scholarly journals Firing Rate Modulation of Motoneurons Activated by Cutaneous and Muscle Receptor Afferents in the Decerebrate Cat

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.

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.


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

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


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.


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

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


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

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


1975 ◽  
Vol 38 (5) ◽  
pp. 1217-1231 ◽  
Author(s):  
J. A. Stephens ◽  
R. M. Reinking ◽  
D. G. Stuart

The responses of 13 Golgi tendon organs to graded force development of 29 motor units in medial gastrocnemius of the cat have been studied in five experiments. Of the 13 tendon organs, 11 were responsive to passive stretch within the physiological range of muscle length and 5 were "spontaneously" active at very short lengths where no passive tension could be recorded. The relationship between passive force and the firing rates of the various afferents ranged from a linear one to a power relation (Y = Axb + c) with b, a widely varying exponent. Results support the general conclusion that although many Ib afferents respond to passive force within the physiological range of muscle stretch, this form of stimulus is not a particularly effective one. The statis responses of Golgi tendon organs to active force development produced by single motor units was studied at different muscle lengths. In all cases the apparent sensitivity (change in firing rate per active force developed) decreased as muscle length approached Lo. The static responses of Golgi tendon organs to force developed by single motor units were also studied during fatiguing contractions. The data suggest a sigmoid relationship between force developed at the tendon and the Ib response. The collective response of all 13 tendon organs to active and passive forces at different muscle lengths was also examined. This analysis offered further support for the viewpoint that active motor unit contractions provide themost significant excitatory input to tendon organs and that changes in passive force during muscle stretch have comparatively little effect on the collective tendon organ response. The interaction between active and passive force inputs to the Golgi tendon organs is discussed in relation to the complicated nature of the relationship between forces measured at the tendon and those acting within the receptor capsule. When these complications were taken into account it was possible to explain the differences in responsiveness of a given tendon organ to active contraction of several motor units and to passive force in terms of a single force-firing rate curve for the receptor. It is concluded that changes in the force of contraction of single motor units result in relatively small changes in Ib afferent firing and that during normal muscle contractions, changes in the number of motor units acting on a single receptor must produce far more significant changes in firing rate than changes in the amount of force developed by any single unit. Changes in dynamic Ib sensitivity to single motor unit contractions are also shown to depend on length and in a similar way to the changes in static Ib sensitivity. During fatiguing contractions, a sigmoid relation was found between the dynamic Ib response and the rate of force development by single motor units.


1991 ◽  
Vol 66 (4) ◽  
pp. 1127-1138 ◽  
Author(s):  
T. C. Cope ◽  
B. D. Clark

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)


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

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


1993 ◽  
Vol 70 (4) ◽  
pp. 1433-1439 ◽  
Author(s):  
B. D. Clark ◽  
S. M. Dacko ◽  
T. C. Cope

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)


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.


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