Influence of overload on recovery of rat plantaris from partial denervation

1989 ◽  
Vol 66 (2) ◽  
pp. 732-740 ◽  
Author(s):  
R. N. Michel ◽  
P. F. Gardiner

A functional index of neural adaptability is the capacity of motoneurons to extend and establish supernumerary connections with neighboring denervated muscle fibers. The purpose of this study was to guage this response in rat plantaris muscles subjected to increased levels of activity resulting from the surgical removal of the synergistic gastrocnemius and soleus muscles. Thirty-seven days of overload increased plantaris absolute (69%) and relative (82%) weight, whole muscle (35%) and individual fiber (37%) mean cross-sectional area, half-relaxation time (1/2RT; 25%), and maximum tetanic tension (P0; 21%). In a separate group of animals that had undergone 30 days of overload, three-quarters of the plantaris muscle fibers were denervated by sectioning radicular nerve L4. At 7 days postlesion, contractile responses were obtained from sprouting motor units remaining in radicular nerve L5, and the results compared to a nonoverloaded group that had undergone this same procedure. Twitch time to peak tension and 1/2RT were prolonged in normal partially denervated (PD) and overloaded partially denervated (OPD) muscles, and this response was significantly greater in the overloaded muscles. Both PD and OPD muscles increased twitch tension (38%) and peak tension developed at 25 Hz (34%) to a similar extent, during recovery from partial denervation. These increases, attributable to sprouting of L5 motor axon collaterals, were matched in PD muscles with a corresponding increase in P0, a response which did not occur in OPD muscles. Additionally, a more extensive decrease in P0 occurred as a result of partial denervation in OPD muscles compared with whole muscle P0 of nondenervated muscle (L4 plus L5 stimulation).(ABSTRACT TRUNCATED AT 250 WORDS)

1978 ◽  
Vol 41 (2) ◽  
pp. 496-508 ◽  
Author(s):  
J. V. Walsh ◽  
R. E. Burke ◽  
W. Z. Rymer ◽  
P. Tsairis

1. Compensatory hypertrophy of the medial gastrocnemius (MG) muscle was produced by denervating or removing its synergists (i.e., the lateral gastrocnemius, soleus, and plantaris muscles) in adult cats. Following survival times of 14-32 wk, intracellular recording and stimulation techniques were used to study the motor-unit population in MG. The data obtained were compared with results from MG motor units in normal unoperated cats of the same body size and weight. 2. Using criteria employed for normal motor units, the units in hypertrophic MG muscles were readily classified into the same groups (types FF, F(int), FR, and S) as in normal MG. There was no detectable difference in the distribution of motor-unit types after hypertrophy. 3. When compared with a normal motor-unit sample, there was a large increase in mean tetanic tension, but no significant change in twitch tension, for each motor-unit type in the hypertrophied muscles. The most marked increase was found among the fatigue-resistant type S and type FR motor units. There was no alteration of twitch contraction times or fatigue resistance in any unit type after hypertrophy. 4. For each motor-unit type, the mean homonymous (MG) group Ia EPSP amplitude was the same in normal and hypertrophic MG populations. There was, however, a significant increase in the average conduction velocity of MG motor axons in the animals with uncomplicated MG synergist removal and maximal MG hypertrophy. 5. On the basis of histochemical staining, muscle fibers from comparable sections of hypertrophic and contralateral (unoperated) MG muscles were presumptively identified as belonging to FF, FR, or S units. There was no significant difference between hypertrophic and contralateral MG muscles in the percentage of each fiber type, although there was some variability in muscle composition from one cat to another. One muscle pair was studied in detail for fiber cross-sectional area. In this cat, with marked hypertrophy by muscle weight, there was a modest increase in the mean fiber areas of histochemical S and FR muscle fibers, but no evident change in FF fibers, on the hypertrophic side. 6. MG motor units were examined in several cats in which synergist removal resulted in scarring and marked limitation of passive ankle mobility, and no evident weight gain in MG. Motor units of all types in these animals showed a decrease in twitch tension and in mean twitch/tetanus ratios, with little alteration in mean tetanic tensions. 7. The main effect of compensatory hypertrophy under the present conditions was a large increase in tetanic tension output from individual motor units due, at least in part, to an increase in fiber cross-sectional area. There was no evidence indicating any "conversion" of motor units or of their muscle fibers from one type to another.


1987 ◽  
Vol 57 (6) ◽  
pp. 1730-1745 ◽  
Author(s):  
S. C. Bodine ◽  
R. R. Roy ◽  
E. Eldred ◽  
V. R. Edgerton

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.


1990 ◽  
Vol 258 (1) ◽  
pp. C62-C70 ◽  
Author(s):  
G. Desypris ◽  
D. J. Parry

Contractile and histochemical properties of reinnervated motor units in soleus muscles of C57BL/6J mice were examined 1 mo after sectioning the soleus nerve. Fifty-one motor units were isolated by the technique of ventral root splitting. Their sizes ranged from 0.4 to 13.6% of whole muscle tetanic tension (Po) with a mean size of 5.3% Po corresponding to 19 motor units. In control unoperated mice, the range was 2.2-8.6% Po, with a mean size of 4.8% Po corresponding to 22 motor units. Although no clear relationship between unit time to peak tension and size was seen in control units, it appeared that in the reinnervated muscle the large units were also slow contracting, whereas the smaller units were predominantly fast contracting. Adenosinetriphosphatase (ATPase) staining revealed an increase in the proportion of muscle area occupied by type I fibers in reinnervated soleus compared with control soleus. Immunohistochemical staining of reinnervated soleus with monoclonal antibodies against type I and IIa myosin showed the presence of hybrid fibers containing both myosins. It is concluded that during reinnervation most motoneurons reinnervate the soleus muscle of the mouse. The hypothesis that slow motoneurons are more adept at expanding their innervating field than fast motoneurons is also supported by the data.


1988 ◽  
Vol 60 (6) ◽  
pp. 2138-2151 ◽  
Author(s):  
A. E. Olha ◽  
B. J. Jasmin ◽  
R. N. Michel ◽  
P. F. Gardiner

1. Rat plantaris muscles were subjected to chronic overload by the surgical removal of the soleus and most of the gastrocnemius muscles. Twelve to 16 wk later whole muscle and motor unit (ventral root dissection technique) contractile properties as well as histochemistry were determined. 2. Motor units were categorized as fast, fatigable (FF), fast, intermediate fatigue-resistant (FI), fast, fatigue-resistant (FR), and slow (S) based on contractile characteristics. Muscle fibers were identified as type I and type II according to myofibrillar ATPase staining. 3. Whole muscles demonstrated increases in wet weight, tetanic force, proportion of type I fibers, and mean cross-sectional areas of both type I and II fibers, as a result of chronic overload. 4. Tetanic tension increased by the same relative magnitude in all motor units whereas twitch tension remained unchanged. A significant change in the proportions of the motor unit types occurred in overloaded muscles, such that the latter contained higher proportions of FF and S units, and lower proportions of FI and FR units, than normal muscles. 5. The fatigue profile of a composite constructed from a summation of motor unit responses revealed that the overloaded plantaris displayed fatigue resistance similar to that of the normal plantaris for a given absolute force output. 6. Glycogen-depleted fibers of hypertrophied single motor units demonstrated uniform myofibrillar ATPase and SDH staining characteristics suggesting that metabolic adaptations among fibers of the same unit were similar after 12-16 wk of overload. 7. The finding that overload caused a uniform increase in the tetanic strength of all motor units, whereas alterations in fatigue resistance varied in degree and direction among unit types, demonstrate that these two properties are not controlled in parallel in this model. The smallest units maintain or even increase their fatigue resistance during the hypertrophic process, whereas high threshold units actually decrease in fatigue resistance.


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.


1986 ◽  
Vol 55 (1) ◽  
pp. 147-162 ◽  
Author(s):  
J. M. Spielmann ◽  
E. K. Stauffer

The glycogen-depletion technique (17, 32) has been used to examine the functional and morphological relationships between single isolated motor units (MUs) and single isolated Golgi tendon organs (GTOs) that were excited by the MUs in the soleus muscle of the cat. All MUs whose twitch contraction generated a brisk discharge from the GTOs during the rising and plateau phase of force development had a muscle fiber attached specifically to the proximal end of the GTOs. A significant (P less than 0.05) linear relationship was found between GTO discharge rate and the cross-sectional area of the muscle fibers that connected to a receptor. This was true when the correlation was calculated between firing rate and 1) the cross-sectional area of the entire collection of muscle fibers that connected in series to the GTOs; and 2) for the cross-sectional areas of the individually depleted muscle fibers that inserted on the GTO sample. These findings support the notion that the most physiologically relevant input for GTOs arises from the MUs that are attached directly in-series with the receptor.


Author(s):  
David Jordan ◽  
Louise Mawn ◽  
Richard L. Anderson

Whereas skeletal muscles generally perform specific limited roles, extraocular muscles (EOMs) have to be responsive over a wider dynamic range. As a result, EOMs have fundamentally distinct structural, functional, biochemical, and immunological properties as compared to other skeletal muscles. At birth, the extraocular muscles are at approximately 50 % to 60 % of their final dimension. Their relative growth within the enlarging orbit and their angular relations with the globe remain nearly constant from infancy to adulthood. The adult rectus muscles are approximately the same length (40 mm) but differ in thickness and in the length of their tendons. There are six extrinsic, or extraocular, muscles of the eye: four recti and two obliques. Only the horizontal and vertical recti insert on the eyeball in front of its equator. Both obliques have their insertions behind the equator of the globe. All six muscles consist of striated muscle fibers with abundant elastic fibers. The EOMs have muscle fibers and innervations that differ from those of skeletal muscle. There are three distinct types of muscle fibers (fine, granular, and coarse) that contribute to the action of the EOMs. The fine fibers are thought to be responsible for slow twitch movements, the granular fibers for fast twitch movements, and the coarse fibers for slow tonic movements. The EOMs are more richly innervated than other voluntary muscles of the body and have three types of nerve terminals: single endplate (driving eye movements), multiple endplates (tonic tension), and palisade endings (can be sensory receptors). In addition, there are both singly and multiply innervated nerve fibers present. EOMs are able to vary their contractile force by small increments. The maximum firing frequency of ocular motor units is about four times greater than those of limb muscle motor units. To allow them to operate at a higher frequency, EOMs also have faster contractile properties, with their time to peak tension and their one-half relaxation time being at least half of those in limb muscles.


1989 ◽  
Vol 67 (5) ◽  
pp. 2049-2054 ◽  
Author(s):  
E. G. Noble ◽  
F. P. Pettigrew

The contractile characteristics of single motor units, isolated from rat plantaris muscles subjected to short-term (30 days) compensatory overload, were assessed to determine whether motor units in transition could be detected. In the control plantaris 88% of the motor units were classified as fast. After overload, a large decline (26.5%) in the proportion of typical fast motor units was noted. The estimated contribution of fast fatigable units to whole muscle tetanic tension (Po 200) also declined (from 55 to 25%), whereas that of fast intermediate motor units increased (from 33 to 55%). In the overloaded plantaris, motor units that exhibited unusual “sag” and contraction time characteristics were detected. These motor units, which could be further subdivided into two distinct types by a variety of indexes, exhibited characteristics intermediate to fast and slow units and therefore were termed “transitional.” Transitional units accounted for 12% of the estimated whole muscle Po200 after overload. These experiments characterize novel classifications of motor units undergoing transformation and further detail the motor unit shift that accompanies compensatory overload.


1990 ◽  
Vol 68 (1) ◽  
pp. 51-56 ◽  
Author(s):  
D. J. Parry ◽  
S. DiCori

Post-tetanic potentiation was measured in motor units, isolated functionally by ventral root splitting, of soleus and extensor digitorum longus muscles of mouse. All motor units from the extensor digitorum longus had times to peak twitch tension less than 13 ms; there was a linear relationship between time to peak tension and post-tetanic potentiation, with the faster units exhibiting greater potentiation. When soleus motor units were similarly analyzed, it appeared that there may be two distinct populations of units. Those units with times to peak tension less than 13 ms were virtually indistinguishable from those of extensor digitorum longus. On the other hand, the slope of the relationship between post-tetanic potentiation and time to peak tension was significantly lower for soleus units with times to peak tension of 13 ms or more. Approximately three-quarters of the soleus units were of the latter slow type, whereas only one-half of the muscle fibres could be classified as type I by means of immunohistochemistry, suggesting that the myosin heavy chain may not be the major determinant of post-tetanic potentiation. Single, chemically skinned fibres of soleus were analyzed for myosin heavy and light chain components by polyacrylamide gel electrophoresis. All fibres with type I heavy chain contained only the two slow light chains. On the other hand, almost all of the fibres with type IIA myosin heavy chain contained both fast and slow light chains. It is suggested that the discrepancy between the proportions of physiologically "fast" motor units and histochemical type IIA fibres may be the consequence of variable amounts of slow light chain associated with the fast IIA myosin heavy chain.Key words: post-tetanic potentiation, motor units, myosin isoforms, fibre types, immunohistochemistry.


1999 ◽  
Vol 82 (2) ◽  
pp. 584-592 ◽  
Author(s):  
Thomas G. Sutlive ◽  
J. Ross McClung ◽  
Stephen J. Goldberg

Investigations of whole muscle and motor-unit contractile properties have provided valuable information for our understanding of the spinal cord and extraocular motor systems. However, no previous investigation has examined these properties in an isolated tongue muscle. The purpose of this study was to determine the contractile properties and muscle fiber types of the rat styloglossus muscle. The styloglossus is one of three extrinsic tongue muscles and serves to retract the tongue within the oral cavity. Adult male Sprague-Dawley rats ( n = 19) were used in these experiments. The contractile characteristics of the whole styloglossus muscle ( n = 9) were measured in response to stimulation of the hypoglossal nerve branch to the muscle. The average twitch tension produced was 3.30 g with a mean twitch contraction time of 13.81 ms. The mean maximum tetanic tension was 19.66 g and occurred at or near the fusion frequency, which averaged 109 Hz. The styloglossus muscle was resistant to fatigue [fatigue index (F. I.) = 0.76]. In separate experiments ( n = 7), the contractile characteristics of 37 single motor units were measured in response to extracellular stimulation of hypoglossal motoneurons. The twitch tension generated by styloglossus motor units averaged 35.7 mg, and the mean twitch contraction time was 12.46 ms. The mean fusion frequency was 92 Hz. Maximum tetanic tension averaged 177.8 mg. Styloglossus single motor units were resistant to fatigue (F. I. = 0.74). The sites of stimulation that yielded a contractile response in the styloglossus muscle were consistent with the location of the styloglossus motoneuron pool reported in earlier anatomy studies. Muscle fiber typing was determined in three animals based on the myofibrillar ATPase reaction at pH 9.8, 4.6, and 4.3. The styloglossus muscle was composed of ≈99% type IIA fibers with a few scattered type I fibers present in the study sample. On the basis of the combined findings of the physiology and histochemistry experiments, the styloglossus muscle appeared to be a homogeneous muscle composed almost exclusively of fast, fatigue-resistant motor units. These properties of the styloglossus muscle and its motor units were compared with findings in other rat skeletal muscles.


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