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Effect of cooling on force oscillations during maximal voluntary eccentric exercise
EXPERIMENTAL
NEUROLOGY
(1985)
%,73-80
Effect of Cooling on Force Oscillations during Maximal Voluntary Eccentric Exercise DENNIS L. HART, Applied Kinesiology Laboratory, and Neurology, West Virginia Received
LISA C. MILLER, Division University
December
AND WILLIAM
T. STAUBER’
of PhysicaI Therapy, and Departments OfPhysiology Medical Center, Morgantown, West Virginia 26506
14, 1984;
revision
received
May
22, 1985
The effect of superficial cooling on force oscillations during maximal eccentric exercises of the quadriceps femoris was studied in 10 adults. Maximal (i) shortening (concentric) and (ii) lengthening (eccentric) exercises were performed at a velocity of 12O”/s through 60” of knee flexion while linear envelope EMG signals were recorded from the surface of the vastus medialis muscle. Force oscillations (12.4 f 2.8 Hz) were present in all subjects in the first series of eccentric exercises. After 30 min of cooling, the oscillations were eliminated in two subjects and were reduced in number in two others of the five subjects in the experimental group. In contrast, all subjects in the control group still had oscillations when retested after a 30-min rest period. During the eccentric exercises, a synchronous silent period in the EMG tracings was evident just before a decrease in force. Subsequently, the EMG activity resumed and the force increased (force oscillation). Because the force oscillations were of large amplitude and occurred only during eccentric exercise, we conclude that the force oscillations were similar to physiological action tremor. Because the force oscillations and EMG patterns were altered by cooling, the mechanisms that initiate such oscillations during maximal eccentric exercise are suspected to include a neural component. 0 1985 Academic Press. Inc.
INTRODUCTION Oscillations in the force output of voluntary isometric contractions (8 to 12 Hz) were recorded as early as 1886 (2 1) and were classified as physiological tremor (PT) (2, 3, 7, 11, 16, 17, 19). To differentiate these tremors from those occurring during dynamic activities, the term physiological action tremor (PAT) (1, 8, 14, 18) was used. Although the mechanisms of either Abbreviations: PAT-physiological action tremor, PT-physiological tremor. ‘The authors thank Dr. Sandy Burkart for his continued financial support and Dr. Paul Brown for critically reading the manuscript. 13
0014-4886/85 $3.00 Copyright 0 1985 by Academic Press. Inc. All rights of reproduction m any form rcscrved.
74
HART,
MILLER,
AND
STAUBER
type of tremor remain unclear, PT and PAT appear to have definite neural (2, 3, 13, 16, 18, 22) and mechanical (6, 19, 22, 26) components. Recently we observed that large-amplitude force oscillations occur during maximal eccentric exercise. As they were not present during concentric exercise of similar magnitude (Hart and Stauber, unpublished observations), muscle stretch was considered the probable stimulus for oscillations in force. It is known that a reduction in either skin (9, 10, 20, 22, 24, 25) or intramuscular (4, 10, 12, 15) temperature will influence the responsiveness of the stretch reflex. If neural factors contribute to the eccentric PAT, then cooling should alter both force oscillations and muscular activity. Therefore we recorded the effects of cooling on the force oscillations and the surface electromyogram during maximal voluntary eccentric exercise. METHODS The subjects were positioned supine with the pelvis strapped to the table of a computer-controlled dynamometer (KIN/COM). The exercise set consisted of one series of four consecutive maxima1 concentric and eccentric knee extension exercises resisted by the KIN/COM with no pause between the concentric and eccentric phases. The dynamometer measured position (in degrees) and force (in Newtons). The computer sampled the angle and force data at 100 samples per second and computed torque (force X radius), velocity (O/s), and instantaneous power (force X velocity). The computer adjusted the velocity with a 2-ms latency to maintain the preset velocity. The operating limit for the strain gauges was 1112 N, and the maximum velocity of movement of the dynamometer was 21O”/s. Therefore, all data collected were within the limits of the equipment. A velocity of 12O”/s was used for both the concentric and eccentric exercise. The range of knee motion was 60” (75 to 15” of knee flexion, with 0 defined as full extension). The full 60” of movement had to be completed before the dynamometer allowed a change in direction of movement. However, the exercise unit would not allow any movement until a 50-N threshold force was applied to the dynamometer at the point of lower leg contact, thus insuring that the muscles were producing tension prior to movement. If the threshold force value was not maintained throughout the range of movement, the machine stopped. Therefore, impulse loading was prevented, and the subjects were protected during eccentric exercise, because the machine would stop if the force was removed (i.e., the leg taken away). Independent studies have confirmed the reliability of the dynamometer in measuring the angle, velocity, and force within an error of 3% (5).
EFFECT OF COOLING
ON FORCE OSCILLATIONS
75
Several submaximal exercises were performed to familiarize each subject with the testing routine. When the subjects were comfortable with the routine, one set of maximal effort, knee extension exercises was performed. Five of the subjects were randomly assigned to the treatment group and ice packs were applied to the medial, anterior, and lateral aspect of the thighs from the hip to the knee. Care was taken to keep the EMG electrodes dry. After performing their initial series of exercises, the control group waited in the same position as the cooling group with the thigh exposed to ambient temperature (25°C) for 30 min. Then each subject performed a second series of identical exercises. Two independent recording devices were used: (i) the KIN/COM and (ii) a Grass model 7 polygraph. The digital values of angular position (degrees) and torque (Newton * meters) were retrieved from the KIN/COM. The polygraph recorded analog signals of force (directly from the force transducer of the KIN/COM), angular displacement (by means of a potentiometer connected to the dynamometer arm), and the EMG signals (pen response = 50 Hz). Electromyographic signals were recorded with bipolar silver/silver-chloride surface electrodes (2-mm diameter, 1S-cm interelectrode distance) placed over the left vastus medialis muscle. A silver/silver-chloride ground electrode was placed over the lateral femoral condyle. Skin preparation with shaving, alcohol, and abrasion reduced skin resistance to less than 5 kQ for each electrode. The EMG was amplified (300X) at the source with a Motion Control EMG preamplifier (CMRR = 100 dB, 10.5 to 27 kHz bandwidth, DC input impedance 10’ a). The signal was voltage divided before further amplification by a Grass 7P3 amplifier which recorded either the raw EMG or its envelope (fullwave rectification, 50-ms time constant, ~-HZ to lo-kHz bandpass). Linear envelope signals were recorded from all subjects and occasional raw signals were recorded for comparison. For a force fluctuation (from the Grass strip chart) to be considered a valid indicator of physiologic action tremor, it had to be: (i) independent of machine function and (ii) of sufficient amplitude (greater than 5 N-m). Machine-introduced oscillations occur only if the applied force is close to the preset threshold force (Hart, unpublished data). The force oscillations that occurred in this study of normal adult subjects were well above 50 N (i.e., free from machine interference). The moments recorded during the eccentric exercises were consistently greater than 200 N . m. For analysis, the force fluctuations were identified on the Grass strip chart and the corresponding data for that time period were retrieved from the KIN/COM. The fluctuations were characterized according to the mean fundamental frequency of oscillation, the angle of their initiation, and the
76
HART,
MILLER,
AND STAUBER
EMG patterns. One cycle of a force oscillation was defined as the signal between two consecutive peaks on the force tracing. The EMG signals were reduced to a percentage of a maximum isometric contraction at 45” of knee flexion. RESULTS Ten subjects participated in the project. Each subject performed one series of exercises before and one series after the cooling or after a comparable waiting period. Therefore, a total of 80 concentric and 80 eccentric exercise repetitions were evaluated. During the first series of exercises the concentric force curves were devoid of large-amplitude (greater than 5 N. m) oscillations, and the linear envelope EMG tracings indicated high muscle activity throughout the range of motion (Fig. 1). The eccentric forces were typically of higher magnitude than the concentric forces and each eccentric exercise had at least one oscillation (Figs. l-3) (Table 1). When the raw EMG signals were recorded, these signals had distinct silent periods associated with a sharp decrease in the linear envelope signals that immediately preceded the eccentric force decrement. Of the five subjects in the experimental group, the force oscillations were eliminated in two of them (Table 1, Fig. 4). Of the three subjects who received cooling but did not have their oscillations eliminated, two of these ECCENTRIC 100
ANGLE
OF FLEXION
FIG. 1. One concentric and one eccentric contraction of a control subject prior to the control wait period. The force and EMG signals were reduced to a percentage of maximum at 45” knee flexion during isometric contraction. The tracings began at 75” of knee flexion, continued to 15” of knee flexion, and returned to 75” of knee flexion (0” is defined as a full extension).
EFFECT OF COOLING
ON FORCE OSCILLATIONS
CONCENTRIC
77
ECCENTRIC
100
50
0 150
0 i5
IO0
50
, 35 ANGLE
55
75
OF FLEXION
FIG. 2. The same subject as in Fig. 1 after the 30-min wait period.
had the number of oscillations reduced from seven to one and from seven to four, but the frequency was unchanged. The fifth subject was unaffected by the cooling. In contrast, the force oscillations were unaltered in the second series of exercises for the control group. The angle of occurrence of the initial oscillation during the first series of eccentric exercises averaged 38.4 ? 12.7” of knee flexion. This value was unaltered after cooling. The within-subject variability of the angle of knee
ECCENTRIC 100 E ;
50
0 75
55
35 ANGLE
15 35 OF FLEXION
55
75
FIG. 3. One concentric and one eccentric contraction from an experimental subject before application of ice. (Similar data reduction as in previous figures.)
78
HART,
MILLER,
AND STAUBER
TABLE 1 Frequency of Force Oscillations during Eccentric Contraction” Ice Subject 1 2 7 8 9
PRE 13.9 f 12.1 + 9.7 k 10.5 f 17.6 +
1.6 1.6 0.7 1.4 0.9
Control POST
Subject
15.8 + 1.0 14.3 * 1.5 12.5 + 0 -
3 4 5 6 10
PRE 11.7 14.3 10.3 11.8 13.9
+ f k h +
POST 0.6 0 4.0 0.6 3.3
10.9 f 11.6 f 13.8 f 10.8 k 12.5 +
1.0 0.9 0.5 5.6 0
Note. Forty-one of sixty (68.3%) contractions had oscillations during the first series of exercises (both groups) and the second series of exercises (control group); 8 of 20 (40%) postcooling contractions had oscillations (treatment group). ’ Frequencies in Hz: X + SD; range: 6.3 to 18.8 Hz.
flexion was small for four of the five subjects in the control group. However, in contrast, the variability in the angle of knee flexion where force oscillation occurred for the three subjects in the treatment group who did not have their oscillations eliminated was larger and not consistent in direction. DISCUSSION During maximal voluntary effort of the knee extensors to resist a forced lengthening (eccentric exercise), oscillations in force output were observed. CONCENTRIC
ECCENTRIC
100 Y 5
50
0 150
0 75
q
55
35 ANGLE
15
35
Dweclion Chonpe
55
75
OF FLEXION
FIG. 4. One concentric and one eccentric contraction of the same subject as in Fig. 3 after a 30-min application of ice. (Similar data reduction as in previous figures.)
EFFECT OF COOLING
ON FORCE OSCILLATIONS
79
These force oscillations could be altered with superficial cooling of the ipsilateral thigh. Because the force oscillations were present during lengthening and not during shortening exercises of similar effort, a peripheral control mechanism of muscle, possibly mediated by stretch, was implicated as a contributing factor (Hart and Stauber, unpublished data). As the force oscillations were eliminated in some subjects while the level of muscle activity and torque production remained high, the hypothesis that the oscillations were primarily neural in origin was supported. Further support for this hypothesis comes from studies in which superficial cooling reduced the amplitude of the force and electromyographic response of a deep tendon reflex (lo), decreased the gamma efferent stimulation of muscle spindles (23), and decreased the passive resistance of muscles to stretch in patients with spasticity (9). The muscle spindle may be primarily responsible for these eccentric force oscillations. After direct cooling of various animal muscles, reductions in Ia and II fiber discharges were observed which resulted in a decreased responsiveness to stretch (4, 12, 15). With a greater decrease in the Ia discharge rate, a greater extensor inhibition to stretch occurred (4). Hence, the lack of silent periods and force oscillations in our study (Fig. 4) and a reduction in the number of oscillations after cooling could be a direct result of a reduced sensitivity to muscle stretch. The effect of cooling of the calf on central mechanisms is not known. However, central mechanisms are altered by certain peripheral stimuli as evidenced by studies on humans. For example, cooling of the calf increased alpha motoneuron excitability and depressed gamma motoneuron excitability (23), whereas exercise of the upper body increased the amplitude of PAT in the plantar flexors (8). Therefore, some of the variation in the angle of initiation of the PAT that follows quadriceps cooling may represent a change in the coordination of the supraspinal centers for volitional effort superimposed on cold-induced alterations of the somatosensory system. REFERENCES G. C., AND G. L. GOTTLIEB. 1977. Oscillation of the human ankle joint in response to applied sinusoidal torque on the foot. J. Physiol. (London) 268: 15 l-176. ALLUM, J. H. J., V. DIET& AND H. J. FREUND. 1978. Neuronal mechanisms underlying physiological tremor. 1. Neurophysiol. 41: 557-57 1. ELBLE, R. J., AND J. E. RANDALL. 1976. Motor-unit activity responsible for 8- to 12-Hz component of human physiological finger tremor. J. Neurophysiol. 39: 370-383. ELDRED, E., D. R. LINDSLEY, AND J. S. BUCHWALD. 1960. The effect of cooling on mammalian muscle spindles. Exp. Neural. 2: 144-157. FARRELL, M.. AND J. E. RICHARDS. 1985. Analysis of the reliability and validity of the Kinetic Communicator exercise device. Submitted.
1. AGARWAL, 2.
3. 4. 5.
80
HART,
MILLER,
AND
STAUBER
6. FOX, J. R., AND J. E. RANDALL. 1970. Relationship between forearm tremor and the biceps electromyogram. J. Appl. Physiol. 29: 103-108. 7. HAGBARTH, K.-E., AND R. R. YOUNG. 1979. Participation of the stretch reflex in human physiological tremor. Brain 102: 509-526. 8. IAIZZO, P. A., AND R. S. POZOS. 1982. Exercise-induced amplitude modification of physiological action tremor of the ankle. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 53: 1164- 1170. 9. KNUTSSON, E. 1970. Topical cryotherapy in spasticity. &and. J. Rehab. Med. 2: 159-163. 10. KNUTSSON, E., AND E. MATTSSON. 1969. Effects of local cooling on monosynaptic reflexes in man. Stand. J. Rehab. Med. 1: 126-132. I 1. LIPPOLD, 0. C. J. 1970. Oscillation in the stretch reflex arc and the origin of the rhythmical 8-12 c/s component of physiological tremor. J. Physiol. (London) 2061 359-382. 12. LIPPOLD, 0. C. J., J. G. NICHOLLS, AND J. W. T. REDFEARN. 1960. A study of afferent discharge produced by cooling a mammalian muscle spindle. J. Physiol. (London) 153: 218-231. 13. LIPPOLD, 0. C. J., J. W. T. REDF’EARN,AND J. Vuco. 1957. The relation between the stretch reflex and the electrical and mechanical rhythmicity in human voluntary muscle. J. Physiol. (London) 13& 14P-15P. 14. MARSHALL, J., AND E. G. WALSH. 1956. Physiological tremor. J. Neural. Neurosurg. Psychiatry 19: 260-267. 15. MICHALSKI, W. J., AND J. J. SEGUIN. 1975. The effects of muscle cooling and stretch on muscle spindle secondary endings in the cat. J. Physiol. (London) 253: 341-356. 16. MORI, S. 1973. Discharge patterns of soleus motor units with associate changes in force exerted by foot during quiet stance in man. J. Neurophysiol. 36: 458-471. 17. MORI, S. 1975. Entrainment of motor-unit discharges as a neuronal mechanism of synchronization. J. Neurophysiol. 38: 859-870. 18. POZOS, R. S., P. A. IAIZZO, AND R. W. PETRY. 1982. Physiological action tremor of the ankle. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 52: 226-230. 19. RIETZ, R. R., AND R. N. STILES. 1974. A viscoelastic-mass mechanism as a basis for normal postural tremor. J. Appl. Physiol. 37: 852-860. 20. SATO, H. 1983. Effects of skin cooling and warming on stretch responses on the muscle spindle primary and secondary afferent fibers from the cat’s tibialis anterior. Exp. Neurol. 81: 446-458. 21. SCHAFER, E. A., H. E. L. CANNEY,
22. 23. 24. 25. 26.
AND J. 0. TUNSTALL. 1886. On the rhythm of muscular response to volitional impulses in man. J. Physiol. (London) 7: 1I l-l 17. STILES, R. N., AND R. R. RIETZ. 1977. Involuntary ankle oscillations from normal subjects. Am. J. Physiol. 233: R8-R14. URBSCHEIT, N., AND B. BISHOP. 1970. Effects of cooling on the ankle jerk and H-response. Phys. Ther. 50: 1041-1049. WOLF, S. L., AND E. KNUTSSON. 1975. Effects of skin cooling on stretch reflex activity in triceps surae of the decerebrate cat. Exp. Neural. 49: 22-34. WOLF, S. L., AND W. D. LETBE~ER. 1975. Effect of skin cooling on spontaneous EMG activity in triceps surae of the decerebrate cat. Brain Res. 91: 15 I- 155. ZAHALAK, G. I., AND S. C. CANNON. 1983. Prediction of the existence, frequency, and amplitude of physiological tremor in normal man based on measured frequency-response characteristics. J. Biomech. Eng. 105: 249-257.
NEUROLOGY
(1985)
%,73-80
Effect of Cooling on Force Oscillations during Maximal Voluntary Eccentric Exercise DENNIS L. HART, Applied Kinesiology Laboratory, and Neurology, West Virginia Received
LISA C. MILLER, Division University
December
AND WILLIAM
T. STAUBER’
of PhysicaI Therapy, and Departments OfPhysiology Medical Center, Morgantown, West Virginia 26506
14, 1984;
revision
received
May
22, 1985
The effect of superficial cooling on force oscillations during maximal eccentric exercises of the quadriceps femoris was studied in 10 adults. Maximal (i) shortening (concentric) and (ii) lengthening (eccentric) exercises were performed at a velocity of 12O”/s through 60” of knee flexion while linear envelope EMG signals were recorded from the surface of the vastus medialis muscle. Force oscillations (12.4 f 2.8 Hz) were present in all subjects in the first series of eccentric exercises. After 30 min of cooling, the oscillations were eliminated in two subjects and were reduced in number in two others of the five subjects in the experimental group. In contrast, all subjects in the control group still had oscillations when retested after a 30-min rest period. During the eccentric exercises, a synchronous silent period in the EMG tracings was evident just before a decrease in force. Subsequently, the EMG activity resumed and the force increased (force oscillation). Because the force oscillations were of large amplitude and occurred only during eccentric exercise, we conclude that the force oscillations were similar to physiological action tremor. Because the force oscillations and EMG patterns were altered by cooling, the mechanisms that initiate such oscillations during maximal eccentric exercise are suspected to include a neural component. 0 1985 Academic Press. Inc.
INTRODUCTION Oscillations in the force output of voluntary isometric contractions (8 to 12 Hz) were recorded as early as 1886 (2 1) and were classified as physiological tremor (PT) (2, 3, 7, 11, 16, 17, 19). To differentiate these tremors from those occurring during dynamic activities, the term physiological action tremor (PAT) (1, 8, 14, 18) was used. Although the mechanisms of either Abbreviations: PAT-physiological action tremor, PT-physiological tremor. ‘The authors thank Dr. Sandy Burkart for his continued financial support and Dr. Paul Brown for critically reading the manuscript. 13
0014-4886/85 $3.00 Copyright 0 1985 by Academic Press. Inc. All rights of reproduction m any form rcscrved.
74
HART,
MILLER,
AND
STAUBER
type of tremor remain unclear, PT and PAT appear to have definite neural (2, 3, 13, 16, 18, 22) and mechanical (6, 19, 22, 26) components. Recently we observed that large-amplitude force oscillations occur during maximal eccentric exercise. As they were not present during concentric exercise of similar magnitude (Hart and Stauber, unpublished observations), muscle stretch was considered the probable stimulus for oscillations in force. It is known that a reduction in either skin (9, 10, 20, 22, 24, 25) or intramuscular (4, 10, 12, 15) temperature will influence the responsiveness of the stretch reflex. If neural factors contribute to the eccentric PAT, then cooling should alter both force oscillations and muscular activity. Therefore we recorded the effects of cooling on the force oscillations and the surface electromyogram during maximal voluntary eccentric exercise. METHODS The subjects were positioned supine with the pelvis strapped to the table of a computer-controlled dynamometer (KIN/COM). The exercise set consisted of one series of four consecutive maxima1 concentric and eccentric knee extension exercises resisted by the KIN/COM with no pause between the concentric and eccentric phases. The dynamometer measured position (in degrees) and force (in Newtons). The computer sampled the angle and force data at 100 samples per second and computed torque (force X radius), velocity (O/s), and instantaneous power (force X velocity). The computer adjusted the velocity with a 2-ms latency to maintain the preset velocity. The operating limit for the strain gauges was 1112 N, and the maximum velocity of movement of the dynamometer was 21O”/s. Therefore, all data collected were within the limits of the equipment. A velocity of 12O”/s was used for both the concentric and eccentric exercise. The range of knee motion was 60” (75 to 15” of knee flexion, with 0 defined as full extension). The full 60” of movement had to be completed before the dynamometer allowed a change in direction of movement. However, the exercise unit would not allow any movement until a 50-N threshold force was applied to the dynamometer at the point of lower leg contact, thus insuring that the muscles were producing tension prior to movement. If the threshold force value was not maintained throughout the range of movement, the machine stopped. Therefore, impulse loading was prevented, and the subjects were protected during eccentric exercise, because the machine would stop if the force was removed (i.e., the leg taken away). Independent studies have confirmed the reliability of the dynamometer in measuring the angle, velocity, and force within an error of 3% (5).
EFFECT OF COOLING
ON FORCE OSCILLATIONS
75
Several submaximal exercises were performed to familiarize each subject with the testing routine. When the subjects were comfortable with the routine, one set of maximal effort, knee extension exercises was performed. Five of the subjects were randomly assigned to the treatment group and ice packs were applied to the medial, anterior, and lateral aspect of the thighs from the hip to the knee. Care was taken to keep the EMG electrodes dry. After performing their initial series of exercises, the control group waited in the same position as the cooling group with the thigh exposed to ambient temperature (25°C) for 30 min. Then each subject performed a second series of identical exercises. Two independent recording devices were used: (i) the KIN/COM and (ii) a Grass model 7 polygraph. The digital values of angular position (degrees) and torque (Newton * meters) were retrieved from the KIN/COM. The polygraph recorded analog signals of force (directly from the force transducer of the KIN/COM), angular displacement (by means of a potentiometer connected to the dynamometer arm), and the EMG signals (pen response = 50 Hz). Electromyographic signals were recorded with bipolar silver/silver-chloride surface electrodes (2-mm diameter, 1S-cm interelectrode distance) placed over the left vastus medialis muscle. A silver/silver-chloride ground electrode was placed over the lateral femoral condyle. Skin preparation with shaving, alcohol, and abrasion reduced skin resistance to less than 5 kQ for each electrode. The EMG was amplified (300X) at the source with a Motion Control EMG preamplifier (CMRR = 100 dB, 10.5 to 27 kHz bandwidth, DC input impedance 10’ a). The signal was voltage divided before further amplification by a Grass 7P3 amplifier which recorded either the raw EMG or its envelope (fullwave rectification, 50-ms time constant, ~-HZ to lo-kHz bandpass). Linear envelope signals were recorded from all subjects and occasional raw signals were recorded for comparison. For a force fluctuation (from the Grass strip chart) to be considered a valid indicator of physiologic action tremor, it had to be: (i) independent of machine function and (ii) of sufficient amplitude (greater than 5 N-m). Machine-introduced oscillations occur only if the applied force is close to the preset threshold force (Hart, unpublished data). The force oscillations that occurred in this study of normal adult subjects were well above 50 N (i.e., free from machine interference). The moments recorded during the eccentric exercises were consistently greater than 200 N . m. For analysis, the force fluctuations were identified on the Grass strip chart and the corresponding data for that time period were retrieved from the KIN/COM. The fluctuations were characterized according to the mean fundamental frequency of oscillation, the angle of their initiation, and the
76
HART,
MILLER,
AND STAUBER
EMG patterns. One cycle of a force oscillation was defined as the signal between two consecutive peaks on the force tracing. The EMG signals were reduced to a percentage of a maximum isometric contraction at 45” of knee flexion. RESULTS Ten subjects participated in the project. Each subject performed one series of exercises before and one series after the cooling or after a comparable waiting period. Therefore, a total of 80 concentric and 80 eccentric exercise repetitions were evaluated. During the first series of exercises the concentric force curves were devoid of large-amplitude (greater than 5 N. m) oscillations, and the linear envelope EMG tracings indicated high muscle activity throughout the range of motion (Fig. 1). The eccentric forces were typically of higher magnitude than the concentric forces and each eccentric exercise had at least one oscillation (Figs. l-3) (Table 1). When the raw EMG signals were recorded, these signals had distinct silent periods associated with a sharp decrease in the linear envelope signals that immediately preceded the eccentric force decrement. Of the five subjects in the experimental group, the force oscillations were eliminated in two of them (Table 1, Fig. 4). Of the three subjects who received cooling but did not have their oscillations eliminated, two of these ECCENTRIC 100
ANGLE
OF FLEXION
FIG. 1. One concentric and one eccentric contraction of a control subject prior to the control wait period. The force and EMG signals were reduced to a percentage of maximum at 45” knee flexion during isometric contraction. The tracings began at 75” of knee flexion, continued to 15” of knee flexion, and returned to 75” of knee flexion (0” is defined as a full extension).
EFFECT OF COOLING
ON FORCE OSCILLATIONS
CONCENTRIC
77
ECCENTRIC
100
50
0 150
0 i5
IO0
50
, 35 ANGLE
55
75
OF FLEXION
FIG. 2. The same subject as in Fig. 1 after the 30-min wait period.
had the number of oscillations reduced from seven to one and from seven to four, but the frequency was unchanged. The fifth subject was unaffected by the cooling. In contrast, the force oscillations were unaltered in the second series of exercises for the control group. The angle of occurrence of the initial oscillation during the first series of eccentric exercises averaged 38.4 ? 12.7” of knee flexion. This value was unaltered after cooling. The within-subject variability of the angle of knee
ECCENTRIC 100 E ;
50
0 75
55
35 ANGLE
15 35 OF FLEXION
55
75
FIG. 3. One concentric and one eccentric contraction from an experimental subject before application of ice. (Similar data reduction as in previous figures.)
78
HART,
MILLER,
AND STAUBER
TABLE 1 Frequency of Force Oscillations during Eccentric Contraction” Ice Subject 1 2 7 8 9
PRE 13.9 f 12.1 + 9.7 k 10.5 f 17.6 +
1.6 1.6 0.7 1.4 0.9
Control POST
Subject
15.8 + 1.0 14.3 * 1.5 12.5 + 0 -
3 4 5 6 10
PRE 11.7 14.3 10.3 11.8 13.9
+ f k h +
POST 0.6 0 4.0 0.6 3.3
10.9 f 11.6 f 13.8 f 10.8 k 12.5 +
1.0 0.9 0.5 5.6 0
Note. Forty-one of sixty (68.3%) contractions had oscillations during the first series of exercises (both groups) and the second series of exercises (control group); 8 of 20 (40%) postcooling contractions had oscillations (treatment group). ’ Frequencies in Hz: X + SD; range: 6.3 to 18.8 Hz.
flexion was small for four of the five subjects in the control group. However, in contrast, the variability in the angle of knee flexion where force oscillation occurred for the three subjects in the treatment group who did not have their oscillations eliminated was larger and not consistent in direction. DISCUSSION During maximal voluntary effort of the knee extensors to resist a forced lengthening (eccentric exercise), oscillations in force output were observed. CONCENTRIC
ECCENTRIC
100 Y 5
50
0 150
0 75
q
55
35 ANGLE
15
35
Dweclion Chonpe
55
75
OF FLEXION
FIG. 4. One concentric and one eccentric contraction of the same subject as in Fig. 3 after a 30-min application of ice. (Similar data reduction as in previous figures.)
EFFECT OF COOLING
ON FORCE OSCILLATIONS
79
These force oscillations could be altered with superficial cooling of the ipsilateral thigh. Because the force oscillations were present during lengthening and not during shortening exercises of similar effort, a peripheral control mechanism of muscle, possibly mediated by stretch, was implicated as a contributing factor (Hart and Stauber, unpublished data). As the force oscillations were eliminated in some subjects while the level of muscle activity and torque production remained high, the hypothesis that the oscillations were primarily neural in origin was supported. Further support for this hypothesis comes from studies in which superficial cooling reduced the amplitude of the force and electromyographic response of a deep tendon reflex (lo), decreased the gamma efferent stimulation of muscle spindles (23), and decreased the passive resistance of muscles to stretch in patients with spasticity (9). The muscle spindle may be primarily responsible for these eccentric force oscillations. After direct cooling of various animal muscles, reductions in Ia and II fiber discharges were observed which resulted in a decreased responsiveness to stretch (4, 12, 15). With a greater decrease in the Ia discharge rate, a greater extensor inhibition to stretch occurred (4). Hence, the lack of silent periods and force oscillations in our study (Fig. 4) and a reduction in the number of oscillations after cooling could be a direct result of a reduced sensitivity to muscle stretch. The effect of cooling of the calf on central mechanisms is not known. However, central mechanisms are altered by certain peripheral stimuli as evidenced by studies on humans. For example, cooling of the calf increased alpha motoneuron excitability and depressed gamma motoneuron excitability (23), whereas exercise of the upper body increased the amplitude of PAT in the plantar flexors (8). Therefore, some of the variation in the angle of initiation of the PAT that follows quadriceps cooling may represent a change in the coordination of the supraspinal centers for volitional effort superimposed on cold-induced alterations of the somatosensory system. REFERENCES G. C., AND G. L. GOTTLIEB. 1977. Oscillation of the human ankle joint in response to applied sinusoidal torque on the foot. J. Physiol. (London) 268: 15 l-176. ALLUM, J. H. J., V. DIET& AND H. J. FREUND. 1978. Neuronal mechanisms underlying physiological tremor. 1. Neurophysiol. 41: 557-57 1. ELBLE, R. J., AND J. E. RANDALL. 1976. Motor-unit activity responsible for 8- to 12-Hz component of human physiological finger tremor. J. Neurophysiol. 39: 370-383. ELDRED, E., D. R. LINDSLEY, AND J. S. BUCHWALD. 1960. The effect of cooling on mammalian muscle spindles. Exp. Neural. 2: 144-157. FARRELL, M.. AND J. E. RICHARDS. 1985. Analysis of the reliability and validity of the Kinetic Communicator exercise device. Submitted.
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