rates in Active Human Muscle

Canadian Journal of Applied Physiology ◽

10.1139/h98-006 ◽

1998 ◽

Vol 23 (1) ◽

pp. 87-94 ◽

Cited By ~ 8

Author(s):

Christopher Rich ◽

George L. O′Brien ◽

Enzo Cafarelli

Keyword(s):

Motor Unit ◽

Vastus Lateralis ◽

Small Diameter ◽

Motor Units ◽

Voluntary Contraction ◽

Human Muscle ◽

Cell Diameter ◽

Unit Recording ◽

Firing Rates ◽

Motor Unit Firing

Motor unit firing rates in human muscle can be determined from recordings made with small-diameter microelectrodes inserted directly into the muscle during voluntary contraction. Frequently, these counts are pooled to give an average motor unit firing rate under a given set of conditions. Since the fibers of one motor unit are dispersed among the cells of several others, it is conceivable that discharge rates can be measured in more than one cell from the same unit. If this occurred frequently, the distribution of firing rates could be influenced by those from units counted more than once. Based on literature values, we made the following assumptions: vastus lateralis contains approximately 300 motor units, with an average innervation ratio of 1500. Muscle cell diameter is about 50 to 100 μm and cells are randomly distributed over a motor unit territory of 10 μm diameter. The recording range of a microelectrode is about 600 μm. Given the distribution of cells normally found in whole human muscle, the probability of recording from two or more cells of the same motor unit at 50% MVC follows a Poisson distribution with a mean of 0.44. This model suggests that although there is a low probability of some duplication in this technique, the extent to which it influences the distribution of average motor unit firing rates is minimal over the entire range of forces produced by vastus lateralis. Key words: probability, motor unit, single unit recording, human muscle, rate coding

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Vastus lateralis surface and single motor unit EMG following submaximal shortening and lengthening contractions

Applied Physiology Nutrition and Metabolism ◽

10.1139/h08-092 ◽

2008 ◽

Vol 33 (6) ◽

pp. 1086-1095 ◽

Cited By ~ 25

Author(s):

Teatske M. Altenburg ◽

Cornelis J. de Ruiter ◽

Peter W.L. Verdijk ◽

Willem van Mechelen ◽

Arnold de Haan

Keyword(s):

Motor Unit ◽

Muscle Activation ◽

Discharge Rate ◽

Vastus Lateralis ◽

Motor Units ◽

Voluntary Contraction ◽

Knee Extensors ◽

Single Motor Unit ◽

Discharge Rates ◽

Active Motor

A single shortening contraction reduces the force capacity of muscle fibers, whereas force capacity is enhanced following lengthening. However, how motor unit recruitment and discharge rate (muscle activation) are adapted to such changes in force capacity during submaximal contractions remains unknown. Additionally, there is limited evidence for force enhancement in larger muscles. We therefore investigated lengthening- and shortening-induced changes in activation of the knee extensors. We hypothesized that when the same submaximal torque had to be generated following shortening, muscle activation had to be increased, whereas a lower activation would suffice to produce the same torque following lengthening. Muscle activation following shortening and lengthening (20° at 10°/s) was determined using rectified surface electromyography (rsEMG) in a 1st session (at 10% and 50% maximal voluntary contraction (MVC)) and additionally with EMG of 42 vastus lateralis motor units recorded in a 2nd session (at 4%–47%MVC). rsEMG and motor unit discharge rates following shortening and lengthening were normalized to isometric reference contractions. As expected, normalized rsEMG (1.15 ± 0.19) and discharge rate (1.11 ± 0.09) were higher following shortening (p < 0.05). Following lengthening, normalized rsEMG (0.91 ± 0.10) was, as expected, lower than 1.0 (p < 0.05), but normalized discharge rate (0.99 ± 0.08) was not (p > 0.05). Thus, muscle activation was increased to compensate for a reduced force capacity following shortening by increasing the discharge rate of the active motor units (rate coding). In contrast, following lengthening, rsEMG decreased while the discharge rates of active motor units remained similar, suggesting that derecruitment of units might have occurred.

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