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Cellular Mechanisms of Muscle Fatigue

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Cellular Mechanisms of Muscle Fatigue PHYSIOLOGICAL REVIEWS Vol. ‘74, No. 1, January 1994 Printed in U.S.A. Cellular Mechanisms of Muscle Fatigue R. H. FITTS Department of Biology, Marquette University, Milwaukee, Wisconsin I. Introduction ......................................................................................... 49 A. Definition and current theories of fatigue ....................................................... 49 B. Muscle fiber type composition ................................................................... 50 C. Exercise intensity and environmental conditions ............................................... 51 II. Mechanical Properties ................................................................. .............. 51 A. Isometric contractile properties ................................................................. 52 B. Maximal shortening speed and peak power ..................................................... 55 III. Excitation-Contraction Coupling .................................................................... 55 A. Sarcolemma resting potential ................................................................... 55 B. Sarcolemma action potential .................................................................... 57 C. T tubular system ................................................................................. 58 D. T tubule-sarcoplasmic reticulum junction and calcium release from terminal cisternae ...... 60 IV. Lactic Acid, Intracellular pH, and Fatigue ......................................................... 62 A. Historical perspective ............................................................................ 62 B. Muscle lactate .................................................................................... 63 C. Hydrogen ion and muscle fatigue ............................................................... 65 V. Inorganic Phosphate and Muscle Fatigue ........................................................... 70 A. Inorganic phosphate concentration in skeletal muscle .......................................... 70 B. Inorganic phosphate and muscle fatigue ........................................................ 70 VI. High-Energy Phosphates and Muscle Fatigue ...................................................... 72 A. Cell concentrations ............................................................................... 72 B. Alterations with high-intensity exercise ........................................................ 72 C. Relationship of adenosine 5’-triphosphate and phosphocreatine to muscle fatigue ............ 72 VII. Blood Glucose and Muscle Glycogen ................................................................ 74 A. Historical perspective ............................................................................ 74 B. Muscle glycogen .................................................................................. 75 C. Blood glucose ..................................................................................... 76 D. Mechanisms linking reduced carbohydrate oxidation with fatigue ............................. 77 VIII. Ultrastructural Changes and the Relationship Between Muscle Fatigue and Muscle Injury ...... 78 A. Relationship between muscle injury and muscle fatigue ....................................... 78 B. Mitochondria ..................................................................................... 79 C. Myofibrils .......................................................................... ............. 80 D. T tubules and sarcoplasmic reticulum ............................................. ............. 80 IX. Summary and Conclusions ............................................................ ............. 81 I. INTRODUCTION ity and power achieved wou 1d also be compromised. De- spitel I considerablel 1 1 1 research, 1 the etiologies of muscle fa- tigue have yet to be clearly established. The problem is A. Definition and Current Theories of Fatigue complex, since multiple factors are clearly involved; the relative importance of each is dependent on the fiber Historically, muscle fatigue has been defined as the type composition of the contracting muscle(s), the in- failure to maintain force output, leading to a reduced tensity, type, and duration of the contractile activity, performance (18, 156, 433). More recently, Edwards and the individuals degree of fitness (183). For example, (15’7) defined fatigue as “failure to maintain the re- fatigue experienced in high-intensity short-duration quired or expected power output.” This definition recog- exercise is surely dependent on different factors from nizes that the ability to sustain a given work capacity those precipitating fatigue in endurance activity. Simi- without decrement requires the maintenance of both larly, fatigue during tasks involving heavily loaded con- force and velocity. Furthermore, any factor that re- tractions such as weight lifting will likely differ from duced the rate of force development (dP/dt) would con- that produced during relatively unloaded movement tribute to fatigue by decreasing the percent of peak (running, swimming). force obtained in the initial period (first few millisec- Bigland-Ritchie (47) identified the major potential onds) following muscle activation. As a result, the veloc- sites of fatigue as 1) excitatory input to higher motor 0031-9333/94 $3.00 Copyright 0 1994 the American Physiological Society 49 50 R. H. FITTS Volume 7h centers, R) excitatory drive to lower motor neurons, 3) motor neuron excitability, 4) neuromuscular transmis- sion, 5) sarcolemma excitability, 6) excitation-contrac- tion coupling, 7) contractile mechanism, and 8) meta- NSVERSE bolic energy supply and metabolite accumulation. Con- ULE siderable controversy exists regarding the role of these sites, in particular, the relative importance of central and neuromuscular transmission (sites l-4) versus pe- ripheral (sites 5-8) mechanisms in the etiology of muscle fatigue (46, 47, 53, X6,163,270). This is not a new con- troversy. In the late 18OOs,Lombard (318) observed the work capacity of finger muscles to be maintained in re- sponse to electrical stimulation but to show consider- Ca*+ able fatigue in response to voluntary contractions. He concluded that the results supported a central mecha- nism of muscle fatigue. However, in 1901, Hough (250) PONIN argued that the electrical and volitional contractions did not recruit exactly the same muscle fibers, in part, because electrical stimulation activated only those fibers directly under the surface electrodes. Conse- quently, the volitional contractions produced consider- ably more work, which in turn elicited a higher rate of fatigue. The controversy (central vs. peripheral fatigue) was rekindled in the 1950s when Merton (346) hypothe- sized that fatigue could be explained entirely by alter- MYUSlN ations within the muscle, while Krnjevic and Miledi (295, 296) and later Stephens and Taylor (454) and FIG. I. Diagrammatic representation of major components of a muscle cell involved in excitation-contraction coupling. Numbers indi- others (221,292,367) emphasized the importance of the cate possible sites of muscular fatigue during heavy exercise and in- failure of neuromuscular transmission. Krnjevic and clude the following: 1) surface membrane, 2) T tubular charge move- Miledi (295) suggested that transmission failure could ment, 3) mechanisms coupling T tubular charge movement with sarco- result from inactivation of presynaptic intramuscular plasmic reticulum (SR) Ca2+ release, 4) SR Ca2+ release, 5) SR Ca2+ reuptake, 6) Ca2+ binding to troponin, and 7) myosin binding to actin, nerve endings and/or from an apparent decreased sensi- ATP hydrolysis, and cross-bridge force development and cycle rate. tivity of the postsynaptic membrane to acetylcholine. [From Fitts and Metzger (184), with permission from S. Karger AG, The latter would decrease the amplitude of the end plate Basel.] potential and, coupled with an increased activation threshold, lead to a reduced sarcolemma activation rate (295). However, Brooks and Thies (69) found no evidence 16,80,95,147,191,342). In this paper, I review all puta- for a change in postsynaptic sensitivity to acetylcholine tive fatigue agents, discuss the relative importance of during stimulation at 20 pulses/s and concluded that each, and consider possible interactions that might col- although the end plate potential declined, it was proba- lectively contribute to fatigue. Although numerous bly not a major rate-limiting factor. Although failure in mechanisms have been suggested as causative in muscle neuromuscular transmission has been observed, it is fatigue, most are related to alterations in excitation or generally associated with unphysiologically high stimu- cell metabolism. Figure I presents the cell sites most lation frequencies (196,295,298). Additionally, high-in- frequently linked to the etiology of skeletal muscle fa- tensity exercise is frequently associated with a reduced tigue. Sites I-4 involve disturbances in excitation-con- neural drive and a-motor nerve activation frequency; traction (E-C) coupling and involve changes in the am- however, rather than precipitate fatigue, this change is plitude and conduction of the sarcolemma and T tubular thought to protect against its development (49,54). The action potential (sites 1 and Z) and the T tubular dihy- preponderance of evidence suggests that the primary dropyridine receptor (charge sensor) and the sarcoplas- sites of fatigue lie within the muscle itself (156, mic reticulum
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