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AAEM minimonograph #3: motor unit recruitment.

Motor unit recruitment is the process by which different motor units are activated to produce a given level and type of muscle contraction. At minimal levels of muscle contraction (innervation), muscle force is graded by changes in firing rate (rate coding) of individual motoneurons (MNs). At higher levels of innervation, recruitment is accomplished by the addition of different motor units firing at or above physiologic tremor rate. During slowly graded and ballistic increases in force, motor units are recruited in rank order of their size. In addition to MN soma diameter, other factors contribute to the selectivity of MN activation. For la afferent MN activation in the cat, synaptic density and efficacy as well as specific membrane resistance are also rank ordered for slow, fatigue resistant, and fast fatigue motor units with slow motor units recruited first. The central drive for motor unit activation is distributed to all the MNs of the pool serving a given muscle. Size-structure organization of the MN pool determines the order of recruitment and how MNs interact with each other. Disorders of the motor unit affect recruitment. A method for the clinical electromyographic assessment of recruitment is suggested. Assessment is made at three levels of innervation: minimal contraction for onset and recruitment firing rates; moderate contraction required to maintain the limb against gravity for the maximum number of motor units, their firing rates, and motor unit spikes/s; maximal voluntary contraction (MVC) for detection of high threshold enlarged motor units characteristic of reinnervation and completeness of the interference pattern (IP). Loss of muscle fibers results in early and excessive recruitment at minimal and moderate levels of innervation. Loss of motor units can result in both an increased rate and range of single motor unit firing at all levels of innervation. With reinnervation and enlargement of motor units, firing rates increase significantly and the interference pattern during MVC is incomplete.

Action Potentials↗

Independence of motor unit recruitment and rate modulation during precision force control.

The vertebrate motor system chiefly employs motor unit recruitment and rate coding to modulate muscle force output. In this paper, we studied how the recruitment of new motor units altered the firing rate of already-active motor units during precision force production in the first dorsal interosseous muscle. Six healthy adults performed linearly increasing isometric voluntary contractions while motor unit activity and force output were recorded. After motor unit discharges were identified, motor unit firing rates were calculated before and after the instances of new motor unit recruitment. Three procedures were applied to compute motor unit firing rate, including the mean of a fixed number of inter-spike intervals and the constant width weighted Hanning window filter method, as well as a modified boxcar technique. In contrast to previous reports, the analysis of the firing rates of over 200 motor units revealed that reduction of the active firing rates was not a common mechanism used to accommodate the twitch force produced by the recruitment of a new motor unit. Similarly, during de-recruitment there was no tendency for motor unit firing rates to increase immediately following the cessation of activity in other motor units. Considerable consistency in recruitment behavior was observed during repeated contractions. However, firing rates during repeated contractions demonstrated considerably more fluctuation. It is concluded that the neuromuscular system does not use short-term preferential motor unit disfacilitation to effect precise regulation of muscular force output.

Action Potentials↗

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

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.

Animals↗

Initial motor unit recruitment in patients with spastic hemiplegia.

Lesions of the first motor neuron provoke abnormal voluntary movements. To clarify the central nervous system mechanisms underlying these changes we analyzed the behavior of the first motor unit recruited during a minimal effort tonic contraction of the deltoid and abductor digiti minimi manus muscles in patients with hemiplegia due to cerebrovascular lesions in the distribution of the middle cerebral artery. We compared data from paretic and healthy muscles in the same subject. The onset and recruitment intervals determined for the single motor unit yielded the range of control. The first recruited motor unit had a lower baseline firing rate and the second recruited motor unit potential appeared significantly earlier (p < 0.01) in plegic than in healthy muscles. Both changes affected distal more than proximal locations. Recordings from plegic muscles, particularly at distal locations, also disclosed a lowered range of control. These findings suggest that in hemiplegic patients the central nervous system loses its ability to modulate the frequency of firing during minimal effort voluntary movements so that distal muscles tend to behave like proximal muscles.

Aged↗

Motor unit recruitment during prolonged isometric contractions.

Motor unit recruitment patterns were studied during prolonged isometric contraction using fine wire electrodes. Single motor unit potentials were recorded from the brachial biceps muscle of eight male subjects, during isometric endurance experiments conducted at relative workloads corresponding to 10% and 40% of maximal voluntary contraction (MVC), respectively. The recordings from the 10% MVC experiment demonstrated a characteristic time-dependent recruitment. As the contraction progressed both the mean number of motor unit spikes counted and the mean amplitude of the spikes increased significantly (P < 0.01). This progressive increase in spike activity was the result of a discontinuous process with periods of increasing and decreasing activity. The phenomenon in which newly recruited motor units replace previously active units is termed "motor unit rotation" and appeared to be an important characteristic of motor control during a prolonged low level contraction. In contrast to the 10% MVC experiment, there was no indication of de novo recruitment in the 40% MVC experiment. Near the point of exhaustion a marked change in action potential shape and duration dominated the recordings. These findings demonstrate a conspicuous difference in the patterns of motor unit recruitment during a 10% and a 40% MVC sustained contraction. It is suggested that there is a close relationship between intrinsic muscle properties and central nervous system recruitment strategies which is entirely different in fatiguing high and low level isometric contractions.

Action Potentials↗

Motor unit recruitment during lengthening contractions of human wrist flexors.

The purpose of this study was to revisit the question of recruitment of motor units during lengthening contractions because of conflicting views in the literature on this subject. Motor unit activity was recorded from the flexor carpi radialis muscle of four human subjects to compare the patterns of recruitment during lengthening and isometric contractions. Lengthening contractions were produced either when the subject voluntarily stopped opposing a background load or when an additional load was imposed on the already contracting muscle. In both cases, lengthening of the active muscle was produced at a variety of speeds, from quite slow to "as fast as possible." No differences in recruitment order were observed between isometric and lengthening contractions at any speed of lengthening contraction. It is concluded that all contractions in normal humans recruit motor units in an orderly fashion from small to large, according to the size principle of motor unit recruitment.

Adult↗

Electromyogram power spectra frequencies associated with motor unit recruitment strategies.

The isolated contributions of motor unit recruitment and firing rate variations to the median frequency of the electromyogram's power density spectrum were determined. Orderly stimulation of the cat gastrocnemius motor units via nerve electrodes gave rise to linearly increasing median frequency regardless of the action potential firing rate of the active motor units. Increase in the discharge rate of all the motor units resulted in nearly constant median frequency. It was concluded that the increasing average conduction velocity during motor unit recruitment is the major contributor to variations in the electromyogram median frequency. The possibility of using the median frequency as the index to identify the recruitment control strategies employed by various muscles during increasing force contraction is suggested.

Action Potentials↗

Simulation of motor unit recruitment and microvascular unit perfusion: spatial considerations.

Muscle fiber activity is the principal stimulus for increasing capillary perfusion during exercise. The control elements of perfusion, i.e., microvascular units (MVUs), supply clusters of muscle fibers, whereas the control elements of contraction, i.e., motor units, are composed of fibers widely scattered throughout muscle. The purpose of this study was to examine how the discordant spatial domains of MVUs and motor units could influence the proportion of open capillaries (designated as perfusion) throughout a muscle cross section. A computer model simulated the locations of perfused MVUs in response to the activation of up to 100 motor units in a muscle with 40,000 fibers and a cross-sectional area of 100 mm2. The simulation increased contraction intensity by progressive recruitment of motor units. For each step of motor unit recruitment, the percentage of active fibers and the number of perfused MVUs were determined for several conditions: 1) motor unit fibers widely dispersed and motor unit territories randomly located (which approximates healthy human muscle), 2) regionalized motor unit territories, 3) reversed recruitment order of motor units, 4) densely clustered motor unit fibers, and 5) increased size but decreased number of motor units. The simulations indicated that the widespread dispersion of motor unit fibers facilitates complete capillary (MVU) perfusion of muscle at low levels of activity. The efficacy by which muscle fiber activity induced perfusion was reduced 7- to 14-fold under conditions that decreased the dispersion of active fibers, increased the size of motor units, or reversed the sequence of motor unit recruitment. Such conditions are similar to those that arise in neuromuscular disorders, with aging, or during electrical stimulation of muscle, respectively.

Adult↗

Motor unit recruitment strategy of antagonist muscle pair during linearly increasing contraction.

The motor unit recruitment control strategy of the antagonist thigh muscles was determined during linearly increasing isometric flexion and extension of the knees. The median frequency (MF) of the power density spectrum of surface electromyograms recorded from eighteen subjects was used as an indicator of motor units recruitment. The results showed that different recruitment strategies were used by the muscles that are antagonist to each other. When quadriceps and hamstrings acted as agonist most of the motor units were recruited in a linear manner up to 60% of maximal voluntary contraction (MVC). When the muscles acted as antagonist, quadriceps motor units were recruited up to 40% MVC during flexion while during extension the antagonist hamstrings recruited motor units up to 60% MVC. In both muscles, when acting as antagonist, the MF decreased after the recruitment phase, whereas when functioning as agonists, the MF remained relatively constant past the recruitment phase. The results suggested that a single muscle can employ different motor units recruitment strategies in accord with the type of contraction it performs and while acting as an agonist muscle as well as an antagonist.

Adult↗

Effect of an electric stimulation facilitation program on quadriceps motor unit recruitment after stroke.

OBJECTIVE: To compare maximum voluntary isometric torque (MVIT) and motor unit recruitment of the quadriceps after an electric stimulation facilitation program in persons affected by cerebrovascular accident (CVA). DESIGN: Three-week, randomized controlled trial with an electric stimulation facilitation program added to standard care. SETTING: Inpatient rehabilitation center. PARTICIPANTS: Twenty patients receiving rehabilitation for first-time CVA (51.8+/-15.2 y; days post-CVA, 38.4+/-40.0 d). Patients were randomly assigned to study and control groups. INTERVENTIONS: All patients received standard physical therapy (PT) care. In addition, the study group received an electric stimulation facilitation program during weight-bearing and ambulatory activities of the PT program. MAIN OUTCOME MEASURES: MVIT and motor unit recruitment measured by interpolated twitch testing. A 2 x 4 repeated-measures analysis of variance was performed on measurements at 4 intervals: pretest, 1 week, 2 weeks, and 3 weeks. RESULTS: MVIT increased by 77% in patients receiving electric stimulation, compared with a 31% increase for the control group. There was a significant effect for assessment time only. Motor unit recruitment increased from 35% to 53% for the study group, whereas the control group recorded no change in recruitment ability. A significant interaction was recorded, indicating improved motor unit recruitment for the study group. CONCLUSIONS: A brief and dynamic electric stimulation facilitation program significantly improved motor unit recruitment in persons after CVA.

Adult↗

Motor unit recruitment strategy changes with skill acquisition.

The modifications of motor unit recruitment strategy due to skill acquisition was determined in the elbow flexor-extensor muscles of normal human subjects. The median frequency of the power density spectra of the electromyograms recorded from the biceps and triceps muscles during a 3-s linear increase in flexion force in the range of 0-100% maximal voluntary contraction (MVC) was calculated for each subject, every 2 weeks over a total 6-week period during which subjects practiced linear flexion force increase three times a week. Electromyograms were recorded with two pairs of electrodes of different size and electrode spacing. It was shown that skill acquisition due to the 360 practice trials over the 6-week period caused an increase in the initial motor unit recruitment phase of the agonist's force generation cycle from about 0-65% MVC to about 0-85% MVC. The increase in the recruitment range was gradual and statistically significant for the measurements made every 2 weeks. The recruitment range of the antagonist triceps demonstrated a minor, but statistically insignificant, decrease over the same training period. There was a minor, but statistically insignificant, advantage of using small electrodes and inter-electrode spacing. It was concluded that skill acquisition, due to repeated functional use of a muscle in the same contraction mode, results in a slower, prolonged recruitment of motor units in the initial segment of the force generation cycle, thereby allowing a more precise and accurate control of the increments of force increase. Such conclusions reinforce the concept advocating the plasticity of motor unit control according to the functional demands imposed on the muscle. The results have significant implications in the design of various athletic, occupational and rehabilitation training modalities for optimal performance of various movement functions.

Adult↗

Roles of motor-unit recruitment in producing force variability of simulated muscle contractions.

The purpose of this study was to examine the effect of motor-unit recruitment on force variability by using computer simulated isometric contractions of a hand muscle (i.e., first dorsal interosseus). The force was simulated at 10 levels of excitation, ranging from 10 to 100% of maximum. Two recruitment conditions were simulated to compare the relative effect of motor-unit recruitment (MUR) on the relationship of force variability and level of force. One condition (40%MUR) recruited all motor units at 40% of the maximum excitation level, and the other (50%MUR) recruited all motor units at 50% of the maximum. The 40%MUR condition had a greater number of motor units than the 50%MUR group before the excitation level reached 50% of the maximum. The results showed that force variability increased at a faster rate before the completion of motor-unit recruitment and, thereafter, increased at a slower rate. In addition, the 40%MUR group showed greater force variability than the 50%MUR group. These data suggest that motor-unit recruitment is an important factor in causing force variability.

Biomechanical Phenomena↗

Effect of motor unit recruitment on functional vasodilatation in hamster retractor muscle.

1. The effect of motor unit recruitment on functional vasodilatation was investigated in hamster retractor muscle. Recruitment (i.e. peak tension) was controlled with voltage applied to the spinal accessory nerve (high = maximum tension; intermediate = approximately 50% maximum; low = approximately 25% maximum). Vasodilatory responses (diameter times time integral, DTI) to rhythmic contractions (1 per 2s for 65s) were evaluated in first, second and third order arterioles and in feed arteries. Reciprocal changes in duty cycle (range, 2.5-25%) effectively maintained the total active tension (tension times time integral, TTI) constant across recruitment levels. 2. With constant TTI and stimulation frequency (40 Hz), DTI in all vessels increased with motor unit recruitment. DTI increased from distal arterioles up through proximal feed arteries. 3. To determine whether the effect of recruitment on DTI was due to increased peak tension, the latter was controlled with stimulation frequency (15, 20 and 40 Hz) during maximum (high) recruitment. With constant TTI, DTI then decreased as peak tension increased. 4. To explore the interaction between recruitment and duty cycle on DTI, each recruitment level was applied at 2.5, 10 and 20 % duty cycle (at 40 Hz). For a given increase in TTI, recruitment had a greater effect on DTI than did duty cycle. 5. Functional vasodilatation in response to rhythmic contractions is facilitated by motor unit recruitment. Thus, vasodilatory responses are determined not only by the total tension produced, but also by the number of active motor units.

Animals↗

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

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.

Animals↗

Comparison of fluctuations of motor unit recruitment and de-recruitment thresholds in man.

Recruitment and de-recruitment thresholds of motor units in the wrist extensor muscles can undergo important random fluctuations, even when they are measured during stereotyped contractions and relaxations. These fluctuations were statistically quantified and compared. The statistical analysis indicated that recruitment and de-recruitment thresholds display the same kind of fluctuations, and that the successive measurements are randomly distributed following a quasi-normal law. We suggest that the notion of force threshold for motor unit recruitment and de-recruitment might be oversimplified and that a motor unit seems to have a range of force in which it can be recruited or de-recruited. Comparison of the mean values of recruitment and de-recruitment thresholds of the motor units in the extensor carpi radialis muscles showed that de-recruitment thresholds were significantly lower than recruitment thresholds. This difference in the thresholds, together with the difference in the motor unit discharge frequency during a contraction and a relaxation, suggests a differential control of the motoneurone activity during contractions and relaxations.

Adult↗

Human motor-unit recruitment during isometric contractions and repeated dynamic movements.

Spike-triggered averaging was used to determine the twitch tensions and contraction times of motor units in the abductor pollicis brevis muscle of two human subjects for two directions of isometric contraction: abduction and opposition of the thumb. During isometric contractions in each direction, the threshold force for motor-unit recruitment and the twitch amplitude were correlated linearly. These data suggested that an orderly pattern of recruitment, according to increasing twitch size, describes the function of the human abductor pollicis brevis muscle for each contraction direction. Rank order of motor-unit recruitment in each isometric contraction direction was correlated, but not identical. All units contributed tension in each direction of contraction, so no clear evidence was found for task-dependent motor units. In two subjects, motor-unit recruitment order during isometric contraction of the first dorsal interosseous and abductor pollicis brevis muscles was then compared with that of motor-unit pairs in both muscles during repetitive dynamic movements. Recruitment according to increasing twitch size was largely preserved during the repetitive opening and closing of scissors. The recruitment reversals that were observed were usually between pairs of units with similar thresholds.

Electromyography↗

Motor-unit recruitment in self-reinnervated muscle.

1. Recruitment order of motor units in self-reinnervated medial gastrocnemius (MG) muscles was studied in decerebrate cats 16 mo after surgical reunion of the cut MG nerve. Pairs of MG motor units were isolated by dual microelectrode penetration of ventral roots to measure their recruitment sequence during cutaneous reflexes in relation to their physiological properties. 2. Physiological properties of reconstituted motor units appeared normal, as expected. Also normal were the relationships among these properties: twitch and tetanic tension tended to increase with axonal conduction velocity and decrease with twitch contraction time. A small fraction of motor units (10/116) in reinnervated muscles produced either no measurable tension or unusually large amounts of tension compared with controls. This was the only distinct feature of the sample of reconstituted units. 3. In muscles reinnervated after nerve section, stretch was notably ineffective in eliciting reflex contraction of MG muscles or their constituent motor units (only 5/116 units). Incomplete recovery from nerve section was probably the cause of this impairment, because stretch reflexes were readily evoked in adjacent untreated muscles and in one reinnervated MG muscle that was studied 16 mo after nerve crush. In contrast with the ineffectiveness of muscle stretch, sural nerve stimulation succeeded in recruiting 49/116 units, a proportion fairly typical of normal MG muscles. 4. The contractions of the first unit recruited in cutaneous reflexes tended to be slower and less forceful than those of the other unit in a pair. By these measures, recruitment obeyed the size principle. This recruitment order with respect to unit contractile properties was not significantly different (P > 0.05) between untreated and reinnervated muscles but was significantly (P < 0.005) different from random order in both groups. The same recruitment pattern was observed for pairs of motor units sampled from the muscle reinnervated after nerve crush, whether units were recruited by muscle stretch or sural nerve stimulation. 5. The usual tendency for motor units with slower conduction velocity (CV) to be recruited in sural nerve reflexes before those with faster CV was not strong in reinnervated muscles. After nerve section the proportion of units exhibiting the usual recruitment pattern was not significantly different (P > 0.05) from a random pattern for CV. 6. The central finding is that the normal recruitment patterns recover from nerve injury in a muscle that is reinnervated by its original nerve. By contrast, stretch reflexes do not recover well from nerve section, and this deficiency may contribute to motor disability.

Animals↗

Motor unit recruitment and firing rates interaction in the control of human muscles.

Muscle contractions are modulated by the number of motor units recruited and their respective firing rates. The work described in this report documents an interplay between recruitment and firing rates of motor units. The recruitment of a new motor unit appears to have a disfacilitatory influence on the firing rates of previously activated motor units. It is speculated that this effect is likely to be mediated, at least partially, via the stretch reflex loop and possibly by the recurrent inhibition of the Renshaw circuit. Such a mechanism would be functionally useful in providing smooth control of muscle output via peripheral circuitry (consisting of proprioceptive reflexes and recurrent inhibition), thus lessening the amount of detailed supervision of the alpha-motoneuron pool required by the central nervous system.

Action Potentials↗