Synaptic and mechanical coupling between type-identified motor units and individual spindle afferents of medial gastrocnemius muscle of the cat

1984 ◽  
Vol 51 (6) ◽  
pp. 1268-1283 ◽  
Author(s):  
J. B. Munson ◽  
J. W. Fleshman ◽  
J. E. Zengel ◽  
G. W. Sypert

Experiments were performed to test the possibility that motor unit-muscle spindle pairs that are coupled especially strongly mechanically will also be coupled especially strongly synaptically ("weighted ensemble input": Ref. 4). Synaptic and mechanical coupling between one or two individual muscle spindle afferents and individual motor units of the medial gastrocnemius (MG) muscle were measured in barbiturate-anesthetized cats. Synaptic coupling was assessed by measuring the amplitude of single-fiber monosynaptic excitatory postsynaptic potentials (EPSPs) generated in motoneurons by individual spindle afferents. Mechanical coupling was assessed by measuring the alteration in discharge rate of these spindle afferents caused by tetanic activation of the same motor units. Afferents were classified as primary or secondary on the basis of conduction velocity and response to muscle stretch and contraction. Motor units were classified as slow twitch (S); fast twitch, fatigue resistant (FR); fast twitch, intermediate fatigue resistance (FI); and fast twitch, fatigue sensitive (FF) on the basis of twitch contraction time and resistance to fatigue. In 85% of 138 motor unit-primary afferent interactions tested, tetanic activation of the single motor unit unloaded (i.e., decreased the discharge rate of) the primary afferent. A very weak though significant correlation was found between tetanic contraction strength and primary afferent unloading. In 66% of 155 motor unit-secondary afferent interactions tested, tetanic activation of the single motor unit unloaded the secondary afferent. Again, afferent unloading was but weakly related to tetanic contraction strength. Single-fiber EPSPs generated by primary or secondary muscle spindle afferents were recorded in type-identified motor units. EPSPs generated by primary afferents were significantly larger in oxidative (S + FR) than in glycolytic (FF) motor units. No such differences were seen for EPSPs generated by secondary afferents. The magnitude of the EPSP generated in a motoneuron by a spindle afferent was compared to the magnitude of the unloading of that afferent by tetanic activation of the corresponding motor unit. Overall, no relationship was found between these measures.(ABSTRACT TRUNCATED AT 400 WORDS)

2014 ◽  
Vol 112 (7) ◽  
pp. 1685-1691 ◽  
Author(s):  
Christopher J. Dakin ◽  
Brian H. Dalton ◽  
Billy L. Luu ◽  
Jean-Sébastien Blouin

Rectification of surface electromyographic (EMG) recordings prior to their correlation with other signals is a widely used form of preprocessing. Recently this practice has come into question, elevating the subject of EMG rectification to a topic of much debate. Proponents for rectifying suggest it accentuates the EMG spike timing information, whereas opponents indicate it is unnecessary and its nonlinear distortion of data is potentially destructive. Here we examine the necessity of rectification on the extraction of muscle responses, but for the first time using a known oscillatory input to the muscle in the form of electrical vestibular stimulation. Participants were exposed to sinusoidal vestibular stimuli while surface and intramuscular EMG were recorded from the left medial gastrocnemius. We compared the unrectified and rectified surface EMG to single motor units to determine which method best identified stimulus-EMG coherence and phase at the single-motor unit level. Surface EMG modulation at the stimulus frequency was obvious in the unrectified surface EMG. However, this modulation was not identified by the fast Fourier transform, and therefore stimulus coherence with the unrectified EMG signal failed to capture this covariance. Both the rectified surface EMG and single motor units displayed significant coherence over the entire stimulus bandwidth (1–20 Hz). Furthermore, the stimulus-phase relationship for the rectified EMG and motor units shared a moderate correlation ( r = 0.56). These data indicate that rectification of surface EMG is a necessary step to extract EMG envelope modulation due to motor unit entrainment to a known stimulus.


1986 ◽  
Vol 55 (5) ◽  
pp. 947-965 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

This study tested the hypothesis that functional connection to muscle is necessary for expression of normal motoneuron electrical properties. Also examined was the time course of self-reinnervation. Properties of individual medial gastrocnemius (MG) motor units were examined following section and reanastomosis of the MG nerve. Stages examined were 3-5 wk (prior to reinnervation, no-re), 5-6 wk (low-re), 9-10 wk (med-re), and 9 mo (long-re, preceding paper) after nerve section. Motor units were classified on the basis of their mechanical response as type fast twitch, fast fatiguing (FF), fast twitch with intermediate fatigue resistance (FI), fast twitch, fatigue resistant (FR), or slow twitch, fatigue resistant (S) (11, 24). Motoneuron electrical properties were measured. Muscle fibers were classified using histochemical methods as type fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) (60). Prior to functional reinnervation, MG motoneurons exhibited increased input resistance, decreased rheobase, decreased rheobase/input resistance, and decreased axonal conduction velocity. There was no change in mean afterhyperpolarization (AHP) half-decay time. Normal relationships between motoneuron electrical properties were lost. These data are consistent with dedifferentiation of motoneuron properties following axotomy (35, 47). At 5-6 wk after reanastomosis, motor-unit tensions were small, and motoneuron membrane electrical properties were unchanged from the no-re stage. There were no differences in motoneuron electrical properties between cells that elicited muscle contraction and those that did not. Motor-unit types were first recognizable at the med-re stage. The proportions of fast and slow motor units were similar to normal MG. Within the fast units, there were fewer type-FF units and more type-FI and type-FR units than normal, reflecting a general increase in fatigue resistance at this stage. Neither motoneuron membrane electrical properties nor muscle contractile properties had reached normal values, although both were changed in that direction from the low-re stage. Normal relationships between muscle properties, between motoneuron properties, and between motoneuron and muscle properties were re-established. The correspondence between motor-unit type and motoneuron type was similar to normal or 9 mo reinnervated MG. Muscle-unit tetanic tensions became larger with time after reinnervation. Most of the increase in muscle tension beyond the med-re stage could be accounted for by increase in muscle fiber area. There was an increased proportion of SO muscle fibers observed in the med-re muscles, as at the long-re stage.(ABSTRACT TRUNCATED AT 400 WORDS)


2008 ◽  
Vol 33 (6) ◽  
pp. 1086-1095 ◽  
Author(s):  
Teatske M. Altenburg ◽  
Cornelis J. de Ruiter ◽  
Peter W.L. Verdijk ◽  
Willem van Mechelen ◽  
Arnold de Haan

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.


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.


Author(s):  
David Burke ◽  
James Howells

The motor unit represent the final output of the motor system. Each consists of a motoneuron, its axon, neuromuscular junctions, and muscle fibres innervated by that axon. The discharge of a motor unit can be followed by recording its electromyographic signature, the motor unit action potential. Motoneurons are not passive responders to the excitatory and inhibitory influences on them from descending and segmental sources. Their properties can change, e.g. due to descending monoaminergic pathways, which can alter their responses to other inputs (changing ‘reflex gain’). Contraction strength depends on the number of active motor units, their discharge rate, and whether the innervated muscle fibres are slow-twitch producing low force, but resistant to fatigue, fast-twitch producing more force, but susceptible to fatigue, or intermediate fast-twitch fatigue-resistant. These properties are imposed by the parent motoneurons, and the innervated muscle fibres have different histochemical profiles (oxidative, glycolytic, or oxidative-glycolytic, respectively).


1986 ◽  
Vol 55 (5) ◽  
pp. 931-946 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

This work tested whether the membrane electrical properties of cat motoneurons, the contractile properties of their muscle units, and the normal relationships among them would be restored 9 mo after section and resuture of their muscle nerve. Properties of medial gastrocnemius (MG) motor units were examined 9 mo following section and resuture of the MG nerve in adult cats. Motoneuron electrical properties and muscle-unit contractile properties were measured. Motor units were classified on the basis of their contractile properties as type fast twitch, fast fatiguing (FF), fast twitch with intermediate fatigue resistance (FI), fast twitch, fatigue resistant (FR), or slow twitch, fatigue resistant (S) (8, 20). Muscle fibers were classified as type fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) on the basis of histochemical staining for myosin adenosine triphosphatase, nicotinamide adenine dinucleotide diaphorase, and alpha-glycerophosphate dehydrogenase (48). Following 9 mo self-reinnervation, the proportions of each motor-unit type were the same as in normal control animals. Motoneuron membrane electrical properties [axonal conduction velocity, afterhyperpolarization (AHP) half-decay time, rheobase, and input resistance] also returned to control levels in those motoneurons that made functional reconnection with the muscle (as determined by ability to elicit measurable tension). The relationships among motoneuron electrical properties were normal in motoneurons making functional reconnection. Approximately 10% of MG motoneurons sampled did not elicit muscle contraction. These cells' membrane electrical properties were different from those that did elicit muscle contraction. Contractile speed and fatigue resistance of reinnervated muscle units had recovered to control levels at 9 mo postoperation. Force generation did not recover fully in type-FF units. The reduced tensions were apparently due to failure of recovery of FG muscle fiber area. Following reinnervation, relationships between motoneuron electrical and muscle-unit contractile properties were similar to controls. This was reflected in a degree of correspondence between motor-unit type and motoneuron type similar to normal units (84 vs. 86%, as defined by Ref. 61). There was a significantly increased proportion of type-SO muscle fibers and a decrease in the fast muscle fibers (especially type FOG) in 9 mo reinnervated MG. Together with the unchanged proportions of motor-unit types, this led to an estimate of average innervation ratios being increased in type-S motor units and decreased in type-FR units.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 59 (4) ◽  
pp. 1128-1142 ◽  
Author(s):  
A. Lev-Tov ◽  
C. A. Pratt ◽  
R. E. Burke

1. We studied the organization of motor units in the tenuissimus (TEN) muscle of pentobarbital-anesthetized cats. The cat TEN is a long, delicate straplike muscle that spans hip and knee, which has a very flat length-tension curve through 22 mm of length change. 2. The TEN motor nucleus, labeled by retrograde transport of several forms of horseradish peroxidase, was composed of 8-31 cells in different cats, of which about half were, on average, in the size range of alpha-motoneurons. TEN motoneurons were scattered through the ventrolateral portion of lamina IX, over a rostrocaudal distance of up to 6.5 mm, making it relatively easy to isolate individual TEN motor axons for single motor-unit stimulation. 3. Individual TEN muscle units were classified into four groups [fast-twitch, fatigable (FF), intermediate, fatigue-resistant (Fint), fast-twitch, fatigue-resistant (FR), and slow-twitch, fatigue resistant (S)] on the basis of "sag" and fatigue index mechanical properties, as in other cat hindlimb muscles. There was a relatively large proportion of Fint units (28%) in the TEN sample, and the range of tetanic tension (approximately 19-fold) was much smaller than found in other cat hindlimb muscles. 4. A majority of TEN muscle fibers could be classified into the three major histochemical types (IIB, IIA, and I) found in other cat muscles, but a substantial minority remained "unclassified." A single type Fint muscle unit was successfully depleted of glycogen for histochemical study. It exhibited a typical type IIB histochemical profile. 5. Despite its unusual morphology, the cat TEN contains the same types of motor units found in larger, more "typical" limb muscles.


1994 ◽  
Vol 72 (4) ◽  
pp. 1885-1896 ◽  
Author(s):  
E. Smits ◽  
P. K. Rose ◽  
T. Gordon ◽  
F. J. Richmond

1. We depleted single motor units in feline sartorius muscles of glycogen by stimulating their motoneurons intracellularly. We mapped the intramuscular distribution of depleted fibers by inspecting histological cross-sections throughout the length of sartorius. 2. We selected ten depleted motor units for detailed study and quantitative analysis. Nine motor units were located in the anterior head of sartorius. One was located in a muscle whose distal half appeared to have been damaged some time before the acute experiment. A single motor unit was located in the medial head of sartorius. 3. Five motor units were composed of fast-twitch glycolytic (FG) muscle fibers, two of fast-twitch oxidative glycolytic (FOG) muscle fibers, and three of slow-twitch oxidative (SO) muscle fibers. Estimates of the numbers of depleted fibers in motor units of anterior sartorius indicated that FG motor units were larger (mean 566 fibers) than FOG and SO motor units (SO mean 190, FOG mean 156 fibers). The SO motor unit in the damaged muscle had 550 fibers. One motor unit depleted in the medial head of sartorius had 270 fibers with FG profiles. 4. Muscle fibers belonging to each anterior motor unit were never distributed throughout the whole cross-section of anterior sartorius at any proximodistal level. Furthermore, fibers were distributed nonuniformly along the proximodistal axis of the muscle. In most muscles at least a few depleted fibers were found at all proximodistal levels. However, in one normal muscle and the damaged muscle, depleted fibers were confined to the proximal end. 5. The fibers in the medial motor unit were confined to a strip that did not extend across the whole cross-section of the muscle head. Fibers within this strip were scattered quite evenly from origin to insertion. This medial FG motor unit occupied a smaller territory and contained fewer fibers than anterior motor units of the same histochemical type. 6. These results show that sartorius motor units are not distributed uniformly in the mediolateral plane; those in anterior sartorius were distributed asymmetrically in the proximodistal axis as well. This finding has important functional implications for the way in which we model force development and transmission in sartorius and other long muscles.


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.


2009 ◽  
Vol 102 (3) ◽  
pp. 1725-1735 ◽  
Author(s):  
Stéphane Baudry ◽  
Thorsten Rudroff ◽  
Lauren A. Pierpoint ◽  
Roger M. Enoka

Twenty subjects participated in four experiments designed to compare time to task failure and motor-unit recruitment threshold during contractions sustained at 15% of maximum as the elbow flexor muscles either supported an inertial load (position task) or exerted an equivalent constant torque against a rigid restraint (force task). Subcutaneous branched bipolar electrodes were used to record single motor unit activity from the biceps brachii muscle during ramp contractions performed before and at 50 and 90% of the time to failure for the position task during both fatiguing contractions. The time to task failure was briefer for the position task than for the force task ( P = 0.0002). Thirty and 29 motor units were isolated during the force and position tasks, respectively. The recruitment threshold declined by 48 and 30% ( P = 0.0001) during the position task for motor units with an initial recruitment threshold below and above the target force, respectively, whereas no significant change in recruitment threshold was observed during the force task. Changes in recruitment threshold were associated with a decrease in the mean discharge rate (−16%), an increase in discharge rate variability (+40%), and a prolongation of the first two interspike intervals (+29 and +13%). These data indicate that there were faster changes in motor unit recruitment and rate coding during the position task than the force task despite a similar net muscle torque during both tasks. Moreover, the results suggest that the differential synaptic input observed during the position task influences most of the motor unit pool.


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