EXPERIMENTAL
NEUROLOGY
81,640-650 (1983)
Effect of Fatigue on Force Sensation L. A. JONES AND I. W. HUNTER' Psychology Depatiment and Biomedical Engineering Unit, McGill University, Montreal, Quebec H3A IBI, Canada Received December 13, 1982; revision received March 30, 1983 Recent experiments have suggested that a senSe of effort can be separated from a sense of developed force or tension in muscular contractions. The evidence for this distinction was examined during submaximal fatiguing contractions. Subjects were required to maintain until maximal endurance a constant isometric force with their right, reference arm, and at 15-s intervals they estimated the magnitude of this force with a matching contraction of the contralateral arm. The matching force produced by the unfatigued limb was the measure of force sensation. Both force and the brachial biceps and triceps EMG were recorded from each arm. During the fatiguing contractions the matching force increased linearly as did the biceps EMG of the fatiguing muscle. The rate of increase was dependent on the level of force exerted. A linear relation between the reference arm EMG and the perceived force was observed, which suggested that the over-estimation of force was due to the increase in the excitatory input to the fatiguing muscle. These results provide support for a centrally mediated theory of force perception, and indicate that during fatigue subjects are unable to estimate accurately the force of contraction. Furthermore, they suggestthat under those conditions a sense of tension is not distinguishable from a sense of effort.
INTRODUCTION The basis on which judgments of the magnitude of muscular contractions are made has been a subject of controversy for more than a century (11) and has reemerged as a contentious issue following the demonstration of a muscular afferent contribution to the perception of movement and position (6). Essentially two mechanisms have been proposed to account for the ability to estimate muscular forces, although these may be complementary rather Abbreviations: EMG-electromyogram, MVC-maximum voluntary contraction. ’ Part of this paper was presented at the Society for Neuroscience Annual Meeting in Minneapolis, November 1982. Requests for reprints should be sent to Lynette A. Jones, Department of Psychology. 640 0014-4886/83 $3.00 Copyright 0 1983 by Academic Press, Inc. All rights of reproduction in any form reserved
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than exclusive systems. First, a centrally mediated mechanism termed a “sense of effort” (12) is based on the notion that concomitant with the efferent command sent to the motoneuron pools, a corollary discharge is transmitted to sensory centers. It is proposed that this signal which reflects the magnitude of the voluntary motor command generated is used in estimating muscular force. The second source of force information, described as a “sense of tension,” is derived from peripheral receptors in the muscle, tendon, and skin which are presumed to signal intramuscular tensions and therefore provide a measure of the actual force exerted (18). Numerous experiments conducted by McCloskey and his colleagues have indicated that variations in the perception of muscular forces parallel changes in the motor command sent to the muscle (11, 12). In their studies on the perceived heaviness of lifted weights they showed that whenever a lifting muscle is weakened so that an increase in the efferent signal is required, there is a corresponding increase in the perceived heaviness of the lifted object as indicated by the weight chosen on the unaffected side to match it. The independent existence of a sense of tension or force was demonstrated in subjects who accurately maintained or estimated constant force during agonist tendon vibration (12) and after gallamine-induced paresis (18). Thus there appears to be at least two sources of force-related information, one that is central in origin and the other which is based on peripheral sensory activity. Because these mechanisms co-exist (17) it is of interest to ascertain under what conditions each assumes the predominant role. Using a contralateral limb matching paradigm, in which forces exerted by a muscle group in one limb (the reference) are matched in subjective magnitude with contractions of the corresponding muscle group (the matching) in the other limb, Cafarelli and Bigland-Ritchie (3) investigated the effect of varying muscle length (and hence maximum force) on force sensation. When the force-generating capacity of the contractile element of a muscle was altered by adjusting muscle length, the matching function changed depending on whether the reference or matching muscle was stronger. However, force sensation remained constant whenever the activation [as measured by the surface electromyogram (EMG)] of the two muscles was the same. Those results were interpreted as providing support for a centrally mediated sensation of force (3). Moreover they suggest that the surface EMG can be considered a measure of the excitatory input to a muscle. When the perceived forces of isometric contractions are measured by a matching contraction of the contralateral muscle group, in the absence of fatigue both the function relating force and the EMG and the relation between the EMGs recorded from each limb are linear (7). However, a nonlinear relation between force and EMG has also been reported for the brachial biceps muscle ( 1, 8, 2 1). During constant force contractions maintained until
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maximal endurance the amplitude of the EMG increases due to failure of the contractile mechanism (4, 9, 10). Under those conditions it is possible to investigate how measurements of force sensation made by the unfatigued limb covary with the actual force exerted and with the excitatory input (EMG) to the fatiguing muscle. If the corollary discharge from the motor command is the preferred signal then forces will be overestimated in proportion to the increase in EMG in the fatiguing muscle, whereas judgments of force will remain essentially constant if intramuscular tension is monitored. This experiment was designed to investigate how force sensation changed during fatigue, a frequently encountered perturbation of the neuromuscular system. Subjects were instructed to estimate the physical force exerted during constant force, isometric contractions maintained until maximal endurance. The interrelations between force, EMG, and perceived force during fatigue were of particular interest. METHODS Six female and four male university students and staff from 22 to 32 years of age (mean age 27 years) participated in this experiment. Subjects gave their informed consent to the procedures described below. All subjects were right-handed and had no known neuromuscular abnormalities. The experimental sessions took place in a shielded room. The forces produced at the wrists (largely by the biceps brachii muscles) were measured by two strain gage force transducers mounted on a wooden and steel frame. A chain was attached to each force transducer and the distal end of each chain was fitted with a leather band (3 cm wide) which was placed around the subject’s wrists over the head of the ulna. The subjects sat facing the apparatus with vertical and parallel forearms spaced 30 cm apart, and with each elbow joint resting in a molded Sansplint support. The upper arm was horizontal and the hand was in a semipronated position. The angle between the left and right upper arm and forearm was 90 degrees. The output from the force transducers was converted and amplified by a strain gage bridge (Tektronix Type 3C66), and low-pass filtered at 10 Hz (Rockland Filter Model 852). The filtered output from the right arm force transducer was displayed on a digital meter affixed to the frame directly in front of the subject. This meter served as a monitor for the subject in achieving reference forces. Electromyographic signals were recorded from the surface of the brachial biceps and triceps muscles of both arms by silver-silver chloride electrodes 9 mm in diameter. These electrodes were placed 45 mm apart along the long axis of the muscles in a bipolar configuration. The raw EMG signals were differentially amplified, band-pass filtered (1 to 1000 Hz), full-wave rectified, and then low-pass filtered at 0.5 Hz.
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The two force and four EMG channels were sampled continuously Hz by a PDP 1 l/34 computer.
643 at 30
Procedure
Prior to the experimental trials the subjects made a series of maximum voluntary contractions (MVC) with each arm consecutively. Isometric strength was assessed as the strongest of two brief voluntary maximal contractions. Three minutes elapsed between contractions. The subjects participated in three experimental conditions which were conducted on different days. There was an average of 3 days between trials. This period of time was necessary for recovery of the endurance capacity of the biceps brachii muscle (5). The subjects were required to maintain a constant force with their right (reference) arm at a specified percentage oftheir MVC (35,50, or 65% MVC). They were instructed to maintain a numeric value on the digital meter which was the force in newtons exerted by the right arm. The order of presentation of the three experimental sessions was random. At the start of each session and at 12-s intervals a warning tone (1 s) followed after 2 s of silence by a tone of 3-s duration was presented through headphones to the subject. Each time the second tone was heard the subjects produced a force with their left arm which they perceived to be the same as the force they were exerting with their right arm. After the matching force was exerted the subjects relaxed their left arm but continued maintaining the designated force with their right arm. When the subjects were no longer able to maintain this force, such that it was below the specified value for 5 s, their maximal endurance for the force was considered to have been attained and the experimental session was terminated. Prior to each experimental session the importance of maintaining a contraction for as long as possible was emphasized to all subjects. There were practice trials before the first experimental session. Due to the considerable intersubject variation in endurance times at each force the durations were normalized by expressing time as a percentage of the endurance time. The perceived force data, as measured by the left arm matching contraction, and the left biceps EMG data were fitted by cubic splines ( 16). One hundred equally spaced samples were then taken from each spline function. This method was chosen to permit normalization of the results from different subjects and forces, both of which yielded different absolute durations. RESULTS Because there were large individual differences in isometric strength (range: 156 N to 490 N) the force data were analyzed in relative form (percentage MVC). There was a significant difference between the left and right arm
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MVCs of the subjects (P < 0.05) with the left arm being on average 7% weaker than the right. The mean coefficient of variation of the maximum forces exerted by each subject at the beginning of the three experimental sessions was 0.05. The total time that a contraction could be maintained was found to vary inversely with the strength of the contraction. The mean endurance times of forces maintained at 35, 50, and 65% MVC were 228 (+76), 123 (*50), and 75 (+26) s, respectively. At each relative force the endurance time of female subjects exceeded that of the males by an average of 70%, however, the average isometric strength of female subjects was less than half (47%) that of male subjects. Three subjects participated in repeat trials conducted several months after the initial experiment. The correlation between the endurance times obtained in those two sets of trials was 0.93. Changes in the matching forces exerted during constant force contractions maintained until maximal endurance are shown in Fig. 1. A summary of the individual data is presented in Table 1. A consistent pattern of overestimation of the amplitude of the constant force was evident in the force estimates of subjects. The increase in the matching forces produced was essentially linear, and the rate of increase was dependent on the force exerted. With higher initial forces and therefore shorter endurance times, the subjects perceived a very rapid increase in the magnitude of the constant force. Nevertheless, during the same relative time scale (as in Fig. 1) there was no significant difference in the rate of the matching force change for different constant forces (P > 0.05).
20
40 % Endurance
60
60
t 100
Time
FIG. 1. Matching forces exerted by the left arm as a function of the percentage duration of constant force contractions maintained by the reference arm at forces of 35,50, and 65% MVC. The solid lines are the means of the cubic spline functions fitted to the 10 subjects’ data. The dotted lines show the matching forces estimated from the linear function described in the text.
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TABLE 1 A Summary of the Individual Data Force (%)
N”
Intercept*
Slope
Mean’
SD
35 50 65
14 II
51.99 67.80 72.34
0.08 -0.0 1 0.35
60.04 66.74 81.96
8.59 3.90 13.01
2
35 50 65
22 15 9
49.96 53.12 75.43
0.05 0.17 0.08
58.46 71.05 80.37
7.19 13.21 6.50
3
35 50 65
20 9 6
29.03 33.06 37.50
0.03 0.27 0.71
33.76 49.4 1 64.02
5.30 12.07 20.31
4
35 50 65
16 5
31.74 52.7 1 71.76
0.10 0.35 0.31
42.7 1 68.21 81.12
9.50 12.48 8.42
5
35 50 65
14 8 4
33.09 57.49 65.88
0.19 -0.0 1 -0.07
51.74 56.91 64.88
13.70 1.79 11.63
6
35 50 65
17 6 5
39.82 43.78 78.96
0.18 0.62 0.17
61.54 66.98 83.92
18.48 19.06 4.97
1
35 50 65
19 12 8
36.87 35.28 16.00
0.11 0.11 -0.07
51.38 44.35 12.56
10.79 9.71 8.10
8
35 50 65
5 3
39.64 52.10 62.32
0.38 0.49 0.12
56.56 66.64 13.17
13.31 11.89 11.51
9
35 50 65
21 9 6
30.76 46.39 57.06
0.04 0.09 -0.06
36.95 51.56 54.95
7.04 10.71 13.43
10
35 50 65
9 6 5
36.43 28.52 58.26
0.35 0.19 0.3 I
51.57 58.12 67.42
15.07 23.31 7.68
Subject
‘N is the number of matching contractions exerted at each level of constant force. b The slope and intercept values were calculated by least-squares linear regression on the matching force data. ‘The means and standard deviations were calculated from the matching forces produced during the constant force contraction.
The matching force on the first trial (at zero time) of each experimental sessionprovided a control estimate of the accuracy of force perception in an unfatigued muscle. The initial mean force estimateswere 38,46, and 63%
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MVC corresponding to contraction levels of 35, 50, and 65% MVC, respectively. Because there was a significant difference between the left and right arm MVC, the matching force exerted by the left arm was expressed as a percentage of that arm’s MVC. During the course of the isometric contractions the matching forces increased until at endurance time a force of 35% MVC was overestimated by 76%. The matching forces exerted at endurance time ranged from 62 to 77% MVC. These forces were significantly less than the maximum forces the subjects were capable of producing with their left arm. Despite the increase in the matching forces exerted, the subjects frequently commented at the end of a session on how accurate they thought their estimates of the constant force were. There was no significant difference between the matching forces produced at maximal endurance (F(2,18) = 3.5 1; P > 0.05). A mathematical model containing only one free parameter was developed to describe the change in perceived force during fatigue. Two factors that influenced the matching force were the initial level of contraction and the effective force range for judgments. Based on those considerations a model of perceived force was formulated, P = (100 - F)aT+ F where P = matching force (% MVC),
F = reference force (% MVC), T = % endurance time, and a = constant.
The least squares value of a calculated from the data in Fig. 1 was 0.0047. This equation was found to provide a good fit to the matching force data, accounting for 91% of the variance. Figure 1 shows the change in perceived force with time together with the matching forces estimated from the above equation. Figure 2 illustrates the change in the amplitude of the EMG recorded from the right biceps brachii muscle during the constant force contractions. The increase in the EMG was essentially linear and was dependent on the magnitude of the constant force exerted. The EMGs recorded at maximal endurance were significantly different (F(2,18) = 15.45; Geisser-Greenhouse P = 0.0009), with the highest amplitude occurring at the end of the contraction maintained at 65% MVC. The amplitude of the right triceps EMG also increased during the sustained isometric contractions, although to a very much smaller extent. There was considerable variation in the degree of activation of the triceps muscle, with increases in the EMG from 15 to 100 pV across subjects in the three trials. The mean increase was 47 _+ 32.4 PV. It is difficult to determine from these data to what extent this increase represents cross-talk rather than cocontraction.
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a
00
20
40
60I
I 100
60
% Endurance lime FIG. 2. Reference arm biceps EMGs during constant force contractions (35, 50, and 65% MVC) of the reference arm as a function of the percentage duration of the contraction. The solid lines are the means of the cubic spline functions fitted to the 10 subjects’ data. The difference between the solid and dotted lines indicates the standard errors of the means.
The relation between the biceps EMG of the reference arm and the matching force is shown in Fig. 3. As the biceps EMG increased due to either larger forces or progressive fatigue in the muscle there was a corresponding increase in the matching force. This force could be quite accurately predicted from
0 0
100
200 Reference
300
400
, 500
Arm EMG (pV)
FIG. 3. Matching forces exerted as a function ofthe reference arm biceps EMG during constant force contractions (35, 50, and 65% MVC) maintained by the reference arm. The data represent the means of the cubic spline functions fitted to the biceps EMG and matching force data of each subject. The least-squares regression line is shown.
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the reference EMG, because it appeared to be irrelevant whether the amplitude of the EMG resulted from a high force contraction or a sustained submaximal contraction. The least-squares linear regression line was drawn only over the range of forces examined because smaller forces (less than 20% MVC) can be sustained indefinitely by the biceps muscle (2). The form of the reference muscle EMG-matching force relation is unknown at low forces requiring minimal muscle excitation. There was no evidence of fatigue in the matching arm during the experimental sessions, and the force-EMG relation of the left biceps muscle was linear over the range 35 to 80% MVC. The mean correlation between the matching force and the left biceps EMG of the 30 trials was 0.87 (+O. 12). DISCUSSION Previous experiments have shown that the sensation of force increases during sustained constant force contractions (12,19). The present experiment confirms those findings and extends those results to a consideration of the relation between myoelectric activity and the perception of force during fatigue. The increase in perceived force that occurs during isometric contractions maintained until maximal endurance is well described by a linear function with one free parameter. It has previously been proposed that the degree of perceived force grows as a power function of both the force and the duration of an isometric contraction (19). However, that model was derived from numerical estimates of perceived force and that procedure appears to introduce nonlinearities into the relation between the magnitude of a physical stimulus and estimates of its amplitude (14). The power function and linear models concur in specifying that force rather than time is the critical factor determining the increase in perceived force or effort during constant force contractions. The importance of instructions in determining subjects’ strategies in estimating force has been reported ( 12,17). In our present experiment emphasis was placed on estimating muscular force, and the concept of effort was not discussed with the subjects. Despite those instructions the subjects consistently overestimated the magnitude of the constant forces, and appeared to be unaware of this exaggeration. The feedback (via the meter) of the forces generated by the right arm did not enable them to judge accurately the force of contraction. No dissociation between estimates of force and effort was evident in their judgments of force during fatigue. The demonstration (18) of such a dissociation during gallamine-induced paresis followed instructions to disregard the increased effort that was required to make a muscular contraction (17). It is possible that by biasing subjects in this manner accurate estimates of the physical force exerted could be made during fatigue. In the
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absence of such instructions subjects demonstrate which sense is normally relied on. Our experiment indicates the preponderance of a sense of effort as the basis of force perception. A linear increase in the EMG during sustained isometric contractions has frequently been reported (4, lo), and it has also been observed that the amplitude of the EMG is a function of both the muscular force exerted and the degree of fatigue induced in the muscle (9). The surface EMG was used as a measure of the excitatory input to the muscle, as it reflects the number of active motor units and their discharge rate. However, an indeterminate amount of the efferent input to a muscle is due to the activation of alpha motoneurons via the gamma loop and muscle spindle afferent fibers (15). The EMG is therefore a biased estimate of the descending motor command. Nevertheless the covariation observed between the amplitude of the EMG of the reference arm and the matching force exerted by the left arm (Fig. 3), is consistent with the results obtained when the length-tension relation is used to alter the maximum force generated by muscles (3). Under both sets of experimental conditions force sensation can be predicted from the amplitude of the EMG of the reference muscle. The overestimation of force in the present experiment results from efferent signals of similar magnitude being dispatched to fatigued and unfatigued muscles, the latter being capable of generating more force. It has been proposed that the sense of effort could be based on some other physiological response such as heart rate or blood pressure, rather than the voluntary motor command ( 17). During fatiguing contractions both the heart rate and mean systolic blood pressure increase, due to the direct action of higher motor centers on the cardiovascular center and reflex responses elicited by afferent activity in the fatiguing muscle ( 13). However, there is no definite evidence indicating that human subjects can perceive those physiological responses. Muscle spindle receptors would also increase their firing rates during constant force contractions due to a coactivation of the gamma and alpha motoneurons (20). It seems unlikely that the overestimation of force can be due to their discharge, because the firing rate of both primary and secondary afferent receptors saturates at greater contractile force (20). A contralateral limb matching paradigm was used to investigate the sensation of force during fatiguing isometric contractions. It was found that there was a linear increase in the perceived force during the constant force contractions, and that the change in force sensation paralleled the increase in the EMG of the fatiguing muscle. These results give further support to the idea that muscular force is estimated on the basis of the voluntary motor command, or some variable proportional to it. They suggest that during fatigue subjects are unable to monitor accurately the force of exertion, and that the surface EMG is predictive of force sensation under those conditions.
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2 1. VREDENBREGT,J., AND G. RAU. 1973. Surface electromyography in relation to force, muscle length and endurance. Pages 607-622 in J. E. DESMEDT, Ed., New Developments in Electromyography and Clinical Neurophysiology. Karger, Basel.