Effects of percutaneous stimulation on motor unit firing behavior in man

Summary Motor unit firing behavior in human first dorsal interosseous (FDI) muscle was studied during controlled constant force isometric contractions. The threshold at which motor units were recruited and the mean firing rate at 50% of maximal voluntary contraction (MVC) were evaluated following stimulation of the skin area over the second digit. Stimulation of cutaneous receptors tended to increase the recruitment threshold of most of the motor units recruited under 20% MVC, while high-threshold motor units (those recruited over 30% MVC) generally exhibited a decrease in recruitment threshold. Less dramatic changes in motor unit firing rates were observed, but those motor units recruited over 30% MVC exhibited some increase in firing rate. The relationship between the change in recruitment threshold and change in motor unit firing rate is not rigid and seems to be susceptible to considerable synaptic noise.     

Determination of the contractile characteristics of the motor units in skeletal muscle through twitch characteristics

A stepwise increase in stimulation voltage was applied to a pair of synchronously firing plate electrodes placed across the spinal roots innervating the soleus, medial and lateral gastrocnemius muscles of the cat. The resultant muscle twitches were stored and analysed by an Intel 8080a microprocessor to determine the speed of contraction and the peak tension of the compound muscle twitches. From these results, the speed of contraction and the strength distribution of the motor units within that muscle were estimated. These data were then compared with the actual fibre composition and speed distribution measured for the same three muscles. The results of these determinations showed that the distribution of strength and speed of contraction of the motor units of these muscles could be approximated through stimulation of their motor nerves.     

Muscle glycogen depletion patterns in fast twitch fibre subgroups of man during submaximal and supramaximal exercise

Summary Muscle glycogen depletion in ST, FTa and FTb fibres were studied in human subjects undergoing two distinctly different modes of bicycle exercise. Two hours of submaximal exercise (60% of V0₂ max) produced a 77% decline in muscle glycogen concentration accompanied by only minor elevations in muscle and blood lactate levels, whereas 10 one minute supramaximal work bouts resulted in a 52% decrease in total glycogen concentration and substantially elevated muscle and blood lactate contents. Moreover the patterns of glycogen depletion in the two conditions were also distinctly different. Based on the PAS staining intensity, glycogen was depleted the most in ST fibres and least in FTb fibres, during submaximal work. During supramaximal work FTb fibres were the lightest in PAS staining, with little loss of glycogen from ST fibres. In both situations the loss of glycogen in the FTa fibres was intermediate compared to the other two fibre types. These data support a selective recruitment of muscle fibres during work of different intensities, and further, suggest a physiological basis for the subgrouping of FT fibres in man.     

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.     

The scaling of motor noise with muscle strength and motor unit number in humans

Understanding the origin of noise, or variability, in the motor system is an important step towards understanding how accurate movements are performed. Variability of joint torque during voluntary activation is affected by many factors such as the precision of the descending motor commands, the number of muscles that cross the joint, their size and the number of motor units in each. To investigate the relationship between the peripheral factors and motor noise, the maximum voluntary torque produced at a joint and the coefficient of variation of joint torque were recorded from six adult human subjects for four muscle/joint groups in the arm. It was found that the coefficient of variation of torque decreases systematically as the maximum voluntary torque increases. This decreasing coefficient of variation means that a given torque or force can be more accurately generated by a stronger muscle than a weaker muscle. Simulations demonstrated that muscles with different strengths and different numbers of motor units could account for the experimental data. In the simulations, the magnitude of the coefficient of variation of muscle force depended primarily on the number of motor units innervating the muscle, which relates positively to muscle strength. This result can be generalised to the situation where more than one muscle is available to perform a task, and a muscle activation pattern must be selected. The optimal muscle activation pattern required to generate a target torque using a group of muscles, while minimizing the consequences of signal dependent noise, is derived.     

Relationships between motor nerve conduction velocities and motor unit contraction characteristics in a slow twitch muscle of the cat

1. Isometric contractions of cat soleus muscles and of functionally isolated motor units have been measured under conditions similar to those of Bagust, Knott, Lewis, Luck & Westerman (1973).2. The muscle lengths at which motor unit twitch and tetanus tensions were maximal were close to the optimal lengths of the parent muscles.3. Motor unit contraction times and tensions were shown to be related to the conduction velocities of the nerve axons supplying them. These relationships were obscured when a number of small samples from several experiments were grouped together.4. The ratios of the twitch to the tetanic tensions of the motor units were directly related to their times to peak tension.     

The effect of muscle length on motor unit discharge characteristics in human tibialis anterior muscle

Summary Muscle length influences the contractile properties of muscle in that when muscle is lengthened the relaxation phase of the muscle twitch is prolonged and when muscle is shortened, the relaxation phase is shorter in duration. As a result, the force exerted by active motor units varies with muscle length during voluntary contractions. To determine if motoneuron spike trains were adjusted to accommodate for changes in the contractile properties imposed by shortened and lengthened muscle, motor unit action potentials were recorded from the tibialis anterior muscle at different muscle lengths. Twenty subjects performed isometric ramp contractions at ankle angles of 20° dorsiflexion, neutral between dorsiflexion and plantar flexion, and 30° plantar flexion, which put the tibialis anterior muscle in a shortened, neutral, or lengthened condition, respectively. During isometric contractions where torque increased at 5% MVC/s, motor unit discharge rate at recruitment was greater in shortened muscle than in lengthened muscle (P<0.05). Brief initial interspike intervals (<40 ms) occurred more frequently in shortened muscle than in either neutral length or lengthened muscle. During steady contractions, motor unit discharge rate was greater per unit torque (N.m) in shortened muscle than in neutral length or lengthened muscle (P<0.05). These findings indicate that muscle length does influence the discharge pattern of motor unit spike trains during isometric ramp contractions. Spike trains with higher discharge rates at recruitment in shortened muscle may take advantage of the catch-like properties in muscle and be useful in taking up the slack in the passive elements of the muscle and tendon. During steady submaximal contractions, the higher discharge rate per unit torque (N.m) in shortened muscle is likely due to the decreased peak tension and shorter one-half relaxation time observed in shortened muscle, and may indicate that the tibialis anterior muscle is operating on the steep portion of the length-tension curve when the ankle is fully dorsiflexed.     

Differential control of fast and slow twitch motor units in the decerebrate cat

Summary In approximately 3/4 of precollicular decerebrate (unanesthetized) cats, tetanic electrical stimulation of the sural nerve, or pinching the ankle skin innervated by the sural nerve, produced predominant excitation (overall increased force output and EMG activity) in the mixed medical gastrocnemius (MG) muscle and simultaneous inhibition in its slow twitch Synergist, soleus (Sol). The present experiments were designed to test whether, as this and other evidence suggests, certain sets of cutaneous afferents can produce activation of particular groups of motor units and simultaneous inhibition of other groups within the same motor unit pool (i.e., units belonging to a single muscle).We recorded, in decerebrate cats, the activity of restricted sets of MG motor units using either fine bipolar EMG wire electrodes or bipolar hook electrodes on small natural filaments of the MG muscle nerve. In preparations exhibiting the differential effect of sural input noted above, we usually found that some low threshold MG motor units (i.e., those responding to stretch or vibration of the MG muscle) exhibited slowing of discharge or complete inhibition at the same time that higher threshold MG units, not responsive to stretch or vibration, were powerfully recruited by either electrical or natural stimulation of sural nerve afferents. The net balance of synaptic effects within the MG motoneuron population may thus be excitatory in some cells and simultaneously inhibitory in others. This finding, together with earlier evidence, suggests the existence of at least two patterns of organization of synaptic input to the MG motoneuron pool.     

Effects of age and life-time physical training on fibre composition of slow and fast skeletal muscle in rats

The effects of age and endurance training on muscle fibre characteristics were studied in a slow (m. soleus, MS) and in a fast (m. rectus femoris, MRF) skeletal muscle. Wistar rats at ages of 1, 2, 4, 10, and 24 months were used as experimental animals. The trained rats were put to run on a motor-driven treadmill 5 d/wk beginning from the age of 1 month. The body weights of the animals increased continuously throughout their lives. The muscle weights increased up to the age of 10 months, after which they tended to decrease. The trained adult rats had lower body weights as well as lower muscle weights than the untrained adult rats. The amount of the intramuscular lipid decreased with age, especially during the first months of life. The activity of isocitrate dehydrogenase (ICDH) decreased during the growth period in both muscles and remained more or less constant thereafter, whereas the activity of phosphofructokinase decreased with age only in MS. In MS, the trained animals tended to have higher ICDH activities than the untrained animals. The cross-sectional area of the different fibre types in both muscles increased up to the age of 10 months. The major fibre types, type I in MS and type IIB in MRF, were smaller for trained than untrained rats. The percentage number of the slower fibre types of both muscles — type I in MS and types I and IIA in MRF —increased with advancing age. The muscles of the trained animals contained higher percentages of the slower fibre types than those of the untrained rats. The present paper indirectly supports the opinion that not only the metabolic but also the contractile properties of different muscle cell types can be changed by age and long-term endurance-type physical training.     

Interactions between motor units in modulating discharge patterns of primary muscle spindle endings

Summary Discharge patterns of group Ia afferents of muscle spindles in the (isometric) cat semitendinosus muscle were recorded when subjected to the influence of contractions of three motor units elicited by stimulation of three -efferents with different regular or stochastic stimulus patterns. In order to study conditioning interactions between motor unit contractions, defined time constellations of stimuli to different motor units were isolated from the stimulus trains by electronic means. This technique was also applied to discharge patterns of two Ia fibres to isolate correlated discharges. The effects of defined time constellations of stimuli upon discharge patterns of single Ia afferents or correlated discharges of pairs of Ia afferents were assessed by poststimulus time histograms (PSTHs). It turned out that the influence exerted by one motor unit on spindle discharges was more or less strongly modulated by actions of the other motor units, dependent on the relative timing of their contractions. These effects could in part be explained by the relative locations of motor units and spindles within the muscle. These results are discussed with respect to possible mechanisms of low-amplitude physiological tremor.Supported by a grant from the Deutsche Forschungsgemeinschaft, SFB 33 (Nervensystem und biologische Information), Göttingen     

Effect of hyperthyroidism on the contractile and histochemical properties of fast and slow twitch skeletal muscle in the rat

Male Wistar rats were made hyperthyroid by intraperitoneal injections on alternate days for 1–6 weeks, of 200 g/kg triiodothyronine (T₃). The effects of this treatment on the contractile properties of the soleus, a slow twitch and the extensor digitorum longus (EDL), a fast twitch skeletal muscle, were studied in vivo in the anaesthetized animal. Post mortem, serial frozen sections of both muscles were stained histochemically for myosin ATPase, succinic dehydrogenase and phosphorylase. Muscle fibres were classified as either slow twitch (SO), fast twitch oxidative glycolytic (FOG) or fast twitch glycolytic (FG).Elevation of plasma T₃ levels is associated with progressive alterations in the muscle fibre populations of both muscles. In the soleus there is conversion of SO to FOG fibres while in the EDL the main effect is FG to FOG conversion. There are also marked changes, mainly confined to the soleus muscle, in contractile properties; progressive increases in isometric twitch and tetanic tension and in the rates of contraction and relaxation during both twitch and tetanus.The effect of T₃ on slow muscle contractility may be related to its effect on muscle phenotype. However, changes in the former precede detectable fibre population changes. T₃ may influence properties such as the Ca²⁺ binding activity of sarcoplasmic reticulum of existing slow twitch fibres before the later changes associated with the interconversion of fibre types occur.     

The relationship of voluntary running to fibre type composition,fibre area and capillary supply in rat soleus and plantaris muscles

Summary Twenty 4-week-old Wistar rats exercised voluntarily in running wheels each day for 45 days. Fibre type composition, fibre cross-sectional area and the number of capillaries around a fibre of the slow-twitch soleus and fast-twitch plantaris muscles were examined and compared with animals which had no access to running wheels. The exercise group had a higher percentage of fast-twitch oxidative glycolytic (FOG) fibres and a lower percentage of fast-twitch glycolytic (FG) fibres in the deep portion of the plantaris muscle. The area of FOG fibres in the surface portion of the plantaris muscle was also greater in the exercise group. In the exercised animals, there was a positive relationship between the running distance and the area of FOG fibres in both the deep and surface portions of the plantaris muscle. In addition, the running distance correlated positively with the percentage of FOG fibres and negatively with that of FG fibres in the deep portion of the plantaris muscle. There were no relationships between the running distance and fibre type composition, or fibre area and capillary supply in the soleus muscle. These results suggested that the increase in the percentage and area of FOG fibres in the fast-twitch muscle was closely related to voluntary running.     

Linear and nonlinear effects in the interactions of motor units and muscle spindle afferents

Summary Successive motor unit (MU) twitches often do not sum linearly. Also, muscle spindle (MS) afferents may react nonlinearly to MU contractions occurring at short intervals. Little data is presently available on the interactions between two (or more) MUs regarding their effects on tension output and MS responses. We have studied these effects in cat Mm. gastrocnemius medialis (MG), soleus and semitendinosus. In adult anaesthetized cats, MUs of the muscle under study were electrically stimulated via their ventral root axons with random sequences of brief pulses having mean rates between 6 and 12 pulses per second. Isometric tension fluctuations were recorded from the muscle under study, and discharge patterns of MS afferents (Ia and group II) were recorded from dorsal root filaments. A crosscorrelation analysis was performed to display linear and nonlinear effects evoked by selected time constellations of MU activations. 1) 18 (67%) of 27 MG MUs showed marked potentiation of the second of two twitches in response to pairs of stimuli separated by 5 to about 25 ms. The remainder of these and 16 of the soleus MUs did not exhibit conspicuous nonlinearities. — 2) MS responses to such pairs of MU activations usually showed a prolonged spindle pause. — 3) About 28% of 36pairs of MG MUs produced twitch tension less than expected for linear summation if activated nearly simultaneously. — 4) If two MUs both produced a spindle pause and possibly a relaxation discharge in an MS afferent, the near-synchronous activation of the units produced respective discharge variations that were less than expected for linear summation. If one MU produced an early discharge, contraction of another MU would often prevent it. — These results are discussed in regard to mechanisms of tremor suppression.     

Event-related cross-correlations between spike trains illustrated on interactions between motor units and muscle spindle afferents

A method is presented for computing correlation coefficients of two (or more) output spike trains in temporal relation to one (or more) input event trains. These event-related correlation functions are computed by convolving the output spike trains, represented as point processes, with rectangular pulses of selectable width, and by then calculating linear correlation coefficients for the pairs of amplitude values obtained from the two convolved processes in temporal relation to the input events. The merits of this technique are illustrated on stimulus trains delivered to motor units (MUs) and output spike trains recorded from muscle spindle afferents of the same cat hindlimb muscle. The correlation functions obtained show the temporal course of the correlated firings of the two afferents (mostly Ia afferents from primary muscle spindle endings) as a function of time from MU activation; they are compared with the conventional cross-correlation histograms (CCHs) between afferents and with peri-stimulus time histograms (PSTHs) between stimulus and afferent firing patterns. Stimulus-related cross-correlation functions as displayed here can be calculated for any three spike trains. Possible extensions of the method to larger numbers of input and output channels are also discussed.     

Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle

Declining motor unit discharge rates and H-reflex amplitude have been observed in separate experiments during fatiguing submaximal contractions in humans. The purpose of this experiment was to investigate motor unit discharge rate, H-reflex amplitude, and twitch contractile properties concurrently during a fatiguing submaximal isometric contraction of the ankle plantarflexors. Eleven healthy subjects performed fatiguing contractions of low force (25% maximal voluntary contraction (MVC)) or high force (42–66% MVC). Hoffmann (H)-reflexes, muscle compound action potentials (M-waves), twitch contractile properties, and motor unit discharges were recorded from the soleus muscle. In the low-force fatigue task, motor unit firing rate increased gradually over time, whereas the resting H-reflex was significantly depressed at 15% of endurance time and remained quasiconstant for the rest of the task. This suggests that the processes mediating the resting H-reflex depression are relatively independent of those modulating the motor unit firing rate during a low-force fatigue task. In the high-force fatigue task, a decline in the average motor unit discharge rate was accompanied by a decrease in the resting H-reflex amplitude and a prolongation of the twitch half-relaxation time (HRT) at the completion of the fatigue task. Overall, motor unit firing rate was modulated in parallel with changes in the twitch HRT, consistent with the muscle wisdom hypothesis.     

Relations among motor unit types,generated forces and muscle length in single motor units of anaesthetized cat peroneus longus muscle

The active length-tension curves of identified single motor units (MUs) belonging to peroneus longus muscle (PL) of anaesthetized adult cats were obtained by eliciting isometric single twitches and tetani. The recorded responses were evaluated by measuring the peak tension amplitude and the tension-time area at muscle lengths extending throughout the physiological length range of the muscle (mean 5.5 mm, standard deviation ±0.8). The muscle lengths at which each tested MU developed its maximal twitch (L _tw) and tetanic (L _te) tensions were determined and compared with the muscle length (L _o) at which the stimulation of all the -axons, innervating PL and contained in L7 ventral root, developed their maximal twitch tension. The mean of single MU L _tw values was at L _o+1.08±1.1 mm. Slow MUs showed the longest values of L _tw(L _o+1.6±1.0 mm). Single MUs stimulated at tetanic frequencies presented their L _te at values shorter than L _o (L _o–2.8±1.7 mm). Slow MUs had the shortest L _te (L _o–3.4±1.5 mm). For all the units L _te was shorter than L _tw. L _tw and L _te were, respectively, negatively and positively correlated with the developed tension. Optimal length values also appeared to be related to the MU types. The possibility is discussed that the muscle and tendon compliances and the high non-linearities to the applied forces are the main factors which can determine the differences among L _o, L _tw and L _te values. The relationships between MU type and optimal length values are suggested to be, at least partly, an epiphenomenon due to the different contraction strengths of the various MU types. However, the heterogeneous distribution of the MU types is brought into account to explain the dependence of L _tw and L _te values on MU type.     

Motor unit action potential rate and motor unit action potential shape properties in subjects with work-related chronic pain

The objective of this study was to investigate differences in motor control of the trapezius muscle in cases with work-related chronic pain, compared to healthy controls. Ten cases with chronic pain and 13 controls participated in the study. Electromyographic (EMG) signals were recorded from the upper trapezius during five computer work-related tasks. Motor control was assessed using global root-mean-square value (RMS_G), motor unit action potential (MUAP) rate (number of MUAPs per second, MR) and two MUAP shape parameters, i.e. root-mean-square (RMS_MUAP) and median frequency (FMED_MUAP). MR and FMED_MUAP were higher for the cases than for the controls (P<0.05). RMS_MUAP showed a trend for higher values in the chronic pain group (P<0.13), whereas RMS_G did not show a significant difference between the groups. The higher MR, FMED_MUAP and the trend for higher RMS_MUAP suggest that more high-threshold MUs contribute to low-level computer work-related tasks in chronic pain cases. Additionally, the results suggest that the input of the central nervous system to the muscle is higher in the cases with chronic pain.     

Voluntary strength,evoked twitch contractile properties and motor unit activation of knee extensors in obese and non-obese adolescent males

Summary The purpose of this study was to determine whether neural and/or muscular factors contributed to the inferior strength-related motor performances of obese adolescents. Subjects were 10 non-obese (14.6% fat) and 11 obese (32.3% fat) males matched for age (15–18 years), level of maturity (Tanner stages IV and V), lean body mass, and height. Peak torque (PT) was measured during maximal voluntary isometric (IS) and isokinetic (IK) knee extension (KE). Peak twitch torque (TT), time to peak torque (TPT), and half-relaxation time (HRT) of the knee extensors were elicited by percutaneous electrical stimulation. The interpolated twitch technique was used to determine the extent of motor unit activation (% MUA) during maximal voluntary IS KE. Knee extensor cross-sectional area (CSA) was determined by computed axial tomography taken at the mid-thigh. All strength and area measurements were made on the right side of the body. Obese subjects had significantly (P < 0.05) lower maximal voluntary IS and IK KE strength normalized for body weight, and significantly lower % MUA during IS KE. There were no significant differences (P > 0.05) between groups for absolute or normalized (for the product of muscle CSA and height) ISPT, IKPT, and TT, knee extensor CSA, or TPT and HRT. These results suggest that reduced MUA and a lower strength per mass ratio (due to excess fat) are probably important contributing factors to the poorer motor performances of the obese, especially for complex motor tasks involving large muscle groups and the support or moving of body weight.     

Creatine kinase MB and citrate synthase in type I and type II muscle fibres in trained and untrained men

Summary Total creatine kinase (CK), creatine kinase MB (CK-MB) and citrate synthase (CS) were determined in isolated and pooled type I and type II skeletal muscle fibres. Determinations were made on biopsies from 3 sedentary men, 3 junior cyclists and 2 elite cyclists. CS and CK-MB activities were higher in the trained groups in both fibre types. The total CK activity was not related to training status, although it was lower in type I fibres than in type II fibres (p<0.05). The reverse relation was observed for CS and CK-MB activities (p<0.01). The ratio of type I/type II for CS was not related to training status, while the corresponding ratio for CK-MB increased with a greater degree of endurance training. For a given increase in CS activity, the increase in CK-MB activity was greater in type I fibres than in type II fibres (p<0.01). Thus, with endurance training there seems to be a specific adaptation for CK-MB, particularly in type I fibres.     

Capillary supply,fibre types and fibre morphometry in rat tibialis anterior and diaphragm muscles after intermittent exposure to hypobaric hypoxia

Three groups of sedentary male rats were exposed to intermittent hypobaric hypoxia (IHH) for 22 days (4 h/day, 5 days/week) in a hypobaric chamber at a simulated altitude of 5,000 m. Tibialis anterior (TA) and diaphragm (DG) were removed at the end of the programme (H group), and 20 or 40 days later (P20 and P40 groups). A control group (C) was maintained at sea-level pressure and their TA and DG were compared to those of the experimental rats at the end of the IHH programme, and also 20 and 40 days later. We measured the fibre morphometry and capillaries of each muscle. Our results demonstrate that IHH does not change the fibre type composition (with reference to either their contractile or oxidative properties) for most muscle regions of the muscles analysed analysed. We found few significant differences in muscle capillarity and fibre morphometry for TA after IHH. However, IHH did induce some statistically significant changes in DG: capillary density of the H rats (736 capillaries/mm²) increased compared to C animals (610 capillaries/mm²). Although IHH did not change the fibre capillarization or morphometric parameters of fast fibre types, we observed reductions ranging from 7 to 13% in fibre area, perimeter and diffusion distances between C and H for slow fibres. Moreover, these morphometric changes accounted for increases of 10–20% in capillarization, fibre unit area and fibre unit perimeter. This indicates that SO fibres are more sensitive to IHH than both fast fibre types.