Encyclopedia of Sports Medicine and Exercise Physiology.



Encyclopedia of Sports Medicine and Exercise Physiology.

Editor - Thomas D. Fahey

Entry: Endurance training , muscular adaptations

Author: Peter J. Abernethy (PhD)

Address: Department of Human Movement Studies

The University of Queensland

Brisbane, QLD, 4072, Australia

Phone: (07) 3656240

FAX: (07) 3656877

Format: Contractile Character

Spectrum of fibre types

Training and contractile character

Fibre Areas and Ultrastructure

Substrate Utilisation

Endogenous glycogen and its utilisation

Endogenous lipid and its utilisation

Phosphagens and their utilisation

Summary

Enzyme Adaptation

Glycolytic enzymes

Oxidative enzymes

Summary

Conclusion

The ability of man to perform endurance exercise resides in the contractile and metabolic properties of the motor unit and its integration by the nervous system. This entry focuses upon the effects of endurance training on the skeletal muscle fibre. Investigation into skeletal muscle adaptations to chronic exercise was made possible by the development of the muscle biopsy technique.

Contractile Character

Spectrum of fibre types

Skeletal muscle is dynamic tissue, presenting a spectrum of metabolic and contractile properties. This heterogeneity is apparent at the level of most contractile proteins. The contractile protein myosin consists predominantly (85%) of myosin heavy chains (MHCs) and a lesser percentage (15%) of myosin light chains (MLCs). Whilst the total level of myosin does not differ significantly between muscles, there are marked inter-muscle variations in the expression of MHCs and MLCs. The mechanical consequences of this variation appear to be significant as MHCs are a major determinant of skeletal muscle function in the adult tissue (e.g., the speed of cross-bridges linkage and disengagement; twitch characteristics; ATP turnover etc.) (6).

The correlation between the presence of MHCs and myosin ATPase activity is important, as myosin ATPase activity has traditionally been used to histochemically discriminate between fibre types. Many systems for the classification of fibres have been based on myosin ATPase activity, for example: slow twitch oxidative (ST), fast twitch oxidative-glycolytic (FTa), fast twitch glycolytic (FTb) and fast-slow twitch intermediate (FTc). Until recently, histochemical discrimination was thought to accurately reflect MHC structure, as ST, FTa and FTb fibres were thought to consist only of type I, IIa and IIb MHC isoforms respectively. However, histochemical discrimination is limited to the predominant MHC isoform and does not reflect the MHC diversity which has been detected using immunocytochemical and electrophoretic techniques (6). In fact, it is common to see two (I and IIa or IIa and IIb), and on occasion three, MHCs coexist within single fibres (10). This has major ramifications. First, many current nomenclatures for fibre classification do not accurately portray the contractile characteristics of fibres (6). Second, care needs to be exercised when interpreting histochemical data. Third, future investigations of contractile characteristics should measure MHC isoforms and not be based upon myosin ATPase activity. Thus, in this entry the reader is urged to always take into account the limitations associated with histochemical techniques.

Training and contractile character

Endurance athletes tend to present a greater proportion of ST fibres than FT fibres. Traditionally, it has been argued that the predominance of ST fibres was genetically determined. This conclusion was based on information arising from three lines of argument. First, it was argued that data collected in cross-sectional and monozygous twin investigations supported the notion of genetic determination (1). However, in a subsequent study of brothers and monozygous twins, the correlation coefficients between siblings clearly suggested that genotype was not the only factor determining fibre type. Furthermore, post-mortem analysis indicated significant differences in the percentage of FT and ST fibres in the extensor carpi radialis brevis in contralateral limbs. Second, it was reported that the trained and untrained muscles of athletes presented similar proportions of FT and ST fibres. However, these investigations monitored changes in contractile character histochemically, a technique which may not have been sufficiently sensitive to detect changes in MHC character (see preceding section). Third, changes in the proportion of fibre type merely reflect the test-retest error of the skeletal muscle biopsy technique (estimates of this error range from 5-12%). Whilst, this measurement error must always be considered, the identification of multiple MHC isoforms within single fibres tends to reduce the potency of this argument.

There are histochemical, immunocytochemical and electrophoretic data which suggest that chronic endurance activity produces a shift from the type II MHCs toward the type I MHC isoform (1, 2, 10). Eight weeks of endurance training produced an accumulation of slow MLCs (2). Furthermore, Klitgaard et al. (10) reported that chronic endurance activity virtually eliminated all fibres composed solely of MHC type IIb isoform, and increased the proportion of fibres coexpressing MHC I and IIa isoforms. Consistent with this, chronic endurance activity has been shown to increase and decrease the proportion of FTa and FTb fibres respectively (1). Extended training at anaerobic threshold increased the percentage of ST fibres, whilst training approximating VO2 max reduced the percentage of ST fibres and increased the proportion of FTc fibres. These data suggest that the contractile character of skeletal muscle is more responsive to endurance training than once thought. However, the extent to which MHC character can be altered by training is not yet clear. Thus, we cannot state whether the high proportion of ST fibres found within elite distance and marathon runners is a function of genetic selection and/or training.

In summary, the traditional categorical view of skeletal muscle fibres (i.e., ST, FTa, FTb) has been replaced with the notion of fibres presenting a spectrum of contractile characteristics. Furthermore, there is some evidence suggesting that the contractile character of fibres can be altered by endurance training. However, it is not clear if these changes act in isolation or synergistically with the process of natural selection to see elite endurance athletes presenting more ST fibres.

Fibre Areas and Ultrastructure

The spectrum of work rates associated with endurance activity ensures that there is a diversity of motor units recruited during, and a variety of patterns of fibre hypertrophy following endurance activity and training respectively. During submaximal tasks there is preferential recruitment of ST fibres. However, the recruitment of FT fibres increases as endogenous carbohydrate is depleted and/or work rate approaches VO2 max. Thus, not surprisingly, the literature is equivocal as to which, and the sequence in which, fibres are hypertrophied with chronic endurance activity (1). On occasion the cross-sectional area of FT and ST fibres from endurance trained subjects has been found to be greater or lesser than that associated with control subjects. Furthermore, within endurance trained individuals the absolute and relative cross-sectional area of FT fibres have on occasion been greater than ST fibres, and vica versa. This explains Houston’s (9) conclusion that it is difficult to size order fibres in endurance athletes. Factors that may determine whether fibre hypertrophy occurs in response to training include training: intensity, duration and history.

Fifty days of low intensity skiing (_ 30km.day-1) did not produce any fibre hypertrophy. Endurance work lasting between two and five months, and at an intensity of between 75 and 90% VO2 max has been shown to produce selective ST fibre hypertrophy, selective FT fibre hypertrophy, and ST and FT fibre hypertrophy. The differences between these studies is not immediately apparent, but may be related to sampling issues and not just training variables (1). The length of time required to produce ST hypertrophy with endurance training is not clear. Some authors suggest that hypertrophy should be evident following four to five months of training, whilst others believe more time is required (1, 3). Whether endurance training causes FT fibre hypertrophy may be influenced by the training history of the individual involved. The initial eight weeks of endurance training has produced significant FT, but not ST, fibre hypertrophy in novice subjects (3). Interestingly, Bylund et al. (3) reported that for weeks eight to 24 there was selective hypertrophy of ST fibres. Furthermore, relative FT fibre hypertrophy may also occur in well trained individuals.

The level of mitochondrial protein is highly correlated with the time that a submaximal work rate can be sustained (1). Specifically, increasing mitochondrial protein enhances oxidative metabolism. The mitochondria of endurance trained individuals are larger and more numerous than their less active counterparts. Thus, it is not surprising to find that chronic endurance activity increases mitochondrial protein by enhancing the size and/or number of mitochondria (3). Mitochondria have been categorised as either interfibrillar or subsarcolemmal. Interestingly, training produces a greater increase in subsarcolemmal mitochondria than interfibrillar mitochondria (8). It has been suggested that this is due to the proximity of subsarcolemmal mitochondria to plasma lipid (8). Whilst increments in mitochondrial protein may be greater in Fta fibres than ST or FTb fibres following training, the mitochondrial content of ST fibres remains greater than that of FT fibres following 24 weeks of training (1).

In summary, endurance training does not produce a consistent change in the cross-sectional area of fibres. The range of responses appears to be a function of the diversity of work that can be classified as endurance activity. Factors implicated in determining the pattern of fibre hypertrophy include training: intensity, duration and history. However, there appear to be other factors also modulating the fibre hypertrophy response to endurance training. Mitochondrial protein is increased by chronic endurance activity, and these increments are related to improvements in the performance of submaximal exercise.

Substrate Utilisation

Endogenous glycogen and its utilisation

Fatigue resulting from an endurance task is highly correlated with the depletion of intramuscular glycogen. This glycogen utilisation is a direct function of exercise intensity. Endurance training acts in two ways to reduce glycogen depletion for a given submaximal exercise intensity: first, endogenous glycogen stores are increased; and second, glycogen utilisation is reduced for a given sub-maximal task (i.e., there is a glycogen sparing effect).

Endurance training may increase the level of endogenous glycogen. This increase in glycogen appears to be caused by enhanced glycogen synthetase activity. Earlier studies reported similar glycogen concentrations for, and increments in, ST and FT fibres following training. More recent evidence however, suggests that ST fibres have lesser concentrations of glycogen than FT fibres. Though this distinction is not clear cut, and may be due to glycogen depletion arising from every day tasks performed prior to the sampling of tissue (1).

For a given absolute work rate there is an increment in lipid utilisation and a concomitant decrement in glycogen use (i.e., a glycogen sparing effect) following training. This increased lipid metabolism appears to be associated with increased oxidative enzyme activity (see section on

oxidative enzymes below). Though a glycogen sparing effect was recently reported after just 12 days of training, despite an absence of change in oxidative enzyme activity (5).

Endogenous lipid and its utilisation

Endogenous lipid is an important source of substrate during exercise, and it is not uncommon for these reserves to be halved by acute endurance exercise (1). Interestingly, endogenous lipid depletion is greatest after two to three hours of activity (7). Whilst this depletion can be extensive, local lipid does not appear to be exhausted by acute exercise (7). The utilisation of endogenous triglyceride appears to be inextricably linked to the oxidation of plasma free fatty acids (FFAs). When plasma FFA availability was reduced by the administration of nicotinic acid, the resultant deficit was not off-set by an increased oxidation of endogenous lipid. Rather, the lipid deficit arising from the inadequate uptake of plasma FFAs (due to factors like poor diffusion characteristics of FFAs and capillary obstruction) appears to be offset by the oxidation of local lipid.

Endogenous lipid stores are normally less in FT fibres than ST fibres. There is also evidence that training significantly increases local lipid stores (8). Specifically, chronic endurance activity appears to: preferentially increase intramuscular stores of FT fibres; and increase local lipid depots directly adjacent to the mitochondria. Increments in intramuscular triglyceride stores following training appear in part to be the due to greater endothelial lipoprotein lipase activity. Finally, following training, much of the increased lipid oxidised at a given submaximal work rate appears to be drawn from endogenous stores (7).

Phosphagens and their utilisation

Adenosine triphosphate (ATP) and creatine phosphate (CP) levels appear to be greater in FT than ST fibres. Phosphagen depletion increases as the submaximal work rate becomes more intense, with reductions in CP being at all times greater than that for ATP (1). Not surprisingly, phosphagen depletion is greater following interval endurance activity than continuous submaximal exercise. Endurance training increases the level of ATP and CP, and reduces phosphagen depletion for a given absolute submaximal task. Interestingly, the reduction in CP utilisation appears to precede the reduction in ATP utilisation (5). However, phosphagen utilisation for a given relative, submaximal load is similar prior to and following training.

Summary

During endurance activity there is carbohydrate, lipid and phosphagen utilisation. Chronic endurance activity increases lipid oxidation and decreases carbohydrate and phosphagen utilisation for a given submaximal load. Furthermore, training increases the endogenous lipid, carbohydrate and phosphagen pools.

Enzyme Adaptation

Metabolic properties have also been used to differentiate between the ST and FT fibre; with the ST and FT fibre being characterized by a greater oxidative and glycolytic capacities respectively. Furthermore, the FTa fibre has been thought to have a greater oxidative and lower glycolytic potential than the FTb fibre. However, single fibre analysis does not support the FTa and FTb dichotomy, but rather a continuum of metabolic capacities across the FT fibre population (1). Thus, similar to contractile character (see earlier section - Spectrum of fibre types) the metabolic character of skeletal muscle fibres should probably be viewed as a metabolic spectrum rather than distinct metabolic categories. The short half lives of metabolic enzymes ensures that these proteins are sensitive markers as to the effects of training (4). Thus, the potential exists for chronic endurance activity to rapidly alter the metabolic character of muscle.

Glycolytic enzymes

Phosphorylase and phosphofructokinase (PFK) may limit the glycolytic pathway. Some, but not all, endurance training studies have reported increments in PFK activity. Where increments in PFK activity occur there appears to be a complex interaction between training duration (>12wks), intensity and modality. The nature of this interaction has yet to be described (1). In contrast, phosphorylase activity does not appear to be affected by endurance training, with elite endurance athletes and untrained controls presenting similar activity levels. Interestingly, endurance training may produce significant decrements in lactic dehydrogenase activity (4).

Oxidative enzymes

For glycogen sparing to occur following training, more acetyl subunits must be derived from fats than carbohydrate. This is despite the fact that citric acid cycle itself cannot discriminate between acetyl units derived from carbohydrates or lipids. However, preferential lipid utilisation may be effected by mitochondrial and oxidative enzyme adaptations producing a Km for citrate synthase which is more conducive to lipid oxidation (1).

Succinic dehydrogenase (SDH) and maleate dehydrogenase (MDH) are oxidative enzymes located within the mitochondria and cytoplasm respectively. MDH activity increases in response to training, then plateaus. SDH activity is sensitive to: training and detraining; the format of training; and anaerobic threshold. Specifically, SDH activity is greater in highly trained individuals than moderately trained individuals, who in turn have greater levels than the untrained. Continuous and interval training selectively increased SDH activity in ST and FT fibres respectively. Furthermore, SDH activity has been correlated with anaerobic threshold. Finally, increments in SDH activity are highly correlated with the increased time for which a submaximal work rate can be sustained following training (1).

Summary

Endurance training does not enhance phosphorylase activity. Whilst on occasion PFK activity has been increased by training, it is not clear what factor(s) is responsible for this enhanced activity. Clearly, an important metabolic adaptation to endurance training is the glycogen sparing effect. This adaptation appears to be underpinned by mitochondrial and oxidative enzymatic adaptations which maintain the Km for citrate synthase at a level which leads to preferential lipid oxidation. Furthermore, SDH activity is highly correlated with the important markers of endurance performance (i.e., time to fatigue and anaerobic threshold).

Conclusion

Endurance is critical to the performance of many athletic, work and every day tasks. Chronic endurance activity is promoted as being necessary to maximise an individual’s performance in each of these settings. In order to optimise the benefits of chronic endurance activity, those prescribing such activity should be aware of the associated central and peripheral adaptations. The purpose of this entry was to summarise some of the skeletal muscle adaptations to endurance training.

References

1. Abernethy, P.J., Thayer, R. and Taylor, A.W. Acute and chronic responses of skeletal muscle to endurance and sprint exercise: a review. Sports Medicine. 10: 365-389, 1990.

2. Baumann, H., Jaggi, M., Soland, S., Howald, H. and Schaub, M.C. Exercise training induces transitions of myosin isoform sub-units within histochemically typed human muscle fibres. Pflügers Archiv. 409:349-360, 1987.

3. Bylund, A.C., Bjuro, T., Cederblad, G., Holm, J., Lundholm, K., Sjostrom, M., Anquist, K.A. and Schertsten, K.A. Physical training in man. Skeletal muscle metabolism in relation to muscle morphology and running ability. Eur J Appl Physiol. 36:151-169, 1977.

4. Chi, M.-Y., Hintz, C.., Coyle, E.F., Martin III, W.H., Ivy, J.L., Nemeth, P.M., Holloszy, J.O. and Lowry, O.H. Effect of detraining on enzyme of energy metabolism in individual human muscle fibers. Am J. Physiol. 244:C276-C287, 1983.

5. Green, H.J., Jones, S., Ball-Burnett, M.E., Smith, D., Livesay, J. and Farrance, B.W. Early muscular and metabolic adaptation to prolonged exercise training in humans. J. Appl. Physiol. 70: 2032-2038, 1991.

6. Green, H.J. Myofibrillar composition and mechanical function in mammalian skeletal muscle. Sport Sciences Reviews. 1:43-64, 1992.

7. Holloszy, J.O. Utilization of fatty acids during exercise. In Taylor, A.W., Gollnick, P.D., Green, H.J., Ianuzzo, C.D., Noble, E.G., Métivier, G. and Sutton, J.R. Biochemistry of Exercise VII. Human Kinetics: Champaign, Il. 1990, 319-327.

8. Hoppeler, H., Howald, H., Conley, K., Lindstedt, S.L., Classen, H., Vock, P. and Weibel, E.R. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol. 59:2:320-327, 1985.

9. Houston, M.E. The use of histochemistry in muscle adaptation: a critical assessment. Can J Appl Sport Sci. 3:109-119, 1978.

10. Klitgaard, H., Bergman, O., Betto, R., Salviati, G., Schiaffino, S., Clausen, T.

Saltin, B. Co-existence of myosin heavy chain I and IIa isoforms in human skeletal muscle fibres with endurance training. Pflügers Archiv, 416:470-472, 1990.

................
................

In order to avoid copyright disputes, this page is only a partial summary.

Google Online Preview   Download