Activation of type-identified motor units during centrally evoked contractions in the cat medial gastrocnemius muscle. III. Muscle-unit force modulation

1996 ◽  
Vol 75 (1) ◽  
pp. 51-59 ◽  
Author(s):  
K. E. Tansey ◽  
A. K. Yee ◽  
B. R. Botterman

1. The aim of this study was to examine the extent of muscle-unit force modulation due to motoneuron firing-rate variation in type-identified motor units of the cat medial gastrocnemius (MG) muscle, and to investigate the contribution of muscle-unit force modulation to whole-muscle force regulation. The motoneuron discharge patterns recorded from 8 pairs of motor units during 12 smoothly graded muscle contractions evoked by stimulation of the mesencephalic locomotor region (MLR) were used to reactivate those units in isolation to estimate what their force profiles would have been like during the evoked whole-muscle contractions. 2. For most motor units, muscle-unit force modulation was similar to motoneuron firing-rate modulation, in that muscle-unit force increased over a limited range (120-600 g) of increasing whole-muscle tension and was then maintained at a near maximal (> 70%) output level as muscle force continued to rise. Most muscle units also decreased their force outputs over a slightly larger range of declining whole-muscle force before relaxing. This second finding was best explained by the counterclockwise hysteresis recorded in the motor units' frequency-tension (f-t) relationships. 3. In those instances when whole-muscle force fluctuated just above the recruitment threshold of a motor unit, a substantial percentage (10-25%) of the change in whole-muscle force could be accounted for by force modulation in that motor unit alone. This finding suggested that few motor units in the pool were simultaneously simultaneously undergoing force modulation. To evaluate this possibility, the extent of parallel muscle-unit force modulation within the 8 pairs of simultaneously active motor units was evaluated. As with parallel motoneuron firing-rate modulation, the extent of parallel muscle-unit force modulation was limited to unit pairs of the same physiological type and recruitment threshold. In several instances, pairs of motor units displayed parallel motoneuron firing-rate modulation but did not show parallel muscle-unit force modulation because of the nature of the motor units' f-t relationships. 4. The limited extent of parallel muscle-unit force modulation seen in these experiments implies that the major strategy for force modulation in the cat MG muscle, involving contractions estimated to reach 30-40% of maximum, may be motor-unit recruitment rather than motor-unit firing-rate variation with resulting force modulation. Given, however, that the majority of motor units are already recruited at these output levels (< 40%), it is proposed that motor-unit firing-rate variation with resulting force modulation may take over as the major muscle force modulating strategy at higher output levels.

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.


1982 ◽  
Vol 47 (5) ◽  
pp. 797-809 ◽  
Author(s):  
P. J. Cordo ◽  
W. Z. Rymer

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.


1997 ◽  
Vol 78 (6) ◽  
pp. 3077-3082 ◽  
Author(s):  
Timothy C. Cope ◽  
Alan J. Sokoloff ◽  
Stan M. Dacko ◽  
Rebecca Huot ◽  
Eleanor Feingold

Cope, Timothy C., Alan J. Sokoloff, Stan M. Dacko, Rebecca Huot, and Eleanor Feingold. Stability of motor-unit force thresholds in the decerebrate cat. J. Neurophysiol. 78: 3077–3082, 1997. To further test the hypothesis that some fixed property of motoneurons determines their recruitment order, we quantified the variation in force threshold (FT) for motoneurons recruited in muscle stretch reflexes in the decerebrate cat. Motor axons supplying the medial gastrocnemius (MG) muscle were penetrated with micropipettes and physiological properties of the motoneuron and its muscle fibers, i.e., the motor unit, were measured. FT, defined as the amount of MG force produced when the isolated motor unit was recruited, was measured from 20 to 93 consecutive stretch trials for 29 motor units. Trials were selected for limited variation in base force and rate of rise of force, which have been shown to covary with FT, and in peak stretch force, which gives some index of motor-pool excitability. Under these restricted conditions, large variation in FT would have been inconsistent with the hypothesis. Analysis of the variation in FT employed the coefficient of variation (CV), because of the tendency for FT variance and mean to increase together. We found that CV was distributed with a median value of 10% and with only 2 of 29 units exceeding 36%. Some of this variation was associated with measurement error and with intertrial fluctuations in base, peak, and the rate of change of muscle force. CV was not significantly correlated with motor-unit axonal conduction velocity, contraction time, or force. In three cases FT was measured simultaneously from two motor units in the same stretch trials. Changes in recruitment order were rarely observed (5 of 121 stretch trials), even when FT ranges for units in a pair overlapped. We suggest that the large variation in recruitment threshold observed in some earlier studies resulted not from wide variation in the recruitment ranking of motoneurons within one muscle, but rather from variation in the relative activity of different pools of motoneurons. Our findings are consistent with the hypothesis that recruitment order is determined by some fixed property of α-motoneurons and/or by some unvarying combination of presynaptic inputs that fluctuate in parallel.


2013 ◽  
Vol 2013 ◽  
pp. 1-10 ◽  
Author(s):  
Rositsa Raikova ◽  
Hristo Aladjov ◽  
Jan Celichowski ◽  
Piotr Krutki

Muscle force is due to the cumulative effect of repetitively contracting motor units (MUs). To simulate the contribution of each MU to whole muscle force, an approach implemented in a novel computer program is proposed. The individual contraction of an MU (the twitch) is modeled by a 6-parameter analytical function previously proposed; the force of one MU is a sum of its contractions due to an applied stimulation pattern, and the muscle force is the sum of the active MUs. The number of MUs, the number of slow, fast-fatigue-resistant, and fast-fatigable MUs, and their six parameters as well as a file with stimulation patterns for each MU are inputs for the developed software. Different muscles and different firing patterns can be simulated changing the input data. The functionality of the program is illustrated with a model consisting of 30 MUs of rat medial gastrocnemius muscle. The twitches of these MUs were experimentally measured and modeled. The forces of the MUs and of the whole muscle were simulated using different stimulation patterns that included different regular, irregular, synchronous, and asynchronous firing patterns of MUs. The size principle of MUs for recruitment and derecruitment was also demonstrated using different stimulation paradigms.


1996 ◽  
Vol 75 (1) ◽  
pp. 26-37 ◽  
Author(s):  
K. E. Tansey ◽  
B. R. Botterman

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.


2004 ◽  
Vol 92 (5) ◽  
pp. 2878-2886 ◽  
Author(s):  
Ping Zhou ◽  
William Zev Rymer

The dependence of the form of the EMG-force relation on key motoneuron and muscle properties was explored using a simulation approach. Surface EMG signals and isometric forces were simulated using existing motoneuron pool, muscle force, and surface EMG models, based primarily on reported properties of the first dorsal interosseous (FDI) muscle in humans. Our simulation results indicate that the relation between electrical and mechanical properties of the individual motor unit level plays the dominant role in determining the overall EMG amplitude-force relation of the muscle, while the underlying motor unit firing rate strategy appears to be a less important factor. However, different motor unit firing rate strategies result in substantially different relations between counts of the numbers of motoneuron discharges and the isometric force. Our simulation results also show that EMG amplitude (estimated as the average rectified value) increases as a result of synchronous discharges of different motor units within the pool, but the magnitude of this increase is determined primarily by the action potential duration of the synchronized motor units. Furthermore, when the EMG effects are normalized to their maximum levels, motor unit synchrony does not exert significant effects on the form of the EMG-force relation, provided that the synchrony level is held similar at different excitation levels.


2018 ◽  
Vol 120 (4) ◽  
pp. 1973-1987 ◽  
Author(s):  
R. Raikova ◽  
J. Celichowski ◽  
S. Angelova ◽  
P. Krutki

The muscle force is the sum of forces of multiple motor units (MUs), which have different contractile properties. During movements, MUs develop unfused tetani, which result from summation of twitch-shape responses to individual stimuli, which are variable in amplitude and duration. The aim of the study was to develop a realistic muscle model that would integrate previously developed models of MU contractions and an algorithm for the prediction of tetanic forces. The proposed model of rat medial gastrocnemius muscle is based on physiological data: excitability and firing frequencies of motoneurons, contractile properties, and the number and proportion of MUs in the muscle. The MU twitches were modeled by a six-parameter analytical function. The excitability of motoneurons was modeled according to a distribution of their rheobase currents measured experimentally. Processes of muscle force regulation were modeled according to a common drive hypothesis. The excitation signal to motoneurons was modeled by two form types: triangular and trapezoid. The discharge frequencies of MUs, calculated individually for each MU, corresponded to those recorded for rhythmic firing of motoneurons. The force of the muscle was calculated as the sum of all recruited MUs. Participation of the three types of MUs in the developed muscle force was presented at different levels of the excitation signal to motoneurons. The model appears highly realistic and open for input data from various skeletal muscles with different compositions of MU types. The results were compared with three other models with different distribution of the input parameters.NEW & NOTEWORTHY The proposed mathematical model of rat medial gastrocnemius muscle is highly realistic because it is based strictly on experimentally determined motor unit contractile parameters and motoneuron properties. It contains the actual number and proportion of motor units and takes into consideration their different contributions to the whole muscle force, depending on the level of the excitation signal. The model is open for input data from other muscles, and additional physiological parameters can also be included.


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.


1982 ◽  
Vol 47 (5) ◽  
pp. 782-796 ◽  
Author(s):  
P. J. Cordo ◽  
W. Z. Rymer

1. Multiunit integrated electromyographic (EMG) signals and single-unit EMG potentials were recorded during isometric and lengthening (stretch reflex) contractions of soleus and medial gastrocnemius (MG) muscles in 20 decerebrate cats. Patterns of motor-unit recruitment and rate modulation were examined in isometric muscles and during constant-velocity stretches. 2. Analysis of multiunit EMG activity and its relationship to active force revealed a marked difference between isometric and lengthening contractions. While the force-EMG relationship for isometric contractions was characteristically linear, the relation recorded during stretch-reflex responses showed a disproportionate early EMG increase, which was most obvious at low force levels, suggesting that the efficacy of force production is reduced in lengthening muscle. 3. Single-unit recruitment patterns were found to be qualitatively similar in isometric and lengthening contractions. In each case, motor units were recruited in order of increasing spike voltage. The numbers of newly recruited units declined steeply with each successive increment in active force. For a given unit, the force at which recruitment occurred was found to be greater in lengthening contractions than in isometric contractions, and in lengthening contractions it was also found to depend on the level of initial force. 4. Two patterns of motor-unit rate modulation were observed during muscle stretch, depending on whether a given unit was firing before the beginning of stretch or whether it was recruited during the course of stretch. Motor units that were active prior to stretch were found to increase firing rate at stretch onset and to vary their rate very little thereafter. Motor units recruited in the course of stretch began firing at an initial rate proportional to their force threshold, gradually increased their firing rate with increasing force, and sometimes reached an apparent maximum rate. 5. These results are discussed in terms of the mechanical properties of lengthening muscle and reflex regulation of these properties. Each identified pattern of motor-unit recruitment and rate modulation is evaluated for its potential contribution to the regulation of muscle properties, especially the prevention of muscle yield. We conclude that at low to moderate levels of initial force, recruitment of new motor units is likely to be the most effective compensatory mechanism.


2007 ◽  
Vol 102 (1) ◽  
pp. 122-129 ◽  
Author(s):  
Christopher A. Knight ◽  
Gary Kamen

This study compared motor unit rate coding and muscular force control in the first dorsal interosseous muscle of older ( n = 11, mean 72.3 yr) and young ( n = 12, mean 18.7 yr) adults. Rate coding during a sinusoidal isometric force-matching task was evaluated using spectral analysis of the time-varying changes in firing rate. The task required force modulations to match a trajectory comprising the sum of 0.15- and 0.45-Hz sine waves. Based on the amplitude of spectral peaks at 0.15 and 0.45 Hz, the amplitude of force modulation was similar in young and older adults at both frequencies ( F = 1.9, P = 0.17). Force modulation gain (FMG) was computed as the ratio of the amplitude of force modulation to the amplitude of firing rate modulation. To account for rate coding differences related to the properties of the motoneuron, recruitment threshold force was used as a covariate in age-group comparisons. At both task frequencies, firing rate was modulated with less amplitude ( F = 0 14, P < 0.001) and FMG was greater ( F = 0 27, P < 0.001) in the older adults. In its transformation of neural input to mechanical output, muscle is known to act as a low-pass filter. Compared with modulation at 0.15 Hz, less change in force per change in firing rate at 0.45 Hz (lower FMG; F = 0 67, P < 0.001), independent of age group, is consistent with this filtering effect. Our conclusion is that there is a reduced amplitude of firing rate modulation in older adults.


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