Voluntary activation of human quadriceps during and after isokinetic exercise.

Voluntary activation of human quadriceps during and after isokinetic exercise D. J. NEWHAM, T. MCCARTHY, AND J. TURNER Physiotherupy Group, Biomedical Sciences Division, King’s CoElegeLondon, London SE5 9RS; and Department of Physiology, University College London, London WCIE 6BT, United Kingdom J. TURNER. Voluntary quadriceps during and after isokinetic exercise. J. Appl. Physiol. 71(6): 2122-2126, 1991.-The extent of NEWHAM,

activation

D. J.,T. M&ARTHY,AND

of human

voluntary activation in fresh and fatigued quadriceps muscles was investigated during isometric and isokinetic voluntary contractions at 20 and 150*/s in 23 normal human subjects. The muscles were fatigued by a total of 4 min of maximal knee extension at an angular velocity of 85*/s. Voluntary activation was determined by the superimposition of tetanic electrical stimulation at 100 Hz for 250 ms, initiated at a constant knee angle. The relationship between voluntary and stimulated force was similar to that found with the established twitch superimposition technique used on isometric contractions. In fresh muscle all the subjects showed full voluntary activation during isometric contractions. Some activation failure was seen in five subjects at 20% [2.0 t 0.9” (SE)] and in two subjects at 150% (0.7 t, 0.5). After fatigue all subjects showed some activation failure at 0 and 20*/s (36.4 -+ 3.1 and 28.8 t 4.1”, respectively), but only two showed any at 15O”/s (1.4 t 5.7). We conclude that brief high-intensity dynamic exercise can cause a considerable failure of voluntary activation. This failure was most marked during isometric and the lower-velocity isokinetic contractions. Thus a failure of voluntary activation may have greater functional significance than previous studies of isometric contractions have indicated. motor unit recruitment;

dynamic exercise; central fatigue

of force fatigue in human skeletal muscles can be divided broadly into those of central and peripheral origin, depending on whether the site is proximal or distal to the neuromuscular junction. A multitude of publications describe the changes that occur during peripheral fatigue - in the propagation of the action potential, excitation-contraction coupling, and biochemistry. Nevertheless, the critical factor/s remains unknown. Central fatigue, a failure of voluntary activation resulting from a decrease in motor unit excitability, recruitment, and/or central drive, has received little attention. In the unfatigued state most individuals are able to activate fully during a brief voluntary isometric contraction (1, 4, 8, 18, 20, 22, 26). During prolonged isometric activity, a continuing ability to activate all motor units fully has been reported by a number of workers (3,4,9, 22, 32). There are reports of activation failure in some individuals during intense exercise lasting more than - 1 min (5,8,11,17), although this can usually be overcome with additional effort. THE MECHANISMS

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The studies cited above have all used isometric contractions to test voluntary activation and, in most cases, to cause fatigue. There is speculation that the sites and mechanisms of force fatigue may be different during dynamic voluntary contractions (10,14,21). The amount of central nervous system activity required for motor control may be less during isometric contractions, which are arguably the simplest motor task performed. The purpose of the present study was to determine whether 1) central mechanisms are a component of voluntary force loss in muscles fatigued by dynamic isokinetic conditions and 2) any differences exist between isometric contractions and those at two additional isokinetic velocities. The measurement of voluntary activation during dynamic contractions required a modification of the established technique, which superimposes twitches on a voluntary contraction (1,3,26). The onset of a short burst of tetanic stimulation was delivered to the muscle at a constant knee angle and, presumably, at a relatively constant point on the length-tension relationship of the muscles studied (quadriceps femoris). The testing of voluntary activation in isometric contractions after fatigue enabled comparison with earlier work on isometric fatigue. METHODS

Subjects. Twenty-three normal healthy subjects (mean age 23.8 yr, range 19-39 yr) were tested. Seven of these subjects were female, and 16 were male. They consented to participate after the nature of the study and the techniques to be used were fully explained. The study had the approval of the local ethical committee. Force recording. Measurements were made from the quadriceps femoris muscle using a Lido dynamometer (Loredan, Davis, CA). The subjects sat in the testing chair and were firmly strapped across the thorax, pelvis, and thigh. The pivot of the lever arm was aligned by eye with the center of rotation of the knee when it was flexed to a right angle. The subjects were positioned so that they were able to see the monitor on which the force records were displayed. A knee angle of 90’ flexion was initially determined with a goniometer and relayed to the dynamometer, which subsequently made automatic calculations of knee angle. A passive movement sequence was used to weigh the limb throughout the defined range, and force measurements were automatically corrected for

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Physiological

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limb weight. Measurements of knee angle and torque were sampled simultaneously at 100 Hz and displayed on the monitor at 50 Hz. Isometric force was measured at intervals throughout a range of O-110* knee flexion. Dynamic studies were carried out over a range of 40-100' knee flexion. Length-tension relationship. It was decided to test for voluntary activation by superimposing electrical stimulation on voluntary contractions at a constant point on the length-tension curve. Any additional force generated by electrical stimulation would be easier to identify if it were on the plateau or descending limb. The length-tension relationship was established on four limbs by testing each 10 times. The subjects performed three maximal isometric voluntary contractions at lo0 increments throughout the joint range tested. Each contraction was held for 1-2 s, with a l-min rest period between successive attempts, and the greatest was taken to be the maximal voluntary contraction (MVC). ElectricaL stimulation. The technique of superimposing single electrical impulses on a voluntary contraction has been shown to be reliable in detecting incomplete activation during isometric contractions, with the use of either motor nerve or percutaneous stimulation (1, 22, 26). However, we found that single twitches were too small and brief to be reliably detected or measured when superimposed on a dynamic contraction because of the shape of the force trace and the lack of a plateau. More force was generated over a longer period of time by a short train of high-frequency stimulation. The relationships between the voluntary force and that generated by the superimposed tetanic stimulation or the stimulation at 1 Hz were compared to evaluate the modification. In all cases the quadriceps muscles were percutaneously stimulated through two 10 X 10 cm dampened electrodes made of aluminum foil wrapped in absorbent paper and bandaged to the anterolateral thigh. Pulses of 50-p duration were used at 300-400 V. During dynamic contractions, a train of stimuli at 100 Hz was delivered for 250 ms. Tetanic stimulation of the resting muscle, held at the test length, generated forces that were 3040% of the isometric MVC at that knee angle. In initial studies, stimulation at both 1 and 100 Hz was used for comparative purposes. Once the technique had been evaluated (see RESULTS), only the stimulation at 100 Hz was used. Superimposed tetunic stimulation. The ability of superimposed tetanic stimulation to detect voluntary activation during voluntary isometric contractions was established initially by repeated studies (n = 10) on four limbs. At a constant knee angle a burst of tetanic stimulation was delivered to the resting muscle. The subjects then performed a series of voluntary isometric contractions varying between 5 and 100% MVC, with target forces presented in random order. Each contraction lasted 2-3 s, and a rest period of 1 min elapsed between contractions. Once a plateau force had been reached, tetanic stimulation was delivered to the muscle while the voluntary contraction was maintained. The amplitude of the force generated by electrical stimulation of the resting muscle was compared with the additional force generated

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by electrical stimulation superimposed on a voluntary contraction. The amount of voluntary activation (VA) was calculated by the formula 1 - (Ps/Pr) (3), where Ps (in mm) is the additional force deflection generated by superimposed electrical stimulation and Pr (in mm) is the force generated by stimulation of the resting muscle at the same joint angle and angular velocity. Activation failure (AF) is given by 1 - VA. Because the measured force of the submaximal voluntary contraction (Pm) and VA are known, the true force of a submaximally contracting muscle can be estimated by PmlAF. VA during dynamic isokinetic contractions. We wished to superimpose electrical stimulation on a voluntary isokinetic contraction at a constant knee angle and, presumably, muscle length that was on the plateau or descending limb of the length-tension curve. To this end, the stimulator was triggered by a micro-switch bolted to the frame of the dynamometer. This was activated mechanically by the passage of the lever arm attached to the lower leg of the subject. The knee angle at which the lever arm would activate the micro-switch was determined manually. A programmed pulse generator (Digitimer) was used to operate a delay, which varied with the isokinetic velocity so that the onset of stimulation occurred at a knee angle of 75' flexion. To determine the force generated by stimulation of the resting muscle, the dynamometer performed passive movements at the selected speeds. Electrical stimulation was initiated at a constant knee angle as described above. VA during isokinetic contractions was tested at 20 and 15O"h angular velocity. The subjects then performed a number of voluntary dynamic contractions at each test velocity. They were asked to generate forces that varied from very weak to maximal, and electrical stimulation was superimposed, the onset occurring at the predetermined joint angle. The additional force generated by electrical stimulation was related to the voluntary force in the same way that single twitches and isometric contractions had been. Fatigue protocol. Before exercise, the extent of VA at ‘W knee flexion was tested during maximal isometric contractions and at the two isokinetic speeds. The muscles were then aggressively fatigued at an intermediate angular velocity of 85*/s. The subjects performed maximal knee extension, followed by passive knee flexion at this velocity for 2 min. This protocol was repeated after a l-min rest period. After the second block of fatiguing exercise, VA was again tested in exactly the same way as before exercise. To minimize the effect of recovery, not more than two of the three possible velocities (0, 20, and 150*/s) were tested on any one occasion. About 1 min elapsed between the end of fatigue and the start of testing. This delay was for technical reasons and also because any mechanical slowing in the fatigued muscles that could have introduced an error into the force measurements would largely have recovered in this time (14). Statistics. The data are presented as means t SE. Significance was determined by the Student’s t test for unpaired data and set at P < 0.05.


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y- 60-c Joint

0

00

20

40 40 60 80 Knee angle [degrees {degrees f lexion)

100

angle\

FIG 3. Superimposition of tetanic electrical stimulation on a submaximal voluntary isokinetic contraction at 2O”/s. Arrow, onset of stimulation. Horizontal line, zero torque.

120

FIG. 1. Length-tension relationship of quadriceps determined during brief isometric contractions. In subsequent studies muscles were electrically stimulated at a knee angle of 75” flexion.

ative ease. As only the onset of any additional force was measured, the differences in the relative duration of stimulation at the two velocities was unimportant. VA before and after fatigue. Before fatigue, none of the RESULTS subjects showed any evidence of AF during isometric conLength- tension relationship. Peak isometric forces tractions. However, during isokinetic contractions at 70-85' flexion (Fig. 1), in 2O"/s, five of them showed some (2.0 t 0.9% for the were generated with the knee at 70-S’ agreement with other published data for these muscles whole group), as did two of the subjects at the higher (12, 13,24,34). We decided to initiate the superimposed velocity (0.7 t 0.5%). electrical stimulation on isokinetic contractions at a After fatigue the situation was very different, and all knee angle of 75’ flexion. the subjects showed some AF during both isometric and Tetunic stimulation superimposed on isometric and iso- the slower isokinetic contractions (36.4 t 3.1 and 28.8 t kinetic contractions. The relationship between the ampli4.l%, respectively). At the higher velocity, only two subtude of the force generated by tetanic electrical stimulajects showed evidence of AF (1.4 t 2.7%). tion and VA during isometric and isokinetic contraction The difference between the measured and estimated is shown in Fig. 2. This relationship was similar in all forces was significant at 0 and 2O"h (P < 0.001) but not three conditions and also similar to that seen when single at the higher velocity (Fig. 4). impulses were used with isometric contractions (26); (26); The fact that there was less inhibition at the higher thus the technique was considered acceptable. velocity had the effect of causing the voluntary force-veThe force generated by tetanic stimulation of the rest- locity values, measured before and after exercise, to coning muscle during isokinetic passive movement at 20 and verge as velocity increased (Fig. 5). 15O”/s (96.5 t 8.4 and 57.4 t 4.5, respectively, of the isometric force at the same knee angle) was in general DISCUSSION agreement with the existing literature on the force-veTo the best of our knowledge, this is the first report of locity relationship of these muscles (19, 24, 30, 33). the ability of healthy normal subjects to activate their A typical record from a submaximal voluntary isokimuscles during and after dynamic isokinetic exercise. In netic contraction is shown in Fig. 3. Because the electrical stimulation during isokinetic movements was not de- fresh muscles the subjects showed full, or virtually full, livered on the ascending limb of the length-tension curve, voluntary activation at the two isokinetic speeds used any additional force was detected and measured with rel- and also, in agreement with earlier studies, during isometric contractions. However, after isokinetic fatigue there

100 80

Meas 00

10

20 20

30 30

40 50 60 70 40 50 60 70 Voluntary Force IX Max)

80 80

90 90

100

FIG. 2. Relationship in fresh muscle (means t SE for 23 subjects) between voluntary and tetanically stimulated force during isometric (solid line) and isokinetic contractions at ZOOIs (dotted line) and 150” /s (dashed line).

Est

Meas

Est

Meas

Est

FIG. 4. Measured (Meas) and estimated (Est) forces of quadriceps (means t SE for 23 subjects) after dynamic fatigue during isometric and isokinetic contractions at 2 velocities. After dynamic fatigue there was a significant difference between measured and estimated forces during isometric contractions and slower isokinetic ones (P < O.OOl), indicating an inability to activate fully.


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230

901“““-

-10 0

r’rL”r”A’r’r~‘r”r””

10 20 30 40 50 60 70 80 90 100 110 120 l-30 140 $50

Angular Velocity (Deg/s) relationship (means rfi SE for 23 subjects) constructed from data acquired before and after dynamic fatigue during maximal voluntary contractions. FIG. 5. Force-velocity

was considerable activation failure in all subjects during both isometric and the slower, but not faster, isokinetic contractions. There has been speculation for some years that the cause of fatigue may be different in isometric and dynamic contractions. A number of workers have raised the possibility that the ability to maintain full activation may be reduced as the complexity and velocity of the task increase (10, 14, 21). Vandervoort et al. (31) reported decreased electromyographic activity in the quadriceps when the number of active muscles and contraction velocity increased. There are few studies that have examined fatigue during dynamic contractions and apparently none that have investigated voluntary activation in these circumstances. In isolated studies, in which a failure of voluntary activation clearly is not possible, there is evidence that isotonic contractions cause greater fatigue than isometric ones (28) and that there is a positively related velocity-dependent effect of fatigue on power output (6,7). Our results show no indication of such an effect, but it must be remembered that both the angular velocities used were relatively low. There are some human studies of fatigue during dynamic exercise, but these have relied solely on measurements of voluntary force so that the contributions of central and peripheral factors could not be examined. Sargeant and Dolan (27) reported that dynamic function, measured on a cycle ergometer, had fully recovered after 2 min of rest after 6 min of exercise at 87% maximal 0, consumption. They measured force production and power output at an isokinetic speed (112 rpm or 67O”/s) that was very much faster than the speeds used in the current studies. In broad agreement with the present studies, Mathiassen (19) reported a greater decline in voluntary force at a low velocity (3O”ls) than at either 120 or 3OO"/s. The fatigue at the two higher velocities was similar. In the present studies we had hoped to investigate voluntary activation during fast dynamic contractions. However, this was not possible, as we were unable to identify with any confidence the stimulated force, as distinct from the voluntary force, at speeds >15O"/s because of the shape of the force record. The finding that activation failure occurred only dur-

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ing isometric contractions and at the lower of the isokinetic velocities is particularly interesting. One might expect more failure at higher velocities, when the time available to reach full activation is reduced. This clearly was not the case, and so we have no evidence of a temporal mechanism. Our results might imply a force-related mechanism, as suggested by other workers (33). If this were the case, the prediction would be either a gradual decrease in the amount of activation failure as velocity increased or, alternatively, a critical force above which none occurred. Our data were acquired at only two velocities, and so we are unable to explore this hypothesis in the current study. Komi and Tesh (16) measured voluntary force changes during dynamic contractions and suggested the possibility of altered recruitment patterns. Grimby et al. (11) reported a temporary inhibition of what were thought to be fast-twitch fibers during maximal isometric activity. In contrast, Minagawa et al. (23) suggested a decreased recruitment of slow-twitch fibers at the highest isometric forces. Nevertheless, the results of the studies cited above indicate that full voluntary activation is usually achieved under isometric conditions. From the current study there is no way of knowing the recruitment patterns, but one would expect the fast-twitch fibers to make a considerable contribution to force generation at higher velocities. The acquisition of these results required the modification of existing techniques, and consideration must be given to the possibility that the results were influenced by technical, rather than physiological, factors. Voluntary activation during isometric contractions can be detected using the superimposition of single twitches, but this was not so during dynamic contractions, even at very slow speeds, because of the shape of the force record. Only when a short burst of tetanic stimulation was applied to the voluntarily contracting muscle could the additional force be detected and measured in a reliable and reproducible manner. It was not possible to make accurate and reproducible measurements at high isokinetic velocities; therefore the highest velocity used ( 150° /s) was restricted by this consideration. Determination of the relationship between the voluntary and the stimulated force by 1) the established and modified technique during isometric contractions and 2) the modified technique during isometric contractions and those at the two velocities selected (Fig. 2) was statistically indistinguishable. Therefore it would appear that the-modification is valid and acceptable for the purposes of this study. The presence of knee joint pathology, even when painfree, can reduce voluntary activation (25, 29), although normal subjects with experimentally induced muscle pain (15) and most patients with myalgia (26) demonstrate full activation. None of our subjects experienced muscle pain during the test contractions or reported any knee joint discomfort, and none were known or suspected of having any joint pathology. The fatigue protocol itself was uncomfortable, but this was of very short duration, and our results in the fresh quadriceps during isometric contractions are entirely in agreement with earlier studies. Another possibility is that the failure to activate fully


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was simply the result of poor motivation, caused perhaps by unfamiliarity with the unpleasant sensations that accompany exhaustive exercise. This seems unlikely, in view of the fact that some subjects were colleagues who were very familiar with the techniques used and had previously shown themselves able to activate fully during and after isometric fatigue protocols. Others were young fit students who regularly participated in such vigorous activities as weight training, distance running, and rowing, in a number of cases at competitive level. In view of the extensive use of dynamic contractions in everyday life, the functional relevance of voluntary activation failure may be greater than predicted by previous studies of isometric contractions. We thank Prof. G. Vrbova (Department of Anatomy, University College London) and M. Bond (Loredan, Davis, CA) for making the Lido dynamometer available for this study. Financial support from The Wellcome Trust is gratefully acknowledged. Address for reprint requests: D. J. Newham, Physiotherapy Group, Biomedical Sciences Div., King’s College London, Denmark Hill Campus, Normanby College, London SE5 9RS, UK. Received 25 September

1990; accepted in final form 10 June 1991.

REFERENCES 1. BELANGER, A. Y., AND A. J. MCCOMAS. Extent of motor unit activation during effort. J. Appl. Physiol. 51: 1131-1135, 1981. 2. BELLEMARE, F., AND N. GARZANITI. Failure of neuromuscular propagation during human maximal voluntary contraction. J. Appl. Physiol. 64: 1084-1093, 1988. 3. BIGLAND-RITCHIE, B., F. FURBUSH, AND J. J. WOODS. Fatigue of intermittent submaximal voluntary contractions: central and peripheral factors. J. Appl. Physiol. 61: 421-429, 1986, B., R. J~HANSSON, 0. C. J. LIPPOLD, AND J. J, 4. BIGLAND-RITCHZE, WOODS. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J. Neurophysiol. 50: 313324,1983.

5. BIGLAND-RITCHIE, B., D. A. JONES, G. P. HOSKING, AND R. H. T. EDWARDS. Central and peripheral fatigue in sustained maximal voluntary contractions of human quadriceps muscles. CLin. Sci. Mol. Med. 54: 609-614, 1978. 6. CROW, M. T., AND M. J. KUSHMERICK.

Correlated reduction of velocity of shortening and the rate of energy utilisation in mouse fast-twitch muscle during a continuous tetanus. J. Gen. Physiol. 82: 703-720,1983.

7. DE HAAN, A., D. A. JONES, AND A. J. SARGEANT. Changes in velocity of shortening, power output and relaxation rate during fatigue of rat medial gastrocnemius muscle, Eur. J. Appl. Physiol. Uccup. Physiol. 413: 422-428,

1989.

8. GANDEVIA, S. C., AND D. K. MCKENZIE. Activation of human diaphragm during static efforts. J. physiol. Lond. 367: 45-56, 1985. 9. GARLAND, S. J., S. H. GARNER, AND A. J. MCCOMAS. Reduced voluntary electromyographic activity after fatiguing stimulation of human muscle. J. Physiol. Land. 401: 547-556, 1988. aspects of fatigue. Can. J. Sport Sci. 10. GREEN, H. J. Neuromuscular Suppl. 12: 7%19S, 1986. 11. GRIMBY, L., J. HANNERZ, AND B. HEDMAN. The fatigue and voluntary discharge properties of single motor units in man. J. Physiol. Lond. 316: 545-554,198l. 12. HERTZOG, W., AND H. E. D. J. TER KEURS. Force-length relation of in vivo human rectus femoris muscle. Pfluegers Arch. 411: 642-647, 1988. 13. Ivy, J. L., R. T. WITHERS, G. BROSE, B. D. MAXWELL, AND D. L.

AND

ISOKINETIC

EXERCISE

contractile properties of the quadriceps with COSTILL. Isokinetic relation to fibre type. Eur. J. Appl. Physiol. Uccup. Physiol. 47: 247255,1981. Electrical and contractile 14. JONES, D. A., AND B. BIGLAND-RITCHIE. changes in muscle fatigue. In: Biochemistry of Exercise. International Series on Sports Science, edited by B. Saltin. Champaign, IL:

Human

Kinetics,

1986, vol. 16, p. 377-392. AND C. TORGAN. Mechanical influences on long lasting human muscle fatigue and delayed onset pain.

15. JONES, D. A., D. J. NEWHAM,

J. Physiol. Lond. 412: 415-427, 1989. 16. KOMI, P. V., AND P. TESCH. EMG frequency

structure and fatigue during dynamic

contractions

spectrum, muscle in man. Eur. J.

Appl. Physiol. &cup. Physiol. 42: 41-50, 1979. 17. KUKULKA, C. G., A. G. RUSSELL, AND M. A. MOORE. Electrical

and mechanical changes in human soleus muscles during sustained maximum isometric contractions. Bruin Res. 326: 47-54, 1986. 18. MARSDEN, C. D., J. C. MEADOWS, AND P. A. MERTON. “Muscular wisdom” that minimises fatigue during prolonged effort in man: peak rates of motoneurone discharge and slowing of discharge during fatigue. In: Motor Control Mechanisms in Health and Disease, edited by J. E. Desmedt. New York: Raven, 1983, p. 169-211. 19. MATHLASSEN, S. E. Influence of angular velocity and movement frequency on development of fatigue in repeated isokinetic knee extensions, Eur. J. Appl. Physiol. &cup. Physiol. 59: 80-88, 1989. 20. MCCOMAS, A. J., S. KERESHI, AND J. QUINLAN. A method for detecting functional weakness. J. Neural, Neurosurg. Psychiatry 46: 280-282,1983. 21. MCLAREN, D. P., H. GIBSON, M. PARRY-BILLINGS, AND R. H. T. EDWARDS. A review of metabolic and physiological factors in fatigue. Exercise Sport Sci. Rev, 17: 29-66, 1989, 22. MERTON, P. A. Voluntary strength and fatigue. J. Physiol. Land. 123:553-564,1954. 23. MINAGAWA, T., H. MATOBA, S. MORITA, Y. KAWAI, AND H. NIU. Physiological properties of motor unit. In: Biomechanics, edited by

E. Asmussen and K. Jorgensen. Baltimore, MD: University Park, 1978, p. 201-206. 24. MOFFROID, M., R. WHIPPLE, J. HOFKOSH, E. LOWMAN, AND H. THISTLE. A study of isokinetic exercise. Phys. Therapy 49: 735747,1969. 25. NEWHAM,

D. J., M. V. HURLEY, AND D. W. JONES. Ligamentous knee injuries and muscle inhibition. J, Orthop. Rheumatol. 2: 163173,1989. 26. RUTHERFORD, 0. M., D. A, JONES, AND D. J. NE~HAM. Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle. J. NeuroZ. Neurosurg. Psychiatry 49: 1288-1291, 1986. 27. SARGEANT, A, J., AND P. DOLAN. Effect of prior exercise on maximal short-term power output in humans. J. Appl. Physiol. 63: 14751480,1987. 28. SEOW, C. Y., AND N. L. STEPHENS. Fatigue in mouse diaphragm muscle in isometric and isotonic contractions, J. Appl. Physiol. 64: 2388-2393,1988. of reflex inhibition 29. STOKES, M., AND A. YOUNG. The contribution to arthrogenous muscle weakness. Clin. Sci. Lund. 64: 7-14,1984. 30. THORSTENSSON, A., G. GRIMBY, AND J. KARLSSON. Force-velocity

relations

and fiber composition

in human knee extensor muscles.

J. Appl. Physiol. 40: 12-16, 1976. 31. VANDERVOORT, A. A., D. G. SALE, AND J. MOROZ. Comparison

motor unit activation

during unilateral

and bilateral

of leg extension.

J. Appl. Physiol. 56: 46-51, 1984. K., 0. M. SEJERSTED, RI BAHR, J.J. WOODS,AND 32. V~LLESTAQN. B. BIGLAND-RITCHIE. Motor drive and metabolic responses during repeated submaximal contractions in humans. J. Appl. Physiol. 64: 1421-1427,1988. 33. WESTING, S. H. Skeletal Muscle Strength in Man with Special Reference to Eccentric Torque- Velocity Characteristics (PhD thesis).

Stockholm,

Sweden: Karolinska Institute, 1990. M., AND L. STUTZMAN. Strength variations through the range of motion. Phys. Therapy Rev. 39: 145-152,1959.

34. WILLIAMS,


Muscle Balance between Hamstrings and Quadriceps during Isokinetic Exercise.

Dynamic joint forces during knee isokinetic exercise.

Isometric and isokinetic measurement of hamstring and quadriceps strength.

Assessment of the quadriceps femoris muscle in women after injury induced by maximal eccentric isokinetic exercise with low angular speed.

Caffeine-induced increase in voluntary activation and strength of the quadriceps muscle during isometric, concentric and eccentric contractions.

Exercise-induced muscle soreness after concentric and eccentric isokinetic contractions.

The effects of rest interval on quadriceps torque during an isokinetic testing protocol in elderly.

Changes in voluntary activation assessed by transcranial magnetic stimulation during prolonged cycling exercise.

Ascertaining maximal voluntary effort production during isokinetic knee strength testing of anterior cruciate ligament-reconstructed patients.

Does pain relate with activation of quadriceps and hamstrings muscles during strengthening exercise in people with knee osteoarthritis?

hamstrings co-activation increases early after total knee arthroplasty.

Does voluntary hypoventilation during exercise impact EMG activity?

quadriceps isokinetic strength ratios and power in tennis, squash and track athletes.

Identification of cardiac repercussions after intense and prolonged concentric isokinetic exercise in young sedentary people.

The Time-Course of Voluntary and Electrically Evoked Muscle Performance During and After Stretch-Shortening Exercise is Different.

Effects of velocity of isokinetic training on strength, power, and quadriceps muscle fibre characteristics.

Phosphagen and lactate contents of m. quadriceps femoris of man after exercise.

Effects of quadriceps strength after static and dynamic whole-body vibration exercise.

Detection of the electromechanical delay and its components during voluntary isometric contraction of the quadriceps femoris muscle.

Significantly worse isokinetic hamstring-quadriceps ratio in patellofemoral compared to condylar defects 4 years after autologous chondrocyte implantation.

Neuromuscular function of the quadriceps muscle during isometric maximal, submaximal and submaximal fatiguing voluntary contractions in knee osteoarthrosis patients.

Angular velocity affects trunk muscle strength and EMG activation during isokinetic axial rotation.

Strength Training to Contraction Failure Increases Voluntary Activation of the Quadriceps Muscle Shortly After Total Knee Arthroplasty: A Cross-sectional Study.

Muscle metabolism during fatiguing isometric quadriceps exercise in adolescents and adults.