Recovery of rat tibialis anterior motor unit properties following partial denervation

1992 ◽  
Vol 70 (10) ◽  
pp. 1324-1329
Author(s):  
Gordon J. Bell ◽  
Kathy Ayer ◽  
Tessa Gordon ◽  
Suresh Devashayam ◽  
Thomas P. Martin

The recovery of selected mechanical, morphological, and metabolic properties of rat tibialis anterior fast motor units was determined following partial denervation (n = 7) or partial denervation and hemispinal cord transection (n = 5) and compared with age-matched control units (n = 7). Following 1–12 months of recovery, the mechanical properties of each unit were measured and the fibres depleted of glycogen by using standard ventral root filament stimulation techniques. Quantitative histohemical techniques were used to determine cross-sectional area and the activities of succinate dehydrogenase and α-glycerolphosphate dehydrogenase in individual unit fibres. Partial denervation increased the mean fibre area but decreased α-glycerolphosphate dehydrogenase activity. Succinate dehydrogenase was unchanged in the denervated groups. The variability in area and enzymatic activities among the unit fibres was unchanged. However, the interrelationship between the enzymes was altered by both denervation procedures. Succinate dehydrogenase activity was directly related to fatigue resistance and inversely related to tetanic tension across the units. These findings suggest that a motor unit reestablishes many of its properties despite marked changes to the composition of the unit brought about by partial denervation. In addition, a reduction in the neuromuscular activity of units during reorganization had a limited effect on recovery.Key words: motor unit, succinate dehydrogenase, α-glycerolphosphate dehydrogenase, spinal cord hemisection.

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.


1992 ◽  
Vol 70 (7) ◽  
pp. 970-976 ◽  
Author(s):  
Thomas P. Martin ◽  
V. R. Edgerton

Using isolated ventral root filament stimulation and glycogen depletion techniques, 14 motor units from the cat tibialis anterior were studied. Based on their mechanical properties, the units were classified as either slow-fatigue resistant, fast-fatigue resistant, fast-fatigue intermediate, or fast-fatigable. Quantitative histochemical and computer assisted image analysis techniques were used to determine the activity of succinate dehydrogenase in a population of fibres in each unit. In addition, the intrafibre distribution of succinate dehydrogenase activity was measured in those same fibres by calculating the enzymatic activity of circumferential layers every 0.5 μm starting from the fibre edge to its centre. It was established that enzymatic activity and radial distance were linearly related in the fibres. A range in succinate dehydrogenase activity (mean coefficient of variation, 29%) was observed among the fibres of a unit. In contrast, the intrafibre distribution of that activity was rather consistent (mean variation, 4%) across the fibres of a unit. Further, the intrafibre distribution was similar among the fibres of units classified as the same type. However, the intrafibre distribution was disparate among the different unit types. These data suggest that the intrafibre distribution of mitochondrial enzymes may contribute to the mechanical properties of a motor unit. In this regard, a hypothesis is proposed that describes how the absolute activity of a mitochondrial enzyme, and the intrafibre distribution of that activity, may interactively contribute to the fatigue resistance of a unit.Key words: mitochondria, quantitative histochemistry, fatigue.


1994 ◽  
Vol 76 (6) ◽  
pp. 2663-2671 ◽  
Author(s):  
L. J. Einsiedel ◽  
A. R. Luff

The aim of the study was to determine whether increased motoneuron activity induced by treadmill walking would alter the extent of motoneuron sprouting in the partially denervated rat medial gastrocnemius muscle. An extensive partial denervation was effected by unilateral section of the L5 ventral root, and it is very likely that all units remaining in the medial gastrocnemius were used in treadmill walking. Rats were trained for 1.5 h/day and after 14 days were walking at least 1 km/day. Motor unit characteristics were determined 24 days after the partial denervation and were compared with units from partially denervated control (PDC) animals and with units from normal (control) animals. In PDC rats, force developed by slow, fast fatigue-resistant, and fast intermediate-fatigable motor units increased substantially compared with control animals; that of fast-fatigable units did not increase. In partially denervated exercised animals, force developed by slow and fast-fatigue-resistant units showed no further increase, but fast-intermediate- and fast-fatigable units showed significant increases compared with those in PDC animals. The changes in force were closely paralleled by changes in innervation ratios. We concluded that neuronal activity is an important factor in determining the rate of motoneuron sprouting.


1994 ◽  
Vol 77 (2) ◽  
pp. 947-955 ◽  
Author(s):  
M. I. Lewis ◽  
S. A. Monn ◽  
W. Z. Zhan ◽  
G. C. Sieck

Interactive effects of emphysema (EMP) and prolonged nutritional deprivation (ND) on contractile, morphometric, and metabolic properties of hamster diaphragm muscle (DIA) were examined. Six months after induction of EMP (intratracheal elastase), saline-treated controls (CTL) and EMP hamsters of similar body weights were subjected to ND over 6 wk. Isometric contractile and fatigue properties of costal DIA were determined in vitro. DIA fibers were histochemically classified as type I or II, and fiber succinate dehydrogenase activity and cross-sectional area were determined using quantitative microscopic procedures. From histochemical sections, the number of capillaries per fiber (C/F) and per fiber cross-sectional area (C/A) were determined. ND resulted in progressive loss of body weight (ND-CTL, 23.8%; ND-EMP, 28.4%; P = NS). ND did not affect reduction in optimal length (Lo) of DIA fibers in EMP compared with CTL and ND-CTL hamsters. Maximum specific force (i.e., force/unit area) was reduced by approximately 25% in EMP animals compared with CTL. ND did not improve or exacerbate the reduction in specific force with EMP. ND attenuated improved fatigue resistance of DIA in EMP animals. No differences in fiber type proportions were noted among experimental groups. Significant atrophy of type I and II DIA fibers was noted after ND. Atrophy was proportionately greater in type II fibers of ND-EMP when referenced to EMP animals. Thus adaptive hypertrophy of type II DIA fibers in EMP animals was abolished. Fiber succinate dehydrogenase activity was significantly increased in type I and II fibers in EMP DIA. ND did not affect this metabolic adaptation of DIA fibers to persistent loads imposed by EMP.(ABSTRACT TRUNCATED AT 250 WORDS)


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.


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)


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Markus E. Harrigan ◽  
Angela R. Filous ◽  
Andrew P. Tosolini ◽  
Renee Morris ◽  
Jan M. Schwab ◽  
...  

Abstract Sensitive and objective biomarkers of neuronal injury, degeneration, and regeneration can help facilitate translation of experimental findings into clinical testing. Whereas measures of upper motor neuron connectivity have been readily established, functional assessments of lower motor neuron (LMN) innervation of forelimb muscles are lacking. Compound muscle action potential (CMAP) and motor unit (MU) number estimation (MUNE) are well-established methods that allow longitudinal MU integrity monitoring in patients. In analogy we refined CMAP and MUNE methods for assessing spinal MU input in the rat forelimb and hindlimb. Repeated CMAP and MUNE recordings are robust (coefficients of variability: 4.5–11.3%), and MUNE measurements from forelimb wrist flexor muscles (415 ± 8 [SEM]) align with back-traced anatomical LMN counts (336 ± 16 [SEM]). For disease validation, cross-sectional blinded electrophysiological and muscle contractility measurements were obtained in a cohort of G93A SOD1 mutant overexpressing rats and compared with controls. Longitudinal assessment of mutant animals demonstrated progressive motor unit decline in the hindlimb to a greater extent than the forelimb. Hindlimb CMAP and MUNE demonstrated strong correlations with plantarflexion muscle contractility. Cross-species assessment of upper/fore- limb and lower/hind- limb motor units using objective electrophysiological CMAP and MUNE values as biomarkers will guide and improve bi-directional translation.


1999 ◽  
Vol 354 (1385) ◽  
pp. 917-925 ◽  
Author(s):  
A. J. Sokoloff ◽  
G. E. Goslow

The M. pectoralis (pars thoracicus) of pigeons ( Columba livia ) is comprised of short muscle fibres that do not extend from muscle origin to insertion but overlap ‘in-series’. Individual pectoralis motor units are limited in territory to a portion of muscle length and are comprised of either fast twitch, oxidative and glycolytic fibres (FOG) or fast twitch and glycolytic fibres (FG). FOG fibres make up 88 to 90% of the total muscle population and have a mean diameter one-half of that of the relatively large FG fibres. Here we report on the organization of individual fibres identified in six muscle units depleted of glycogen, three comprised of FOG fibres and three comprised of FG fibres. For each motor unit, fibre counts revealed unequal numbers of depleted fibres in different unit cross-sections. We traced individual fibres in one unit comprised of FOG fibres and a second comprised of FG fibres. Six fibres from a FOG unit (total length 15.45 mm) ranged from 10.11 to 11.82 mm in length and averaged (±s.d.) 10.74±0.79 mm. All originated bluntly (en mass) from a fascicle near the proximal end of the muscle unit and all terminated intramuscularly. Five of these ended in a taper and one ended bluntly. Fibres coursed on average for 70% of the muscle unit length. Six fibres from a FG unit (total length 34.76 mm) ranged from 8.97 to 18.38 mm in length and averaged 15.32 ±3.75 mm. All originated bluntly and terminated intramuscularly; one of these ended in a taper and five ended bluntly. Fibres coursed on average for 44% of the muscle unit length. Because fibres of individual muscle units do not extend the whole muscle unit territory, the effective cross-sectional area changes along the motor unit length. These non-uniformities in the distribution of fibres within a muscle unit emphasize that the functional interactions within and between motor units are complex.


1980 ◽  
Vol 43 (6) ◽  
pp. 1615-1630 ◽  
Author(s):  
R. P. Dum ◽  
T. T. Kennedy

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.


1978 ◽  
Vol 44 (3) ◽  
pp. 431-437 ◽  
Author(s):  
L. C. Maxwell ◽  
J. A. Faulkner ◽  
S. A. Mufti ◽  
A. M. Turowski

Fifty extensor digitorium longus muscles of 25 cats were autografted, 33 with and 17 without prior denervation. After 50 days, no significant differences were observed between predenervated and nonpredenervated autografts. Autografted muscles weighed 48% of the weight of control muscles. Few original muscle fibers survived and within 2 wk autografts contained regenerating muscle fibers. The mean cross-sectional area of muscle fibers in the autografts reached 125% of the value for control nontransplanted muscles. The mean percentage of fibers classified high oxidative in autografted muscles was 67% of values for control muscles. SDH activity of autografted muscle homogenates reached 55% of control values. Up to 60 days after surgery autografts had only fast-twitch fibers. At 170 days autografts remained 95% fast twitch in composition. Revascularization began within 4 days, but the capillary to fiber ratio of long term autografts reached only 60% of control values. Although fiber hypertrophy suggests that cats use autografted muscles, lower than control succinate dehydrogenase activity may result from altered recruitment.


Sign in / Sign up

Export Citation Format

Share Document