Perceptual and Motor
Skills, 1992, 74, 91-98. O Perceptual and Motor Skills 1992
A N E W PROCEDURE FOR ASSESSMENT O F PROPRIOCEPTION ' BERND LEPLOW, VOLKERT SCHLUTER, ROMAN FERSTL Christian-Albrechts Universi!y
Summary.-A new method for the assessment of proprioception was developed and tested with 40 healthy subjects on two facial muscles (i.e., masseter and zygomatic muscles). The experiment was repeated after 3 % months. In our study, proprioceprion was studied with respect to sensations arising from the muscle spindles and tendon organs. Therefore, myesthesia was investigated, which was assessed by the correspondence between a voluntary muscle contraction and its immediate replication. Good perception was defined by a small integral of differences, standardized by duration and intensity of the contraction, and its replication. Results show that this measure is independent of the characteristics of muscle activation. In concordance with our hypothesis, myesthesia was superior in a muscle richly supplied with muscle spindles and afferent fibers (i.e., masseter muscle), to that for a muscle less prepared for afferent information processing (i.e., zygomatus major).
Perception of muscle activity is a frequent issue in applied psychophysiology, especially in closed loop theories of motor behavior (Adams, 1987), facial feedback theories of emotional expression (Levenson, Ekman, & Friesen, 1990), and theories of psychophysiological disorders, e.g., tension headaches (Haynes, Cuevas, & Gannon, 1982). In these paradigms, sufficient and accurate feedback from effector activity is crucial for effective attempts at self-regulation. The receptors for proprioception and myesthesia, respectively, are muscle spindles and tendon organs (DeJong, 1979). Perception of receptor activity can be assessed by methods of "magnitude estimation," "magnitude production," and "response discrimination " The magnitude estimation of muscle tension can be done by direct scaling of perceived muscle activity (Lehrer, Bateg, Woolfolk, Remde, & Garlick, 1988; Shedivy & Kleinmann, 1977). Recently, however, it has been questioned whether the mechanisms underlying such a matching between myesthesia and a rating scale are comparable to those in spontaneous muscle activity and its perception (Epste~n, 1990). Another method of estimating muscle tension requires the subject to attend to the muscle tension of an ongoing trial and to compare it to the most prior one. Within a biofeedback-paradigm, subjects had to estimate whether the actual tension was greater or smaller than that on the preceding trial (Kinsman, O'Banion, Robinson, & Staudenmayer, 1975; Staudenmayer & Kinsman, 1976). As under biofeedback, information about muscle tension can be either drawn from "true" myesthesia or from the biofeedback signal, Sime and deGood 'Address correspondence to Dr. B. Leplow, Department of Psychology, Christian-Albrechts University, Olshausenstrasse 61, W-2300 Kiel, F.R.G.
92
B. LEPLOW, ET AL
(1977) and Bayles and Clearly (1986) had circumvented this problem by s c h e d d n g separate trials, on which estimates had to be performed without the assistance of biofeedback. Furthermore, myesthesia has been assessed by the "magnitude production" method, where the subject has to activate a target muscle to certain percentages of either maximum strength (e.g., Bohannon & Endemann, 1989; Epstein, 1990), to predefined levels of muscle strength (Bayles & Clearly, 1986; Blanchard, Jurish, Andrasik, & Epstein, 1981; Epstein, 1990; Pollard & Katkin, 1984; Stilson, Matus, & Ball, 1980), or to the tension of the contralateral limb (Gandevia & Kilbreath, 1990). O n the contrary, on response-discrimination tasks subjects have to discriminate responses within a signal-detection paradigm. Subjects are either required to detect changes in training criterion (Jones & Dickson, 1978) or in the application of correct versus false feedback (Burnette & Adams, 1987; Leplow & Ferstl, 1990). As has been shown by Burnette and Adams (1987), the perception of false feedback is heavily influenced by extraneous variables. Similarly, we showed in a previous study that sensitivity scores were highly dependent on exteroceptive cues, whereas response bias was related to interoception (Leplow & Ferstl, 1990). Measurements of myesthesia then are related to very different functions. In the magnitude-estimation procedures, the subject has to perform quite a complex cognitive task of matching muscle tension against a rating scale or against an amount of perceived tension, remembered from a preceding trial. Within the magnitude-production paradigm, deficits in myesthesia may be due to dysfunctions of the direct, kinesthetic pathway or to deficiencies in the performance of the motor command. Response discrimination, however, can be biased by differences in use of supplementary feedback pathways or extraneous information. And, finally, all of these procedures are prone to inter- and intraindividual variations of attention-focussing processes. This study was designed to develop a method for the assessment of perception of facial muscle activity, which requires only minimal attention and memory load and which does not depend on subjective decision-making processes or compliance to external standards. Therefore, we requested the subjects to repeat single voluntary muscle contractions. Good myesthesia was operationally defined by a high correspondence between a contraction and its immediate replication. Intensity and duration of each initial muscle contraction could be chosen by the subject, so the subject did not have to match a physiological event against an external standard. By means of such a procedure, differences in perception across muscles should be mainly due to differences in afferent information processing, i.e., a physiological feedback mechanism. That means, in muscles richly supplied with muscle spindles and sensory
ASSESSMENT OF PROPRIOCEPTION
93
fibers, perception should be superior with respect to perception of contractions of muscles only less-well provided with muscle spindles.
Subjects Forty undergraduates, 22 women and 18 men, aged 20 to 40 years, served as subjects. Mean age was 24% yr., with 50% being between 20.7 and 27.6 years of age. All participants were volunteers and without medical complaints or medication. Procedure Study design.-A two-factor within-subject design was used, where perception of each subject was tested in two sessions 3.5 months apart and on both of two facial muscles, i.e., the zygomaticus major and masseter muscle on the dominant side. Handedness was assessed by carefully taking the subject's history with a standardized interview. The masseter muscle was chosen because it is known to be richly supplied with muscle spindles and afferent fibers from the mandibular branch of the trigeminal nerve (Rim, 1984). The zygomatic muscle, however, is innervated by the facial nerve, which is primarily motor and, therefore, less prepared for afferent information processing. Experimental sessions.-After subjects were briefed about the aim of the study, electrodes were attached. Subjects then learned selective contractions of the masseter and zygomatic muscles under the condition of visual feedback. Participants were advised to try different intensities and durations of activation. After about five minutes of practice, feedback was removed and the subject was advised that various muscle contractions had to be performed and that each contraction had to be repeated as exactly as possible. Although the exact time interval between a contraction and its replication could be chosen by the subject, the latency usually was between one and two seconds. Each pair, i.e., a muscle contraction and its replication, constituted one trial. Maximum duration of each contraction and its respective replication was limited to three seconds. O n e hundred trials had to be performed, in which the order of muscles was randomized. During the trials, no further instructions were given. Only at the beginning of the experiment had the subjects been advised that the amount of contraction had to be varied across trials. At the end of each trial knowledge of results was provided by means of graphic representations of the muscle contraction and its replication. Insh.umentation.-Facial electromyographic (EMG) responses were recorded using Ag-AgC1 Beckmann miniature electrodes and electrode placements as described by Fridlund and Cacioppo (1986). Skin was prepared as usual until resistance was below 10 kOhms. Recordings were done by means of a Langer, Inc. monitoring system and an Olivetti M24 computer. The band-
94
B. LEPLOW, ETAL.
width of the amplifier ranged from 3 to 500 Hz. The signal was dampened with -3 dB and filtered by a 50-Hz band-pass filter. AID-conversion was done every 0.6 msec, and then averaged across 20 data points. In this manner, the raw signal could be rectified and integrated across a time period of 12 msec. At a sampling frequency of 1 kHz, each 3-sec. interval was represented by 250 data points. Each contraction for respective replication was started by a computer-generated tone. Within the 3-sec, interval the subject had to activate the muscle selected. The onset of the 3-sec. time-course was triggered by the subject, i.e., the interval was started only if the muscle activation was above a predefined level of 240 msec. duration above the 1.5-fold baseline. During a muscle contraction, a maximum duration of 60 msec. below the 1.5-fold baseline was allowed. Measures.-For each activation three measures were calculated, i.e., duration, integral, and intensity (integral divided by duration) of activation. Proprioception (P) was defined as
with the numerator being the integral of the drfference between the contraction and the replication within the 3-sec. interval (to to t,), and the denominator being the mean of the integrals of the contraction and the replication. Each trial was performed 50 times per muscle. P will be zero, if activation and replication are identical. Minimal identity is shown by a P score which approximates 2, then the difference integral approximately equals the sum of the integrals. If the difference of the integral equals the mean of the integrals, the P score becomes 1. Analysis of data.-Analysis was performed on P scores using a two-way analysis of variance with repeated measures on the factors of muscle group (masseter, zygomatic) and experimental session (pretest, posttest). Also, Pearson correlation coefficients were computed between P scores and both intensity and duration of contractions. Table 1 shows the Pearson computations which had been performed between various difference scores on each trial and the means from contraction and replication of muscles and sessions, respectively. As it can be seen, the difference score, as well as the ratio and the relative difference of contraction and replication, are significantly correlated with descriptive parameters of muscle activation. Only the P score was not correlated with duration, in-
95
ASSESSMENT O F PROPRIOCEPTION TABLE 1 PEARSON CORRELATION COE~CIENT BETWEEN S DIFFERENTMEASURES OF RE.PLICATION ACCURACY AND D E S C ~ NPARAMETERS E OF MUSCLESTRENGTH Measures
Differencet
Diff.jDuratlon
Quotient
Quot,/Dura-
P Score
L I O ~
Integral Masseter Muscle Pretest -.I4 .92 .65 .59 .25 -.I9 Posttest .89 .80 .64 .40 Zygomatus Major Pretest .91 -81 .65 .30 .10 Pos ttes t .94 .73 .76 .42 .09 Duration Masseter Muscle Pretest .76 .05 .89 .17 .33 .62 .20 .83 .22 .12 Posttest Zygomatus Major Pretest .67 .31 .83 .22 .03 Posttest .60 .14 .88 .04 -.I4 Intensity Masseter Muscle .50 .85 .04 .25 -.37 Pretest Posttest .69 .84 .32 .35 -.31 Zygomatus Major Pretest .76 .88 .36 .24 .06 Posttest .85 .89 .50 .55 .20 *Integral oE differences between activation and replication; Diff./Duration =Difference divided by the muscle activation of longer duration; Quot./Duration =Quotient divided by muscle activation oE shorter length; P score see text; bold numerals = p < .01, italicized numerals = p < .05.
tensity, and the integral of either muscle or session. Thus, it seems to be an appropriate measure for myesthesia of either duration or intensity. Two-way analysis of variance with repeated measures gave a significant main effect for muscles (F,,,, = 9.00, pC.01) but not for sessions (F,,,, = .33, p < .57). No interaction could be detected (F,,,, = .75, p < .40). Table 2 shows higher P scores for the zygomatic muscle, indicating worse myesthesia in both sessions.. Post hoc analysis yielded a significant difference for the TABLE 2 MEANSAND STANDARD ERRORS OF P SCOREBETWEEN TWOSESSIONS AND Two MUSCLES ( N = 40) Muscle Masseter Muscle Zygomatus Major
Time Pretest Posttest Pretest Posttest
P Score M
SE
0.371 0.354 0.395 0.396
0.013 0.013 0.012 0.011
96
B. LEPLOW, ET AL.
second session (t = -2.89, p
Skills, 1992, 74, 91-98. O Perceptual and Motor Skills 1992
A N E W PROCEDURE FOR ASSESSMENT O F PROPRIOCEPTION ' BERND LEPLOW, VOLKERT SCHLUTER, ROMAN FERSTL Christian-Albrechts Universi!y
Summary.-A new method for the assessment of proprioception was developed and tested with 40 healthy subjects on two facial muscles (i.e., masseter and zygomatic muscles). The experiment was repeated after 3 % months. In our study, proprioceprion was studied with respect to sensations arising from the muscle spindles and tendon organs. Therefore, myesthesia was investigated, which was assessed by the correspondence between a voluntary muscle contraction and its immediate replication. Good perception was defined by a small integral of differences, standardized by duration and intensity of the contraction, and its replication. Results show that this measure is independent of the characteristics of muscle activation. In concordance with our hypothesis, myesthesia was superior in a muscle richly supplied with muscle spindles and afferent fibers (i.e., masseter muscle), to that for a muscle less prepared for afferent information processing (i.e., zygomatus major).
Perception of muscle activity is a frequent issue in applied psychophysiology, especially in closed loop theories of motor behavior (Adams, 1987), facial feedback theories of emotional expression (Levenson, Ekman, & Friesen, 1990), and theories of psychophysiological disorders, e.g., tension headaches (Haynes, Cuevas, & Gannon, 1982). In these paradigms, sufficient and accurate feedback from effector activity is crucial for effective attempts at self-regulation. The receptors for proprioception and myesthesia, respectively, are muscle spindles and tendon organs (DeJong, 1979). Perception of receptor activity can be assessed by methods of "magnitude estimation," "magnitude production," and "response discrimination " The magnitude estimation of muscle tension can be done by direct scaling of perceived muscle activity (Lehrer, Bateg, Woolfolk, Remde, & Garlick, 1988; Shedivy & Kleinmann, 1977). Recently, however, it has been questioned whether the mechanisms underlying such a matching between myesthesia and a rating scale are comparable to those in spontaneous muscle activity and its perception (Epste~n, 1990). Another method of estimating muscle tension requires the subject to attend to the muscle tension of an ongoing trial and to compare it to the most prior one. Within a biofeedback-paradigm, subjects had to estimate whether the actual tension was greater or smaller than that on the preceding trial (Kinsman, O'Banion, Robinson, & Staudenmayer, 1975; Staudenmayer & Kinsman, 1976). As under biofeedback, information about muscle tension can be either drawn from "true" myesthesia or from the biofeedback signal, Sime and deGood 'Address correspondence to Dr. B. Leplow, Department of Psychology, Christian-Albrechts University, Olshausenstrasse 61, W-2300 Kiel, F.R.G.
92
B. LEPLOW, ET AL
(1977) and Bayles and Clearly (1986) had circumvented this problem by s c h e d d n g separate trials, on which estimates had to be performed without the assistance of biofeedback. Furthermore, myesthesia has been assessed by the "magnitude production" method, where the subject has to activate a target muscle to certain percentages of either maximum strength (e.g., Bohannon & Endemann, 1989; Epstein, 1990), to predefined levels of muscle strength (Bayles & Clearly, 1986; Blanchard, Jurish, Andrasik, & Epstein, 1981; Epstein, 1990; Pollard & Katkin, 1984; Stilson, Matus, & Ball, 1980), or to the tension of the contralateral limb (Gandevia & Kilbreath, 1990). O n the contrary, on response-discrimination tasks subjects have to discriminate responses within a signal-detection paradigm. Subjects are either required to detect changes in training criterion (Jones & Dickson, 1978) or in the application of correct versus false feedback (Burnette & Adams, 1987; Leplow & Ferstl, 1990). As has been shown by Burnette and Adams (1987), the perception of false feedback is heavily influenced by extraneous variables. Similarly, we showed in a previous study that sensitivity scores were highly dependent on exteroceptive cues, whereas response bias was related to interoception (Leplow & Ferstl, 1990). Measurements of myesthesia then are related to very different functions. In the magnitude-estimation procedures, the subject has to perform quite a complex cognitive task of matching muscle tension against a rating scale or against an amount of perceived tension, remembered from a preceding trial. Within the magnitude-production paradigm, deficits in myesthesia may be due to dysfunctions of the direct, kinesthetic pathway or to deficiencies in the performance of the motor command. Response discrimination, however, can be biased by differences in use of supplementary feedback pathways or extraneous information. And, finally, all of these procedures are prone to inter- and intraindividual variations of attention-focussing processes. This study was designed to develop a method for the assessment of perception of facial muscle activity, which requires only minimal attention and memory load and which does not depend on subjective decision-making processes or compliance to external standards. Therefore, we requested the subjects to repeat single voluntary muscle contractions. Good myesthesia was operationally defined by a high correspondence between a contraction and its immediate replication. Intensity and duration of each initial muscle contraction could be chosen by the subject, so the subject did not have to match a physiological event against an external standard. By means of such a procedure, differences in perception across muscles should be mainly due to differences in afferent information processing, i.e., a physiological feedback mechanism. That means, in muscles richly supplied with muscle spindles and sensory
ASSESSMENT OF PROPRIOCEPTION
93
fibers, perception should be superior with respect to perception of contractions of muscles only less-well provided with muscle spindles.
Subjects Forty undergraduates, 22 women and 18 men, aged 20 to 40 years, served as subjects. Mean age was 24% yr., with 50% being between 20.7 and 27.6 years of age. All participants were volunteers and without medical complaints or medication. Procedure Study design.-A two-factor within-subject design was used, where perception of each subject was tested in two sessions 3.5 months apart and on both of two facial muscles, i.e., the zygomaticus major and masseter muscle on the dominant side. Handedness was assessed by carefully taking the subject's history with a standardized interview. The masseter muscle was chosen because it is known to be richly supplied with muscle spindles and afferent fibers from the mandibular branch of the trigeminal nerve (Rim, 1984). The zygomatic muscle, however, is innervated by the facial nerve, which is primarily motor and, therefore, less prepared for afferent information processing. Experimental sessions.-After subjects were briefed about the aim of the study, electrodes were attached. Subjects then learned selective contractions of the masseter and zygomatic muscles under the condition of visual feedback. Participants were advised to try different intensities and durations of activation. After about five minutes of practice, feedback was removed and the subject was advised that various muscle contractions had to be performed and that each contraction had to be repeated as exactly as possible. Although the exact time interval between a contraction and its replication could be chosen by the subject, the latency usually was between one and two seconds. Each pair, i.e., a muscle contraction and its replication, constituted one trial. Maximum duration of each contraction and its respective replication was limited to three seconds. O n e hundred trials had to be performed, in which the order of muscles was randomized. During the trials, no further instructions were given. Only at the beginning of the experiment had the subjects been advised that the amount of contraction had to be varied across trials. At the end of each trial knowledge of results was provided by means of graphic representations of the muscle contraction and its replication. Insh.umentation.-Facial electromyographic (EMG) responses were recorded using Ag-AgC1 Beckmann miniature electrodes and electrode placements as described by Fridlund and Cacioppo (1986). Skin was prepared as usual until resistance was below 10 kOhms. Recordings were done by means of a Langer, Inc. monitoring system and an Olivetti M24 computer. The band-
94
B. LEPLOW, ETAL.
width of the amplifier ranged from 3 to 500 Hz. The signal was dampened with -3 dB and filtered by a 50-Hz band-pass filter. AID-conversion was done every 0.6 msec, and then averaged across 20 data points. In this manner, the raw signal could be rectified and integrated across a time period of 12 msec. At a sampling frequency of 1 kHz, each 3-sec. interval was represented by 250 data points. Each contraction for respective replication was started by a computer-generated tone. Within the 3-sec, interval the subject had to activate the muscle selected. The onset of the 3-sec. time-course was triggered by the subject, i.e., the interval was started only if the muscle activation was above a predefined level of 240 msec. duration above the 1.5-fold baseline. During a muscle contraction, a maximum duration of 60 msec. below the 1.5-fold baseline was allowed. Measures.-For each activation three measures were calculated, i.e., duration, integral, and intensity (integral divided by duration) of activation. Proprioception (P) was defined as
with the numerator being the integral of the drfference between the contraction and the replication within the 3-sec. interval (to to t,), and the denominator being the mean of the integrals of the contraction and the replication. Each trial was performed 50 times per muscle. P will be zero, if activation and replication are identical. Minimal identity is shown by a P score which approximates 2, then the difference integral approximately equals the sum of the integrals. If the difference of the integral equals the mean of the integrals, the P score becomes 1. Analysis of data.-Analysis was performed on P scores using a two-way analysis of variance with repeated measures on the factors of muscle group (masseter, zygomatic) and experimental session (pretest, posttest). Also, Pearson correlation coefficients were computed between P scores and both intensity and duration of contractions. Table 1 shows the Pearson computations which had been performed between various difference scores on each trial and the means from contraction and replication of muscles and sessions, respectively. As it can be seen, the difference score, as well as the ratio and the relative difference of contraction and replication, are significantly correlated with descriptive parameters of muscle activation. Only the P score was not correlated with duration, in-
95
ASSESSMENT O F PROPRIOCEPTION TABLE 1 PEARSON CORRELATION COE~CIENT BETWEEN S DIFFERENTMEASURES OF RE.PLICATION ACCURACY AND D E S C ~ NPARAMETERS E OF MUSCLESTRENGTH Measures
Differencet
Diff.jDuratlon
Quotient
Quot,/Dura-
P Score
L I O ~
Integral Masseter Muscle Pretest -.I4 .92 .65 .59 .25 -.I9 Posttest .89 .80 .64 .40 Zygomatus Major Pretest .91 -81 .65 .30 .10 Pos ttes t .94 .73 .76 .42 .09 Duration Masseter Muscle Pretest .76 .05 .89 .17 .33 .62 .20 .83 .22 .12 Posttest Zygomatus Major Pretest .67 .31 .83 .22 .03 Posttest .60 .14 .88 .04 -.I4 Intensity Masseter Muscle .50 .85 .04 .25 -.37 Pretest Posttest .69 .84 .32 .35 -.31 Zygomatus Major Pretest .76 .88 .36 .24 .06 Posttest .85 .89 .50 .55 .20 *Integral oE differences between activation and replication; Diff./Duration =Difference divided by the muscle activation of longer duration; Quot./Duration =Quotient divided by muscle activation oE shorter length; P score see text; bold numerals = p < .01, italicized numerals = p < .05.
tensity, and the integral of either muscle or session. Thus, it seems to be an appropriate measure for myesthesia of either duration or intensity. Two-way analysis of variance with repeated measures gave a significant main effect for muscles (F,,,, = 9.00, pC.01) but not for sessions (F,,,, = .33, p < .57). No interaction could be detected (F,,,, = .75, p < .40). Table 2 shows higher P scores for the zygomatic muscle, indicating worse myesthesia in both sessions.. Post hoc analysis yielded a significant difference for the TABLE 2 MEANSAND STANDARD ERRORS OF P SCOREBETWEEN TWOSESSIONS AND Two MUSCLES ( N = 40) Muscle Masseter Muscle Zygomatus Major
Time Pretest Posttest Pretest Posttest
P Score M
SE
0.371 0.354 0.395 0.396
0.013 0.013 0.012 0.011
96
B. LEPLOW, ET AL.
second session (t = -2.89, p
