EXPERIMENTAL
NEUROLOGY
20, 135-142 (1968)
Effect of Different Frequencies of Vibration on Pain-Threshold Detection RICHARD
Second
The City (Cornell)
Received August
SULLIVAN
l
College of New York, and the Neurology Sem’ce, Bellewe Hospital New York, N.Y. 10016
28, revisiolc received September
29, 1967
Radiant-heat pain threshold judgments were obtained from human subjects while the stimulated region was simultaneously vibrated with one of three vibration frequencies. Threshold detection of pain was found to be a function of the frequency of applied vibration. The results are interpreted in terms of a current theory of pain reception. Introduction
Melzack and Wall (6) recently proposed a theory of pain reception based primarily on the differential effect of impulses arriving in the substantia gelatinosa and the first central transmission (T) cells in the dorsal horn from small C and large A peripheral fibers. The authors suggested that peripheral interference with pain reception may be accomplished by stimulating the receptor area with stimuli which alter the balance of activity in small and large fibers. According to the theory, tonically active small fibers reduce an inhibitory influence of the substantia gelatinosa on T-cell transmission while relatively inactive large fibers tend to increase the inhibitory effect of the substantia gelatinosa. Melzack and Wall (6) claimed that the factor which initiates a pain reaction in the action system responsible for the experience of pain is the characteristic of impulses transmitted from the T cells. Since the nature of impulse output from the T cells is modulated by the substantia gelatinosa, the authors labeled it as a gate-control system in pain reception. According to the model, when a stimulus of low intensity is applied to the skin surface the large fibers transmit a burst of impulses to the substantia 1 The author expresses appreciation for Lawrence Mark’s aid in the experiment and Dr. Fletcher McDowell’s comments on the manuscript. Author’s present address: Pain Study Group, Department of Medicine, New York University Medical Center, 550 First Avenue, New York 10016. 135
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gelatinosa and the T cells. Since large-fiber activity tends to close the gate-control system, after the initial burst, no further impulse passage occurs until small fiber activity increases to a level which reduces the inhibitory effect of large-fiber activity. Increasing the intensity of the stimulus both increases small-fiber activity and the adaptation rate of large fibers. Consequently, the gate-control system gradually opens permitting the heightened activity arriving at the T cells to be transmitted to the action system. Since it is the relative rate of activity in the small and large fibers which determines the nature of impulse transmission to the action system, an increase in large-fiber activity could offset an increase in smallfiber activity caused by an increase in stimulus intensity. Melzack and Wall (6) suggested that stimuli which effect large-fiber activity and vary in terms of their spatiotemporal patterning would be most effective in altering pain reception. Supportive evidence for the theory is found in the work of Wall and Cronly-Dillon (12) who found evidence on both the behavioral and neurophysiological levels that the detection of itch, warm, electric shock, and radiant-heat pain stimuli was altered when the cutaneous area being stimulated was surrounded by vibration. Similar results with noxious stimuli were reported by Melzack et al. (7) and Melzack and Schecter (8). The reported findings were obtained using a single frequency of vibration. In an attempt to reduce the pain emmanating from neuromas Russell and Spalding (10) applied repeated percussion of differing frequencies to the limb stumps of amputees. While some patients reported relief others reported that the percussion increased the pain. It is not clear whether different frequencies of vibration obtained different reports. Wall and Cronly-Dillon (12) suggested that vibration may reduce the effect of low-intensity pain stimuli but increase the effect of high-intensity pain stimuli. It is also possible that with low-intensity pain stimuli, differing frequencies of vibration applied to an area receiving noxious stimulation would obtain different values of threshold-pain detection. The present experiment was designed to determine whether each of three vibration frequencies applied simultaneously to an area of the forearm being stimulated with radiant heat would have a differential effect on the ability of subjects to detect a pain threshold. Method
Ten male undergraduate students (ages B-22) from an experimental psychology course at the City College served as subjects. The area chosen for stimulation was the dorsal surface of the forearm approximately midway between the elbow and the wrist.
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The setting for the experiment was a darkened lab room kept at a temperature of 23-25 C. The subjects were blindfolded and seated with their right side to a table upon which was placed the vibration and pain apparatus. Vibration was applied by using an apparatus consisting of a rectangular box (53 X 17.5 X 15 cm) constructed of Plexiglass on the sides and top to afford a view of arm placement within the box. Inside the box were two adjustable plates used to raise or lower the subject’s arm to ensure that a constant distance was maintained between the skin surface and the vibrating annulus. The subject’s arm was fitted into a troughlike arrangement on the first plate and his right hand was held in place by use of a padded clamp attached to the second plate. Both fittings served to reduce extraneous arm movement during stimulation. Directly below the hand clasp on the floor of the box was a button in circuit with a clutch-driven clock and the radiant-heat apparatus. By moving his index finger on and off the button the subject started and stopped the clock and the radiantheat stimulation. Vibration was applied to the skin surface through a metal plate positioned above the midline of the upper surface of the forearm. The vibratory ring was constructed of aluminum and had a brass plate (12.5 cm2) affixed to its underside. It was the brass plate that was in contact with the skin surface. Both fixtures had apertures of 25 cm’ cut from their centers. It was through the aperture that the radiant heat was applied to the skin surface, The annulus was attached at each side to rods which were connected to an eccentric cam fitted to a O.l-hp motor. The vertical peak-to-peak distance traversed by the moving ring was 4.8 mm. The motor was in circuit with a variac. By altering voltage movement of the cam, frequency of vibration was varied (maximum, 58 cycle/set). Calibration of the experimental frequencies of 15, 30, and 45 cycle/set was done with a strobe light. The vibration apparatus rested on four legs which in turn were placed on springs fitted on S-cm rubber casings and positioned snugly into hardrubber bases. To reduce the effect of extraneous vibration, all mountings had rubber casings and the entire ensemble rested on a sponge-rubber bed which was clamped to the table. To reduce the noise of the motor and cam action, subjects wore disconnected earphones during all trials. The radiant-heat source was the Hardy-Goodell-Wolff (5) Dolorimeter.Z Basically, this consists of a SOO-watt bulb, a variac transformer and a calibrated voltmeter. The bulb is within a gunlike fitting and was placed through an opening in the top of the vibratory box immediately above the aperture in the vibratory ring. The distance between the tip of the 2 Williamson
Development Co.
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gun and the skin surface was kept constant at 32 mm. The timing device on the Dolorimeter was in circuit with the subject button. For practical reasons the method of radiant-heat stimulation used in the present experiment consisted of keeping the output of the Dolorimeter set at 75 meal/ sec/cm2 and allowing time to vary. The present method is similar to that used by Berlin ef al. (1) in their study of the radiant-heat pain threshold. Procedure. The subjects were told that the experiment dealt with the ability of people to detect a minimal or threshold heat pain with and without masking stimulation. After coating the skin with burnt cork the subject’s arm was placed in the vibration box and clamps adjusted so that the annulus in the down position rested on the skin surface. A single frequency was presented to the subject to ensure that he felt the tap of the brass plate on the skin surface. Using grids on the side and top of the vibration box the subject’s arm placement was measured to establish the same approximate area as that receiving the stimulation on subsequent occasions. The subjects were instructed in the use of the button and reminded that the experiment dealt with minimal pain-threshold detection. They were also informed that threshold pain often followed a period of undulating warmth after which an itch or sharp prick sensation was experienced followed by a sharp increase in the heat sensation. Threshold pain, they were told, was likely to be the itch or sharp prick sensation. All subjects received ten practice trials with radiant-heat stimulation, after which they received 15 set of vibration at each of the three experimental frequencies. No subject reported being bothered by the vibration stimulus. On five subsequent occasions radiant-heat pain thresholds were determined in the following order: without vibration ; with vibration frequency set at 4.5 ._+ 8 cycle/set ; with vibration frequency set at 15 k 3 cycle/set ; with vibration frequency set at 30 -+ 5 cycle/set; and with vibration set at 45 cycle/set but with the vibratory ring removed. The last condition was used as a control for both practice effects and the effects of extraneous vibration on judgment. Five trials were given under each of the five conditions. A single trial began when, upon signal, the subject removed his finger from the button starting the radiant heat and clock; it ended when he placed his finger on the button. During vibration trials the motor was turned on immediately prior to the signal being given to the subject and stopped immediately after the clock had stopped. A rest of 2 mm was given between all trials. Since the subject denoted his threshold by pressing a button which stopped the clock the response measure was duration or length of detection time.
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Results
Mean pain threshold detection times under the five conditions are plotted in Fig. 1. Inspection of individual subject plots indicated no essential difference with the mean plot. As witnessed in the graph an increase in the frequency of vibration applied to the area receiving radiant-heat stimulation led to an increase in the length of time necessary to detect threshold pain. The result of a “Treatment by Subjects” 3 analysis of variance of the data is presented in Table 1. While the ordering of conditions was manipulated in the experimental design to reduce the possible effects of an ordinal set in the judgment of pain thresholds, the effects of order and sequence may have contributed to the treatments mean square. However, 3 Lindquist, E. F. 1953. “Design Education,” Houghton, Boston.
5 s 0 t E w I +
and Analysis of Experiments
in Psychology
and
32 _ 30_ *8_ 26-
8 E
24-
-
j
22:
I
20-
! E
1817 I CONDITION
I
I
I
I
I
II
III
Ip
Y
times under the five conditions : I. no vibraFIG. 1. Mean pain-threshold-detection tion; II. extraneous vibrations ; III. vibrations at 15 ; IV. 30; and V. 45 cycle/set. TABLE
1
ANALYSIS OF VARIANCE OF RADIANT-HEAT PAIN THRESHOLD UNDER FIVE TREATMENT CONDITIONS
Source Treatments Subjects Interaction Total
(conditions) (T
x
aError term for MS. *p<.OO1.
S)
df
MS
F
4 9 36 49
lJ61.2 85.2 6.8a
156.0* 12.5
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the absence of an ordinal presentation of vibration frequencies and the level of significance obtained (F, 4, 36, =156.0, p < .OOl) suggest that the differences are not likely due to the effects of either order or sequence. A t-test for dependent samples between mean detection time without vibration and with extraneous vibration (Condition I vs. II) was found to be insignificant (t = .58. p > .50). Discussion
The results confirm previous reports (7, 8) of a change in the detection of low-intensity pain stimuli when the stimulated area is simultaneously surrounded by vibration. The present results further indicate that different frequencies of vibration have a differential effect in altering threshold values of radiant-heat pain. While the instructions to the subjects may have implicitly suggested that the vibration would “mask” the pain stimulus. there was no suggestion given that would imply that each frequency of applied vibration would have a differential effect on pain-threshold detection. Consequently, it is unlikely that the differences in threshold pain found for each frequency of vibration were due to suggestion or the distracting nature of the vibration stimulus. While inspection of the individual plots indicated that subjects reacted differently to the vibration, introspective reports of the subjects suggest that the threshold sensation of pain was the same regardless of condition. The lack of a significant difference between thresholds obtained during the first and fifth sessions further suggests that the subject’s criterion for judging threshold pain was relatively consistent and stable. Simultaneous vibration of a skin surface seems to be an effective means of altering pain detection when the frequency is below approximately 50 cycle/set and the pain stimulus is of low intensity. While the curve in Fig. 1 suggests the possibility of a linear relationship frequency of vibration and increase in pain threshold such an interpretation would be invalid since it is unlikely that the relation between Dolorimeter output and skin temperature is linear ( 11). Other reasons for not interpreting the curve in Fig. 1 relate to the variance inherent in the applied frequencies, the limited range of frequencies used, and the lack of control over the spread of vibration below the skin surface. Indeed, the uncontrolable variance within a given frequency may have fortuitously contributed to the over-all significance of the results. A steady nonvarying vibratory stimulus may not have been as effective as the stimulus used in the present study. As Melzack and Wall (6) have suggested, the most effective stimulus for altering reception of pain stimuli would be one which varied in its spatiotemporal patterning. According to the theory a stationary wave pattern would increase the adaptation of the large fibers
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and thereby allow the gate-control system to pass activity arising from noxious stimulation. By implication it is also possible that stimulus waves of high amplitude or frequency would enhance the pain reaction. Limitations in the design of the present apparatus did not permit the testing of the possibility that higher frequencies would, perhaps, lower the radiantheat pain threshold. However, it was noted in the subjective reports of sensation arising from stimulation with the 4.5 cycle/set stimulus that the tapping was felt in a broader and deeper location than that experienced with the other frequencies. It is possible that vibratory stimuli of higher frequencies than those used in the present experiment would set off patterns of impulses in fibers which would not transmit at lower frequencies. The recent findings of Mountcastle et al. (9), suggesting the existence of flutter-vibration mechanoreceptors which respond to a range of frequencies of Z-300 cycle/set, are of interest with respect to both the present findings and those of the Wall and Cronly-Dillon (12). Mountcastle et al. (9) reported that the detection of oscillation on the skin surface appears to be subserved by at least two sets of class-A afferent fibers. From psychophysical and neurophysiological observation they proposed that the derma1 ridges are innervated by fibers respondent to frequencies within the approximate range of 2-40 cycle/set and that the deeper tissues are innervated by fibers respondant to frequencies of approximately 40-300 cycle/set. An overlap in responding occurs in the approximate range of 40-50 cycle/set. As reported by subjects in the present experiment, Mountcastle et al. (9) found that above 60 cycle/set subjects experienced the vibration as being deeper and less readily localized. The interference effects of vibration suggested by Melzack and Wall (6) may be restricted, therefore, to stimuli selectively effecting large fibers which innervate the dermal ridges. Mountcastle et al. (9) findings may also support Wall and Cronly-Dillon’s (12) suggestion that higher frequencies of vibration enhance the pain reaction. In view of the findings of Mountcastle et al. (9) the theory of Melzack and Wall (6) would have to be modified to include the difference in stimulation of different layers of the skin of the gate: control system. In a previous study 4 of psychophysical judgment of the critical flutter fusion (CFF) threshold, using the same apparatus as. described herein, the mean threshold value was found to be 37.5 cycIe/sec “(range 2S,4-44.5) lor stimulation of the upper forearm in 18 subjects. Two other subjects did not report a CFF and it was assumed that their threshold was above the limiting frequency of approximately 58 cycle/set. For the other subjects the range of frequencies wherein an experience of vibration changes 4 Sullivan, R., R. Giordano, and G. Haas. 1965. “Critical Vibratory Stimulus.” Unpublished manuscript.
Flutter
Frequency of a
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to one of a constant wavelike movement below the skin surface is close to the range found by Mountcastle et al. (9) as being the range of overlap between the two sets of afferent flutter receptors. The range of CFF values obtained for the subjects suggests that the variables of skin texture and, perhaps, thermal- and tactile-receptor differences effect individual judgment of oscillation or vibration in psychophysical tasks. Geldard (2-4)) for example, in reviewing the psychophysical evidence of a separate sense of vibration, has argued that the appreciation of oscillation on the skin surface is served by pressure receptors which are differentially effected by the spread of stimulation. The findings of Mountcastle et al. (9) warrant a closer inspection of psychophysical judgment around the range of 40-50 cycle/set. The practical aspects of such research would be to determine whether impairment in either set of fibers could be ascertained on the behavorial level of observation. Impairment in either or both sets of fibers may considerably alter the reception and transmission of pain impulses. The spatiotemporal pattern of stimuli effecting an area receiving noxious stimulation may determine whether the pain experience is one of “aching” or of a sharp-pricking type. References
1. BERLIN, L., GOODELL, H., and H. G. WOLFF. 1958. Studies on pain. A.M.A. Newel.
Psychiat.
Avch.
80: 533-543.
2. GELDARD, F. A. 1940. The perception of mechanical vibration. I. History of a controversy. .I. Gen. Psychol. 22: 243-269. 3. GELDARD, F. A. 1940. The perception of mechanical vibration. II. The response of pressure receptors. J. Gee. Psychol. 22: 271-280. 4. GELDARD, F. A. 1940. The perception of mechanical vibration. IV. Is there a separate “vibratory sense”? J. Gen. Psychol. 22: 291-308. 5. HARDY, J, D., H. G. WOLFF, and H. GOODELL. 1940. Studies on pain; a new method for measuring pain threshold: Observations on spatial summation of pain. J. Clin. Invest. 19: 649-657. 6. MELZACK, R., and P. D. WALL. 1965. Pain mechanisms: A new theory. Science 15Q: 971-978. 7. MELZACK, R., P. D. WALL, and A. Z. WEISZ. 1963. Masking and metaconrast
phenomena in skinsensorysystems.Exptl.
Neurol.
8: 35-45.
8. MELZACK, R., and B. SCHECTER. 1965. Itch and vibration. Science 147: 10471048. 9. MOUNTCASTLE, V. B., W. H. TALBOT, I. DARIAN-SMITH, and H. H. KORNHUBER. 1967. Neural basis of the sense of flutter vibration. Science 155: 597-600. 10. RUSSELL, W. R., and J. M. K. SPALDING. 1950. Treatment of painful amputation stumps. Brit. Med. J. 2: 68-73. 11. SWEET, W. H., 1959. Pain, pp. 459-506. Iu “Handbook of Physiology,” sec. 1, “Neurophysiology,” vol. 1. J. Field, H. W. Magoun, and V. E. Halls reds.], Am. Physiol. Sot., Washington. 12. WALL, P. D., and J. R. CRONLY-DILLON. 1960. Pain, itch and vibration. arch. New-01. 2: 365-375.