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Adaptations of skeletal muscle that favour athletic ability H.M. Gunn H.M.Gunn M.V.B. M.R.C.V.S.
a
a
Department of Veterinary Anatomy , Royal (Dick) School of Veterinary Studies , Edinburgh, EH9, 1QH, Scotland Published online: 23 Feb 2011.
To cite this article: H.M. Gunn H.M.Gunn M.V.B. M.R.C.V.S. (1975) Adaptations of skeletal muscle that favour athletic ability, New Zealand Veterinary Journal, 23:11, 249-254, DOI: 10.1080/00480169.1975.34253 To link to this article: http://dx.doi.org/10.1080/00480169.1975.34253
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
1975
NEW ZEALAND VETERINARY JOURNAL
249
ADAPTATIONS OF SKELETAL MUSCLE THAT FAVOUR ATHLETIC ABILITY H. M.
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INTRODUCTION
The fundamental principles explaining how the athletic performance of some indi viduals regularly excels that of their fellows is of essential interest to the trainer and/or breeder of animal athletes, and to human athletes and their coaches. The identifica tion of factors that favour enhanced athletic ability may permit the evolution of train ing and/or breeding programmes which may aim at mimicking the athletically de sirable properties of superior athletes and be of maximum benefit to the athlete. Numerous factors influence athletic per formance. Many of these can be assess,ed in the living being - such as the effect of exercise on cardiac, respiratory and circu latory function which have been reviewed by Astrand (1956). However, the morpho logical and biochemical properties of an athlete's propulsive machine - his musculo skeletal system - have not been studied extensively in relation to athletic ability. Therefore', skeletal muscle has now been in vestigated! in relation to physical performc ance in two species, strains of which have been selected by man for athletic ability over a long period. This study describes some of the changes that have been pro duced by selection for this trait and, there fore, aims to describe athletic characteris tics, by comparing the skeletal muscle of greyhounds and thoroughbreds with mem bers of their species less specialized for athletic performance. The greyhound dog has been selected :1'01' swiftness for approxi mately 3000 years (Clarke, 1965) and the thoroughbred hOrrse for approximately 300 years (Willett, 1970). Unlike man, who has not been selected for athletic ability, these animals typify extremes of their species and are, therefore, more suitable subjects for an investigation into athletic characteristics. This study of skeletal muscle has cmploy ed gros1sl dissection and histochemical methods. Comparisons based on gross dis section have required the determination of the changes in muscle distribution during growth. Differences in the histochemical properties of muscle fibres of representa ive muscles are investigated in re'lation to the athletic capacity of the breed. *H. M. Gunn, M.V.B., M.R.C.V.S., Department of Veterinary Anatomy, Royal (Dick) School of Veterinary Studies, Edinburgh, EH9, lQH, Scot land.
GUNN*
MATERIALS AND METHODS GROSS DISSECTION
Total body weight was recorded before or as soon as possible after death. The right halves only of the carcasses were dis sected. Muscles were grouped into six func tional units and weighed. The muscle groups considered were the distal fore' limb group, which comprises those muscles, having their origins on the (dlistal end of the humerus and on the bones distal to the humerus; the proximal fore limb group, which con sists of the intrinsic muscles of the fore limb that act over the shoulder and elbow joint; the pectoral girdle group, the muscles attaching the fore limb to the body; the longissimus muscle; those muscles acting over the hip joint, called the femoral muscle group; and the distal hind limb muscle group which is composed of the remainder of the muscles of the hind limb. The num bers of samples from each of the six func tional units are given in Table 1. Allometric growth rat10s were calculateld from the data of muscle groups and rele vant liveweights. Analysis of covariance was also carried out at the 5% level of signifi cance, in addition to the 95% confidence limits of the values of the weight of each functional unit at total body weights of 0.5 kg and 30 kg in dogs, and 3 kg and 500 kg in horses. These calculations were carried out using computer facilHtes and the statis tical methods of Dixon (1971) and Diem and Lentner (1970). Samples for the histochemical study were taken from some of the specimens used for the dissection study. HISTOCHEMICAL PROCEDURES
In 12 greyhounds and 8 other dogs, the complete cross-section of the middle third of the left m. semitendinosus was removed as soon as possible after death. Samples were also taken from the left m. pectoralis transversus at the manubrium sterni in 7 thoroughbreds and 16 other horses. All the animals used were aidults. After rapid freez ing of a block of fresh muscle, about 10 consecutive serial sections 10[.J.m thick were cut transversely to the long axis of the muscle fibres. The methods of Nachlas et al. (1957) to demonstrate succinate dehydro genase activity, Takeuchi and Kuriaki (1955) to demonstrate glycogen phos-
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phorylasE; activity, and Padylcula and Her IJ?an (~955) to demonstrate myosin adeno ~me tnphosphat~se (myosin ATPase) activ Ity, all as modIfied by Davies and Gunn (1972), were used to demonstrate the activ ity of the relevant enzymes. The serial sections from the muscle blocks were then projected on to tracing paper so that individual fibres could be outlined and their metabolic profiles con structed Where there was a continuous spectrum of activity between fibres a simple division into high and low acti~ity was made for each fibre, mlative to the overall level of activity of fibres in each section. The mean transverse sectional area of each fibre type was ldietermined by cut tin~ out and weighing the tracing paper on WhICh the profiles were constructed. The entire transverse sections of m. semiten dinosus of the dog were sampled and the mean proportion of fibre types obtained in this way was taken as representative of the muscle. Similar areas near the super fidal border of the muscle were sampled in m. pectoralis transversus of the horse. RESULTS GROSS DISSECTION
The regression coefficients of the logari th mic equations comparing the growth of the six functiona,l units relative to liveweight are Hsted in Table 1. There is no significant difference between the two types of d'og in: the growth of the six muscle groups rela tive to liveweight. Significant differences occur between them in the adjusted group means of the brachial, pectoral and femoral groups of m. longissimus - those for the greyhounds being greater. Also, when the 95% confidence limits of the estimates of the weight of the six functional units in the two types of dog are made at 0.5 kg and 30 kg liveweight, no overlap of these limits occurs in the values for m. longissimus and the femo,ral muscle groups, corresponding to 30 kg liveweight in the tW(> types of dog - the values being greater for the grey hound. In horses the growth of both the upper and lower hind limb muscle groups rela tive to liveweight is significantly greater (P < 0.05) in the thoroughbred than in other horses. There are no significant differences in the adjusted group means of the six groups of muscles between the two types of horse, nor are there significant differ ences in the weights of the six functional units when calculated to correspond with 3 kg and 500 kg liveweight, as judged by the overlap of the 95% confidence limits.
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TABLE 1: Regression equations comparing the grow,th of six muscle groups relative to liveweight in greyhounds from birth to 37 kg Iiveweight, othel' dogs from birth to 46.5 kg liveweight; thoroughbreds from 0.6 kg to 483.6 kg and other horses from 3 kg to 534.5 kg
Muscle Group and Type of Animal Distal fore limb: Greyhounds .... Other dogs .... Thoroughbreds Other horses Brachial: Greyhounds .... Other dogs Thoroughbreds Other horses Pectoral girdle: Greyhounds .... Other dogs .... Thoroughbreds Other horses Distal hind limb: Greyhounds .... Other dogs Thoroughbreds Other horses Femoral: Greyhounds .... Other dogs Thoroughbreds Other horses Longissimus: Greyhounds .... Other dogs .... Thoroughbreds Other horses
*Regression
No. of Animals
Growth Ratio b*
18 9 7 7
1.103 1.097 1.020 1.041
18 9 7 7
1.203 1.158 1.052 1.014
18 9 6
1.153 1.208 1.042 0.987
19 9 8 10
1.227 1.130 1.l08 0.966
24 21 19 17
1.357 1.315 1.150 1.049
18 9 7 6
1.420 1.255 0.994 0.690
7
coefficient b.
The grading of the muscle groups accord ing to their growth ratios indicates a trend of distoproximal increasing gradients in the limbs of both species, as well as sug ges,ting an increasing gradient of growth, craniocaudally in dogs. HISTOCHEMICAL RESULTS
Two types of fibres were found in the canine m. semite][]dinosus - those having a high activity of myosin ATPase, succinate dehydrogenase and glycogen phosphorylase, and tho'se having a low activity of myosin ATPase, a high activity of succinate de hydrogenase, and a low activity of glyco' gen phospho'rylase. For the purposes of this
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FIG. 1: Fresh frozen transverse sections of m. pectoralis transversus of horses, stained to show the activity of myosin ATPase. Left: Female thoroughbred, live weight 445 kg. Right: Gelding WeJsh Mountain pony, liveweight 178 kg.
study the myosin ATPase reaction ade quately differentiates both types of fibres in adult dogs. The results obtained by assess ing the proportion of the total area of m. semitendinosus occupied by myosin ATPase high-reacting fibres in 12 greyhounds and 8 other dogs are given in Table 2. There are nO significant differences in the proportional area of m. semitendinosus occupied by myosin ATPase high-reacting fibres between male and female greyhounds, or male and female other dogs. The area occupied by myosin ATPase high-reacting fibres in the greyhound is significantly greater than in other dogs (P < 0.01). In horses the myosin ATPase reaction is again used to diffeI1entiate fibre types as only two types of fibres are present in significant proportions in the equine m. pectoralis transverstls: those having a high activity for the myosin ATPase, succinate dehydro. genase and glycogen phosphorylase re actions, and those having a low activity for the myosin ATPase reaction but high activities for both the succinate dehydro genase and glycogen phosphorylase re actions. In samples from similar areas of m. pectoralis transversus of 7 thorough· breds and 16 other horses, the area occu pied by myosin ATPase high-reacting fibres is significantly greater (P < 0.01) in thoroughbreds than in other horses (Table 3). The type of material used is illustrated in Fig. 1. (The dark fibres are high-reacting and the lighter fibres low-reacting.) Two of the thoroughbreds were out of training for over a year, but there is no significant dif ference between them and horses in train ing in the percentage numbers and per centage area of myosin ATPase high-react ing fibres in m. pectoralis transversus. Like c
TABLE 2: QUANTITATIVE HISTOCHEMISTRY OF THE CANINE SEMITENDINOSUS MUSCLE Proportion of the total transverse sectional area occupied by myosin ATPase high-reacting (fasttwitch) fibres
Dog No.
Sex
Body Weight (kg)
F M M M M M M
22 25 26 27 29 30 31
%
GREYHOUNDS:
1 2 3 4 5 6
7 8 9 10 11
M
M F M M
12
31
34 34 34 37 Mean S.D.
91.1 96.7 98.4 96.8 99.2 99.7 94.9 97.2 97.2 98.4 96.7 96.7 96.9 2.2
OTHER BREEDS:
1 2 3 4 5 6 7 8
Terrier X Collie Collie Collie Afghan Afghan Labrador Great Dane
F F M F
F M
F M
10
12 14 22 25 32 33 47 Mean S.D.
85.8 73.4 87.2 89.8 89.0 93.0 85.1 95.6 87.4 6.7
Difference between means is significant at the 0.1 % level. F = Female. M = Male.
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TABLE 3: QUANTITATIVE HISTOCHEMISTRY OF THE EQUINE TRANSVERSE PECTORAL MUSCLE Proportion of the transverse sectional area of samples of m. pectoralis transversus occupied by myosin ATPase high-react,ing (fast-twitch) fibres Sex
Body Weight (kg)
%
THOROUGHBREDS:
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F F F F* M
F
G*
445 458 471 471 484 484 496 Mean S.D.
85 84 90 82 79 79 84.1 4.6
154 178 204 229 280 305 305 318 318 356 356 369 407 420 433 445 Mean S.D.
62 55 68 79 66 72 64 63 65 71 66 68 42 50 79 46 63.5 10.6
~
OTHER HORSES:
Shetland Welsh Mt Shetland Welsh Mt Shetland Pony Arab Connemara X Piebald Tb xt Pony Tb xt Pony Pony Tb xt Connemara
G G G F G
F F F F
F G G
F
F G
F
Diffe'rence between means is significant at the 0.1 % level. *Horses out of training. tThoroughbred crosses. F = Mare. M = Stallion. G = Gelding.
wise, there is no significant difference be tween the females and entire and castrated male horses within each type of horse. DISCUSSION GROSS ATTRIBUTES OF DOG AND HORSE MUSCLE
The weight of a muscI.e provides an esti mate of its potential work capacity. There fore, weight measurements of the gross contractile apparatus of dogs and horses should indicate to what extent the ability to perform propulsive work is different be tween animals selected for athletic ability and other members of their species. This
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study demonstrates that the greyhound and thoroughbred differ from other members of their species by having an enhanced de velopment of the more important propul sive units - those acting on the spinal column and hip of the dog and hind limb of the horse. The difference in growth impe tus of m. longissimus between the dog and horse presumably reflects the greater usage of the spinal column of the dog during run ning. The greater weight of the more im nortant propulsive muscles in the grey hound when related to liveweight and a similar tendency in the thoroughbred is associated with a greater thickness or trans verse sectional area (T.S.A. ) of these muscles in bo,th animals. The T.S.A. of m. semitendiinosus (the development of which presumablv represents the femoral muscle groun of both dogs and horses) is larger relative to liveweight in the greyhound and thoroughbred than in other types of dog and horse (Gunn, unpubl.). Thus, the great er mass of muscle may be considered to indicate a !'!-reater force-nroducing canacitv relative to liveweight in the greyhound and thoroughbred. Variation in the distribution of muscle weight in the carcasses of differen.t breeds of cattle is considered to be generallv of little economic significance (Butterfield, 1974). However. Davies (1974) finds that the sunerior muscularity of the Belgian Pietrain nip: in comparison· with the British Large White nig is due to a greater muscle mass acting along the back and over the hip joint. sugrresting- that in this breed the: normal craniocaudal growth gradients are exagger ated. It issuge'ested bv Davies (1974) that this qrowth nattern - i.e., increasing cranio caudal growth gradients - is an attempt by an animal to maintain a constant propulsive acceleration d1urinl~ growth. The present findings sw!gest that selection for swiftness ;11. cur"orial animals is associated with en hanced growth gradients in the more im portant propulsive units. HISTOCHEMICAL ATTRIBUTES OF DOG AND HORSE MUSCLE
The c'/idence that the succinate dehydro genase and glycogen phosphorylase activity of a fibre indicates its capacity for aerobic and anaerobic metabolism is given by Davies and Gunn (1972). Training regimes may cause an increase in the aerobic and anaerobic capacity of the muscles of labora tory animals and man (Holloszy, 1967; Sal tin and Hermansin, 1967; Faulkner et al., 1971; Staudte et al., 1973; Taylor et aI., 197.4). The end of the myosin molecule formmg a crossbridge from the thick filament (com-
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posed predominantly of nlyosin) to the thin filament (compose:d predominantly of actin) of the myofibril, has the ability to split ATP enzymatically. The work of Guth and Samaha (1969) confirms the view that the histochemical technique of Padykula and Herman (1955) is specific for myosin ATPase. They indicate that the fibres shown to react highly to the myosin ATPase histo chemical reaction are fast-contracting and that the myosin ATPase low-reacting fibres are slow-contracting. This concept is based on Barany'S' (1967) work which shows that the activity of myosin ATPase is' directly proportional to the intrinsic speed of sar comere shortening in normal muscles with widely varying speeds of contraction. Also Burke ct aI. (1973) indicate that motor units in the cat gastrocn~mius with a high activity of myosin ATPase as shown histo chemically are faster contracting than those with a low activity of myosin ATPase. The proportions of myosin ATPase high reacting fibres in whole muscles bears a reciprocal relationship to contraction time (Cardinet et aI., 1972; Peter et aI., 1972). Davies (1972) lists data indicating a rela tionship between the myosin ATPase reac tion and its speed of contraction. Training does not alter the proportions of fibre types as differentiated by the myosin ATPase re action in adult animals (Barnard et al., 1970; Maxwell et al., 1973). In general, therefore, the canine semi tendinorsus has two types of fibres - fast contracting (fast-twitch) fibres with a high capacity for both aerobic and anaerobic metabolism, and slow-contracting (slow twitch) fibres with a high aerobic capacity. In the horse transverse pectoral muscle both the fast-twitch and slow-twitch fibres have a high aerobic and anaerobic capacity. These findings indicate that in these muscles fibres having a high aerobic capace ity (erstwhile called red fibres) need not necessarily be slow-contracting. When compared over a range of body sizes, mammals tend to have a decreasing proportion of fast-twitch fibres in their muscles (Davies andJ Gunn, 1972 ). This feature oorresponds with the lower respira tory rate and lower frequency of limb move ment of larger, compared with smaller mam mals. On a body size basis, therefore, it might be expected that large horses and do'!'s would have a smaller area of their skeletal mUiscle occupied by fast-contract ing fibres than smaller members of their species. However, as greyhounds and thoroughbreds have a smaller proportion of slow-oontracting fibres in their limb muscles than do smaller members of their species, a procedure of selection for rapid movement may have overridden the influence of body
size. Thus, selection for high speed run ning over a large number of generations has produced animals with subtle differ ences in their musculature. These differ ences do not appear to be a result of train ing of the individual adult animal, but rather to be neurogenically determined since the myosin ATPase activity of a fibre is known to be determined by its type of innervation (see Davies, 1972). Therefore. the differences seen in the proportion of different types of fibres in the muscles of these animals may be allied to differences in their nervous system. A resume of the factors that dictate speed of running is given in Fig. 2. The preferen tial development of the more important propulsive (force-producing) units relative to liv·eweight should aid a longer stride length in these animals. Also, since grey hounds and thoroughbreds have a larger proportion of fibres with a higher intrinsic speed of sarcomere contraction, their stride' frequency should be increased. The com bined effect of these quantitative and qualic tative attributes of skeletal muscle favours high speed running in greyhounds and thoroughbreds. The relevanoe of these findings to the quantitative and qualitative aspects of SPEED OF RUNNING
]
CO·ORDINATED GAIT
t
I
I
STRIDE LENGTH X STRIDE FREQUENCY LENGTH OF LIMBS
NATURAL FREQUENCY OF LIMBS
RANGE OF MOVE· MENT OF JOINTS
MECHANICAL ADVANTAGE OF MUSCLES
INTRINSIC SPEED OF ACCELERATION CAPACITY SARCOMERE (Force produced by muscle CONTRACTION relative to body weight) INTERNAL MUSCLE ARCHITECTURE
FIG. 2:
REPETITIVITY OF LIMB MOVEMENT (Anaerobic and aerobic energy supply mechan isms)
Interrelationships of factors dictating the speed of running in animals.
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NEW ZEALAND VETERINARY JOURNAL
meat production as well as the creation of athletically superior beings by selective breeding and/or training policies should be come mo,re apparent in the future.
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SUMMARY
This stUidy compares the skeletal muscles of greyhounds and thoroughbreds with those of other members of their species, using gross dissection and histochemical methods to identify factors that may favour the superior athletic capacity of these breeds. An enhanced growth of the more impor tant propulsive muscle groups relative to liveweight occurs in greyhounds and thoroughbreds when compared with their fellows. This feature: would aid a greater propulsive power in the adlllts of these breeds. A difference between the mode of running of the horse and dog may be re lated! to the differences in the. development of certain of their propulsive units. Greyhounds and thoroughbreds also have a higher proportion of myosin adenosine triphosphatas~ high-reacting (fast-twitch) fibres in their limb muscles than other breeds of dog and horse. These quantitative anidi qualitative attri butes of greyhound and thoroughbred skele tal muscle should permit a longer stride length and a greater stride frequency, so allowing these breeds to have a faster speed of running than their fellows. ACKNOWLEDGEMENT
The author is indebted to the late Profes sor A. R. Muir for providing facilities and -encouragement for this study. REFERENCES Astrand, P. O. (1956): Human physical fitness with special reference to sex and age. Physiol. Rev., 36: 307-35. Barany, M. (1967): ATPase activity of myosin cor related with speed of muscle shortening. f. Gen. Physiol., 50: 197-218. Barnard, R. J.; Edgerton, V. R.; Peter, J. B. (1970): Effe,ct of exercise on skeletal muscle. I. Bio chemical and histochemical properties. f. appl. Physiol., 28: 762-6. Burke, R. E.; Levine, D. N.; Tsairis, P.; Zajac, F. E. (1973): Physiological types and histochemical profiles in motor units of the cat gastrocnemius. f. Physiol. Lond., 234: 723-48. Butterfield, R. M. (1974): Beef carcase composition. Aust. Meat Res. Comm. Rev., June, 1-13. Cardinet, G. H.; Fedde, M. S.; Tunnell, G. (1972): Correlates of histochemical and physiologic pro perties in normal and hypotrophic pectineus muscles of the dog. Lab. Invest., 27: 32-8.
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Clarke, H. E. (1965): The Greyhound. Popular Dogs Publishing Co., London. Davies, A. S. (1972): Postnatal changes in the histo chemical fibre types of porcine skeletal muscle. f. Anal., 113: 213-40. - - - (1974): A comparison of tissue develop ment in Pietrain and Large White pigs from birth to 64 kg liveweight. 2. Growth changes in muscle distribution. Anim. Prod., 19: 377-87. Davies, A. S.; Gunn, H. M. (1972): Histochemical fibre types in the' mammalian diaphragm. f. Anat., 112: 41-60. Diem, K.; Lentner, C. ([970): Documenta Geigy, Scientific Tables. Statistical Methods, pp. 145-98. 7th ed. J. R. Geigy, Basle. Dixon, W. J. (1971): Biomedical Computer Pro grammes. University of California Press. Faulkner, J. A.; Maxwell, L. C.; Brook, D. A.; Lieberman, D. A. (1971): Adaptation of guinea pig plantaris muscle fibers to endurance train ing. Am. ,. Physiol., 221: 291-7. Guth, L.; Samaha, F. J. (1969): Qualitative dif ferences between actomyosin ATPase of slow and fast mammalian muscle. Expl Neurol., 25: 138-52. Holloszy, J. O. (1967)1: Biochemical adaptation in muscle. Effects of exercise on mitochondrial oxy gen uptake and respiratory enzyme activity in skeletal muscle. ,. biol. Chem" 242: 2278-82. Maxwell, L. C.; FaUlkner, J. A.; Lieberman, D. A. (1973): Histochemical manifestation of age and endurance training in skelC'tal muscle fibers. Am. ,. Physiol., 224: 356-61. Nachlas, M. M.; Tsou, K.; de Souza, E.; Cheng, C.; Seligman, A. M. (1957): Cytochemical demon stration of succinic dehydrogenase by the use of new p-nitrophenyl substituted ditetrazole. ,. Histochem. Cytochem., 5: 420-36. Padykula, H. A.; Herman, E. (1955): The specificity of the histochemical method for adenosine tri phosphatase. ,. Histochem. Cytochem., 3: 170-95. Peter, J. B.; Barnard, R. J.; Edgerton, V. R.; Gilles pie, C. A.; Stempel, K. E. (1972): Metabolic profiles of three fibre types of skeletal muscle in guinea pigs and rabbits. Biochemistry, 11: 2627-33. Saltin, B.; Hermansen, L. (1967): Glycogen stores and prolonged severe exercise. Symp. Swedish Nutr. Foundatn, 5: 32-46. Staudte, H. W.; Exner, G. U.; Pette, D. (1973): Effects of short-term, high intensity (sprint) training on some contraotile and metabolic char acteristics of fast and slow muscle of the rat. Pflugers Arch., 344: 159-68. Takem:hi, T.; Kuriaki, H. (1955): Histochemical detection of phosphorylase in animal tissues. ,. H istochem. Cytochem., 3: 153-60. Taylor, A. W.; McNulty, M.; Carey, S.; Garrod, J,; Secord, D. C. (1974): The effects of pair feed ing and exercise upon blood and tissue energy substrates. Rev. Can. Biol., 33 (1): 27-32. Willett, P. (1970): The Thoroughbred. Weidenfeld & Nicholson, London.
New Zealand Veterinary Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnzv20
Adaptations of skeletal muscle that favour athletic ability H.M. Gunn H.M.Gunn M.V.B. M.R.C.V.S.
a
a
Department of Veterinary Anatomy , Royal (Dick) School of Veterinary Studies , Edinburgh, EH9, 1QH, Scotland Published online: 23 Feb 2011.
To cite this article: H.M. Gunn H.M.Gunn M.V.B. M.R.C.V.S. (1975) Adaptations of skeletal muscle that favour athletic ability, New Zealand Veterinary Journal, 23:11, 249-254, DOI: 10.1080/00480169.1975.34253 To link to this article: http://dx.doi.org/10.1080/00480169.1975.34253
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
1975
NEW ZEALAND VETERINARY JOURNAL
249
ADAPTATIONS OF SKELETAL MUSCLE THAT FAVOUR ATHLETIC ABILITY H. M.
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INTRODUCTION
The fundamental principles explaining how the athletic performance of some indi viduals regularly excels that of their fellows is of essential interest to the trainer and/or breeder of animal athletes, and to human athletes and their coaches. The identifica tion of factors that favour enhanced athletic ability may permit the evolution of train ing and/or breeding programmes which may aim at mimicking the athletically de sirable properties of superior athletes and be of maximum benefit to the athlete. Numerous factors influence athletic per formance. Many of these can be assess,ed in the living being - such as the effect of exercise on cardiac, respiratory and circu latory function which have been reviewed by Astrand (1956). However, the morpho logical and biochemical properties of an athlete's propulsive machine - his musculo skeletal system - have not been studied extensively in relation to athletic ability. Therefore', skeletal muscle has now been in vestigated! in relation to physical performc ance in two species, strains of which have been selected by man for athletic ability over a long period. This study describes some of the changes that have been pro duced by selection for this trait and, there fore, aims to describe athletic characteris tics, by comparing the skeletal muscle of greyhounds and thoroughbreds with mem bers of their species less specialized for athletic performance. The greyhound dog has been selected :1'01' swiftness for approxi mately 3000 years (Clarke, 1965) and the thoroughbred hOrrse for approximately 300 years (Willett, 1970). Unlike man, who has not been selected for athletic ability, these animals typify extremes of their species and are, therefore, more suitable subjects for an investigation into athletic characteristics. This study of skeletal muscle has cmploy ed gros1sl dissection and histochemical methods. Comparisons based on gross dis section have required the determination of the changes in muscle distribution during growth. Differences in the histochemical properties of muscle fibres of representa ive muscles are investigated in re'lation to the athletic capacity of the breed. *H. M. Gunn, M.V.B., M.R.C.V.S., Department of Veterinary Anatomy, Royal (Dick) School of Veterinary Studies, Edinburgh, EH9, lQH, Scot land.
GUNN*
MATERIALS AND METHODS GROSS DISSECTION
Total body weight was recorded before or as soon as possible after death. The right halves only of the carcasses were dis sected. Muscles were grouped into six func tional units and weighed. The muscle groups considered were the distal fore' limb group, which comprises those muscles, having their origins on the (dlistal end of the humerus and on the bones distal to the humerus; the proximal fore limb group, which con sists of the intrinsic muscles of the fore limb that act over the shoulder and elbow joint; the pectoral girdle group, the muscles attaching the fore limb to the body; the longissimus muscle; those muscles acting over the hip joint, called the femoral muscle group; and the distal hind limb muscle group which is composed of the remainder of the muscles of the hind limb. The num bers of samples from each of the six func tional units are given in Table 1. Allometric growth rat10s were calculateld from the data of muscle groups and rele vant liveweights. Analysis of covariance was also carried out at the 5% level of signifi cance, in addition to the 95% confidence limits of the values of the weight of each functional unit at total body weights of 0.5 kg and 30 kg in dogs, and 3 kg and 500 kg in horses. These calculations were carried out using computer facilHtes and the statis tical methods of Dixon (1971) and Diem and Lentner (1970). Samples for the histochemical study were taken from some of the specimens used for the dissection study. HISTOCHEMICAL PROCEDURES
In 12 greyhounds and 8 other dogs, the complete cross-section of the middle third of the left m. semitendinosus was removed as soon as possible after death. Samples were also taken from the left m. pectoralis transversus at the manubrium sterni in 7 thoroughbreds and 16 other horses. All the animals used were aidults. After rapid freez ing of a block of fresh muscle, about 10 consecutive serial sections 10[.J.m thick were cut transversely to the long axis of the muscle fibres. The methods of Nachlas et al. (1957) to demonstrate succinate dehydro genase activity, Takeuchi and Kuriaki (1955) to demonstrate glycogen phos-
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phorylasE; activity, and Padylcula and Her IJ?an (~955) to demonstrate myosin adeno ~me tnphosphat~se (myosin ATPase) activ Ity, all as modIfied by Davies and Gunn (1972), were used to demonstrate the activ ity of the relevant enzymes. The serial sections from the muscle blocks were then projected on to tracing paper so that individual fibres could be outlined and their metabolic profiles con structed Where there was a continuous spectrum of activity between fibres a simple division into high and low acti~ity was made for each fibre, mlative to the overall level of activity of fibres in each section. The mean transverse sectional area of each fibre type was ldietermined by cut tin~ out and weighing the tracing paper on WhICh the profiles were constructed. The entire transverse sections of m. semiten dinosus of the dog were sampled and the mean proportion of fibre types obtained in this way was taken as representative of the muscle. Similar areas near the super fidal border of the muscle were sampled in m. pectoralis transversus of the horse. RESULTS GROSS DISSECTION
The regression coefficients of the logari th mic equations comparing the growth of the six functiona,l units relative to liveweight are Hsted in Table 1. There is no significant difference between the two types of d'og in: the growth of the six muscle groups rela tive to liveweight. Significant differences occur between them in the adjusted group means of the brachial, pectoral and femoral groups of m. longissimus - those for the greyhounds being greater. Also, when the 95% confidence limits of the estimates of the weight of the six functional units in the two types of dog are made at 0.5 kg and 30 kg liveweight, no overlap of these limits occurs in the values for m. longissimus and the femo,ral muscle groups, corresponding to 30 kg liveweight in the tW(> types of dog - the values being greater for the grey hound. In horses the growth of both the upper and lower hind limb muscle groups rela tive to liveweight is significantly greater (P < 0.05) in the thoroughbred than in other horses. There are no significant differences in the adjusted group means of the six groups of muscles between the two types of horse, nor are there significant differ ences in the weights of the six functional units when calculated to correspond with 3 kg and 500 kg liveweight, as judged by the overlap of the 95% confidence limits.
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TABLE 1: Regression equations comparing the grow,th of six muscle groups relative to liveweight in greyhounds from birth to 37 kg Iiveweight, othel' dogs from birth to 46.5 kg liveweight; thoroughbreds from 0.6 kg to 483.6 kg and other horses from 3 kg to 534.5 kg
Muscle Group and Type of Animal Distal fore limb: Greyhounds .... Other dogs .... Thoroughbreds Other horses Brachial: Greyhounds .... Other dogs Thoroughbreds Other horses Pectoral girdle: Greyhounds .... Other dogs .... Thoroughbreds Other horses Distal hind limb: Greyhounds .... Other dogs Thoroughbreds Other horses Femoral: Greyhounds .... Other dogs Thoroughbreds Other horses Longissimus: Greyhounds .... Other dogs .... Thoroughbreds Other horses
*Regression
No. of Animals
Growth Ratio b*
18 9 7 7
1.103 1.097 1.020 1.041
18 9 7 7
1.203 1.158 1.052 1.014
18 9 6
1.153 1.208 1.042 0.987
19 9 8 10
1.227 1.130 1.l08 0.966
24 21 19 17
1.357 1.315 1.150 1.049
18 9 7 6
1.420 1.255 0.994 0.690
7
coefficient b.
The grading of the muscle groups accord ing to their growth ratios indicates a trend of distoproximal increasing gradients in the limbs of both species, as well as sug ges,ting an increasing gradient of growth, craniocaudally in dogs. HISTOCHEMICAL RESULTS
Two types of fibres were found in the canine m. semite][]dinosus - those having a high activity of myosin ATPase, succinate dehydrogenase and glycogen phosphorylase, and tho'se having a low activity of myosin ATPase, a high activity of succinate de hydrogenase, and a low activity of glyco' gen phospho'rylase. For the purposes of this
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FIG. 1: Fresh frozen transverse sections of m. pectoralis transversus of horses, stained to show the activity of myosin ATPase. Left: Female thoroughbred, live weight 445 kg. Right: Gelding WeJsh Mountain pony, liveweight 178 kg.
study the myosin ATPase reaction ade quately differentiates both types of fibres in adult dogs. The results obtained by assess ing the proportion of the total area of m. semitendinosus occupied by myosin ATPase high-reacting fibres in 12 greyhounds and 8 other dogs are given in Table 2. There are nO significant differences in the proportional area of m. semitendinosus occupied by myosin ATPase high-reacting fibres between male and female greyhounds, or male and female other dogs. The area occupied by myosin ATPase high-reacting fibres in the greyhound is significantly greater than in other dogs (P < 0.01). In horses the myosin ATPase reaction is again used to diffeI1entiate fibre types as only two types of fibres are present in significant proportions in the equine m. pectoralis transverstls: those having a high activity for the myosin ATPase, succinate dehydro. genase and glycogen phosphorylase re actions, and those having a low activity for the myosin ATPase reaction but high activities for both the succinate dehydro genase and glycogen phosphorylase re actions. In samples from similar areas of m. pectoralis transversus of 7 thorough· breds and 16 other horses, the area occu pied by myosin ATPase high-reacting fibres is significantly greater (P < 0.01) in thoroughbreds than in other horses (Table 3). The type of material used is illustrated in Fig. 1. (The dark fibres are high-reacting and the lighter fibres low-reacting.) Two of the thoroughbreds were out of training for over a year, but there is no significant dif ference between them and horses in train ing in the percentage numbers and per centage area of myosin ATPase high-react ing fibres in m. pectoralis transversus. Like c
TABLE 2: QUANTITATIVE HISTOCHEMISTRY OF THE CANINE SEMITENDINOSUS MUSCLE Proportion of the total transverse sectional area occupied by myosin ATPase high-reacting (fasttwitch) fibres
Dog No.
Sex
Body Weight (kg)
F M M M M M M
22 25 26 27 29 30 31
%
GREYHOUNDS:
1 2 3 4 5 6
7 8 9 10 11
M
M F M M
12
31
34 34 34 37 Mean S.D.
91.1 96.7 98.4 96.8 99.2 99.7 94.9 97.2 97.2 98.4 96.7 96.7 96.9 2.2
OTHER BREEDS:
1 2 3 4 5 6 7 8
Terrier X Collie Collie Collie Afghan Afghan Labrador Great Dane
F F M F
F M
F M
10
12 14 22 25 32 33 47 Mean S.D.
85.8 73.4 87.2 89.8 89.0 93.0 85.1 95.6 87.4 6.7
Difference between means is significant at the 0.1 % level. F = Female. M = Male.
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TABLE 3: QUANTITATIVE HISTOCHEMISTRY OF THE EQUINE TRANSVERSE PECTORAL MUSCLE Proportion of the transverse sectional area of samples of m. pectoralis transversus occupied by myosin ATPase high-react,ing (fast-twitch) fibres Sex
Body Weight (kg)
%
THOROUGHBREDS:
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F F F F* M
F
G*
445 458 471 471 484 484 496 Mean S.D.
85 84 90 82 79 79 84.1 4.6
154 178 204 229 280 305 305 318 318 356 356 369 407 420 433 445 Mean S.D.
62 55 68 79 66 72 64 63 65 71 66 68 42 50 79 46 63.5 10.6
~
OTHER HORSES:
Shetland Welsh Mt Shetland Welsh Mt Shetland Pony Arab Connemara X Piebald Tb xt Pony Tb xt Pony Pony Tb xt Connemara
G G G F G
F F F F
F G G
F
F G
F
Diffe'rence between means is significant at the 0.1 % level. *Horses out of training. tThoroughbred crosses. F = Mare. M = Stallion. G = Gelding.
wise, there is no significant difference be tween the females and entire and castrated male horses within each type of horse. DISCUSSION GROSS ATTRIBUTES OF DOG AND HORSE MUSCLE
The weight of a muscI.e provides an esti mate of its potential work capacity. There fore, weight measurements of the gross contractile apparatus of dogs and horses should indicate to what extent the ability to perform propulsive work is different be tween animals selected for athletic ability and other members of their species. This
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study demonstrates that the greyhound and thoroughbred differ from other members of their species by having an enhanced de velopment of the more important propul sive units - those acting on the spinal column and hip of the dog and hind limb of the horse. The difference in growth impe tus of m. longissimus between the dog and horse presumably reflects the greater usage of the spinal column of the dog during run ning. The greater weight of the more im nortant propulsive muscles in the grey hound when related to liveweight and a similar tendency in the thoroughbred is associated with a greater thickness or trans verse sectional area (T.S.A. ) of these muscles in bo,th animals. The T.S.A. of m. semitendiinosus (the development of which presumablv represents the femoral muscle groun of both dogs and horses) is larger relative to liveweight in the greyhound and thoroughbred than in other types of dog and horse (Gunn, unpubl.). Thus, the great er mass of muscle may be considered to indicate a !'!-reater force-nroducing canacitv relative to liveweight in the greyhound and thoroughbred. Variation in the distribution of muscle weight in the carcasses of differen.t breeds of cattle is considered to be generallv of little economic significance (Butterfield, 1974). However. Davies (1974) finds that the sunerior muscularity of the Belgian Pietrain nip: in comparison· with the British Large White nig is due to a greater muscle mass acting along the back and over the hip joint. sugrresting- that in this breed the: normal craniocaudal growth gradients are exagger ated. It issuge'ested bv Davies (1974) that this qrowth nattern - i.e., increasing cranio caudal growth gradients - is an attempt by an animal to maintain a constant propulsive acceleration d1urinl~ growth. The present findings sw!gest that selection for swiftness ;11. cur"orial animals is associated with en hanced growth gradients in the more im portant propulsive units. HISTOCHEMICAL ATTRIBUTES OF DOG AND HORSE MUSCLE
The c'/idence that the succinate dehydro genase and glycogen phosphorylase activity of a fibre indicates its capacity for aerobic and anaerobic metabolism is given by Davies and Gunn (1972). Training regimes may cause an increase in the aerobic and anaerobic capacity of the muscles of labora tory animals and man (Holloszy, 1967; Sal tin and Hermansin, 1967; Faulkner et al., 1971; Staudte et al., 1973; Taylor et aI., 197.4). The end of the myosin molecule formmg a crossbridge from the thick filament (com-
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posed predominantly of nlyosin) to the thin filament (compose:d predominantly of actin) of the myofibril, has the ability to split ATP enzymatically. The work of Guth and Samaha (1969) confirms the view that the histochemical technique of Padykula and Herman (1955) is specific for myosin ATPase. They indicate that the fibres shown to react highly to the myosin ATPase histo chemical reaction are fast-contracting and that the myosin ATPase low-reacting fibres are slow-contracting. This concept is based on Barany'S' (1967) work which shows that the activity of myosin ATPase is' directly proportional to the intrinsic speed of sar comere shortening in normal muscles with widely varying speeds of contraction. Also Burke ct aI. (1973) indicate that motor units in the cat gastrocn~mius with a high activity of myosin ATPase as shown histo chemically are faster contracting than those with a low activity of myosin ATPase. The proportions of myosin ATPase high reacting fibres in whole muscles bears a reciprocal relationship to contraction time (Cardinet et aI., 1972; Peter et aI., 1972). Davies (1972) lists data indicating a rela tionship between the myosin ATPase reac tion and its speed of contraction. Training does not alter the proportions of fibre types as differentiated by the myosin ATPase re action in adult animals (Barnard et al., 1970; Maxwell et al., 1973). In general, therefore, the canine semi tendinorsus has two types of fibres - fast contracting (fast-twitch) fibres with a high capacity for both aerobic and anaerobic metabolism, and slow-contracting (slow twitch) fibres with a high aerobic capacity. In the horse transverse pectoral muscle both the fast-twitch and slow-twitch fibres have a high aerobic and anaerobic capacity. These findings indicate that in these muscles fibres having a high aerobic capace ity (erstwhile called red fibres) need not necessarily be slow-contracting. When compared over a range of body sizes, mammals tend to have a decreasing proportion of fast-twitch fibres in their muscles (Davies andJ Gunn, 1972 ). This feature oorresponds with the lower respira tory rate and lower frequency of limb move ment of larger, compared with smaller mam mals. On a body size basis, therefore, it might be expected that large horses and do'!'s would have a smaller area of their skeletal mUiscle occupied by fast-contract ing fibres than smaller members of their species. However, as greyhounds and thoroughbreds have a smaller proportion of slow-oontracting fibres in their limb muscles than do smaller members of their species, a procedure of selection for rapid movement may have overridden the influence of body
size. Thus, selection for high speed run ning over a large number of generations has produced animals with subtle differ ences in their musculature. These differ ences do not appear to be a result of train ing of the individual adult animal, but rather to be neurogenically determined since the myosin ATPase activity of a fibre is known to be determined by its type of innervation (see Davies, 1972). Therefore. the differences seen in the proportion of different types of fibres in the muscles of these animals may be allied to differences in their nervous system. A resume of the factors that dictate speed of running is given in Fig. 2. The preferen tial development of the more important propulsive (force-producing) units relative to liv·eweight should aid a longer stride length in these animals. Also, since grey hounds and thoroughbreds have a larger proportion of fibres with a higher intrinsic speed of sarcomere contraction, their stride' frequency should be increased. The com bined effect of these quantitative and qualic tative attributes of skeletal muscle favours high speed running in greyhounds and thoroughbreds. The relevanoe of these findings to the quantitative and qualitative aspects of SPEED OF RUNNING
]
CO·ORDINATED GAIT
t
I
I
STRIDE LENGTH X STRIDE FREQUENCY LENGTH OF LIMBS
NATURAL FREQUENCY OF LIMBS
RANGE OF MOVE· MENT OF JOINTS
MECHANICAL ADVANTAGE OF MUSCLES
INTRINSIC SPEED OF ACCELERATION CAPACITY SARCOMERE (Force produced by muscle CONTRACTION relative to body weight) INTERNAL MUSCLE ARCHITECTURE
FIG. 2:
REPETITIVITY OF LIMB MOVEMENT (Anaerobic and aerobic energy supply mechan isms)
Interrelationships of factors dictating the speed of running in animals.
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meat production as well as the creation of athletically superior beings by selective breeding and/or training policies should be come mo,re apparent in the future.
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SUMMARY
This stUidy compares the skeletal muscles of greyhounds and thoroughbreds with those of other members of their species, using gross dissection and histochemical methods to identify factors that may favour the superior athletic capacity of these breeds. An enhanced growth of the more impor tant propulsive muscle groups relative to liveweight occurs in greyhounds and thoroughbreds when compared with their fellows. This feature: would aid a greater propulsive power in the adlllts of these breeds. A difference between the mode of running of the horse and dog may be re lated! to the differences in the. development of certain of their propulsive units. Greyhounds and thoroughbreds also have a higher proportion of myosin adenosine triphosphatas~ high-reacting (fast-twitch) fibres in their limb muscles than other breeds of dog and horse. These quantitative anidi qualitative attri butes of greyhound and thoroughbred skele tal muscle should permit a longer stride length and a greater stride frequency, so allowing these breeds to have a faster speed of running than their fellows. ACKNOWLEDGEMENT
The author is indebted to the late Profes sor A. R. Muir for providing facilities and -encouragement for this study. REFERENCES Astrand, P. O. (1956): Human physical fitness with special reference to sex and age. Physiol. Rev., 36: 307-35. Barany, M. (1967): ATPase activity of myosin cor related with speed of muscle shortening. f. Gen. Physiol., 50: 197-218. Barnard, R. J.; Edgerton, V. R.; Peter, J. B. (1970): Effe,ct of exercise on skeletal muscle. I. Bio chemical and histochemical properties. f. appl. Physiol., 28: 762-6. Burke, R. E.; Levine, D. N.; Tsairis, P.; Zajac, F. E. (1973): Physiological types and histochemical profiles in motor units of the cat gastrocnemius. f. Physiol. Lond., 234: 723-48. Butterfield, R. M. (1974): Beef carcase composition. Aust. Meat Res. Comm. Rev., June, 1-13. Cardinet, G. H.; Fedde, M. S.; Tunnell, G. (1972): Correlates of histochemical and physiologic pro perties in normal and hypotrophic pectineus muscles of the dog. Lab. Invest., 27: 32-8.
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Clarke, H. E. (1965): The Greyhound. Popular Dogs Publishing Co., London. Davies, A. S. (1972): Postnatal changes in the histo chemical fibre types of porcine skeletal muscle. f. Anal., 113: 213-40. - - - (1974): A comparison of tissue develop ment in Pietrain and Large White pigs from birth to 64 kg liveweight. 2. Growth changes in muscle distribution. Anim. Prod., 19: 377-87. Davies, A. S.; Gunn, H. M. (1972): Histochemical fibre types in the' mammalian diaphragm. f. Anat., 112: 41-60. Diem, K.; Lentner, C. ([970): Documenta Geigy, Scientific Tables. Statistical Methods, pp. 145-98. 7th ed. J. R. Geigy, Basle. Dixon, W. J. (1971): Biomedical Computer Pro grammes. University of California Press. Faulkner, J. A.; Maxwell, L. C.; Brook, D. A.; Lieberman, D. A. (1971): Adaptation of guinea pig plantaris muscle fibers to endurance train ing. Am. ,. Physiol., 221: 291-7. Guth, L.; Samaha, F. J. (1969): Qualitative dif ferences between actomyosin ATPase of slow and fast mammalian muscle. Expl Neurol., 25: 138-52. Holloszy, J. O. (1967)1: Biochemical adaptation in muscle. Effects of exercise on mitochondrial oxy gen uptake and respiratory enzyme activity in skeletal muscle. ,. biol. Chem" 242: 2278-82. Maxwell, L. C.; FaUlkner, J. A.; Lieberman, D. A. (1973): Histochemical manifestation of age and endurance training in skelC'tal muscle fibers. Am. ,. Physiol., 224: 356-61. Nachlas, M. M.; Tsou, K.; de Souza, E.; Cheng, C.; Seligman, A. M. (1957): Cytochemical demon stration of succinic dehydrogenase by the use of new p-nitrophenyl substituted ditetrazole. ,. Histochem. Cytochem., 5: 420-36. Padykula, H. A.; Herman, E. (1955): The specificity of the histochemical method for adenosine tri phosphatase. ,. Histochem. Cytochem., 3: 170-95. Peter, J. B.; Barnard, R. J.; Edgerton, V. R.; Gilles pie, C. A.; Stempel, K. E. (1972): Metabolic profiles of three fibre types of skeletal muscle in guinea pigs and rabbits. Biochemistry, 11: 2627-33. Saltin, B.; Hermansen, L. (1967): Glycogen stores and prolonged severe exercise. Symp. Swedish Nutr. Foundatn, 5: 32-46. Staudte, H. W.; Exner, G. U.; Pette, D. (1973): Effects of short-term, high intensity (sprint) training on some contraotile and metabolic char acteristics of fast and slow muscle of the rat. Pflugers Arch., 344: 159-68. Takem:hi, T.; Kuriaki, H. (1955): Histochemical detection of phosphorylase in animal tissues. ,. H istochem. Cytochem., 3: 153-60. Taylor, A. W.; McNulty, M.; Carey, S.; Garrod, J,; Secord, D. C. (1974): The effects of pair feed ing and exercise upon blood and tissue energy substrates. Rev. Can. Biol., 33 (1): 27-32. Willett, P. (1970): The Thoroughbred. Weidenfeld & Nicholson, London.
