| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
1 Exercise Biochemistry Laboratory, Faculty of Physical Education and Recreation2 Division of Physical Medicine and Rehabilitation3 Centre for Neuroscience, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, AB, Canada T6G 2H9
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
RT), half-fall time (FT), twitch force (TWf) tetanic force (TETf) and the sag ratio as applied to the slow soleus (SOL) and the fast-twitch extensor digitorum longus (EDL) and medial gastrocnemius (MG) muscles of the rat hindlimb. In addition, the relationship of each individual isometric measure was examined with regard to the pattern of myosin heavy chain (MHC) isoform expression. Measures of TTP, RT, FT and sag ratio were negatively correlated with MHCIId(x) and MHCIIb (P < 0.0001), and positively correlated with MHCI (P < 0.0001). TWf and TETf were negatively correlated with MHCI content (P < 0.0001) and positively with MHCIId(x) (P < 0.0001) and MHCIIb (P < 0.001). Comparisons of isometric measures using a paired Student's t test revealed that they were not different between the right and left legs; all measures displayed high correlations between the left and right legs (r= 0.71–0.85, P < 0.0001). In contrast to standard tests of statistical significance, these functional measures exhibited a considerable range of RAb when individual muscles were studied in only one hindlimb. When averaged across all muscles, however, the FT, RT, TWf and TTP measures possessed high overall reliability; measures of TETf and sag ratio were moderately reliable. The results of this study show that the isometric measures studied possess significant predictive value with regard to MHC isoform content; the left and right legs are interchangeable but display a considerable range of reliability when only one hindlimb is studied.
(Received 14 March 2004;
accepted after revision 10 June 2004; first published online 15 July 2004)
Corresponding author C. T. Putman: E-417 Van Vliet Centre, University of Alberta, Edmonton, Alberta, Canada, T6G 2H9. Email: tputman{at}ualberta.ca
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Isometric measures used to assess whole muscle contraction speed commonly include the time-to-peak tension development (TTP) and the half-rise-time (RT; Stein et al. 1982; Gordon & Stein, 1985) and are primarily determined by the pattern of MHC isoforms expressed. The rate of relaxation, however, is typically measured by the half-fall time (FT). In fast-twitch fibres, this property is dependent on the expression of the fast Ca2+-ATPase (SERCA1) isoform and parvalbumin (Hämäläinen & Pette, 1997; Schwaller et al. 1999). By comparison, in slow fibres, the FT is related to the expression of the slow SERCA2a isoform (Hämäläinen & Pette, 1997). Twitch (TWf) and tetanic (TETf) force production are frequently used to assess whole muscle strength; these measures reflect aspects of the muscle phenotype that include fibre type composition (i.e. myosin ATPase activity), architecture, and the number of contractile units in parallel and series (Rafuse et al. 1997; Tötösy et al. 1992). At the motor unit level, the ‘sag’ and force generated during subtetanic stimulation varies systematically with these other isometric measures (Tötösy de Zepetnek et al. 1992; Gordon et al. 1997; Rafuse et al. 1997). Thus, it follows that at the whole muscle level the sag ratio should reflect the average motor unit properties, and may be useful to investigate functional differences between muscles composed of different fibre types.
The primary purpose of this study was to assess the reliability of isometric measures of TTP, RT, FT, TWf, TETf and the sag ratio in several hindlimb muscles when only one limb is studied and thereby to establish the interchangeability between muscles of the right and left hindlimb. A secondary objective was to examine the sensitivity of TTP, RT, FT, TWf, TETf and the sag ratio, especially with regard to the ability of these measures to differentiate between two fast-twitch muscles (i.e. extensor digitorum longus, EDL, and medial gastrocnemius, MG) that differ in their respective MHC isoform contents. The range of our analysis was expanded to include the slow soleus (SOL) muscle. The results of this investigation show that small variations in the MHC isoform contents of fast-twitch rodent muscles are reflected in whole muscle TTP, RT and FT. Measures of TWf, TETf and sag ratio also varied systematically with MHC isoform contents but displayed considerable dependence of other morphological properties. Overall the right and left legs were interchangeable, but displayed a large range of reliability when only one hindlimb was studied.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Twelve adult male Sprague–Dawley rats (595 ± 33 g body weight) were obtained from the local animal facility at the University of Alberta and used in the present study. All experiments were completed in accordance with the guidelines of the Canadian Council for Animal Care and received ethical approval from the University of Alberta. All animals were maintained under controlled environmental conditions (22°C and 12 h alternating light and dark cycles) and received standard chow and 5% dextrose solution ad libitum.
Surgery
Surgery was performed under general anaesthesia (45 mg kg–1 sodium pentobarbit I.P., MTC Pharmaceutical, Cambridge, Ontario, Canada) according to Tam et al. (2001). Briefly, an indwelling catheter (PE 50, Fisher Scientific, Edmonton, Alberta, Canada) was placed in the external jugular vein and the trachea was cannulated for mechanical ventilation if necessary. Additional anaesthetic (diluted 1:5) was administered intravenously in a saline solution containing 5% glucose, as required. Incisions were made along the dorsum of the right and left hindlimbs, the EDL, SOL and MG muscles were exposed, and the tibialis anterior (TA) denervated. A Silastic nerve cuff embedded with two multistranded stainless-steel wires (Cooner Wire Co., Chatsworth, CA, USA, AS 632) was placed around the sciatic nerve for electrical stimulation. The distal tendons of each muscle were subsequently isolated and individually secured with 2.0 silk (metric 3) to a Kulite strain gauge (model KH-102). Extreme care was taken to ensure that the arterial supply and venous drainage remained intact during the isolation of each muscle. Skin incisions were then sutured before beginning functional measurements. Animals were placed in a prone position and secured with clamps at the knees and ankle joints. Core body temperature was maintained at 39°C with a heating pad and continuously monitored with a rectal probe. Animals were killed with an overdose of anaesthetic and muscles were collected, snap-frozen in liquid nitrogen (–196°C) and stored at –80°C until analysed. The mean muscle weights of the SOL, EDL and MG were 0.235 ± 0.017, 0.248 ± 0.022 and 1.405 ± 0.113 g, respectively.
Functional measurements
Isometric muscle function measures were completed according to Tam et al. (2001). Before each series of recordings, the optimal resting length (L0) required to generate maximum force was determined for each muscle. Maximum twitch (TWf, in mN) and tetanic forces (TETf, in mN) were sequentially recorded in the right and then left EDL, SOL and MG. TWf was determined as the average of peak forces generated by five individual twitches elicited at 1 Hz. Time-to-peak tension (TTP, in ms) was determined as the time elapsed from time 0 to peak force production. The half-rise time (RT, in ms) was calculated as the time from the onset of contraction to 50% of the maximum force produced. The half-fall time (FT, in ms) was recorded as the time required for the twitch peak force to decay by 50%. The presence of whole muscle ‘sag’ was calculated as the ratio of final-to-initial force generated from an unfused tetanic contraction using an interval of 1.25 x TTP for 800 ms. Traditionally the sag ratio has been used to classify single motor units as ‘slow’ if the ratio is 
1.0 or ‘fast’ if the ratio is <1.0. In the present study, we investigated the degree to which the sag test may also reflect changes in the average motor unit composition at the whole muscle level. TETf was determined as the force produced by 21 pulses (100 Hz) given at an interstimulus interval of one-third of the muscle contraction time (Gordon & Stein, 1985; Tötösy de Zepetnek et al. 1992). In addition, the TWf and TETf measures were normalized by dividing the individual twitch and tetanic forces by the average wet muscle weights. Finally, the twitch-to-tetanus (TWf:TETf) ratio was calculated by dividing the twitch force by the tetanic force. All measurements were amplified, viewed on an oscilloscope, averaged using a PDP-11 laboratory computer and stored on disks.
Electrophoretic analysis of myosin heavy chain
Myosin heavy chain (MHC) isoforms were analysed according to the methods described by Hämäläinen & Pette (1996). Muscles were homogenized on ice in a buffer containing 100 mM Na4P2O7 (pH 8.5), 5 mM EGTA, 5 mM MgCl2, 0.3 M KCl, 10 mM DTT and 5 mg ml–1 of a protease inhibitor cocktail (CompleteTM, Roche Diagnostic, Laval, PQ, Canada). Samples were subsequently stirred for 30 min on ice, centrifuged at 12 000g for 5 min at 4°C, diluted 1:1 with glycerol, and stored at –20°C until analysed. Prior to gel loading, muscle extracts were diluted to 0.2 µg µl–1 in Laemmli-lysis buffer and boiled for 7 min. Five microlitres from the resulting MHC extracts were electrophoresed in duplicate for 24 or 48 h (275 V and 12°C) on 7% polyacrylamide gels containing glycerol under denaturing conditions. Gels were immediately fixed, and MHC isoforms were detected by silver staining (Oakley et al. 1980) and evaluated by densitometry (Syngene ChemiGenius, GeneTools, Syngene, Cambridge, UK). The gel running time and loading conditions were optimized for each muscle in order to maximize MHC isoform separation.
Statistical analyses
Data are presented as means ± s.e.m. Absolute reliability (RAb) was defined as the consistency or repeatability of a measure, expressed as a ratio of the variance of the ‘true score’ to the variance of the measured score, and was calculated as follows:
|
|
R2 is the estimate of the rat variance component, L2 represents the estimate of the leg variance component, nL (number of legs) = 1, nD (number of days) = 1, and SDe2 is the estimate of the residual variance component. R2, L2 and SDe2 were calculated by ANOVA. Differences between group means were assessed using a paired dependent sample Student's t test. Right and left legs were also compared by individual correlation analyses (r). Isometric measures were evaluated against each of the various MHC isoforms by multiple regression analysis according to Talmadge et al. (2002); correlation coefficients derived from this analysis (R) are reported. Differences were considered significant at P < 0.05, but actual P values are cited. |
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
The slow SOL displayed the longest TTP at 55.0 ± 3.1 ms, followed by the EDL (39.5 ± 0.8 ms, P < 0.00003), and the faster contracting MG (25.1 ± 0.4 ms, P < 0.000001; Fig. 1A). The MG was considerably faster (P < 0.000001) than the EDL. The SOL also displayed the longest RT at 32.1 ± 2.04 ms (P < 0.000001; Fig. 1B). In addition, the RT of the EDL (19.2 ± 0.4 ms) was 24% slower than that of the MG (14.6 ± 0.3 ms, P < 0.000001). The FT of the SOL was greater than 2-fold longer (57.3 ± 3.6 ms, P < 0.000001) compared with all other muscles (Fig. 1C); the FT of the remaining muscles followed the order EDL (23.5 ± 1.5 ms) > MG (12.3 ± 0.5 ms, P < 0.000001).
|
30% less TETf than the MG (5403 ± 191 mN, P < 0.000001; Fig. 2B). However, when the TWf was normalized for muscle weight the EDL produced the most force (6.17 ± 0.45 mN mg–1) followed by the SOL (2.84 ± 0.28 mN mg–1), and lastly the MG (1.14 ± 0.08 mN mg–1; Fig. 2D). The EDL also generated the greatest normalized TETf (14.5 ± 0.80 mN mg–1, P= 0.07) compared with the SOL (12.4 ± 0.81 mN mg–1) and MG (3.8 ± 0.14 mN mg–1; Fig. 2E). The TWf:TETf ratios were as follows: EDL (0.44 ± 0.14) > MG (0.26 ± 0.018) > SOL (0.25 ± 0.006; Fig. 2C). The whole muscle SOL sag ratio was 2.6- to 5.4-fold greater than observed for the mixed fast-twitch EDL and MG muscles (P < 0.000001); the sag ratio for the EDL (0.83 ± 0.02) differed from the MG by 53% (P < 0.000001; Fig. 2F).
|
The MHC isoform contents of the different muscles are qualitatively represented in the gels of Fig. 3, and quantitatively illustrated in Fig. 4. MHCI content (Fig. 4A) was most abundant in the SOL, where it comprised 89.5 ± 2.0% of the total MHC content and was 13- to 30-fold greater than in the other muscles studied (P < 0.000001). Within the mixed fast-twitch EDL, the MHCI content was 3.1 ± 0.4%; it was approximately 2-fold greater (P < 0.002) in the MG, reaching 5.9 ± 0.4%.
|
|
Correlation analyses
Table 1 summarizes the correlation coefficients derived from multiple regression analysis (R) of MHC isoforms and isometric functional measures. The TTP, RT, FT and sag ratio were negatively correlated with MHCIId(x) and MHCIIb (P < 0.0001). Conversely, the TTP, RT, FT and sag ratio displayed high positive correlations with MHCI. The TWf and TETf measures displayed a wide range of correlation coefficients (R), most of which were statistically significant. Normalized TWf was not highly correlated to any of the MHC isoforms. R values for normalized TETf were also low, with the exception of MHCIId(x) (R=–0.38, P < 0.05). The TWf:TETf ratio was significantly correlated with MHCI and MHCIId(x), where the R values were –0.34 and 0.49 (P < 0.05), respectively.
|
Differences between the right and left legs were evaluated by performing a paired dependent sample Student's t test. Isometric functional measures were not different between the right and left legs (Fig. 5A–F). The lone exception was TETf, where the left SOL was 17% lower than the right (P < 0.003; Fig. 5E). In addition, individual correlation coefficient analyses (r) were completed to further compare the left and right legs (Fig. 5). All measures showed high correlations between the left and right legs.
|
RAb 0.60. RAb values less than 0.4 were considered low by comparison. In the present study, the TTP, RT, FT, TWf, TETf and sag ratio displayed a range of RAb for the individual muscles studied (Fig. 6A and B). However, when averaged across all of the muscles, the RAb was high for TTP, RT, FT and TWf, and within the moderate range for TETf and sag ratio (Fig. 6C and D).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
RT and FT of isometric twitch contractions describe the speed characteristics of whole muscle, while the TWf and TETf characterize the force parameters; for each of these measures our data were similar to previous reports for rat (Close, 1969; Petrofsky & Fitch, 1980) and other mammalian muscles (Gordon & Stein, 1985; Gillespie et al. 1986; Gordon et al. 1997). Because the ‘sag test’ has been used to reliably identify individual motor unit types (Gordon et al. 1997), we also sought to determine whether this test could predict the average motor unit composition of whole muscle, as reflected by the MHC isoform profile. These isometric measures were highly correlated with the prevailing pattern of MHC isoform expression. Although only the speed parameters are known to possess a causal relationship with MHC, the remaining functional properties varied systematically with the MHC isoform profile, and thus displayed significant predictive value. Isometric functional measurements in relation to MHC isoform content
The relationship between the pattern of MHC isoform expression and functional properties of single fibres has been well established in vitro (Metzger et al. 1985; Bottinelli et al. 1991; Bottinelli et al. 1994b), where measures that reflect fibre contraction time have been shown to be directly proportional to myosin-ATPase activity (Bottinelli et al. 1994b). On the motor unit level, the sag ratio is inversely proportional to myosin-ATPase activity owing to its close coordinate relationship with other aspects of fibre phenotype, such as the capacity to generate energy via oxidative pathways (Larsson et al. 1991; Gordon, 1995; Rafuse et al. 1997). Measures of TWf and TETf are also proportional to myosin-ATPase activity; TTP, RT, TWf and TETf are further dependent on aspects of muscle architecture that include cross-sectional area (Segal et al. 1986), muscle and fibre lengths (Huijing et al. 1989; Huijing et al. 1994) and fibre pennation angle (Woittiez et al. 1984; Huijing et al. 1989; Huijing et al. 1994).
The design of our study allowed us to examine isometric contractile force, speed and fatigability in slow- and fast-twitch skeletal muscles within the same rat. With regard to the fast-twitch muscles, a modest difference in MHC content, reflecting different fibre type proportions, was detectable by measures of contractile speed. The MG was considerably faster than the EDL (Fig. 1), which was primarily related to the 7% greater MHCIIb content and 7% lower MHCIId(x) content (Fig. 4). Although the MG is known to posses a greater fibre pennation angle compared to the EDL (i.e. mean ±S.D.: 10.0 ± 1.41 versus 20.4 ± 5.53 deg), the mean fibre lengths of these two muscles are similar (Huijing et al. 1994); since TTP and RT vary inversely with the angle of pennation, the faster contraction time of the MG must have resulted from different patterns of MHC isoform expression between these fast-twitch muscles. This finding indicates that TTP and RT are sensitive enough to detect comparatively modest differences in the patterns of MHC isoform expression. It is also clear from the present study that the FT varied systematically with these speed parameters and was similarly sensitive. Additionally, a comparison of these two fast-twitch muscles with the SOL further demonstrates considerable utility across a broad physiological range.
Similarly, the force characteristics are, to varying degrees, dependent on muscle architectural structure and MHC isoform content. The graded phenomena observed for the TWf and TETf measures (Fig. 2A and B) can be attributed to differences in muscle mass, fibre length (i.e. sarcomeres in series) and fibre pennation angle as well as the pattern of MHC isoform expression. However, when these measures were normalized to muscle mass, the MG obviously produced less twitch and tetanic force (Fig. 2D and E). The greater normalized TWf of the EDL compared to SOL undoubtedly resulted from the greater proportion of fast MHC isoforms present in the former, since the architectural differences between these two muscles are minimal (Woittiez et al. 1984). In contrast, normalized TWf of the MG was approximately 6-fold lower than that of the EDL, which appears to be primarily due to its much greater pennation angle (Woittiez et al. 1984). The inherent architectural differences between the MG and EDL probably also form the basis for a similar pattern of low efficiency with regard to normalized TETf displayed by the former.
While the utility of the sag ratio is well established at the motor unit level (Gordon et al. 1997; Rafuse et al. 1997), the utility of this measure at the level of whole muscle is limited. In the present study, the sag ratio of the MG was not strictly correlated with its known motor unit profile, based on the patterns of MHC isoform expression. When compared with the fast EDL (i.e. 1.0) and slow SOL (>>1.0), which displayed values within their expected ranges, the larger than expected values observed for the faster MG probably reflect the impact of structural or metabolic differences compared with the EDL. Thus, when applied to whole muscle, measures of sag appear to be suitable only to compare muscles of the same type.
Reliability
The RAb is the ratio of the animal variance to the total variance. In the present study, we minimized animal variance by maximizing the homogeneity of our sample population, which allowed us to expose the comparatively greater variance associated with select isometric functional measurements. Standard tests of statistical significance indicated that these measures were reliable. Student's t test for dependent means, for instance, showed that the left and right legs were not different for any of the fast-twitch muscles studied, and for most measures of the slow soleus (Fig. 5). Moreover, correlation analyses comparing mean values for the right and left legs revealed that these measures were highly correlated for all muscles (Fig. 5, P < 0.00001). Estimates of the individual RAb, however, revealed that these isometric measures were more variable than previously assumed. The MG displayed the highest overall reliability for all measures (i.e. 0.62–1.00) except TETf, which was low (i.e. 0.2). The EDL also displayed high reliability for TTP, TWf and RT (0.70–1.00), but low RAB for the sag ratio, FT or TETf (0.1–0.4). In contrast the TTP, RT and TETf (0.52–0.80) proved reliable for the SOL; however, the sag ratio, FT and TWf displayed low RAb (0.1–0.38).
However, when the individual functional tests were examined across all muscles studied, the mean reliability was moderate to high for all measures. Thus the discrepancies displayed between standard tests of statistical significance and calculated RAb suggests that caution must be exercised when making inferences about data obtained from isometric measures of TTP, RT, FT, TWf, TETf and the sag ratio. In this regard, measurements of the same muscle on both hindlimbs or of two or more muscles within a single leg are indicated. Collectively the results of this investigation validate the use of these isometric measures to establish the functional impact associated with differences in patterns of MHC isoform expression and morphology across a broad physiological range, but also point to some limitations associated with their application.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Bottinelli R, Canepari M, Reggiani C & Stienen GJ (1994b). Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol 481, 663–675.[Medline]
Bottinelli
R, Schiaffino
S
&
Reggiani
C (1991). Force–velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle. J Physiol
437, 655–672.
Caiozzo
V, Haddad
F, Baker
MJ, Herrick
RE, Prietto
N
&
Baldwin
KM (1996). Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J Appl Physiol
81, 123–132.
Close
R (1969). Dynamic properties of fast and slow skeletal muscles of the rat after nerve cross-union. J Physiol
204, 331–346.
Dunn S & Michel RN (1997). Coordinated expression of myosin heavy chain isoforms and metabolic enzymes within overloaded rat muscle fibers. Am J Physiol 273, C371–C383.
Galler S, Hilber K & Pette D (1996). Force responses following stepwise length changes of rat skeletal muscle fibre types. J Physiol 493, 219–227.[Medline]
Galler S, Schmitt TL & Pette D (1994). Stretch activation, unloaded shortening velocity, and myosin heavy chain isoforms of rat skeletal muscle fibres. J Physiol 478, 513–521.[Medline]
Gillespie
M, Gordon
T
&
Murphy
PR (1986). Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve. J Physiol
372, 485–500.
Gordon T (1995). Fatigue in adapted systems. Overuse and underuse paradigms. Adv Exp Med Biol 384, 429–456.[Medline]
Gordon T & Stein RB (1985). Temperature effects on the kinetics of force generation in normal and dystrophic mouse muscles. Exp Neurol 89, 348–360.[Medline]
Gordon
T, Tyreman
N, Rafuse
VF
&
Munson
JB (1997). Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. I. Muscle and motor unit properties. J Neurophysiol
77, 2585–2604.
Hämäläinen N & Pette D (1996). Slow-to-fast transitions in myosin expression of rat soleus muscle by phasic high-frequency stimulation. FEBS Lett 399, 220–222.[CrossRef][Medline]
Hämäläinen N & Pette D (1997). Coordinated fast-to-slow transitions of myosin and SERCA isoforms in chronically stimulated muscles of euthyroid and hyperthyroid rabbits. J Muscle Res Cell Motil 18, 545–554.[CrossRef][Medline]
Huijing P, Nieberg SM, vd Veen EA & Ettema GJ (1994). A comparison of rat extensor digitorum longus and gastrocnemius medialis muscle architecture and length-force characteristics. Acta Anat 149, 111–120.[Medline]
Huijing P, Lookeren Campagne AAH & Koper JF (1989). Muscle architecture and fibre characteristics of rat gastrocnemius and semimembranosus muscles during isometric contractions. Acta Anat 135, 46–52.[Medline]
Irintchev A, Zweyer M, Cooper RN, Butler-Browne GS & Wernig A (2002). Contractile properties, structure and fiber phenotype of intact and regenerating slow-twitch muscles of mice treated with cyclosporin A. Cell Tissue Res 308, 143–156.[CrossRef][Medline]
Larsson
L, Ansved
T, Edstrom
L, Gorza
L
&
Schiaffino
S (1991). Effects of age on physiological, immunohistochemical and biochemical properties of fast-twitch single motor units in the rat. J Physiol
443, 257–275.
Larsson L, Li X, Teresi A & Salviati G (1994). Effects of thyroid hormone on fast- and slow-twitch skeletal muscles in young and old rats. J Physiol 481, 149–161.
Metzger
J, Scheidt
KB
&
Fitts
RH (1985). Histochemical and physiological characteristics of the rat diaphragm. J Appl Physiol
58, 1085–1091.
Oakley B, Kirsch DR & Morris NR (1980). A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal Biochem 105, 361–363.[CrossRef][Medline]
Petrofsky J & Fitch CD (1980). Contractile characteristics of skeletal muscles depleted of phosphocreatine. Pflugers Arch 384, 123–129.[CrossRef][Medline]
Pette D & Staron RS (1997). Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 170, 143–223.[Medline]
Pette D & Staron RS (2000). Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50, 500–509.[CrossRef][Medline]
Rafuse V, Pattullo MC & Gordon T (1997). Innervation ratio and motor unit force in large muscles: a study of chronically stimulated cat medial gastrocnemius. J Physiol 499, 809–823.
Schwaller B, Dick J, Dhoot G, Carroll S, Vrbová G, Nicotera P et al. (1999). Prolonged contraction–relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am J Physiol 276, C395–C403.
Segal S, White TP & Faulkner JA (1986). Architecture, composition, and contractile properties of rat soleus muscle grafts. Am J Physiol 250, C474–C479.[Medline]
Stein
R, Gordon
T
&
Shriver
J (1982). Temperature dependence of mammalian muscle contractions and ATPase activities. Biophys J
40, 97–107.
Talmadge
R, Roy
RR, Caiozzo
VJ
&
Edgerton
VR (2002). Mechanical properties of rat soleus after long-term spinal cord transection. J Appl Physiol
93, 1487–1497.
Tam
S, Archibald
V, Jassar
B, Tyreman
N
&
Gordon
T (2001). Increased neuromuscular activity reduces sprouting in partially denervated muscles. J Neurosci
21, 654–667.
Tötösy de Zepetnek
J, Zung
HV, Erdebil
S
&
Gordon
T (1992). Motor-unit categorization based on contractile and histochemical properties: a glycogen depletion analysis of normal and reinnervated rat tibialis anterior muscle. J Neurophysiol
67, 1404–1415.
Woittiez R, Huijing PA & Rozendal RH (1984). Twitch characteristics in relation to muscle architecture and actual muscle length. Pflugers Arch 401, 374–379.[Medline]
|
Acknowledgements |
|---|
This article has been cited by other articles:
|
|
 |
|
  M. Gallo, I. MacLean, N. Tyreman, K. J. B. Martins, D. Syrotuik, T. Gordon, and C. T. Putman Adaptive responses to creatine loading and exercise in fast-twitch rat skeletal muscle Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2008; 294(4): R1319 - R1328. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
