Changes in muscle stiffness produced by motor units of different types in peroneus longus muscle of cat

1. The effects of maximal tetanic contractions of varying numbers of motor units of the same type [slow (S), fast fatigue-resistant (FR), or fast fatigable (FF)] on the mechanical responses to muscle stretch were studied in the peroneus longus muscle of anesthetized cats. 2. Two types of stiffness measurements were made: 1) an average stiffness, defined as the tension change from the beginning to end of a 0.5-mm ramp stretch; and 2) a dynamic stiffness, defined as the ratio of peak-to-peak tension to amplitude of a maintained 85-microns sinusoidal stretch at frequencies of 10-80 Hz. 3. Contractions of slow and fast units elicited different increases in average stiffness. Type S units, although developing much smaller tetanic tensions than fast ones, produced a resistance to stretch comparable with or greater than that of fast units developing much higher tensions. 4. For comparable tetanic tensions, slow units also elicited a greater dynamic stiffness than fast units. During sinusoidal stretch, changes in muscle tension led changes in muscle length during contraction of S units, but the reverse was observed for frequencies 30-50 Hz during contraction of FF units. This suggests that the latter perform oscillatory work on the driving apparatus. 5. Type S units, whose low-threshold motoneurons are the first to be recruited, appear well adapted to play a role in posture and in slow movements because of the resistance they offer to forces tending to change joint position or to oppose the progression of slow movements.     

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.     

Distribution of physiological types of motor units in the cat peroneus tertius muscle

Summary Motor units of the cat peroneus tertius muscle were systematically analyzed using the criteria established by Burke et al. (1973). On the basis of their speed of contraction and resistance to fatigue, 121 (97%) of 125 motor units examined in ten adult cats could be classified as belonging to one of four types: fast-fatiguable (FF), fast-resistant (FR), fast-intermediate (FI), and slow-resistant (S).Peroneus tertius was found to contain 30% FF motor units, 9% FI units, 39% FR units, and 22% S units. Contraction times of fast motor units (FF, FR, and FI) ranged from 15 to 27 ms and those of S units from 26 to 42 ms. The mean tetanic tensions were 37 g for FF units, 29 g for FI units, 7.5 g for FR units, and 1.1 g for S units.Fast motor units displayed considerable post-tetanic potentiation of twitch tension. Under similar conditions of stimulation, FF units appeared able to potentiate more and faster than FR units.Supported in part by the Fondation pour la Recherche Médicale Française     

Power developed by motor units of the peroneus tertius muscle of the cat

The mechanical properties of motor units have been extensively studied under isometric conditions. Under dynamic conditions, the relationship between the force developed by single motor units and the muscle shortening velocity was determined for relatively high frequencies of activation. However, the interaction between the force-shortening velocity relation and the force-rate of activation relation was still unknown. We studied the power (which is the product of force and velocity) developed by single or groups of motor units during sinusoidal muscle stretches of 1-, 2-, 4-, 6-, and 8-Hz frequency. Motor units were stimulated with frequencies of 20, 40, 60, 80, 100, and 120 Hz during the shortening phase of the muscle stretch. The relationships, for different shortening velocities, between the power developed by single or groups of motor units and the frequency of stimulation were sigmoidal. However, these relations were not proportional to the shortening velocity. The relationships, for different frequencies of stimulation, between the power and the shortening velocity exhibited a maximum. The shortening velocity at which this maximum occurred increased with the frequency of stimulation. Slow motor units showed the lowest of those shortening velocities, whereas the fast fatigable motor units showed the highest. Groups of slow (or fast fatigue resistant) motor units had similar shortening velocities to those of single slow (or fast fatigue resistant) motor units. A mathematical function was fitted, using regression analysis, for all single and groups of motor units to the relationship among the power, the shortening velocity, and the frequency of activation. This function allowed examination, for different shortening velocity-frequency of activation combinations, of the relationship between the power developed by single and groups of motor units and the maximal isometric tetanic force they developed. These relationships were usually not monotonic but a monotonic relation could be obtained if slow, fast resistant, and fast fatigable motor units were activated at different frequencies. These results suggest that during a movement, the frequency of activation of motor units is mainly adjusted to the movement velocity and that the power developed by a muscle is mainly adjusted by the number of recruited motor units.     

Summation of tension in motor units of the soleus muscle of the cat

In the cat soleus muscle which is exclusively composed of slow motor units the discrepancy between the sum of individual tensions and the tension on combined stimulation of several motor units was found to be much less than previously reported for slow motor units of peroneus longus. In peroneus the tension on combined stimulation was systematically larger than the value predicted from the sum of individual tensions. For both muscles it was possible to reduce the difference between observed and expected values by comparing the tension on combined stimulation with the sum of tensions, not of single motor units, but of groups of units. It is concluded that whenever tension is measured for single motor units, especially slow units in mixed muscles, the values obtained may be modified by frictional forces. The size of the effect appears to vary from one preparation to the next.     

Cross-reinnervated motor units in cat muscle. I. Flexor digitorum longus muscle units reinnervated by soleus motoneurons

The properties of flexor digitorum longus (FDL) muscles and of individual motor units were studied in cats 30-50 wk after self-reinnervation by FDL motoneurons (FDL----FDL) or cross-reinnervation by soleus (SOL) motoneurons (SOL----FDL). Individual motor units were functionally isolated by intracellular recording and stimulation of identified SOL alpha-motoneurons. Glycogen-depletion methods permitted histochemical study of muscle fibers belonging to physiologically characterized muscle units. The observations were compared with data from normal cat FDL muscles and motor units (27). Intentionally self-reinnervated FDL muscles (FDL----FDL; n = 5) were normal in size and wet weight. FDL----FDL motor units could be classified into the same physiological categories found in normal FDL [types: fast contracting, fatigable (FF), fast contracting, fatigue resistant (FR), and slow (S); n = 24], with approximately the same proportions as normal. The histochemical muscle fiber types associated with these categories were also qualitatively normal although there was evidence of marked distortion of the normal histochemical mosaic. These data confirm other studies of self-reinnervation and suggest that self-reinnervation can produce complete interconversion of muscle fiber types. Cross-reinnervation of FDL muscle by SOL motoneurons (SOL----FDL; n = 12) produced muscles that were smaller (about half the normal wet weight) and more red than normal. SOL----FDL muscle contracted more slowly than normal or FDL----FDL muscles and had much higher proportions of histochemical type I muscle fibers. In those SOL----FDL muscles, in which little or no unwanted self-reinnervation could be demonstrated, greater than 95% of the muscle fibers were type I. Forty-one individual motor units in SOL----FDL muscles were isolated by intracellular penetration in functionally identified SOL alpha-motoneurons. Their muscle units were all type S by physiological criteria (absence of "sag" in unfused tetani and marked resistance to fatigue). SOL----FDL muscle units had contraction times and fatigue properties that were essentially identical to those of type S units in the normal FDL. All of the seven units, successfully studied by glycogen depletion, exhibited histochemical type I fibers. SOL motoneurons that innervated FDL muscle units had slightly shorter afterhyperpolarization durations than normal SOL cells, but axonal conduction velocities were normal.(ABSTRACT TRUNCATED AT 400 WORDS)     

Gradation of isometric tension by different activation rates in motor units of cat flexor carpi radialis muscle

Single motor units of the flexor carpi radialis (FCR) muscle were activated with a series of constant-rate stimulus trains to study the relation between the frequency of activation and isometric tension development (F-T relation). The tension produced by each stimulus train was expressed as a percentage of the maximum tension-time area (Amax) found for a given unit. Between 25 and 75% Amax a clear separation was seen in the rates needed to produce the same relative tension for the F-T curves of slow-twitch (type S) and fast-twitch (type F) units. Over the steepest portion of the F-T curve (25-50% Amax), where tension output was most sensitive to changes in activation rate, type F units required substantially higher stimulation rates (30 pps) to achieve the same relative tension output as type S units. Furthermore, the frequency range that corresponded to the steep portion of the curve was 2.3 times greater for type F units. For both type S and F units, twitch duration was deemed to be an important determinant of the F-T curve, as has been shown previously. A direct continuous relation was seen between the integrated twitch time (ITT) and the stimulus interval needed to produce 50% Amax (r = 0.94, P less than 0.001). Thus, units that had relatively brief twitches required higher activation rates to achieve the same relative percentage of Amax. Comparison of F-T curves from FCR with those derived by other investigators for cat hindlimb units (medial gastrocnemius and peroneus longus) revealed that significant differences in activation rates were needed to produce the same percentage of Amax throughout the midrange of the F-T curve. At 50% Amax, type F units in FCR required activation rates approximately 20 pps higher than type F units in the hindlimb. Type S units in FCR required only slightly higher rates (approximately equal to 5 pps). Based on a number of well-founded assumptions, F-T curves derived from FCR units were used to estimate the potential contribution of rate coding to total muscle tension by type S and F units. This analysis leads to the conclusion that rate modulation is a potentially important factor in the gradation of tension for the FCR muscle.     

Cross-reinnervated motor units in cat muscle. II. Soleus muscle reinnervated by flexor digitorum longus motoneurons

The properties of whole soleus (SOL) muscles and of individual motor units were studied in cats 30-50 wk after self-reinnervation by soleus (SOL) motoneurons (SOL----SOL) or cross-reinnervation by flexor digitorum longus (FDL) motoneurons (FDL----SOL). As in the preceding paper (22), intracellular and glycogen-depletion methods were used to examine the physiological and histochemical properties of individual motor units. The results were compared with data from normal SOL motor units (8, 12). Intentionally self-reinnervated SOL muscles (SOL----SOL; n = 6) were normal in size and wet weight, and all of the five SOL----SOL motor units studied had physiological and histochemical characteristics that matched those of normal SOL units. Cross-reinnervation of SOL by FDL alpha-motoneurons (FDL----SOL; n = 7) produced muscles with wet weights and appearance essentially identical to normal SOL. However, whole-muscle twitch contraction times were much shorter (mean 60.4 ms) than those of normal (mean 136.9 ms, n = 18) or SOL----SOL muscles (mean 115.3 ms; n = 6). Despite this difference, none of the FDL----SOL muscles contained more than 7% histochemical type II muscle fibers, all of which were type IIA. Normal cat SOL muscles can contain up to 5% type IIA fibers, but none of our SOL----SOL muscles showed any type II fibers. Two FDL----SOL muscles had significant amounts of unintended self-reinnervation, permitting side-by-side comparison of FDL----SOL and SOL----SOL muscle fibers. The twitch contraction times of the two populations differed markedly, but they were histochemically indistinguishable except for the fact that SOL----SOL fibers had high neutral fat content (as do normal SOL fibers), whereas FDL----SOL showed much lower fat content. The 23 FDL----SOL muscle units studied were classified as physiological type S by criteria ("sag" test and fatigue resistance) used to identify motor-unit types in normal cat muscles. All five of the FDL----SOL units studied histochemically after glycogen depletion showed the type I histochemical profile, which is characteristic of the normal cat SOL. In marked contrast to the preceding study, cross-reinnervation of cat SOL by FDL motoneurons produced no conversion of muscle-unit properties into those associated with fast-twitch unit types, despite significant decreases in isometric twitch contraction time. The altered twitch speed was not associated with evident changes in conventional myofibrillar adenosine triphosphatase (ATPase) histochemistry.(ABSTRACT TRUNCATED AT 400 WORDS)     

Properties of motor units in nerve-intact autografts of cat extensor digitorum longus muscles

1. In cats, isometric contractile properties were measured on five extensor digitorum longus (EDL) muscles and four EDL muscle grafts 150-270 days after autografting with nerves intact. Comparisons were made between the properties of whole muscles and grafts and between 36 motor units in control EDL muscles and 41 motor units in grafts. 2. The time-to-peak twitch force (TPT) of 23 +/- 1.7 (SE) ms for grafts was significantly prolonged compared with the value of 17 +/- 0.7 ms observed for whole EDL muscles. The mean values for the TPT of motor units were not different from the respective values for whole grafts or for whole muscles. The maximum specific force of whole grafts of 19.7 +/- 0.6 (SE) N/cm2 was significantly less than the control value of 23.6 +/- 0.6 N/cm2, an observation consistent with all previous data on the maximum specific force of grafts and control muscles. 3. Based on the presence or absence of sag and an index of fatigue, motor units were classified as fast fatigable (FF), fast intermediate (FI), fast fatigue-resistant (FR), and slow (S). Motor units were classified 33% FF, 22% FI, 27% FR, and 17% S in control muscles and 17% FF, 43% FI, 29% FR, and 12% S in autografted muscles. Compared with control muscles, the number of small FF units increased significantly in the autografts, but no significant difference was observed in the fatigue properties of motor units.(ABSTRACT TRUNCATED AT 250 WORDS)     

Maximum tension predicts relative endurance of fast-twitch motor units in the cat

1. The relationships between maximum tetanic tension (P0), endurance time, and axonal conduction velocity (CV) were investigated in fast-twitch motor units of the cat flexor carpi radialis (FCR) and medial gastrocnemius (MG) muscles, and in one flexor digitorum longus (FDL) muscle. Endurance time was the length of time that a unit could maintain 25% of its maximum tetanic tension during a sustained contraction. Motor-unit tension was "clamped" at 25% of maximum by altering the stimulation rate of a unit's motor axon through computer feedback control. 2. In individual experiments, including the one investigated FDL muscle, an inverse relation was consistently found between maximum tension and endurance time. Pooled data from the FCR and MG muscles also resulted in significant correlations between maximum tetanic tension and endurance time. 3. Following the force-clamp contraction, some motor units were subjected to the standard fatigue test of Burke and colleagues (6). Motor units were classified as type FR (fast twitch, fatigue resistant) or type FF* (fast twitch, fast fatiguing after the force-clamp contraction). For both type FR and FF* units, maximum tetanic tension and endurance time were found to be inversely related. However, no correlation was found between maximum tetanic tension and fatigue index for type FR units. Only when all type F (FR + FF*) units were considered as a population was there a significant correlation between these two properties. 4. Other investigators have shown that maximum tetanic tension and axonal conduction velocity are highly correlated with the recruitment order of motoneurons (e.g., Refs. 2, 26). Endurance time was found to be more tightly coupled with contraction strength than with conduction velocity. In 12 of 14 experiments, significant Spearman rank correlation coefficients were found between endurance time and tension, whereas significant correlations were found in only 3 of 14 experiments for endurance time and conduction velocity. 5. Pairs of motor units isolated from the same muscle were formed to see if the unit with the smaller tension had the slower conduction velocity and the longer endurance time. Across all muscles, the probability that the unit with the smallest tension had the greatest endurance time was 0.91 (441 of 487 pairs). By contrast, the probability that the least forceful unit of the pair had the slowest conduction velocity was 0.61. 6. In four experiments, pairs of type-identified units were examined. Among FR-FR pairs, the least forceful unit had the greatest endurance time in 88% of 43 pairs. For FF*-FF* pairs, the percentage was somewhat lower, 72% of 29 pairs.(ABSTRACT TRUNCATED AT 400 WORDS)     

An investigation into the site of termination of static gamma fibres within muscle spindles of the cat peroneus longus muscle.

1. The distribution of static fusimotor fibres to intrafusal muscle fibres of cat peroneus longus muscle spindles was investigated using the glycogen-depletion technique of Edstr?m & Kugelberg (1968). Single static gamma fibres were stimulation intermittently at high rates for 3 hr with the blood supply occluded for some of this time. Subsequently the portion of muscle containing the activated spindles was fixed, sectioned and stained for glycogen with the periodic acid-Schiff (PAS) method. 2. Ten static axons caused depletion in eleven spindles. In five of these the only glycogen-depleted fibres were nuclear chain fibres. In the other six spindles one nuclear bag fibre was depleted in addition to chain fibres and this was always the larger of the two within the spindle. 3. These results on a medium-sized hind limb muscle are compared with findings concerning the distribution of static gamma fibre axons previously investigated only in very small muscles. The results agree in showing that nearly all static gamma fibres innervate nuclear chain fibres but that in 50-75% of the times in which static gamma fibres innervate spindles the distribution is to bag fibres as well as to chain fibres. The interpretation to be put upon this is uncertain. One possibility with which the results from peroneus longus are consistent is that the bag fibres which are usually innervated by static axons are the 'intermediate' bag fibres whose ultrastructure has recently been shown to resemble that of chain fibres.     

Classification of motor units in flexor carpi radialis muscle of the cat

Motor units in the cat flexor carpi radialis (FCR) muscle, one of two primary wrist flexors, were classified into three groups: slow twitch, fatigue resistant (S); fast twitch, fatigue resistant (FR); and fast twitch, fatigue sensitive (FF). Classification was based on 1) the ratio of the tension-time area produced by a train of stimuli delivered at 40 pps and the maximum tension-time area (A40/Amax), and 2) the cumulative force index (CFI), calculated from a series of trains (40 pps) delivered intermittently for a period of 4 min. The CFI is defined as the ratio between the force accumulated in the last 2 min of stimulation to the first 2 min of stimulation. Motor units with values for A40/Amax greater than 0.50 were classified as type S units, and less than 0.50 as type F. A40/Amax is essentially equivalent to the "sag" profile of an unfused tetanus in its ability to separate units into "slow" and "fast" contracting units. In general, units with area ratios less than 0.50 had twitch contraction times less than 25 ms, whereas units with area ratios greater than 0.50 had contraction times greater than 25 ms. Separation of type F units into two groups was based on the CFI, with ratios less than or equal to 0.75 corresponding to type FF units and greater than 0.75 as type FR units. Type S units also had CFIs greater than 0.75. Based on this classification scheme, 40.4% of FCR motor units were type S, 37.5% type FR, and 22.1% type FF. The a priori assumption of three motor-unit types based on the distributions of A40/Amax and CFI was evaluated by cluster analysis. The analysis supported the assumption of three primary groups of motor units. Furthermore, when cluster formation proceeded to the point where only three clusters remained in the analysis, each of these clusters consisted exclusively of one type of unit (i.e., S, FR, or FF). The validity of the classification scheme was further tested by stepwise discriminant analysis. Units classified as types S, FR, and FF were predicted to be classified with 100% accuracy. All units had a high probability (a posteriori) of having group membership in their originally classified group (P greater than 0.99 for 129 units; P greater than 0.90 for 7 units). The duration of potentiated twitch contractions for type FR and FF units was found to be less than reported for most populations of hindlimb units.(ABSTRACT TRUNCATED AT 400 WORDS)     

Summation of forces from multiple motor units in the cat soleus muscle

Nearly all muscle models and most motor control concepts assume that forces from individual muscle fibers and motor units sum in an additive manner once effects of in-series tendon compliance are taken into account. Due to the numerous mechanical linkages between individual fibers, though, it is unclear whether this assumption is warranted. This work examined motor unit force summation over a wide range of muscle forces in the cat soleus. Nonadditive summation implies a nonlinear summation of motor unit forces. Summation nonlinearities were quantified during interactions of 10 individual motor units and 4 motor unit bundles containing approximately 10 units each. These protocols allowed motor unit force summation to be examined from approximately 0 to 25% of tetanic muscle force. Nonlinear summation was assessed by comparing the actual forces to the algebraic sum of individual units and bundles stimulated in isolation. Superadditive summation meant that the actual force exceeded the algebraic sum, whereas subadditive summation meant that the actual force was smaller than the algebraic sum. Experiments tested the hypothesis that superadditive summation occurs at low force levels when few motor units are recruited, whereas subadditive summation prevails above 10% of tetanic force. Results were consistent with this hypothesis. As in previous studies, nonlinear summation in the soleus was modest, but a clear transition from predominately superadditive to predominantly subadditive summation occurred in the range of 6-8% of tetanic force. The largest nonlinearities were transient and appeared at the onset of recruitment and derecruitment of groups of motor units. The results are discussed in terms of the mechanical properties of the connective tissue forming the tendon and linking muscle fibers.     

Physiological and histochemical characteristics of motor units in cat tibialis anterior and extensor digitorum longus muscles

1. Intracellular recording and stimulation techniques were used to study the normal motor-unit population of tibialis anterior (TA) and extensor digitorum longus (EDL) muscles in the cat. Histochemical staining of the whole muscle and glycogen depletion of single motor units were performed. These results may be compared to those of their extensor antagonist, medial gastrocnemius (MG), as reported in studies by Burke and co-workers (7, 11, 13). 2. On the basis of two physiological properties, "sag" and fatigue resistance, the motor units in both TA and EDL could be classified into the same categories (types FF, F(int), FR, and S) as in MG (11). In contrast to MG, TA and EDL had nearly twice as many type-FR motor units and only half as many type-S motor units. 3. Glycogen depletion of representative single motor units of types FF and FR suggests a close correspondence between the physiological classification and a unique histochemical profile. No type-S units were depleted. 4. On the basis of histochemical staining, the muscle fibers in TA were presumed to belong to type-FF, -FR, or -S motor units. TA had a higher proportion of type-FR and a lower proportion of type-S muscle fibers than are found in MG. A striking feature was the variation in the proportion of each fiber type in different regions of TA. The anterolateral portion had mostly types FF and FR, while the posteriomedial portion had more types FR and S. 5. The twitch time to peak (TwTP) of isometric motor-unit contractions was generally quite fast with none having TwTP greater than 55 ms. The mean TwTP (not in EDL) and the mean tetanic tension of each motor-unit type were significantly different from each other. Most of the motor units exhibited significant postetanic potentiation of twitch tension and a corresponding lengthening of half-relaxation time and to a lesser degree, twitch contraction time. 6. There was a significant relationship between the inverse of motoneuronal input resistance and either tetanic tension or twitch contraction time. These relationships were not apparent when axonal conduction velocity rather than input resistance was used as an index of motoneuron size. The mean input resistances of the three major motor-unit types were significantly different while the mean conduction velocities of types FF and FR were nearly identical. A weak positive correlation was observed between the TwTP and the afterhyperpolarization of TA and EDL motoneurons. 7. In general, the mechanical characteristics and intrinsic motoneuronal properties of TA and EDL appear to parallel the organization of their extensor antagonist, MG, with some important quantitative differences that may reflect their different functional roles.