Ronald L. Terjung, Ph.D.
SPORTS SCIENCE EXCHANGE
MUSCLE ADAPTIONS TO AEROBIC TRAINING
SSE#54-Volume 8 (1995) Number 1
Ronald L. Terjung, Ph.D.
Professor, Department of Physiology
State University of New York Health Science Center Syracuse
Syracuse, New York
Member, GSSI Sports Medicine Review Board
1. Muscle adapts to aerobic exercise training to become a more effective energy provider. An improved capacity for oxygen extraction from the blood supply and an altered cellular control of energy metabolism likely contribute to the improved muscle performance evident with training. Of course, performance is also enhanced by improvements in maximal cardiac output and other adaptations not related to biochemical changes in the muscles.
2. Training adaptations are induced specifically in the muscles actively used in the exercise; these adaptations are sustained by continued activity and lost following inactivity. Both intensity and duration of exercise training sessions are important factors influencing muscle adaptations.
3. Although the development of optimal muscle adaptations is expected to enhance performance in competitive sport, meaningful adaptations developed in non-athletic populations by routine physical activity may also be important in promoting healthier living.
The ability to sustain an exercise task such as running or cycling requires that the energy utilization within the active muscle (i.e., the rate of adenosine triphosphate (ATP) breakdown) is fully matched by energy supply processes (i.e., ATP resynthesis). If the energy demand is not met, muscle fatigue ensues. During any physical activity that can be sustained for longer than a few minutes, this energy provision is supplied primarily by aerobic metabolism, i.e., the consumption of oxygen to drive the oxidation of carbohydrates and fatty acids. The mitochondria within the muscle fibers respond to chemical signals produced during the contractions by using the energy derived through oxygen consumption to resynthesize ATP from adenosinediphosphate (ADP) plus phosphate (the products of ATP breakdown). This process requires a sufficient delivery of oxygen to the active muscle fibers and an adequate fuel supply within the cell to support oxygen consumption. These fuels include carbohydrates (glycogen and glucose) and fatty acids supplied from within the cell or from the circulation. Oxygen must be derived from an adequate blood flow and must diffuse from the red blood cells in the capillaries to the mitochondria in the muscle fibers. Thus, disruption in energy provision could occur if fuel supplies within the muscle fibers are exhausted and/or if the circulation does not provide an adequate supply of fuels or oxygen. Participation in endurance types of exercise training causes muscular adaptations that influence these processes controlling energy provision. Such training adaptations serve to redesign muscle and lead to an improved capacity for oxygen exchange between capillary and tissue and to an improved control of metabolism within the muscle fibers. Both factors provide a better foundation for improved physical performance.
Muscle Fiber Type
Adult human skeletal muscle is comprised of approximately equal proportions of slow-twitch (type I) and fast-twitch (type II) muscle fibers (Saltin & Gollnick, 1983). The slow-twitch fibers exhibit a relatively high blood flow capacity, a high capillary density, and a high mitochondrial content. This fiber type is impressively fatigue resistant, as long as blood flow is sufficient. The fast-twitch fibers can be conveniently divided into two primary subtypes--type IIa, relatively high blood flow capacity, high capillary density, and high mitochondrial content; and type IIb, relatively low blood flow capacity, low capillary density, and low mitochondrial content. The type IIa fibers have a great capacity for oxidative metabolism and are relatively fatigue resistant, whereas the type IIb fibers fatigue rapidly when recruited to contract. The ability to exercise at increasing intensities from mild-to-moderate-to-severe is in large part achieved by the recruitment of more muscle fibers, generally in order from type I, type IIa, and type IIb. Recognizing the differences in fiber type characteristics, it is easy to see why exercise performance can be prolonged at relatively easy submaximal intensities, but relatively short lived at an extremely high intensity. While there are meaningful adaptations in skeletal muscle fibers induced by exercise training, training does not seem to cause marked shifts between slow (type I) and fast (type II) fiber type distributions. Thus, the very high proportion of type I fibers (e.g., 70-90%) observed in the muscles of elite endurance athletes (Fink et al., 1977) is probably a genetic endowment rather than an adaptation to training.
One fundamental biochemical adaptation induced by exercise training is an increase in the mitochondrial content throughout the trained muscle fibers (Holloszy, 1967). This greater mitochondrial content increases the capacity for aerobic energy provision from both fatty acid and carbohydrate oxidation and can be found in both slow-twitch and fast-twitch fibers when they are prompted to adapt by the exercise program. Although it was previously thought that this increased enzymatic capacity was not utilized because the mitochondrial content was considered in excess of maximal needs even in normal untrained muscle (Gollnick & Saltin, 1982), there is now evidence to indicate that an increase in mitochondrial content is necessary to realize the increased potential for aerobic ATP provision induced in muscle by training (Robinson et al., 1994). In addition, it is likely that the increase in mitochondrial content improves the control of energy metabolism, influences the muscle fibers to oxidize more fatty acids and less glycogen, and improves muscle performance (see below).
Exercise training increases the number of capillaries surrounding individual muscle fibers. In effect, when a fiber is recruited it becomes more effectively 'bathed' in the flow of blood delivered to the muscle. Although the increased capillarity is most easily observed in the low-oxidative (type IIb) fiber regions where the capillary density is normally the least, this development of new capillaries can occur in all fiber types (Saltin & Gollnick, 1983; Yang et al., 1994). An increase in the number of capillaries surrounding each fiber should improve the oxygen exchange between capillary and fiber by presenting a greater surface area for the diffusion of oxygen, by shortening the average distance required for oxygen to diffuse into the muscle, and/or by increasing the length of time for diffusion to occur (i.e., the red blood cell spends more time in the capillary). These effects of increased capillarity would contribute to the increased oxygen extraction that occurs in trained muscles of laboratory animals (Bebout et al., 1993; Yang et al., 1994) and human beings (Saltin et al., 1976) and account, in part, for the increase in whole body maximal oxygen consumption that is observed in endurance trained individuals.
Blood Flow Capacity
The blood flow capacity of normal skeletal muscle is exceptionally high; it is so high, in fact, that cardiac output cannot increase sufficiently to perfuse all of the blood vessels in our muscle mass, if they were to maximally dilate. (Anderson & Saltin, 1985). Thus, even during intense exercise requiring maximal oxygen consumption, this limitation of cardiac output means that only a fraction of an individual's entire muscle mass can be active, and then it functions only at a fraction of its blood flow capacity. Nevertheless, there is evidence that the peak flow capacity of muscle is increased by endurance training (Mackie & Terjung, 1983; Sexton & Laughlin, 1994), but the value of this adaptation that further increases the 'unused' flow reserve in muscles is unclear. It is likely that the important features of vascular adaptations to training involve the optimal utilization of the flow delivered to the muscle and the exchange of nutrients between capillaries and fibers. This places importance on the vasomotor control of the arterial supply/resistance vessels (Delp et al., 1993; Segal, 1994) and on diffusion exchange properties of vessels surrounding the
The increase in mitochondrial content of trained muscles should have a number of metabolic effects that serve to improve performance, at least during prolonged exercise. First, the increase in mitochondria should make it possible for a greater rate of fatty acid oxidation after training, even when the circulating fatty acid concentration available to the muscle is not elevated (Mol† et al., 1971). Second, an increase in mitochondrial content of a muscle fiber alters the biochemical signals controlling energy metabolism during submaximal exercise (Dudley et al., 1987). In effect, when compared to the untrained state, the signals within trained muscle fibers that accelerate metabolism during exercise are attenuated, thereby reducing the rate of carbohydrate breakdown and probably contributing to the sparing of muscle glycogen observed in trained subjects (Karlsson et al., 1972). Thus, the biochemical adaptations in muscle help provide the foundation for metabolic changes favorable to endurance performance in trained subjects (Holloszy & Booth, 1976; Holloszy & Coyle, 1984).
Duration and Intensity of Exercise
At present, the underlying mechanisms responsible for inducing the training adaptations in muscle are not known. However, it is clear that the muscles must be recruited during the exercise task in order to adapt to the training program (Holloszy, 1967). Those muscles (or fibers within a muscle) not involved in the exercise task do not adapt. Thus, the critical stimulus for adaptation is something very specific to the active fibers and not likely to be some generalized factor circulating in the blood that influences all muscles. Further, for a given exercise program, training must be performed for a sufficient duration of days or weeks to allow the muscle-specific biochemical adaptations to reach steady-state (Figure 1). For example, muscle mitochondrial content appears to reach a steady-state after approximately 4-5 wk of training (Terjung, 1979).
The magnitude of the training-induced increase in mitochondrial content is also influenced by the duration of the daily exercise bout. As illustrated by the individual lines in Figure 2, longer exercise bouts generally produce greater increases in mitochondrial content. However, the influence of exercise bout duration is not linear (Dudley et al., 1982); as training sessions become increasingly prolonged, the additional training time appears to be relatively less important as a signal inducing an increase in mitochondrial content. Further, exercise intensity interacts with the duration of the exercise bout to make the initial minutes of exercise even more effective in establishing a stimulus for adaptation. Note in Figure 2 that the peak adaptation in mitochondrial content seems to occur with shorter durations of exercise as the intensity of each training bout is increased. The benefit of very prolonged training sessions in enhancing performance may be related to adaptations in cardiovascular function, fluid balance, substrate availability, or other factors not directly related to muscle-specific adaptations.
At least part of the beneficial effect of increasing exercise intensity on training induced adaptations in muscles can be attributed to the effect of intensity on muscle fiber recruitment (Dudley et al., 1982). This is illustrated in Figure 3. Once peak performance (e.g., force development and/or power output) is obtained from an involved set of muscle fibers (illustrated in Figure 3 as the high-oxidative fibers), a greater power output is achieved by recruitment of additional muscle fibers. This is illustrated by the marked adaptation that becomes apparent in the lowoxidative fibers as they are recruited to meet the demands of the more intense exercise task.
Figure 1. Time-course training/detraining adaptations in mitochondrial content of skeletal muscle. Note that about 50% of the increase of mitochondrial content was lost after one unit, i.e., 1 week, of detraining (a) and that all of the adaptation was lost after five units of detraining. Also, it took four units, i.e., 4 weeks, of training (b) to regain the adaptation lost in the first week of detraining. Adapted from booth (1977).
Not all of the improvement in exercise performance that accompanies training can be accounted for by long-term biochemical adaptations. For example, even within days of beginning an exercise program, there is evidence for an improvement in the performance of muscle and in metabolism (Cadefau et al., 1994; Green et al, 1992), perhaps because the brief training causes an initial shift in neuromuscular and/or cardiovascular control that improves muscle fiber utilization, metabolism, and blood flow distribution. This is an example of the complexity of changes and the variety of training durations required to achieve particular adaptations that occur in the transition from a relatively inactive condition to an optimally trained state. All of the improvement in exercise performance after training cannot be attributed solely to the muscle adaptations developed in this summary. Other changes (e.g., neuromuscular, cardiovascular, and endocrine) can be instrumental in contributing to enhanced exercise performance after training for many weeks or months.
Figure 2. Influences of exercise bout duration on muscle adaptation. For a practical perspective, one might assume that training program a was conducted at an intensity of 40% of VO2 max, b at 50% VO2 max, c at 70% VO2 max, d at 85% VO2 max and e at 100% VO2 max. Adapted from Dudley et al., (1982).
Just as meaningful adaptations are induced by physical activity, they are gradually lost in persons who become inactive. The extent and time course of regression are not known for many variables and are likely related to the exact process under consideration. For example, as illustrated in Figure 1, roughly 50% of the increased muscle mitochondrial content induced by training can be lost within 1 wk of detraining (Henriksson & Reitman, 1977; Terjung, 1979). A return to training will recover the muscle adaptations; however, the time required to reestablish the steady-state trained condition can take longer than the detraining interval (Booth, 1977). For example, in Figure 1 compare the relatively long time (identified as b) necessary to recover from the abbreviated time a of detraining that caused the decline in mitochondrial content.
Figure 3. Influence of exercise bout intensity on training-induced adaptations in muscle mitochondrial content. As the training bouts become more intense, more of the low oxidative (type IIb) fibers are recruited and become adapted to the training. Adapted from Dudley et al. (1982).
While the adaptations to an endurance type of training are very complex and multifaceted, changes within the active muscles are probably fundamental to the metabolic and functional alterations that support the enhanced endurance performance observed after training. The adaptations that involve remodeling of the muscle (e.g., enhanced mitochondrial content and increased capillarity) are influenced by the duration and intensity of daily exercise, require an extended training period to achieve a steady-state adaptation, and are lost with inactivity.
Andersen, P., and B. Saltin (1985). Maximal perfusion of skeletal muscle in man. J. Physiol., London 366: 233-249.
Bebout, D.E., M.C. Hogan, S.C. Hempleman, and P.D.Wagner (1993). Effects of training and immobilization on VO2 and DO2 in dog gastrocnemius muscle in situ.
J. Appl. Physiol. 74: 1697-1703.
Booth, F.W. (1977). Effects of endurance exercise on cytochrome c turnover in skeletal muscle. Annals N. Y. Acad. Sci. 301: 431-439.
Cadefau, J., H.J. Green, R. Cusso, M. Ball-Burnett, and G.Jamieson (1994). Coupling of muscle phosphorylation potential to glycolysis during work after shortterm training. J. Appl. Physiol. 76: 2586-2593.
Delp, M.D., R.M. McAllister, and M.H. Laughlin (1993). Exercise training alters endothelium-dependent vasoreactivity of rat abdominal aorta. J. Appl. Physiol. 75: 1354-1363.
Dudley, G.A., W.M. Abraham, and R.L. Terjung (1982). Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle. J. Appl. Physiol. 53: 844-850.
Dudley, G.A., P.C. Tullson, and R.L. Terjung (1987). Influence of mitochondrial content on the sensitivity of respiratory control. J.Biol. Chem. 262: 9109-9114. Fink, W.J., D.L. Costill, and M.L. Pollock (1977). Submaximal and maximal working capacity of elite distance runners. Part II. Muscle fiber composition and enzyme activities. Annals N. Y. Acad. Sci. 301:323-327.
Gollnick, P.D., and B. Saltin (1982). Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin. Physiol. 2: 1-12.
Green, H.J., R. Helyar, M. Ball-Burnett, N. Kowalchuk, S. Symon, and B. Farrance (1992). Metabolic adaptations to training precede changes in muscle mitochondrial capacity. J. Appl. Physiol. 72: 484-491.
Henriksson, J., and J.S. Reitman (1977). Time course of changes in human skeletal muscle succinate dehydrogenase and cytochrome oxidase activities and maximal oxygen uptake with physical activity and inactivity. Acta Physiol. Scand. 99: 91-97.
Holloszy, J.O. (1967). Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242: 2278-2282.
Holloszy, J.O., and F.W. Booth (1976). Biochemical adaptations to endurance exercise in muscle. Ann. Rev. Physiol. 38: 273-291.
Holloszy, J.O., and E.F. Coyle (1984). Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56: 831-838. Karlsson, J., L.O. Nordesjo, L. Jorfeldt, and B. Saltin (1972). Muscle lactate, ATP, and CP levels during exercise after physical training in man. J. Appl. Physiol. 33: 199-203.
Mackie, B.G., and R.L. Terjung (1983). Influence of training on blood flow to different skeletal muscle fiber types. J. Appl. Physiol. 55:1072-1078.
Mol†, P.A., L.B. Oscai, and J.O. Holloszy (1971). Adaptation of muscle to exercise. Increase in levels of palmityl Co-a synthetase, carnitine palmityltransferase, and palmityl Co-a dehydrogenase, and in the capacity to oxidize fatty acids. J. Clin. Invest. 50: 2323-2330.
Robinson, D.M., R.W. Ogilvie, P.C. Tullson, and R.L.Terjung (1994). Increased peak oxygen consumption of trained muscle requires increased electron flux capacity. J. Appl. Physiol. 77: 1941-1952.
Saltin, B., and P.D. Gollnick (1983). Skeletal muscle adaptability: significance for metabolism and performance. In: L.D. Peachey (ed.) Handbook of Physiology, Sec. 10, Skeletal Muscle. Baltimore, MD: Williams and Wilkins, pp. 555-631.
Saltin, B., K. Nazar, D.L. Costill, E. Stein, E. Jansson, B. Essen, and P.D. Gollnick (1976). The nature of the training response: peripheral and central adaptations of one-legged exercise. Acta Physiol. Scand. 96: 289-305.
Segal, S.S. (1994). Cell-to-cell communication coordinates blood flow control. Hypertension 23: 1113-1120.
Sexton, W.L., and M.H. Laughlin (1994 ). Influence of endurance exercise training on distribution of vascular adaptations in rat skeletal muscle. Am. J. Physiol. 266: H483-90.
Terjung, R.L. (1979). The turnover of cytochrome c in different skeletal-muscle fibre types of the rat. Biochem. J. 178: 569-574.
Yang, H.T., R.W. Ogilvie, and R.L. Terjung (1994 ). Peripheral adaptations in trained aged rats with femoral artery stenosis. Circ. Res. 74: 235-243.
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