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

1985 ◽  
Vol 54 (4) ◽  
pp. 837-851 ◽  
Author(s):  
R. P. Dum ◽  
M. J. O'Donovan ◽  
J. Toop ◽  
P. Tsairis ◽  
M. J. Pinter ◽  
...  

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)

1985 ◽  
Vol 54 (4) ◽  
pp. 818-836 ◽  
Author(s):  
R. P. Dum ◽  
M. J. O'Donovan ◽  
J. Toop ◽  
R. E. Burke

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)


1991 ◽  
Vol 66 (6) ◽  
pp. 1838-1846 ◽  
Author(s):  
R. K. Powers ◽  
M. D. Binder

1. The tension produced by the combined stimulation of two to four single motor units of the cat tibialis posterior muscle was compared with the algebraic sum of the tensions produced by each individual motor unit. Comparisons were made under isometric conditions and during imposed changes in muscle length. 2. Under isometric conditions, the tension resulting from combined stimulation of units displayed marked nonlinear summation, as previously reported in other cat hindlimb muscles. On average, the measured tension was approximately 20% greater than the algebraic sum of the individual unit tensions. However, small trapezoidal movements imposed on the muscle during stimulation significantly reduced the degree of nonlinear summation both during and after the movement. This effect was seen with imposed movements as small as 50 microns. 3. The degree of nonlinear summation was not dependent on motor unit size or on stimulus frequency. The effect was also unrelated to tendon compliance because the degree of nonlinear summation of motor unit forces was unaffected by the inclusion of different amounts of the external tendon between the muscle and the force transducer. 4. Our results support previous suggestions that the force measured when individual motor units are stimulated under isometric conditions is reduced by friction between the active muscle fibers and adjacent passive fibers. These frictional effects are likely to originate in the connective tissue matrix connecting adjacent muscle fibers. However, because these effects are virtually eliminated by small movements, linear summation of motor unit tensions should occur at low force levels under nonisometric conditions.(ABSTRACT TRUNCATED AT 250 WORDS)


2007 ◽  
Vol 103 (5) ◽  
pp. 1706-1714 ◽  
Author(s):  
Keith N. Bishop ◽  
J. Ross McClung ◽  
Stephen J. Goldberg ◽  
Mary S. Shall

The ferret has become a popular model for physiological and neurodevelopmental research in the visual system. We believed it important, therefore, to study extraocular whole muscle as well as single motor unit physiology in the ferret. Using extracellular stimulation, 62 individual motor units in the ferret abducens nucleus were evaluated for their contractile characteristics. Of these motor units, 56 innervated the lateral rectus (LR) muscle alone, while 6 were split between the LR and retractor bulbi (RB) muscle slips. In addition to individual motor units, the whole LR muscle was evaluated for twitch, tetanic peak force, and fatigue. The abducens nucleus motor units showed a twitch contraction time of 15.4 ms, a mean twitch tension of 30.2 mg, and an average fusion frequency of 154 Hz. Single-unit fatigue index averaged 0.634. Whole muscle twitch contraction time was 16.7 ms with a mean twitch tension of 3.32 g. The average fatigue index of whole muscle was 0.408. The abducens nucleus was examined with horseradish peroxidase conjugated with the subunit B of cholera toxin histochemistry and found to contain an average of 183 motoneurons. Samples of LR were found to contain an average of 4,687 fibers, indicating an LR innervation ratio of 25.6:1. Compared with cat and squirrel monkeys, the ferret LR motor units contract more slowly yet more powerfully. The functional visual requirements of the ferret may explain these fundamental differences.


2004 ◽  
Vol 92 (3) ◽  
pp. 1357-1365 ◽  
Author(s):  
Miho Sugiura ◽  
Kenro Kanda

The mechanical properties of individual motor units in the medial gastrocnemius muscle, as well as the whole muscle properties and innervating motor nucleus, were investigated in dietary-restricted, male Fischer 344/DuCrj rats at ages of 4, 7, 12, 21/22, 27, 31, and 36 mo. The tetanic tension of the type S units continuously increased until the age of 36 mo. Those of type FF and FR units declined from 21/22 to 27 mo of age but did not change further while the whole muscle tension decreased greatly. The atrophy of muscle fibers, the decline in motoneuron number and axonal conduction velocity, and the decrease in the posttetanic potentiation of twitch contraction of motor units seemed to start after 21/22 mo of age and were accelerated with advancing age. Prolongation of twitch contraction time was evident for only type S and FR units in 36-mo-old rats. The fatigue index was greatly increased for type FF units in 36-mo-old rats. These findings indicated that the progress of changes in various properties occurring in the senescent muscle was different in terms of their time course and degree and also dependent on the types of motor unit. The atrophy and decrease in specific tension of muscle fibers affected the decline in tension output of motor units. This was effectively compensated for by the capture of denervated muscle fibers over time.


1983 ◽  
Vol 97 (3) ◽  
pp. 756-771 ◽  
Author(s):  
G F Gauthier ◽  
R E Burke ◽  
S Lowey ◽  
A W Hobbs

Immunocytochemical characteristics of myosin have been demonstrated directly in normal and cross-reinnervated skeletal muscle fibers whose physiological properties have been defined. Fibers belonging to individual motor units were identified by the glycogen-depletion method, which permits correlation of cytochemical and physiological data on the same fibers. The normal flexor digitorum longus (FDL) of the cat is composed primarily of fast-twitch motor units having muscle fibers with high myosin ATPase activity. These fibers reacted with antibodies specific for the two light chains characteristic of fast myosin, but not with antibodies against slow myosin. Two categories of fast fibers, corresponding to two physiological motor unit types (FF and FR), differed in their immunochemical response, from which it can be concluded that their myosins are distinctive. The soleus (SOL) consists almost entirely of slow-twitch motor units having muscle fibers with low myosin ATPase activity. These fibers reacted with antibodies against slow myosin, but not with antibodies specific for fast myosin. When the FDL muscle was cross-reinnervated by the SOL nerve, twitch contraction times were slowed about twofold, and motor units resembled SOL units in a number of physiological properties. The corresponding muscle fibers had low ATPase activity, and they reacted with antibodies against slow myosin only. The myosin of individual cross-reinnervated FDL muscle units was therefore transformed, apparently completely, to a slow type. In contrast, cross-reinnervation of the SOL muscle by FDL motoneurons did not effect a complete converse transformation. Although cross-reinnervated SOL motor units had faster than normal twitch contraction times (about twofold), other physiological properties characteristic of type S motor units were unchanged. Despite the change in contraction times, cross-reinnervated SOL muscle fibers exhibited no change in ATPase activity. They also continued to react with antibodies against slow myosin, but in contrast to the normal SOL, they now showed a positive response to an antibody specific for one of the light chains of fast myosin. The myosins of both fast and slow muscles were thus converted by cross-reinnervation, but in the SOL, the newly synthesized myosin was not equivalent to that normally present in either the FDL or SOL. This suggests that, in the SOL, alteration of the nerve supply and the associated dynamic activity pattern are not sufficient to completely respecify the type of myosin expressed.


1988 ◽  
Vol 64 (1) ◽  
pp. 291-298 ◽  
Author(s):  
M. Fournier ◽  
G. C. Sieck

A somatotopic organization in the segmental innervation of the cat diaphragm (DIA) was determined using evoked electromyographic responses and glycogen depletion of stimulated type II muscle fibers. With the use of the glycogen depletion method, the specific location and proportion of muscle fibers innervated by the fifth (C5) or sixth (C6) cervical ventral roots were determined for different regions of the DIA. The sternal and ventral portions of the costal and crural DIA regions were innervated primarily by C5. The dorsal portions of both the costal and crural regions were innervated primarily by C6. Thus the somatotopic organization in the segmental innervation of the DIA was not correlated with the anatomic division of the sternal, costal, and crural regions. Instead, the somatotopic projections of cervical ventral roots were organized in the ventrodorsal axis of each DIA region. This topographical pattern resulted in an extensive overlap of the DIA territories innervated by C5 and C6. Within a region, the fibers innervated by a specific ventral root were not randomly distributed but often followed fascicle divisions. This frequently resulted in a wide range in the proportion of fibers innervated by a ventral root even within a specific region.


Development ◽  
1990 ◽  
Vol 109 (3) ◽  
pp. 723-732
Author(s):  
T. Fladby ◽  
J.K. Jansen

We studied the fiber type composition and contractile properties of mouse soleus motor units at 2 days, 5 days and 2 weeks of age. We used Lucifer Yellow injection to mark muscle fibers belonging to the same motor unit in the two youngest age groups, and the traditional method of glycogen depletion in the oldest. The age groups were chosen because 2 days is at the end of muscle fiber production; 5 days is at the start of synapse elimination in the muscle and 2 weeks is at the end. Muscle fibers were classified as fast (F) or slow (S) on the basis of their myosin heavy chain (MHC) content, as determined by different monoclonal antibodies. Motor units are already dominated by either F- or S-fibers at 2 days, suggesting an early preferential innervation of the two types of fibers. A substantial part of the remaining refinement of the innervation takes place during the next 3 days, while the total number of terminals in the muscle remains constant. This is most easily explained by an exchange of aberrant for correct synapses during this period. A smaller part of the refinement of the innervation occurs during the subsequent period of synapse elimination.


1988 ◽  
Vol 60 (1) ◽  
pp. 30-45 ◽  
Author(s):  
J. B. Armstrong ◽  
P. K. Rose ◽  
S. Vanner ◽  
G. J. Bakker ◽  
F. J. Richmond

1. The neck muscle biventer cervicis is supplied by five separate nerve bundles that originate from segments C2-C5 and enter the muscle at different rostrocaudal levels. We have used the glycogen-depletion method to investigate the distribution of muscle fibers supplied by each nerve bundle and also the extent of motor-unit territories supplied by single motoneurons in the C3 segment. 2. Prolonged intermittent stimulation of each nerve bundle produced glycogen depletion in a compartment of muscle fibers that ran only a fraction of the whole-muscle length. The depleted compartment was separated by tendinous inscriptions from adjacent, serially arranged compartments that were supplied by different nerve bundles. Thus the muscle was divided into five in-series compartments, arranged in the same rostrocaudal sequence as the nerves by which they were supplied. 3. Six fast, glycolytic (FG) and five fast, oxidative-glycolytic (FOG) motor units were depleted by repetitive intracellular stimulation of their antidromically identified motoneurons in the C3 segment. The fibers of each motor unit were confined to a striplike subvolume whose cross-sectional area was only 20-40% of that for the whole compartment in which it was located. Single motor units contained an average of 408 extrafusal fibers (range: 262-582 fibers), and these were distributed with an average density of 20 fibers/mm2 in cross sections through their motor domains. No significant differences were found between the numbers or densities of fibers in FG and FOG motor units. 4. The specialized in-series organization of compartments has functional implications because the forces generated by one compartment of motor units must be transmitted through other in-series compartments of muscle fibers rather than directly onto skeletal attachments. The confined distribution of muscle fibers belonging to a single motor unit suggests that an additional level of organization may exist within individual compartments. The implications of these features for the physiological behavior and neural control of biventer cervicis are discussed.


1991 ◽  
Vol 261 (1) ◽  
pp. C93-C101 ◽  
Author(s):  
L. Larsson ◽  
L. Edstrom ◽  
B. Lindegren ◽  
L. Gorza ◽  
S. Schiaffino

Determinations of fatigue ratio, twitch and tetanus tension, and contraction and half-relaxation times of the isometric twitch were made in 21 single fast-twitch motor units from the rat tibialis anterior muscle. Single motor units were functionally isolated by microdissection of the ventral root, and the glycogen depletion technique was used to demonstrate the muscle fibers in the unit. Morphological and immuno- and enzyme-histochemical methods were applied to serial muscle cross sections to characterize the muscle fibers in the unit. Three of the units had muscle fibers of the IIa type according to staining both for myofibrillar adenosinetriphosphatase after acid preincubation and with the use of monoclonal antibodies specific for myosin heavy chains (MHCs), i.e., the IIa-MHC isoform. The other 18 units were of the IIb type according to enzyme-histochemistry, but immunohistochemistry showed that in six of these units the muscle fibers exhibited the novel type IIx-MHC isoform and in the other 12 units the IIb-MHC isoform. It was found that the IIx motor units have contraction and half-relaxation times similar to those of types IIa and IIb units but have morphological, physiological, and biochemical properties that distinguish them from the latter two types.


Sign in / Sign up

Export Citation Format

Share Document