Stimulation pulse characteristics and electrode configuration determine site of excitation in isolated mammalian skeletal muscle: implications for fatigue

2007 ◽  
Vol 103 (1) ◽  
pp. 359-368 ◽  
Author(s):  
Simeon P. Cairns ◽  
Eva R. Chin ◽  
Jean-Marc Renaud
Keyword(s):  
Skeletal Muscle ◽  
Action Potential ◽  
Soleus Muscle ◽  
Action Potentials ◽  
Surface Membrane ◽  
Electrical Field Stimulation ◽  
Mammalian Skeletal Muscle ◽  
Voltage Dependent ◽  
Flexor Digitorum Brevis ◽  
Edl Muscle

We examined whether electrical field stimulation with varying characteristics could excite isolated mammalian skeletal muscle through different sites. Supramaximal (20-V, 0.1-ms) pulse stimulation with transverse wire or parallel plate electrodes evoked similar forces in nonfatigued slow-twitch soleus and fast-twitch extensor digitorum longus (EDL) muscles from mice. d-tubocurarine shifted the twitch force-stimulation strength relationship toward higher pulse strengths with both electrode configurations in soleus muscle, suggesting that weaker pulses excite muscle via neuromuscular transmission. With wire stimulation, movement of the recording electrode along the muscle caused a delay between the stimulus artifact and the peak of the action potential, consistent with action potential propagation along the sarcolemma. TTX abolished all contractions evoked with 20-V, 0.1-ms pulses, suggesting that excitation occurred via voltage-dependent Na+ channels and, hence, muscle action potentials. TTX did not prevent force development with ≥0.4-ms pulses in soleus or 1-ms pulses in EDL muscle. Furthermore, myoplasmic Ca2+ (i.e., the fura 2 ratio) and sarcomere shortening were greater during tetanic stimulation with 2.0-ms than with 0.5-ms pulses in flexor digitorum brevis fibers from rats. TTX prevented all shortening and Ca2+ release with 0.5-ms, but not 2.0-ms, pulses, indicating that longer pulses can directly trigger Ca2+ release. Hence, proper interpretation of mechanistic studies requires precise understanding of how muscles are excited; otherwise, incorrect conclusions can be made. Using this new understanding, we showed that disrupted propagation of action potentials along the surface membrane is a major cause of fatigue in soleus muscle that is focally and continuously stimulated at 125 Hz.

Changes of action potentials and force at lowered [Na+]o in mouse skeletal muscle: implications for fatigue

2003 ◽  
Vol 285 (5) ◽  
pp. C1131-C1141 ◽  
Author(s):  
Simeon P. Cairns ◽  
Sarah J. Buller ◽  
Denis S. Loiselle ◽  
Jean-Marc Renaud
Keyword(s):  
Skeletal Muscle ◽  
Action Potential ◽  
Soleus Muscle ◽  
Action Potentials ◽  
Extensor Digitorum Longus ◽  
Large Range ◽  
Action Potential Amplitude ◽  
Mouse Skeletal Muscle ◽  
Fatigued Muscle ◽  
Slow Twitch

We examined 1) whether the effects of lowered trans-sarcolemmal Na+ gradient on force differed between nonfatigued fast- and slow-twitch muscles of mice and 2) whether effects on action potentials could explain the decrease of force. The Na+ gradient was reduced by lowering the extracellular [Na+] ([Na+]o). The peak force-[Na+]o relationships for the twitch and tetanus were the same in nonfatigued extensor digitorum longus and soleus muscles: force was maintained over a large range of [Na+]o and then decreased abruptly over a much smaller range. However, fatigue was significantly exacerbated at a lowered [Na+]o that had little effect in nonfatigued soleus muscle. This finding suggests that substantial differences exist in the Na+ effect on force between nonfatigued and fatigued muscle. The reduced contractility in nonfatigued muscles at lowered [Na+]o was largely due to 1) an increased number of inexcitable fibers and threshold for action potentials, 2) a reduction of action potential amplitude, and 3) a reduced capacity to generate action potentials throughout trains.

K+-induced twitch potentiation is not due to longer action potential

2002 ◽  
Vol 283 (1) ◽  
pp. C169-C177 ◽  
Author(s):  
Craig Yensen ◽  
Wadih Matar ◽  
Jean-Marc Renaud
Keyword(s):  
Action Potential ◽  
Soleus Muscle ◽  
Action Potentials ◽  
Muscle Twitch ◽  
Similar Action ◽  
Twitch Force ◽  
Relaxation Phase ◽  
Time To Peak ◽  
Twitch Potentiation ◽  
Edl Muscle

The objective of this study was to determine whether an increased duration of the action potential contributes to the K+-induced twitch potentiation at 37°C. Twitch contractions were elicited by field stimulation, and action potentials were measured with conventional microelectrodes. For mouse extensor digitorum longus (EDL) muscle, twitch force was greater at 7–13 mM K+ than at 4.7 mM (control). For soleus muscle, twitch force potentiation was observed between 7 and 11 mM K+. Time to peak and half-relaxation time were not affected by the increase in extracellular K+ concentration in EDL muscle, whereas both parameters became significantly longer in soleus muscle. Decrease in overshoot and prolongation of the action potential duration observed at 9 and 11 mM K+ were mimicked when muscles were respectively exposed to 25 and 50 nM tetrodotoxin (TTX; used to partially block Na+ channels). Despite similar action potentials, twitch force was not potentiated by TTX. It is therefore suggested that the K+-induced potentiation of the twitch in EDL muscle is not due to a prolongation of the action potential and contraction time, whereas a longer contraction, especially the relaxation phase, may contribute to the potentiation in soleus muscle.

How to sample the entire length of a single muscle fiber quick-frozen after electrical point stimulation for high resolution EM

1992 ◽  
Vol 50 (1) ◽  
pp. 776-777
Author(s):  
Joachim R. Sommer ◽  
Teresa High ◽  
Betty Scherer ◽  
Isaiah Taylor ◽  
Rashid Nassar
Keyword(s):  
Skeletal Muscle ◽  
High Resolution ◽  
Action Potential ◽  
Muscle Fiber ◽  
Freeze Fracture ◽  
Freeze Substitution ◽  
Electrical Field Stimulation ◽  
Skeletal Muscle Fiber ◽  
Freeze Dried ◽  
Quick Freezing

We have developed a model that allows the quick-freezing at known time intervals following electrical field stimulation of a single, intact frog skeletal muscle fiber isolated by sharp dissection. The preparation is used for studying high resolution morphology by freeze-substitution and freeze-fracture and for electron probe x-ray microanlysis of sudden calcium displacement from intracellular stores in freeze-dried cryosections, all in the same fiber. We now show the feasibility and instrumentation of new methodology for stimulating a single, intact skeletal muscle fiber at a point resulting in the propagation of an action potential, followed by quick-freezing with sub-millisecond temporal resolution after electrical stimulation, followed by multiple sampling of the frozen muscle fiber for freeze-substitution, freeze-fracture (not shown) and cryosectionmg. This model, at once serving as its own control and obviating consideration of variances between different fibers, frogs etc., is useful to investigate structural and topochemical alterations occurring in the wake of an action potential.

Skeletal muscle collagen type I and III mRNA, [corrected] prolyl 4-hydroxylase, and collagen in hypobaric trained rats

1996 ◽  
Vol 80 (6) ◽  
pp. 2226-2233 ◽  
Author(s):  
M. Perhonen ◽  
X. Han ◽  
W. Wang ◽  
J. Karpakka ◽  
T. E. Takala
Keyword(s):  
Skeletal Muscle ◽  
Soleus Muscle ◽  
Collagen Type ◽  
Mrna Level ◽  
Collagen Type I ◽  
Synthesis Rate ◽  
Type I ◽  
Mrna Levels ◽  
Edl Muscle ◽  
And Training

Skeletal muscle collagen expression was studied in normobaric sedentary (NS) and training (NT) and hypobaric sedentary (HS) and training (HT) rats after experimental periods of 10, 21, and 56 days. The weights of fast-twitch extensor digitorum longus (EDL) and slow-twitch soleus muscles were increased between the experimental period of 21 and 56 days so that EDL weight was 57 (P < 0.01) and 36% (P < 0.05) higher in 56 days HS (56HS) and 56 days HT (56HT), respectively, than in 56 days NS (56NS). Soleus muscle weight was higher in 56HS (61%; P < 0.01) and in 56HT (27%; P < 0.05) than in 56NT. In EDL muscle, collagen type I mRNA level was lower in 56HT than in 56NS (36%; P < 0.05) and 56NT (44%; P < 0.01). In 56HT, collagen type III mRNA level was 39 (P < 0.01) and 42% (P < 0.05) lower than in 56NS and 56HS, respectively. In soleus muscle, prolyl 4-hydroxylase activity was greater (P < 0.05) in 56NT, 56HS, and 56HT than in 56NS. Total hydroxyproline content in EDL muscle was increased in 56HS and 56HT and in soleus muscle of 56HS. In conclusion, although collagen types I and III mRNA levels in EDL muscle decreased in 56HT, the prolyl 4-hydroxylase data suggest unchanged synthesis of total collagen. Exposure to hypobaric conditions as such, its combination to endurance training, as well as training in normobaric conditions increased prolyl 4-hydroxylation capacity in soleus muscle, which may indicate respective change in collagen synthesis rate.

scholarly journals Radial propagation of muscle action potential along the tubular system examined by potential-sensitive dyes.

1980 ◽  
Vol 76 (6) ◽  
pp. 751-762 ◽  
Author(s):  
S Nakajima ◽  
A Gilai
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Time Course ◽  
Surface Membrane ◽  
Simultaneous Recording ◽  
Conduction Delay ◽  
Muscle Action Potential ◽  
Tubular System ◽  
Intracellular Action ◽  
T System

Isolated single (Xenopus) muscle fibers were stained with a non-permeant potential-probing dye, merocyanine rhodanine (WW375) or merocyanine oxazolone (NK2367). When the fiber was massively stimulated, an absorption change (wave a), which seemed to reflect the action potential, occurred. Simultaneous recording of optical changes and intracellular action potentials revealed that the time-course of wave a was slower than the action potential: the peak of wave a was attained at 1 ms, and the peak of action potential was reached at 0.5 ms after the stimulation. This difference suggests that wave a represents the potential changes of the whole tubular membrane and the surface membrane, whereas the action potential represents a surface potential change. This idea was substantiated by recording absorption signals preferentially from the surface membrane by recording the absorption changes at the edge of the fiber. Wave a obtained by this method was as quick as the intracellular action potential. The value of radial conduction velocity of action potential along the T system, calculated by comparing the action potential with wave a, was 6.4 cm/s at 24.5 degrees C, in fair agreement with González-Serratos (1971. J. Physiol. [Lond.]. 212:777-799). The shape of wave a suggests the existence of an access delay (a conduction delay at the orifice of the T system) of 130 microseconds.

Mechanisms underlying the modulation of arrhythmogenic events by components of ischemia in guinea pig cardiac myocytes

1994 ◽  
Vol 72 (4) ◽  
pp. 382-393 ◽  
Author(s):  
Qi-Ying Liu ◽  
Mario Vassalle
Keyword(s):  
Guinea Pig ◽  
Action Potential ◽  
Voltage Clamp ◽  
Action Potentials ◽  
Ventricular Myocytes ◽  
Resting Potential ◽  
Spontaneous Discharge ◽  
High K ◽  
Voltage Dependent ◽  
Dependent Mechanism

The effects of some components of ischemia on the oscillatory (Vos) and nonoscillatory (Vex) potentials and respective currents (Ios and Iex), as well as their mechanisms, were studied in guinea pig isolated ventricular myocytes by means of a single-microelectrode, discontinuous voltage clamp method. Repetitive activations induced not only Vos and Ios, but also Vex and Iex. A small decrease in resting potential caused an immediate increase in Vos followed by a gradual increase due to the longer action potential. Immediate and gradual increases in Ios also occurred during voltage clamp steps. A small depolarization increased Vos and Vex, and facilitated the induction of spontaneous discharge by fast drive. At Vh where INa is inactivated, depolarizing steps induced larger Ios and Iex, indicating the importance of the Na-independent Ca loading. High [K]odecreased the resting potential, but also Vos, Vex, Ios, Iex, and ICa. In high [K]o, depolarization still increased Vos and Vex. Norepinephrine (NE) enhanced Vos and Vex, and also Ios and Iex, during voltage clamp steps. High [K]o antagonized NE effects, and NE those of high [K]o. In conclusion, on depolarization, Vos and Ios immediately increase through a voltage-dependent mechanism; and then Vos and Ios gradually increase, apparently through an increased Ca load related to the longer action potentials and the Na–Ca exchange. The depolarization induced by Vex may contribute to increase Vos size. Vos and Vex are similarly influenced by different procedures that modify Ca load. The arrhythmogenic events are enhanced by the simultaneous presence of depolarization, faster rate, or NE. Instead, high [K]o decreases Vos and Vex by decreasing ICa and opposes the effects of NE. The voltage clamp results show that potentiation and antagonism between different components of ischemia are due primarily to changes in Ca loading and not to changes in action potential configuration.Key words: ischemia, arrhythmias, oscillatory and nonoscillatory potentials and currents, norepinephrine, potassium.

Regulation of phosphatidylinositol 3-kinase by insulin in rat skeletal muscle

1993 ◽  
Vol 265 (5) ◽  
pp. E736-E742 ◽  
Author(s):  
K. S. Chen ◽  
J. C. Friel ◽  
N. B. Ruderman
Keyword(s):  
Skeletal Muscle ◽  
Soleus Muscle ◽  
Protein Tyrosine Kinase ◽  
Kinase Activity ◽  
Receptor Protein ◽  
Mammalian Skeletal Muscle ◽  
Phosphatidylinositol 3 Kinase ◽  
Phosphatidylinositol 3

The presence of phosphatidylinositol 3-kinase (PI 3-kinase) in mammalian skeletal muscle and its response to insulin stimulation were investigated. PI kinase, immunoprecipitated from rat soleus muscle with antibodies directed toward its 85-kDa subunit phosphorylated PI, phosphatidylinositol 4-phosphate [PI(4)P], and phosphatidylinositol 4,5,-bisphosphate [PI(4,5)P2] to yield phosphatidylinositol 3-phosphate [PI(3)P], phosphatidylinositol 3,4,-bisphosphate, and phosphatidylinositol trisphosphate in vitro. PI 3-kinase activity was also immunoprecipitated with antiphosphotyrosine [alpha-Tyr(P)] antibodies and with antibodies raised against IRS-1, a substrate of the insulin receptor protein tyrosine kinase that associates with and activates PI 3-kinase. Incubation of the soleus with insulin in vitro, or injection of insulin into rats in vivo, produced three- to fivefold increases in alpha-Tyr(P)- and alpha-IRS-1-immunoprecipitable PI 3-kinase activity. In nonstimulated soleus muscle, PI 3-kinase activity immunoprecipitated with alpha-IRS-1 or with alpha-Tyr(P) antibodies was evenly distributed between particulate (200,000-g pellet) and soluble fractions. Insulin treatment increased immunoprecipitable PI 5-kinase activity in both fractions, but the increase in alpha-Tyr-(P)-precipitable activity was greater in the particulate fraction, whereas the increase in alpha-IRS-1-precipitable activity was greater in the soluble fraction. In intact soleus muscles incubated with 32PO4, insulin increased the labeling of PI(3)P but did not affect the labeling of PI(4)P or PI(4,5)P2. Activation of PI 3-kinase by insulin was unaffected by prior denervation of the muscle, a manipulation that has been shown to cause both insulin resistance and hypersensitivity in muscles, depending on the parameter measured.(ABSTRACT TRUNCATED AT 250 WORDS)

scholarly journals Control of action potential duration by calcium ions in cardiac Purkinje fibers.

1976 ◽  
Vol 67 (5) ◽  
pp. 599-617 ◽  
Author(s):  
R S Kass ◽  
R W Tsien
Keyword(s):  
Action Potential ◽  
Calcium Ions ◽  
Action Potentials ◽  
Cardiac Purkinje Fibers ◽  
Voltage Dependent ◽  
Two Factors ◽  
K Current ◽  
Ca Ions ◽  
Current Change ◽  
Plateau Level

It is well known that cardiac action potentials are shortened by increasing the external calcium concentration (Cao). The shortening is puzzling since Ca ions are thought to carry inward current during the plateau. We therefore studied the effects of Cao on action potentials and membrane currents in short Purkinje fiber preparations. Two factors favor the earlier repolarization. First, calcium-rich solutions generally raise the plateau voltage; in turn, the higher plateau level accelerates time- and voltage-dependent current changes which trigger repolarization. Increases in plateau height imposed by depolarizing current consistently produced shortening of the action potential. The second factor in the action of Ca ions involves iK1, the background K current (inward rectifier). Raising Cao enhances iK1 and thus favors faster repolarization. The Ca-sensitive current change was identified as an increase in iK1 by virtue of its dependence on membrane potential and Ko. A possible third factor was considered and ruled out: unlike epinephrine, calcium-rich solutions do not enhance slow outward plateau current, ikappa. These results are surprising in showing that calcium ions and epinephrine act quite differently on repolarizing currents, even though they share similar effects on the height and duration of the action potential.

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