Influence of weight bearing on the adaptations of rat plantaris to ablation of its synergists

1989 ◽  
Vol 67 (2) ◽  
pp. 636-642 ◽  
Author(s):  
R. N. Michel ◽  
A. E. Olha ◽  
P. F. Gardiner

The present study was designed to determine the contribution of weight bearing to the adaptations of the plantaris (PL) to synergist removal. PL from female rats were exposed to 28 days of a simultaneous condition of synergist ablation and hindlimb suspension. At 28 days, contractile responses and morphological measures were obtained and compared with muscles that either had synergists intact or were weight bearing or a combination of both. Synergist ablation prolonged PL maximum isometric twitch tension (Pt), time to peak tension (12%), and one-half relaxation time (12%); increased Pt (26%), maximum isometric tetanic tension (Po, 44%), fatigue resistance (FI, 42%), and fast fiber cross-sectional area (FT CSA, 20%); and decreased Pt/Po (13%) over nonablation counterparts. Suspension decreased PL Pt (26%), Po (26%), rest length (16%), FT CSA (31%), and slow-twitch fiber (ST) number (24%) but increased FI (75%) over weight-bearing counterparts. PL from weight-bearing animals were heavier than from suspended animals, and the extent of this response was greatest after synergist removal. Whole muscle and ST CSA and ST area contribution were greater only in weight-bearing synergist ablation muscles. Daily weight bearing (4 h) in synergist ablation hindlimb suspension groups caused PL weights and ST expressions to be halfway between 24-h suspension and 24-h weight-bearing groups. Our results suggest that weight bearing is not essential to the induction of several adaptations associated with synergist ablation but is required to cause the large muscle mass and ST expression characteristic of this model.

2003 ◽  
Vol 95 (6) ◽  
pp. 2425-2433 ◽  
Author(s):  
Julian E. Stelzer ◽  
Jeffrey J. Widrick

Cross-sectional area (CSA), peak Ca2+-activated force (Po), fiber specific force (Po/CSA), and unloaded shortening velocity ( Vo) were measured in slow-twitch [containing type I myosin heavy chain (MHC)] and fast-twitch (containing type II MHC) chemically skinned soleus muscle fiber segments obtained from three strains of weight-bearing and 7-day hindlimb-suspended (HS) mice. HS reduced soleus slow MHC content (from ∼50 to ∼33%) in CBA/J and ICR strains without affecting slow MHC content in C57BL/6 mice (∼20% of total MHC). Two-way ANOVA revealed HS-induced reductions in CSA, Po, and Po/CSA of slow and fast fibers from all strains. Fiber Vo was elevated post-HS, but not consistently across strains. No MHC × HS treatment interactions were observed for any variable for C57BL/6 and CBA/J mice, and the two significant interactions found for the ICR strain (CSA, Po) appeared related to inherent pre-HS differences in slow vs. fast fiber CSA. In the mouse HS models studied here, fiber atrophy and contractile dysfunction were partially dependent on animal strain and generally independent of fiber MHC isoform content.


1982 ◽  
Vol 52 (2) ◽  
pp. 473-478 ◽  
Author(s):  
R. R. Roy ◽  
I. D. Meadows ◽  
K. M. Baldwin ◽  
V. R. Edgerton

Chronic overload of a skeletal muscle by removing its synergists produces hypertrophy and marked changes in its metabolic and biochemical properties. In this study alterations in the contractile properties of the plantaris 12–14 wk after bilateral removal of the soleus and gastrocnemius were investigated. In situ isometric and isotonic contractile properties of overloaded plantaris (OP), normal plantaris (NP), and normal soleus (NS) were tested at 33 +/- 1 degree C. Op were 97% heavier than NP and produced 43 and 46% higher twitch (Pt) and tetanic (Po) tensions. However, NP produced more tension per cross-sectional area than OP (mean 26.2 vs. 21.6 N/cm2; P less than 0.001). Isometric twitch time to peak tension (TPT) and half-relaxation time (1/2RT) were significantly longer in OP (mean 36.4 vs. 32.5 ms and 23.9 vs. 18.4 ms). Mean maximum shortening velocity (Vmax, mm/s per 1,000 sarcomeres) were 34.1 for NP and 18.1 for OP (P less than 0.001). The degree of conversion toward the Vmax of NS was 74% compared with only 19 and 14% for TPT and 1/2RT. OP produced a higher proportion of Po at a given stimulation frequency than NP and showed less fatigue than NP after repetitive stimulation. Chronic overload of the fast plantaris modified to varying degrees the contractile properties studied toward that resembling a slow muscle. Although the maximum tension of OP was markedly enhanced it was not in proportion to the increase in muscle mass.


1981 ◽  
Vol 240 (4) ◽  
pp. H472-H480 ◽  
Author(s):  
G. F. Tibbits ◽  
R. J. Barnard ◽  
K. M. Baldwin ◽  
N. Cugalj ◽  
N. K. Roberts

The present studies were conducted to investigate further the mechanisms by which the myocardium adapts to exercise training. Sixty female rats were randomly divided into sedentary control (group C) and trained (group T) groups. Group T was progressively trained for 12 wk. After the rats were killed, left ventricular papillary muscles were mounted in a tissue bath for mechanical studies. Muscles from group T generated greater peak isometric twitch tension per unit cross-sectional area than muscles from group C with [Ca2+]o ranging from 0.25 to 3.5 mM. Analyses of these data indicated that the Km for Ca2+ was not different but that the predicted number of sarcolemmal Ca2+ binding sites was 63% higher in group T. The ATPase activity of the purified cardiac myofibrils was not different between the two groups in the pCa range of 8.53-4.42. Action potentials were recorded with microelectrodes impaled into left ventricular muscle fibers of the subendocardium. Although there was no difference in the resting membrane potential, overshoot, or 90% duration, there was a significant prolongation of the action potential at 0 mV (20.2 +/- 1.0 vs 30.0 +/- 1.3 ms) in group T. These data further support the hypothesis that treadmill exercise enhances cardiac performance by increasing Ca2+ availability to the contractile element. This adaptation is mediated, at least in part, by a sarcolemmal adaptation induced by the exercise paradigm.


1987 ◽  
Vol 62 (6) ◽  
pp. 2348-2357 ◽  
Author(s):  
R. R. Roy ◽  
M. A. Bello ◽  
P. Bouissou ◽  
V. R. Edgerton

Hindlimb suspension (HS) results in whole muscle atrophic and metabolic changes that vary in magnitude in different hindlimb muscles. The present study was designed to investigate these effects in single fibers. Fiber type and size and the activities of two metabolic marker enzymes were determined in a deep (close to the bone) and a superficial (away from the bone) region of the medial gastrocnemius (MG) and the tibialis anterior (TA) of control (CON) and 28-day HS adult female rats. Fibers were classified as dark or light adenosinetriphosphatase (ATPase) based on their qualitative staining reaction for myosin ATPase following alkaline preincubation. Fiber area and succinate dehydrogenase (SDH) and alpha-glycerophosphate dehydrogenase (GPD) activities were determined in tissue sections by use of an image analysis system. After 28 days of HS, the mean body weights of the CON and HS were similar. MG atrophied 28%, whereas TA weight was maintained in the HS. Both dark and light ATPase fibers in the deep region of the MG had smaller cross-sectional areas following HS, with the atrophic response being approximately twice as great in the light ATPase fibers. No significant changes in fiber type composition in either muscle or in fiber sizes in the superficial region of the MG or in either region of the TA were observed. Mean SDH activities of both fiber types were significantly lower in the MG and TA following HS. In contrast, mean GPD activities were either increased or maintained in light and dark ATPase fibers of both muscles in HS. Changes in SDH and GPD activity could not be directly linked to changes in fiber cross-sectional area. In summary, these data suggest an independence of the mechanisms determining muscle fiber size and metabolic adaptations associated with HS.


2005 ◽  
Vol 288 (2) ◽  
pp. C360-C365 ◽  
Author(s):  
D. A. Riley ◽  
J. L. W. Bain ◽  
J. G. Romatowski ◽  
R. H. Fitts

Single skinned fibers from soleus and adductor longus (AL) muscles of weight-bearing control rats and rats after 14-day hindlimb suspension unloading (HSU) were studied physiologically and ultrastructurally to investigate how slow fibers increase shortening velocity ( V0) without fast myosin. We hypothesized that unloading and shortening of soleus during HSU reduces densities of thin filaments, generating wider myofilament separations that increase V0 and decrease specific tension (kN/m2). During HSU, plantarflexion shortened soleus working length 23%. AL length was unchanged. Both muscles atrophied as shown by reductions in fiber cross-sectional area. For AL, the 60% atrophy accounted fully for the 58% decrease in absolute tension (mN). In the soleus, the 67% decline in absolute tension resulted from 58% atrophy plus a 17% reduction in specific tension. Soleus fibers exhibited a 25% reduction in thin filaments, whereas there was no change in AL thin filament density. Loss of thin filaments is consistent with reduced cross bridge formation, explaining the fall in specific tension. V0 increased 27% in soleus but was unchanged in AL. The V0 of control and HSU fibers was inversely correlated ( R = −0.83) with thin filament density and directly correlated ( R = 0.78) with thick-to-thin filament spacing distance in a nonlinear fashion. These data indicate that reduction in thin filament density contributes to an increased V0 in slow fibers. Osmotically compacting myofilaments with 5% dextran returned density, spacing, and specific tension and slowed V0 to near-control levels and provided evidence for myofilament spacing modulating tension and V0.


1987 ◽  
Vol 62 (6) ◽  
pp. 2180-2186 ◽  
Author(s):  
R. W. Tsika ◽  
R. E. Herrick ◽  
K. M. Baldwin

The purpose of this study was to investigate the role of chronic weight-bearing activity as the primary inducer of compensatory muscle growth and changes in myosin isoform expression in rodent fast-twitch plantaris muscle. Thus, female rats were subjected to the independent and simultaneous exposure of functional overload (induced via synergist removal) and hindlimb unweighting (suspension) for 6 wk. Groups (n = 7/group) consisted of normal-control (NC); overload (OV); normal-suspension (N-SUS); and overload-suspension (OV-SUS). Body weight of both suspension groups was significantly less than both the NC and OV groups (P less than 0.001). Compared with the NC group, normalized plantaris weight (mg/g body wt) of both the OV and OV-SUS groups was greater, whereas that of the N-SUS was lower (P less than 0.001). However, normalized plantaris weight was greater in OV compared with OV-SUS by 35% (P less than 0.001). Myofibril protein content (mg/g) and Ca2+-regulated myofibril adenosinetriphosphatase (ATPase) specific activity were similar for all groups except that ATPase was lower in the OV group compared with the other groups (P less than 0.05). Native myosin isoform analysis revealed a significant increase in the expression of slow and intermediate myosin and the repression of fast myosin 1 (Fm1) in OV compared with NC. This shift in expression was not as pronounced in the OV-SUS group. Interestingly, only traces of slow myosin were observed in the N-SUS group compared with the other groups. These results suggest that weight bearing is an essential component of the overload model for inducing significant increases in both muscle mass and slow myosin isoform expression. Second, lack of weight bearing, while not markedly affecting fast myosins, appears to repress the expression of slow myosin.


1988 ◽  
Vol 65 (3) ◽  
pp. 1231-1237 ◽  
Author(s):  
E. O. Hauschka ◽  
R. R. Roy ◽  
V. R. Edgerton

The morphological and histochemical properties of the rat soleus were studied after 1 wk of hindlimb suspension, one model that removes the weight-bearing function of the hindlimbs. To examine the effectiveness of weight support activity in maintaining soleus mass, fiber size, and succinate dehydrogenase (SDH) activity, the hindlimbs of adult male Sprague-Dawley rats were suspended (HS) and half of these rats were walked on a treadmill for 40 min/day (10 min every 6 h) at 5 m/min and a 19 degree grade (HS-WS). Significant reductions in soleus mass and fiber size were found after 1 wk of HS. Weight support activity decreased the atrophic response by approximately 50%. In the alkaline myofibrillar adenosine triphosphatase (ATPase) dark-staining fibers, SDH activity was higher in the HS than control rats, whereas it was similar to control in the HS-WS rats. Total SDH activity (SDH activity X cross-sectional area) in fibers staining lightly for ATPase in HS and HS-WS rats was lower than in control rats, whereas in the darkly stained ATPase fibers it was similar among the three groups. No changes were observed in fiber type percentages after 1 wk of HS or HS-WS. The results suggest that short-duration, daily weight support activity can ameliorate, but not prevent, soleus atrophy induced by HS. Furthermore, fiber cross-sectional area is more responsive to periodic weight support in dark than light ATPase fibers. These results also demonstrate that muscle fiber atrophy need not be associated with a loss in SDH activity.


2008 ◽  
Vol 295 (5) ◽  
pp. R1585-R1592 ◽  
Author(s):  
J. J. Widrick ◽  
G. F. Maddalozzo ◽  
H. Hu ◽  
J. C. Herron ◽  
U. T. Iwaniec ◽  
...  

To better understand how atrophied muscles recover from prolonged nonweight-bearing, we studied soleus muscles (in vitro at optimal length) from female rats subjected to normal weight bearing (WB), 15 days of hindlimb unloading (HU), or 15 days HU followed by 9 days of weight bearing reloading (HU-R). HU reduced peak tetanic force (Po), increased maximal shortening velocity (Vmax), and lowered peak power/muscle volume. Nine days of reloading failed to improve Po, while depressing Vmax and intrinsic power below WB levels. These functional changes appeared intracellular in origin as HU-induced reductions in soleus mass, fiber cross-sectional area, and physiological cross-sectional area were partially or completely restored by reloading. We calculated that HU-induced reductions in soleus fiber length were of sufficient magnitude to overextend sarcomeres onto the descending limb of their length-tension relationship upon the resumption of WB activity. In conclusion, the force, shortening velocity, and power deficits observed after 9 days of reloading are consistent with contraction-induced damage to the soleus. HU-induced reductions in fiber length indicate that sarcomere hyperextension upon the resumption of weight-bearing activity may be an important mechanism underlying this response.


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)


2004 ◽  
Vol 97 (5) ◽  
pp. 1859-1865 ◽  
Author(s):  
J. M. Welch ◽  
C. M. Weaver ◽  
C. H. Turner

Impact exercise can have beneficial effects on the growing skeleton. To understand what changes it promotes in the shafts and ends of weight-bearing bones, we measured the effects of impact from repetitive free falls in growing rats. Fischer 344 female rats, 6.5 wk old, were assigned to one of three groups ( n = 10 each). Controls were not dropped, whereas those subjected to impact were dropped from 30 or 60 cm. Rats in both free-fall groups were dropped 10 times per day for 8 wk. Leg bones were mechanically tested, and their cross-sectional area (CSA), cross-sectional moments of inertia, and volumetric bone mineral density (BMD) were measured by peripheral quantitative computed tomography. In the shafts of the forelimbs, but not the hindlimbs, free-fall impact resulted in greater ultimate breaking force, minimum and maximum second moments of area, and CSA but not BMD. In the bone ends of the forelimb and tibial bones, trabecular BMD increased but CSA did not. Landing from 30 and 60 cm produced peak impact forces of 12.0 and 16.7 times the standing forefoot weight for each front leg and of 4.5 and 7.7 times the standing hind foot weight for each hind foot. Overall, free-fall impact affected the forelimbs by increasing trabecular bone density in the bone ends and improving the strength at the shaft as a result of geometric improvements. These results indicate that adaptation to impact may occur by different mechanisms in bone end and shaft regions.


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