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

1987 ◽  
Vol 57 (4) ◽  
pp. 921-937 ◽  
Author(s):  
M. J. Gillespie ◽  
T. Gordon ◽  
P. R. Murphy

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)

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)


1995 ◽  
Vol 268 (2) ◽  
pp. C527-C534 ◽  
Author(s):  
G. A. Unguez ◽  
R. R. Roy ◽  
D. J. Pierotti ◽  
S. Bodine-Fowler ◽  
V. R. Edgerton

To examine the influence of a motoneuron in maintaining the phenotype of the muscle fibers it innervates, myosin heavy chain (MHC) expression, succinate dehydrogenase (SDH) activity, and cross-sectional area (CSA) of a sample of fibers belonging to a motor unit were studied in the cat tibialis anterior 6 mo after the nerve branches innervating the anterior compartment were cut and sutured near the point of entry into the muscle. The mean, range, and coefficient of variation for the SDH activity and the CSA for both motor unit and non-motor unit fibers for each MHC profile and from each control and each self-reinnervated muscle studied was obtained. Eight motor units were isolated from self-reinnervated muscles using standard ventral root filament testing techniques, tested physiologically, and compared with four motor units from control muscles. Motor units from self-reinnervated muscles could be classified into the same physiological types as those found in control tibialis anterior muscles. The muscle fibers belonging to a unit were depleted of glycogen via repetitive stimulation and identified in periodic acid-Schiff-stained frozen sections. Whereas muscle fibers in control units expressed similar MHCs, each motor unit from self-reinnervated muscles contained a mixture of fiber types. In each motor unit, however, there was a predominance of fibers with the same MHC profile. The relative differences in the mean SDH activities found among fibers of different MHC profiles within a unit after self-reinnervation and those found among fibers in control muscles were similar, i.e., fast-2 < fast-1 < or = slow MHC fibers.(ABSTRACT TRUNCATED AT 250 WORDS)


1966 ◽  
Vol 49 (6) ◽  
pp. 1177-1198 ◽  
Author(s):  
PAUL BACH-y-RITA ◽  
FUMIO ITO

In anesthetized in vivo preparations, responses of two types of extraocular muscle fibers have been studied. The small, multiply innervated slow fibers have been shown to be capable of producing propagated impulses, and thus have been labeled slow multi-innervated twitch fibers. Fast and slow multi-innervated twitch fibers are distinguished by impulse conduction velocities, by ranges of membrane potentials, by amplitudes and frequencies of the miniature end plate potentials, by responses to the intravenous administration of succinylcholine, by the frequency of stimulation required for fused tetanus, and by the velocities of conduction of the nerve fibers innervating each of the muscle fiber types.


1990 ◽  
Vol 64 (3) ◽  
pp. 847-861 ◽  
Author(s):  
R. C. Foehring ◽  
J. B. Munson

1. This study addresses the following questions. 1) In a previous experiment, when the combined lateral gastrocnemius-soleus nerve was cross-innervated by the medial gastrocnemius (MG) nerve, was the predominance of slow muscle units in soleus muscle a result of selective routing of slow motor axons into soleus? 2) Is MG-nerve-induced conversion of soleus muscle fibers from slow to fast more complete at very long (18 mo vs. 9-11 mo) postoperative times? 3) Do MG motoneurons that cross-innervate soleus muscle recover their normal membrane electrical properties at very long postoperative times? 2. The proximal portion of approximately one-third of the MG nerve was coapted directly with the distally isolated soleus nerve. The MG muscle remained innervated by the unoperated portion of the MG nerve. At 6, 10, or 18 mos postoperative, motoneuron and/or muscle-unit properties were determined for MG motoneurons innervating MG, soleus, or neither muscle, and for axotomized soleus motoneurons. 3. In the partially denervated MG muscle, the proportions of motor units of each type were normal. This suggests that the population of MG motor axons that had been directed to the soleus nerve also contained a representative distribution of MG motoneuron types. 4. Most motor units (74%) in cross-innervated soleus (Xsoleus) were type S (based on muscle-unit contractile properties), in spite of the soleus nerve's having been cross-connected by approximately 75% fast MG motoneurons. Thus, even at very long postoperative times, slow soleus muscle units resisted conversion by fast MG motoneurons. 5. Thirty-two percent of MG motoneurons that had been cross-connected to soleus nerve elicited no measurable muscle contraction, compared with approximately 10% in previous reinnervation experiments in which the MG nerve was coapted with the MG or lateral gastrocnemius-soleus nerve. Thus MG motoneurons may be disadvantaged in their ability to innervate soleus muscle fibers. 6. It appears that at long postoperative times, those fast MG motoneurons tha had innervated large soleus muscle units had failed to convert those muscle fibers to fast types and had failed also to recover their normal motoneuron electrical properties. Conversion and recovery did occur for fast MG motoneurons that innervated small soleus muscle units and for slow MG motoneurons.


1987 ◽  
Vol 57 (4) ◽  
pp. 1210-1226 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

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.


2009 ◽  
Vol 385 (1) ◽  
pp. 44-48 ◽  
Author(s):  
Stefan Galler ◽  
Oleg Andruchov ◽  
Gabriela M.M. Stephenson ◽  
D. George Stephenson

1984 ◽  
Vol 52 (1) ◽  
pp. 114-125 ◽  
Author(s):  
A. W. English

Cat lateral gastrocnemius (LG) muscle is composed of four compartments, each of which is supplied by a primary branch of the LG muscle nerve and each of which contains a discrete population of motor units/muscle fiber types. The activation patterns of these different motor-unit populations were examined from recordings made using selective electromyographic (EMG) electrodes, which were carefully placed into the different LG compartments. Recordings were made as the cats stepped overground along a wooden walkway at a variety of different stepping speeds. Electrical activity was correlated with stepping movements using high-speed cinematography. A number of different activation patterns of the different compartments were noted during stepping. In one such pattern, more intense EMG activity was found in distal than proximal compartments at slow stepping speeds, but at moderate to fast stepping speeds the intensity of activity in proximal compartments was equal to or greater than in distal compartments. In other patterns, a less consistent relationship between compartment EMG intensity and stepping speed was observed. These results are generally consistent with an orderly pattern of activation of motor units in the LG during stepping but also indicate that more than one activation pattern exists.


1989 ◽  
Vol 98 (3) ◽  
pp. 202-208 ◽  
Author(s):  
Yasuo Hisa ◽  
Leslie T. Malmgren ◽  
Richard R. Gacek

By use of actomyosin ATPase histochemistry, it was found that there were large differences among the three cat infrahyoid muscles (sternohyoid, sternothyroid, and thyrohyoid) with respect to their percentages of different muscle fiber types. It has been established that the individual activity patterns of the component motor units in each muscle drive the biochemical and physiologic differentiation of the muscle fibers associated with each motor unit. Therefore, the data obtained in the present investigation provide an indication of the characteristics of long-term use of each of the various types of motor units, as well as the associated differences in the physiologic capacities of the different motor unit types composing each of these infrahyoid muscles.


2009 ◽  
Vol 57 (8) ◽  
pp. 787-800 ◽  
Author(s):  
Hannah S. Rhee ◽  
Catherine M. Steel ◽  
Frederik J. Derksen ◽  
N. Edward Robinson ◽  
Joseph F.Y. Hoh

We used immunohistochemistry to examine myosin heavy-chain (MyHC)-based fiber-type profiles of the right and left cricoarytenoideus dorsalis (CAD) and arytenoideus transversus (TrA) muscles of six horses without laryngoscopic evidence of recurrent laryngeal neuropathy (RLN). Results showed that CAD and TrA muscles have the same slow, 2a, and 2x fibers as equine limb muscles, but not the faster contracting fibers expressing extraocular and 2B MyHCs found in laryngeal muscles of small mammals. Muscles from three horses showed fiber-type grouping bilaterally in the TrA muscles, but only in the left CAD. Fiber-type grouping suggests that denervation and reinnervation of fibers had occurred, and that these horses had subclinical RLN. There was a virtual elimination of 2x fibers in these muscles, accompanied by a significant increase in the percentage of 2a and slow fibers, and hypertrophy of these fiber types. The results suggest that multiple pathophysiological mechanisms are at work in early RLN, including selective denervation and reinnervation of 2x muscle fibers, corruption of neural impulse traffic that regulates 2x and slow muscle fiber types, and compensatory hypertrophy of remaining fibers. We conclude that horses afflicted with mild RLN are able to remain subclinical by compensatory hypertrophy of surviving muscle fibers.


1987 ◽  
Vol 57 (4) ◽  
pp. 1227-1245 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

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)


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