Maximal force as a function of anatomical features of motor units in the cat tibialis anterior

In 11 tibialis anterior muscles of the cat, a single motor unit was characterized physiologically and subsequently depleted of its glycogen through repetitive stimulation of an isolated ventral root filament. Muscle cross sections were stained for glycogen using a periodic acid-Schiff reaction, and single-fiber optical densities were determined to identify those fibers belonging to the stimulated motor unit. Innervation ratios were determined by counting the total number of muscle fibers in a motor unit in sections taken through several levels of the muscle. The average innervation ratios for the fast, fatigueable (FF) and fast, fatigue-resistant (FR) units were similar. However, the slow units (S) contained 61% fewer fibers than the fast units (FF and FR). Muscle fibers belonging to S and FR units were similar in cross-sectional area, whereas fibers belonging to FF units were significantly larger than fibers belonging to either S or FR units. Additionally, muscle fibers innervated by a single motoneuron varied by two- to eightfold in cross-sectional area. Specific tensions, based on total cross-sectional area determined by summing the areas of all muscle fibers of each unit, showed a modest difference between fast and slow units, the means being 23.5 and 17.2 N X cm-2, respectively. Variations in maximum tension among units could be explained principally by innervation ratio, although fiber cross-sectional area and specific tension did contribute to differences between unit types.     

Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. I. Influence of motoneurons on muscle

This study addresses two questions: is reinnervation of mammalian skeletal muscle selective with respect to motor-unit type? And to what degree may muscle-unit contractile properties be determined by the motoneuron? Properties of individual motor units were examined following cross-reinnervation (X-reinnervation) of lateral gastrocnemius (LG) and soleus muscles by the medial gastrocnemius (MG) nerve in the cat. We examined animals at two postoperative times: 9-10 wk (medX) and 9-11 mo (longX). For comparison, properties of normal LG and soleus motor units were studied. Motor units were classified on the basis of their contractile response as fast contracting fatigable, fast intermediate, fast contracting fatigue resistant, or slow (types FF, FI, FR, or S, respectively) (13,29). Muscle fibers were classified on the basis of histochemical properties as fast glycolytic, fast oxidative glycolytic, or slow oxidative (types FG, FOG, or SO, respectively) (61). Reinnervation of LG and soleus was not selective with respect to motor-unit type. Both muscles were innervated by a full complement of MG motoneuron types, apparently in normal MG proportions. MG motoneurons determined LG muscle fibers' properties to a similar degree as reinnervated MG muscle fibers. In contrast, soleus muscle fibers "resisted" the influence of MG motoneurons. Thus, although longX-reinnervated LG muscle (longX LG) had a motor-unit type distribution similar to normal or self-reinnervated MG, longX soleus contained predominantly type S motor units. Overall mean values for muscle-unit contractile properties reflected this motor-unit type distribution. Muscle units in longX LG and longX soleus had contractile properties typical of the same motor-unit type in normal LG or soleus, respectively. Motor-unit types were recognizable at 10 wk X-reinnervation, although muscle-unit tensions were lower than after 10 mo. The proportions of fast and slow motor units in medX LG were similar to longX LG, although a greater proportion of fast units were resistant to fatigue at 10 wk. There were fewer fast units in medX soleus than longX soleus, which suggested that motor-unit type conversion or innervation of muscle fibers by fast motoneurons is not complete at 10 wk. We conclude that reinnervation of the LG and soleus muscles by MG motoneurons was not selective with respect to motor-unit type. MG motoneurons determined LG muscle properties to a similar degree as self-reinnervated MG muscle fibers. Soleus muscle fibers resisted the influence of MG motoneurons, representing a limit to neural determination of muscle properties.     

Comparison of physiological and histochemical properties of motor units after cross-reinnervation of antagonistic muscles in the cat hindlimb

1. Physiological and histochemical properties of the cat ankle extensor muscles, the lateral and medial gastrocnemius, and the soleus were studied after cross-reinnervation by flexor motoneurons. 2. Tibial and common peroneal nerves were cut and cross-united in the popliteal fossa of 2- to 6-mo-old cats. Eighteen to 24 mo later, single motor units were isolated by dissection and stimulation of ventral root filaments and classified into four types: fast-twitch, fatigable (FF), fast-twitch with intermediate fatigue resistance (FI), fast-twitch, fatigue-resistant (FR), and slow, fatigue-resistant (S). Muscle fibers were classified as fast glycolytic (FG), fast, oxidative glycolytic (FOG), and slow oxidative (SO) on the basis of histochemical staining. 3. Although motor-unit force was normally well correlated with the size of the innervating motor axon in the cross-reinnervated muscles, the force of different unit types overlapped considerably. The reinnervated motor units also showed a higher than normal degree of fatigability. 4. The range of muscle unit forces in cross-reinnervated triceps surae muscles was the same as in the normally innervated triceps surae muscles. This range is 2-3 times greater than the flexor muscles, which the common peroneal nerve normally supplies. The range of contraction speed of units in the cross-reinnervated extensor muscles was comparable to that in the flexor muscles, consistent with a motoneuron-specific determination of muscle speed (28). 5. SO and FOG muscle fibers were found in all reinnervated triceps surae muscles, but FG fibers were only found in reinnervated medial gastrocnemius (MG) and lateral gastrocnemius (LG) muscles, consistent with previous findings of the resistance of soleus muscles to complete conversion (10, 16, 20, 21). Type grouping of muscle fibers was characteristic of the reinnervated muscles. 6. Reinnervated SO muscle fibers were larger than the corresponding fibers in normally innervated muscles as were the estimated number of muscle fibers innervated by slow motor axons. Nonetheless, the force generated by the S motor units remained relatively smaller than FR and FF units. The relative contributions of the number, cross-sectional area and specific tension to the force generation of reinnervated motor units are discussed.     

Anatomy and innervation patterns of cat lateral gastrocnemius and plantaris muscles

The anatomy, fiber architecture, and innervation patterns of cat lateral gastrocnemius (LG) and plantaris (P) muscles are described. The plantaris is a simple unipennate muscle arising from an aponeurosis in common with LG and inserting primarily into the tendon of m. flexor digitorum brevis, but with ligamentous connections to the calcaneus. The lateral gastrocnemius is more complex and contains three distinctly identifiable heads, each of which is a unipennate band of fibers coursing between a proximally attached aponeurosis of origin and a distal aponeurosis of insertion that gives rise to the tendocalcaneus. Following microdissection of the LG and P nerves, and using glycogen depletion of the primary muscle nerve branches, discrete motor subvolumes are demonstrated in both muscles. Despite large specific differences in fiber architecture between the LG and P muscles, their organization into compartments about primary muscle nerve branches is fundamentally similar. This principle of organization may be a basis for the observed functional and structural properties of other vertebrate muscles. It may thus constitute a unifying concept in the organization of motor control mechanisms.     

A histochemical analysis of identified compartments of cat lateral gastrocnemius muscle

The lateral gastrocnemius muscle of cats can be divided into four discrete subvolumes or compartments which are supplied by the primary branches of its muscle nerve. The histochemical profile of each compartment was determined from the reaction for myosin ATPase after acid preincubation. Fibers were classified as fast-twitch glycolytic (FG), fast-twitch oxidative-glycolytic (FOG), or slow-twitch oxidative (SO). Each compartment in each cat examined was found to contain a relatively uniform distribution of different types of fibers. The most proximal LG compartment contains mainly type FG fibers, with relatively few type SO fibers; the most distal compartment, while still predominated by type FG fibers, contains a significantly larger proportion of type SO fibers. The histochemical profile of the intermediate compartments indicates that they contain fibers which lie intermediate in composition between these two. These results are consistent with the notion that LG compartments consist of aggregations of motor units, arranged such that muscle fibers comprising a single motor unit are contained within a single compartment.     

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)     

Motor units and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation

A reexamination of the question of specificity of reinnervation of fast and slow muscle was undertaken using the original "self" nerve supply to the fast lateral gastrocnemius (LG) and slow soleus muscles in the rat hindlimb. This paradigm takes advantage of the unusual situation of a common nerve branch, which supplies both a fast and slow muscle, and of the opportunity to keep the reinnervating nerve in its normal position. In addition it provides a test of the effects of cross-reinnervation among muscles of the same functional group. The properties of soleus and LG muscles and of individual muscle units were characterized in normal rats and in rats 4-14 mo after cutting the lateral gastrocnemius-soleus (LGS) nerve and suture of the proximal stump to the dorsal surface of the LG muscle. Individual muscle units were functionally isolated by stimulation of single motor axons to LG or soleus muscle contained in teased filaments in the L4 and L5 ventral roots. Motor units were classified as fast contracting fatiguable (FF), fast contracting fatigue resistant (FR), and slow (S) on the basis of criteria described in the cat by Burke et al. and applied to rat muscle units by Gillespie et al. Muscle fibers were classified as fast glycolytic (FG), fast oxidative glycolytic (FOG), and slow oxidative (SO) on the basis of histochemical staining for myosin ATPase, nicotinamide-adenine dinucleotide diaphorase (NADH-D), and alpha-glycerophosphate (alpha-GPD). Reinnervated muscles developed less force and weighed less in accordance with having fewer than normal motor units and having lost denervated muscle fibers. Normal LG contained a small proportion of S-type motor units (9%), whereas the majority (80%) of control soleus units were S type. After reinnervation, each muscle contained similar proportions of fast and slow motor units with S-type units constituting 30% of units in both muscles. When compared with the normal motor-unit sample, there was no significant change in average twitch and tetanic force in reinnervated muscles for each type of motor unit. However, the range within each type was greater, and there was considerable overlap between types. Twitch contraction time was inversely correlated with force in normal and reinnervated muscles as shown previously in self- and cross-reinnervated LGS in the cat. Changes in proportions of motor units in reinnervated LG were accompanied by corresponding changes in histochemical muscle types. This contrasted with reinnervated soleus in which the proportion of muscle fiber types was not significantly changed from normal despite significant change in motor-unit proportions.(ABSTRACT TRUNCATED AT 400 WORDS)     

Fast-conducting skeletofusimotor axons supplying intrafusal chain fibers in the cat peroneus tertius muscle.

1. In six experiments on cat peroneus tertius muscle, from 12 to 23 motor axons with conduction velocities above 85 m/s were repetitively stimulated so as to produce glycogen depletion in the muscle fibers they innervated. 2. The whole muscle was then quick-frozen, serially cut, stained to demonstrate glycogen, and examined for intrafusal glycogen depletion. 3. Zones of glycogen depletion were found in 27 of the 99 examined spindles: they were almost invariably located on chain fibers and specifically on the longest of the chain fibers in affected spindles. 4. Since it was shown that there are no purely fusimotor fast axons in the motor supply to peroneus tertius, it is concluded that skeletofusimotor axons are present among the fastest motor axons to this muscle.     

The motor-unit population of the cat tenuissimus muscle

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.     

Internal structure of cat extraocular muscle.

Teasing preparations of cat extraocular muscles (EOM) were used to study the arrangement of muscle fibers and the distribution of the different cholinesterase-positive sites, i.e. (1) large motor endplates, (2) small motor endings of the 'en grappe' type, (3) myotendinous junctions and (4) myomyous junctions. The distribution of these cholinesterase-positive structures gives clear evidence of a complex muscle architecture of cat EOM. In the global layer of cat EOM, only multiply innervated muscle fibers run the whole length of the muscle. The focally innervated muscle fibers are generally shorter; they are usually arranged in series of two to three fibers being interconnected by myomyous junctions. Moreover, muscle fiber splitting is frequently present resulting in a netlike arrangement of muscle fibers. Most of the myomyous junctions occur between focally innervated muscle fibers, but also end-to-side connections of focally to multiply innervated muscle fibers are observed; multiply innervated muscle fi0ers have not been found connected to each other. In this layer, large motor endplates are distributed in several bands between origin and insertion. In the orbital layer all muscle fibers run from tendon to tendon, focally as well as multiply innervated ones. Here, large motor endplates are confined to a band in the middle of the muscle, and myomyous junctions are generally absent. Some functional implications of this complex architecture of cat EOM are discussed.     

Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. II. Influence of muscle on motoneurons

We tested whether the muscle innervated may influence the expression of motoneuron electrical properties. Properties of individual motor units were examined following cross-reinnervation (X-reinnervation) of cat lateral gastrocnemius (LG) and soleus muscles by the medial gastrocnemius (MG) nerve. We examined animals at two postoperative times: 9-10 wk (medX) and 9-11 mo (longX). For comparison, normal LG and soleus motoneuron properties were also studied. Motor units were classified on the basis of their contractile responses as fast contracting fatigable, fast intermediate fast contracting fatigue resistant, and slow types FF, FI, FR, or S, respectively) (9, 21). Motoneuron electrical properties (rheobase, input resistance, axonal conduction velocity, afterhyperpolarization) were measured. After 9-11 mo, MG motoneurons that innervated LG muscle showed recovery of electrical properties similar to self-regenerated MG motoneurons. The relationships between motoneuron electrical properties were largely similar to self-regenerated MG. For MG motoneurons that innervated LG, motoneuron type (65) predicted motor-unit type in 74% of cases. LongX-soleus motoneurons differed from longX-LG motoneurons or self-regenerated MG motoneurons in mean values for motoneuron electrical properties. The differences in overall means reflected the predominance of type S motor units. The relationships between motoneuron electrical properties were also different than in self-regenerated MG motoneurons. In all cases, the alterations were in the direction of properties of type S units, and the relationship between normal soleus motoneurons and their muscle units. Within motor-unit types, the mean values were typical for that type in self-regenerated MG. Motoneuron type (65) was a fairly strong predictor of motor-unit type in longX soleus. MG motoneurons that innervated soleus displayed altered values for axonal conduction velocity, rheobase, and input resistance, which could indicate incomplete recovery from the axotomized state. However, although mean afterhyperpolarization (AHP) half-decay time was unaltered by axotomy (25), this parameter was significantly lengthened in MG motoneurons that innervated soleus muscle. There were, however, individual motoneuron-muscle-unit mismatches, which suggested that longer mean AHP half-decay time may also be due to incomplete recovery of a subpopulation of motoneurons. Those MG motoneurons able to specify soleus muscle-fiber type exhibited motoneuron electrical properties typical of that same motoneuron type in self-regenerated MG.(ABSTRACT TRUNCATED AT 400 WORDS)     

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)     

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.     

Anatomy and innervation ratios in motor units of cat gastrocnemius

1. Muscle fibres belonging to single motor units of identified type were studied in frozen sections of cat medial and lateral gastrocnemius muscles. Reconstruction of the distribution of fibres in individual units showed that the territories of all three physiological types present in the cat medial gastrocnemius were quite extensive. Within its territory, fibres belonging to the studied unit were distributed more or less uniformly without localized collections. The density of unit fibres suggests that, in cat medial gastrocnemius, a given region of the muscle may be shared by as many as fifty different muscle units.

2. Direct determination of innervation ratios in identified muscle units required complete reconstruction of the three-dimensional distribution of unit fibres within the whole medial gastrocnemius. Satisfactory results were obtained with two type FF units and one type FR unit.

3. Indirect estimates of the average innervation ratios expected for muscle units of different physiological type were obtained using counts of muscle fibres with characteristic histochemical profiles and data on relative frequencies of motor units of known type in the medial gastrocnemius unit pool. Such indirect estimates of innervation ratios agreed with the results of direct fibre counts in identified units for types FF and FR muscle units. Taken in sum, the available evidence suggests that an average muscle unit in the cat medial gastrocnemius contains between 400 and 800 muscle fibres, irrespective of physiological type.

4. Tension production by single muscle units depends on a number of factors, including innervation ratio, the cross-sectional areas of unit fibres and the specific tension outputs of the unit fibres. The present results suggest that the specific tension output of gastrocnemius type S unit muscle fibres is considerably smaller (about 0·6 kg/cm²) than in either FF units (about 1·5-2·0 kg/cm²) or type FR units (2·6-2·9 kg/cm²).

     

Spatial distribution of muscle fibers in a lumbrical muscle of the rat

The spatial distributions of two differnt populations of muscle fibers were measured in cross-sections taken from the mid-belly of adult 4DL muscles. Muscle fibers belonging to a single motor unit (identified by glycogen depletion) were distributed randomly in most muscles. Muscle fibers which contained slow myosin (identified immunohistochemically) were distributed nonrandomly, being evenly distributed throughout most of the muscle cross-section, but excluded from the edge of the muscle. Interpreted from a developmental perspective, the results are consistent with the proposals that slow myosin-containing fibers in the adult represent the original population of primary myotubes, and that the adult pattern of motor unit fiber type is achieved by synapse elimination from mismatched fibers rather than by conversion of fiber type. © 1993 Wiley-Liss, Inc.     

Physiological types and histochemical profiles in motor units of the cat gastrocnemius

1. A variety of physiological properties of single motor units have been studied in the gastrocnemius muscle (primarily in the medial head) of pentobarbitone-anaesthetized cats. Intracellular stimulation of individual motoneurones ensured functional isolation of the muscle units innervated by them.2. A system for muscle unit classification was developed using a combination of two physiological properties. Almost all of the units studied could be classified into one of three major types, including two groups with relatively short twitch contraction times (types FF and FR, which were differentiable from one another on the basis of sensitivity to fatigue) and one group with relatively long contraction times (type S, which were extremely resistant to fatigue and were differentiable from FF and FR units on the basis of the shape of unfused tetani). Post-tetanic potentiation of twitch responses was observed in all three muscle unit types. The distributions of axonal conduction velocities for motoneurones innervating FF and FR muscle units were essentially the same, while conduction velocities for motoneurones innervating type S units were, in general, slower.3. Histochemical profiles of muscle units representative of each of the physiological classes present in the gastrocnemius pool were determined using a method of glycogen depletion for muscle unit identification. Each of the physiological categories of muscle units exhibited a corresponding unique set of muscle fibre staining reactions, or histochemical profile. Within each physiological type, all of the units examined had the same histochemical profile. The results generally support the hypothesis that the histochemical characteristics of muscle fibres are meaningfully related to the physiological properties of the same fibres. However, certain limitations in the detailed application of the hypothesis were also apparent.4. Systematic assessment of the histochemical profiles of relatively large numbers of fibres belonging to single muscle units provided strong support for the hypothesis that all of the muscle fibres innervated by a single alpha-motoneurone are histochemically identical.     

Changes in properties of the medial gastrocnemius motor units in aging rats

1. The properties of motor units were investigated in the medial gastrocnemius (MG) of old rats [27.5 +/- 1.6 (SD) mo old, n = 18]. Individual motor units were functionally isolated by ventral root fiber splitting and grading stimulus intensity. The muscle-unit portion of the motor unit was identified by the glycogen depletion method. The physiological properties of 77 motor units in 6 animals and the histological results of 7 slow-twitch (type S) muscle units were compared with data from motor units in the same muscle of middle-aged rats (12.8 +/- 1.6 mo old, n = 33). 2. The motor units were classified into four types of categories [FF (fast-twitch motor units with a fatigue index less than or equal to 0.5), FI (fast-twitch motor units with a fatigue index greater than 0.5 but less than 0.75), FR (fast-twitch motor units with a fatigue index greater than or equal to 0.75), S (slow-twitch motor units with a fatigue index greater than 0.75)] using the same criteria (i.e., presence or absence of the "sag" property and fatigability) used for middle-aged rats. No significant difference in the relative distributions of these unit types was detected, although the MG muscle in old rats exhibited a relatively high proportion of type S units and fewer type FR units. 3. The mean tetanic tensions for type FF + FI and FR units were significantly smaller than those in the middle-aged rats. On the other hand, type S motor units produced more tension than in the middle-aged rats. 4. The conduction velocity of motor axons was considerably slower in any unit type of old motor units, and the most marked change was found in type FR units. 5. The general morphological features of the old rat MG were fiber-type grouping, disseminated atrophic or angulated fibers, a decrease in the total number of muscle fibers, and an increase in the number of type I muscle fibers. The major distribution patterns of fibers of different types were the same as those in the middle-aged MG. 6. Seven type S units that produced large tetanic tension were depleted of glycogen in the muscle-unit portions. These units had a large innervation ratio compared with those in the middle-aged rats, whereas the mean cross-sectional area of muscle fibers and the calculated specific tension remained unaltered.(ABSTRACT TRUNCATED AT 400 WORDS)     

Types of intra- and extrafusal muscle fibre innervated by dynamic skeleto-fusimotor axons in cat peroneus brevis and tenuissimus muscles, as determined by the glycogen-depletion method.

1. The types of intra- and extrafusal muscle fibre innervated by dynamic skeleto-fusimotor (beta) axons were determined by using a modification of the glycogen-depletion method of Edstr?m & Kugelberg (1968) combined with histochemical tests for various enzyme reactions. A single beta axon was prepared in each of the experiments, which were carried out on six peroneus brevis and two tenuissimus muscles. 2. The intrafusal distribution of dynamic beta axons is almost exclusively restricted to bag1 fibres. The bags fibre was depleted in each of twenty-four beta-innervated spindle poles; the only fibres of a different type depleted intrafusally were a bag2 fibre in one pole and a long chain in another. 3. Depletion in the bag1 fibres was usually restricted to one zone in one pole, generally in a mid-polar location. 4. The extrafusal muscle fibres depleted by dynamic beta axons belong to the slow oxidative type as defined by Ariano, Armstrong & Edgerton (1973). The number of such fibres in each motor unit could not be accurately determined, but is almost certainly small. 5. The slow oxidative muscle fibres innervated by dynamic beta axons were not depleted over their entire length. Since there is no reason to assume that they are not twitch fibres, it would seem that the localized depletions result from the conditions required to obtain glycogen depletion, i.e. long periods of motor stimulation applied during the occlusion of the muscle's blood supply. Under similar experimental conditions depletion of glycogen was also restricted to portions of fibres in fast oxidative-glycolytic motor units, but extended over most of the length of the fibres in fast glycolytic units.     

Enlarged motor units resulting from partial denervation of cat hindlimb muscles

1. It was the aim of this study to determine the extent to which a mammalian motoneuron can sprout in a partially denervated muscle, which motor unit types are involved in sprouting, and whether polyneuronal innervation exists between sprouted units. 2. The fast-twitch flexor digitorum longus (FDL) and slow-twitch soleus were partially denervated by unilateral section of the L7 ventral root in 12-wk-old kittens. After approximately 100 days single motor units were isolated, and their isometric contractile characteristics were determined. FDL units were also tested for their resistance to fatigue and categorized as fast-twitch, fatiguing fibers (FF), fast-twitch, fatigue-resistant fibers (FR), and slow-twitch, fatigue-resistant fibers (S). The presence of polyneuronal innervation was investigated between pairs of like and unlike units. 3. The extent of the original denervation was variable and was estimated from the distribution of motor axons innervating the muscle via the L7 and S1 (soleus) or L6 and L7 (FDL) ventral roots on the contralateral side. In soleus, denervations ranged from 75 to 98%; in FDL, 60 to 97% (denervations less than 60% were not investigated). In general, motor-unit force increased in proportion to the extent of the denervation. 4. Within soleus, unit force increased to over 2 N, which was about 16 times greater than the average for a normal muscle (133 mN). However, most units increased in force to between five and 12 times normal. 5. Within FDL, the force development of type S units was unaffected by partial denervation. Type FF units increased by up to 11 times (4.3 N) compared with normal FF units (395 mN) with most increasing between two and four times. FR units exhibited the greatest relative increase in force [up to 19 times (4.3 N) compared with normal (225 mN)]. Most units were two to seven times the normal. 6. A few FDL units were glycogen depleted, the muscles frozen, and cross sections prepared for histochemical analysis. This indicated that the largest units contained approximately 5,000 fibers, and there was little fiber hypertrophy. In the extensively denervated soleus muscle, large numbers of small, presumably denervated fibers were observed. The innervation ratio of several large units was determined indirectly using mean fiber area. This gave estimates of 3,000-4,000 fibers for the largest units. Again, fiber hypertrophy contributed little to the increase in unit force. It was concluded that the increased force of units in both muscles was largely attributable to terminal and axonal sprouting of the intact motor axons. 7. No evidence for polyneuronal innervation was found in either FDL or soleus muscle.(ABSTRACT TRUNCATED AT 400 WORDS)     

Characterstics of motor innervation of muscle spindles in the monkey

The motor nerve supplies of four whole muscle spindles and 16 half spindles (equator and one pole) from lumbrical muscles of the monkey were reconstructed by light microscopy of serial, 1-μm-thick transverse sections. The 24 poles of spindle were innervated by 37 fusimotor (γ) axons and 18 skeletofusimotor (β) axons. Sixty-seven percent of spindle poles received γ axons only, 25% were supplied by both γ and β axons or β axons only, and 8% were not innervated by motor axons. All β axons except one and 35% of the γ axons innervated one type of intrafusal fiber only. The other 65% of γ axons coinnervated two or three different types of intrafusal fiber. Gamma axons innervated the (dynamic) bag₁ intrafusal fiber together with the (static) bag₂ and/or chain fibers in 65% of the poles of spindle in which the bag₁ fiber received motor supply. The bag₂ fiber shared γ-innervation with either the bag₁ or chain fibers in nearly every spindle pole. The chain fibers were usually coinnervated with the bag₂ fiber by γ axons. Compared to spindles in the cat tenuissimus muscle, the monkey spindle received fewer γ axons and had a higher incidence of shared γ-innervation between the dynamic and static intrafusal fibers. Unlike cat tenuissimus spindles, the monkey spindles lacked γ axons selective to the bag₂ fiber. However, the β motor system within the monkey lumbrical muscle was organized in a manner similar to the cat tenuissimus muscle. The significance of these observations is discussed relative to the general motor organization and function of spindles in different muscles and species of mammals.