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Skin sensitivity to thermal stimuli
EXPERIMENTAL
NEUROLOGY
6,
300-314
(1962)
Skin Sensitivity R. MELZACK, Psychology
Section
to Thermal
G. ROSE,
and Research Laboratory of Technology, Cambridge, Received
June
AND
of
D.
Stimuli
MCGINTY~
Electronics, Massachusetts
Massachusetts
Institute
7, 1962
Distribution patterns of cutaneous thermal sensitivity in human subjects were studied by mapping large areas of skin with stimulators the tip temperatures and diameters of which were controlled. The maps show that skin sensitivity to cold and warm stimuli is distributed in the form of large sensory fields rather than isolated “spots.” These sensory fields have a variety of sizes and shapes. Generally, they consist of highly sensitive areas, ranging in size from 6 cm2 to spot-like peaks, surrounded by larger, less sensitive regions. Moreover, there are persistent fluctuations of thermal sensitivity in successive maps of the same area of skin. Fluctuation usually took two forms: marked changes primarily at the boundaries of the sensory fields; and “fragmentation” and “coalescence” of the fields themselves. It was also observed that small, warm stimuli produce frequent reports of pricking, stinging sensations at temperatures that evoke pleasant warmth when applied normally to large areas of skin. This observation suggests that the spatial properties of warm stimuli play an important role in determining the quality of cutaneous experience. Introduction
The traditional view of thermal sensitivity of the human skin is that it consists of a mosaic of “cold spots” and “warm spots.” This belief, which originated with Blix (2), Goldscheider (7), and Donaldson (4), is the basis of von Frey’s (5) classic theory of cutaneous sensation. It assumes that a single specific receptor lies beneath each sensory “spot” on the skin. It assumes, moreover, that there is a one-to-one relationship between the receptor and the quality of sensation projected by the nervous system onto the “spot” of skin above it (see 17). The “skin spot” thus 1 This work was supported in part by the U.S. Army Signal Corps, the Air Force Office of Scientific Research, and the Office of Naval Research, and in part by the National Institutes of Health (grant M-4235Cl). We wish to thank Mr. H. Rosenthal and Mr. R. Swanson for their assistance in the experiment. Mr. Rose is now at the Psychology Department, University of California at Los Angeles; Mr. McGinty, at the Psychology Department, University of Pennsylvania. 300
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SENSITIVITY
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plays a fundamental role in current concepts of skin sensory mechanisms since it is widely believed to be the basic unit for cutaneous sensation. Recent studies of skin sensory mechanisms argue strongly against the traditional view. Jenkins (12, 13, 14) has provided convincing psychological evidence that “spots” do not represent a true picture of the distribution of thermal sensitivity. The characteristic feature of his maps are “gradients of sensitivity”-highly sensitive areas surrounded by regions of decreasing sensitivity. Similarly, recent physiological data (1, 10, 11, 16, 19, 20) demonstrate that a given area of skin is innervated by widelybranching nerve endings of numerous fibers, whose receptive fields are of varying size and overlap extensively. Spotlike innervation is the exception rather than the rule (10, 11)) and even then, the spots are embedded in larger receptive fields. The psychological and physiological data thus suggest that the “skin spot,” once believed to represent a single specific receptor lying beneath it, is the result of the ability of the central nervous system to integrate the impulses of many fibers having overlapping receptive fields. This picture of skin sensory mechanisms is complicated still further by the fact that there is never perfect correspondence among maps of thermal sensitivity of the same area: Many spots fail to respond on successive examinations while new spots frequently appear (3). That these fluctuations of thermal sensitivity represent a basic biological phenomenon has been proposed by Waterston (21, 22). He observed that an area of skin made anesthetic by nerve or spinal injury does not have a fixed margin, but a zone of varying width in which sensitivity fluctuates from one examination to the next. He found similar fluctuation at the margin of areas of hyperalgesia. Waterston argued on the basis of the experimental and clinical evidence that there is a constant coming and going of activity of different parts of the skin so that onIy a small portion of the sensory surface is active at any one time. It is astonishing that the work of Jenkins and Waterston has been virtually forgotten during the past quarter-century, while the traditional concept of a static, punctate skin sensitivity has been perpetuated. Indeed, there have been few recent studies of thermal sensitivity of human skin even though the physiological evidence of overlapping receptive fields suggests that thermal sensitivity may be distributed in the form of large sensory fields rather than isolated spots. The purpose of this study is to investigate the distributions of sensitivity to warm and cold stimuli in
302
MELZACK,
ROSE,
AND
MC
GINTY
large areas of skin so that evidence of overlapping receptive fields and their properties might become manifest. Methods
Areas ranging in size from 20 cm2 to approximately a quarter of the back were mapped with stimulators whose tip diameters and temperatures could be varied. Most of the maps of cold sensitivity were made with a copper rod that had a tip diameter of 2.5 mm and which extended into a large test tube containing crushed ice. The test tube was covered with thick asbestos insulation, painted with rubber cement and was closed with a rubber stopper holding the copper rod. Calibration of the tip with a thermocouple and temperature measuring device showed a temperature of 10 & 1 C. Fresh ice was placed in the test tube approximately every 1.5 min to prevent fluctuation of the stimulus temperature. Additional experiments of sensitivity to cold were carried out with a “thermovari-probe” apparatus ( 15)2 which permitted even more precise control over the stimulating temperature. The subjects were twelve male and five female students and technicians between the ages of 18 and 25. Aftera series of preliminary test trials with the cold stimulus, a grid with cross-section lines 5 mm apart was stamped on the back of the hand, on the forearm or on the back. An identical grid was stamped on a sheet of paper and the subjects’ reports of intensity of perceived cold were recorded in the corresponding area. The subjects were asked to report their perceptions by using the following scale: 0 = touch, no cold; I = mild cold; 2 = moderate cold; 3 = strong cold. The stimulus was moved randomly from area to area within the grid and the subjects’ reports were recorded. They were unable to see where the stimulus was being presented. It was applied lightly to the skin for approximately 0.5 set and presentations were separated by about S-set intervals. Pressures and durations varied slightly on a random basis from spot to spot, but were well within the limits found by Heiser (8) and Heiser and McNair (9) to have negligible effects on maps of skin sensitivity. The experiments on fluctuation of skin sensitivity were usually carried out in an air-conditioned room after the subjects had been exposed to 2 We are grateful to Dr. lending us this apparatus.
P. P. Lele
of the Massachusetts
General
Hospital
for
SKIN
SENSITIVITY
303
the room temperature for at least an hour. A grid of 5 X 5 cm was chosen to study fluctuation because it could be mapped in a reasonably short time (about 20 min), yet was large enough to permit the appearance of at least portions of large sensitive fields. Most maps of warmth sensitivity were made with thermal probes connected to the ‘Lthermo-vari-probe” machine. Some were made with a copper rod that extended into a test tube filled with warm water. The procedure was similar to that used for the cold mapping, except that S-mm diameter tips were generally used and the subjects were asked to report perceived warmth intensity on a scale of 0, 1, 2, 3, comparable to that used for cold. In addition to reports of sensory intensity, notes were also made of the subjects’ difficulties with the scale and their description of the perceptions were recorded in detail. Results
Stinging Pain Produced by Small Warm Stimuli. It became clear at the outset that small warm stimuli, ranging in temperature between 42 and 44 C, produce persistent reports of pricking or stinging pain. Tips of l-mm diameter, within this temperature range, frequently elicit sharp pricks. Larger tips of 2.5 and 5 mm often produce stinging pain. Some of the subjects actually objected that they were being jabbed with a pin, although they were being stimulated as gently as possible with the warm flat tip. Even with tips as large as 10 mm, there were reports of burning, stinging sensations, although immersion of the fingers or the whole hand in water within this temperature range was perceived unequivocally as pleasant warmth. For some of the subjects the frequency of reports of sting decreased as the tip diameter increased. Nevertheless, reliable scaling turned out to be a difficult task. Although the subjects scaled their perceptions as 0, f, 2, 3, many of them reported that they used the following criteria: 1 meant sting alone or more sting than warmth, 2 was warmth or more warmth than sting, and 3, stinging warmth or hot. The map of warmth sensitivity presented below is based on these criteria. Taking these limitations into consideration, the general principles of sensitivity distribution for warmth appear to be essentially similar to those for cold. These difficulties were not encountered with the cold stimuli. Cold applied with small-diameter tips were perceived as having a “natural” quality, without any biting, painful concomitants, even with temperatures
304
MELZACK,
ROSE,
AND
MC
GINTY
as low as 10 C. With a tip diameter of 2.5 mm, the perceptions varied primarily in intensity and the subjects had little difficulty in making the intensity judgments. There were marked individual differences among observers, however. A few failed to develop the ability to scale their thermal perceptions, while some learned to do so only after a few initial stimulations. Most of the observers acquired confidence in their judgments only after one or more complete maps had been made. The results described below were found in all observers who developed confidence in their ability to scale their perceptions of the cold and warm stimuli. Patterns of Skin Sensitivity to Small Thermal Stimuli. More than a hundred maps of various sizes were made of distributions of cold sensitivity on the back of the hand, on the upper forearm and on the back. Figure 1 shows a map of cold sensitivity made on approximately a quarter of the back. The salient feature of all the maps is that they contain one or more large sensitive areas stimulation of which produce reports of strong cold, surrounded by less sensitive areas that elicit moderate and mild cold. The characteristics of these sensitive areas are observed clearly only when maps are made of sufficiently large areas of skin. They demonstrate that the thermally-sensitive surface of the skin consists of large fields having a definite circumscribed area with distinct boundaries. Since the size of some of these fields is larger than the total areas of the maps made by earlier investigators, it becomes obvious why they have not been found in previous studies. When the relative frequencies of 0, 1, 2, 3 are viewed in the perspective of the whole map, it is seen that the areas that fail to elicit reports of cold are small and few in number. Large insensitive regions are rare (Fig. 3, right). Moreover, isolated sensitive spots are infrequent, although there are pointlike peaks of sensitivity lying within a large sensitive field. Maps of sensitivity to warm stimuli, obtained from the back and other areas of the body (Fig. 2), show large sensitive fields having the same variety of sizes and shapes as those observed for cold. When the same area is mapped for sensitivity to both cold and warm stimuli, however, the two distributions are always found to be different. Portions of the sensitive fields in the two maps often overlap, but there appears to be no systematic relationship between the two distributions.
B
STRONG
COLD
%i MODERATE tti
MILD
0
TOUCH,NOCOLD
\
COLD
COLD
FIG. 1. Distribution of cold sensitivity of approximately a quarter of the back. The position and size of the area tested is drawn in the lower right corner. The sensitivity distribution was mapped with a round stimulator tip 2.5 mm in diameter at a temperature of 10 C. The cold intensities reported by the subject are represented by different shades of stipple. 305
306
MELZACK,
ROSE,
AND
MC
GINTY
Fluctuation of Thermal Sensitivity Distributions. Fluctuation of sensitivity in successive maps of the same area generally took two forms: (a) marked changes that occurred primarily at the boundaries of the large sensory fields while the central portions remained stable, and (b) “fragmentation” and “coalescence” of sensory fields, forming new distribution patterns that remained in the same general portion of the map.
FIG. 2. Distributions upper left, cold sensitivity; area tested. Tip diameter:
of cold and warm sensitivity in the same area of skin: lower left, warm sensitivity; right, location of the forearm 2.5 mm. for both maps. Intensity scale: see Fig. 1 and text.
(a) Typical maps of fluctuation at the boundaries of sensitive fields are shown in Fig. 3. Figure 3 (left) illustrates the most commonly observed changes. Despite fluctuation, the two successive maps of cold sensitivity remain strikingly similar. An opportunity to observe these changes in greater detail is provided by the maps in Fig. 3 (right) in which a large area of skin that is insensitive to cold permits clear visualization of the boundaries of the sensitive regions. (b) The second major form of change observed in successive maps of the same area is the “fragmentation” and “coalescence” of sensitive areas, shown in Fig. 4. Three maps of cold sensitivity (Fig. 4, left) were
SKIN
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307 *
made in the morning and three (Fig. 4, right) were made 4 hours later. The maps made in each session were separated by lo-min intervals. It is seen that the sensitive fields in the upper right-hand corner fluctuate from map to map, producing continually-changing patterns. Nevertheless,
FIG. 3. Fluctuation of cold sensitivity: changes at the boundaries of sensory fields. Left, two successive maps based on the cold intensity scale shown in Fig. 1. Right, two maps from another subject based on reports of “cold” (stipple) or “no cold” (white areas). Each map was completed in approximately 20min; ZO-min interval between two successive maps.
the distribution of sensitivity to cold remains in the same general area in all the maps. Effects of Adaptation on Thermal Sensitivity Distributions: Intermittent Point Stimulation. The following procedure was carried out to study the
effects of repeated, brief stimulation on the distribution patterns of cold sensitivity: First a cold map was obtained in the usual way; then three
e 308
MELZACK,
ROSE,
AND
MC
GINTY
“simultaneous maps” were made in which each point was stimulated three times at approximately 20-set intervals; a final cold map was then obtained using the normal procedure.
FIG. 4. Fluctuation of cold sensitivity: sensory fields. Left, three successive maps of the same area made 4 hours later. Intensity
“fragmentation” and “coalescence” of made in the morning; right, three maps scale: see Fig. 1.
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Maps obtained with this procedure are shown in Fig. 5. The general effect of brief, intermittent stimulation was to produce a widespread reduction in sensitivity. An examination of the changes in the “simultaneous” maps (Fig, 5, lower) shows the progressive lowering of sensitivity during the test. However, the distribution of cold sensitivity in the final conventional map (Fig. 5, upper right) has some similarities to the first map (Fig. 5, upper left) despite the over-all increase in the reports of mild cold.
FIG. 5. Sensitivity reduction brought about by brief, intermittent stimulation. maps in which each Upper left, conventional cold map. Lower, three “simultaneous” point was stimulated three times in succession at approximately to-set intervals. Upper right, final conventional cold map. Stimulus diameter: 2.5 mm. Intensity scale: see Fig. 1.
Effects of Adaptation on Thermal Sensitivity Distributions: Continuous Whole-Area Stimulation. To study the effects of continuous cold stimulation on sensitivity distributions, two successive maps were obtained, and a cellophane bag of ice and water was placed over the area for ten minutes before a third map was made. A cellophane bag of hot water was similarly used to study the effects of continuous warmth stimulation on the sensitivity distribution to cold stimuli. Figure 6 (left) shows the effects of continuous cold stimulation on the distribution of cold sensitivity. It tended to produce a marked narrowing
. I
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.. .. . .. .
. .. ., .. .. ... ... ..
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of the sensory fields, together with an over-all reduction in sensitivity. Warming the skin had the opposite effect of increasing its sensitivity to cold. The effect in Fig. 6 (right) is small, but was found consistently in all experiments. The effects of intermittent and continuous stimulation on warm maps produced equivocal results. Eflects of Stimulus Temperature on Thermal Sensitivity Distributions. Figure 7 shows that as stimulus temperature decreases, the regions sensi-
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FIG. 7. Orderly increase in size of cold sensory fields brought about by decreasing stimulus temperature. Left, map obtained with a stimulus temperature of 18 C. Right, map of same area with stimulus temperature of 16 C. Tip diameter: 2.5 mm. Intensity scale: see Fig. 1.
tive to cold tend to increase was obtained with a stimulus stimulus 2 degrees colder. It not appear randomly across already found to be present.
in size in an orderly manner. Map 7 (left) temperature of 18 C, and 7 (right) with a is seen that the newly-responsive areas do the map, but adjacent to sensitive areas
The picture of skin sensitivity suggested by this study stands in marked contrast to the traditional view. The results show (a) that skin sensitivity to cold and warm stimuli is distributed in the form of large fields rather than spots, (b) that there is a persistent fluctuation of sensitivity in successive maps of the same area, and (c) that the spatial properties
312
MELZACK,
ROSE,
AND
MC
GINTY
of warm stimuli play an important role in determining the quality of cutaneous experience. The maps of large sensory fields confirm and extend Jenkins’ (12,13, 14) observations of “gradients of sensitivity.” The small area covered by his maps, however, precluded the finding of definite, circumscribed regions. Their presence becomes strikingly clear when maps are made of areas as large as a quarter of the back. Figure 1 exhibits some of the variety of sizes and shapes of the sensitive fields of the skin, ranging from spotlike peaks within larger, less sensitive fields, to regions of peak sensitivity having an area greater than 6 cm2 (which is the entire area of Jenkins’ usual maps). These observations of large sensitive fields, obtained with psychological testing methods, are consistent with the physiological data showing overlapping receptive fields in the skin. It is clear that the sensory fields found in this study do not represent a single receptive field. Successive maps show that these large sensory fields may “fragment” and “coalesce,” producing a number of different patterns of sensitivity distribution. It seems likely that these sensory fields represent many smaller receptive fields overlapping one another. These data provide only indirect evidence regarding cutaneous receptor units; but they demonstrate that the thermally sensitive areas of the human skin tend to consist of large fields such as we would expect from the recent physiological data, but not from the concept of isolated, randomly distributed receptors. The mechanisms underlying the persistent fluctuations in thermal sensitivity are unknown. They may be due to change in transmission capacity’ at one or more relays in the central nervous system, possibly brought about by stimulation of inhibitory areas in the course of mapping (IS), or to continuous changes in receptor sensitivity brought about by a continually changing blood flow in the skin capillary beds (see 6, 21). The results (Figs. 5 and 6). show, however, that the act of stimulation itself, at a given moment, determines the sensitivity of the area to subsequent stimulation. But the cause of this “adaptation,” whether neural or circulatory, is also unknown. Whatever the mechanism, it is clear that continuous changes in the distribution of skin sensitivity could prevent total adaptation in peripheral and central neurons, so that information . would be transmitted from the skin to the central nervous system at all times. Perhaps the most surprising result in this study in the difference in
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effects produced by small cold and warm stimuli. While cold felt “natural” regardless of stimulus size, the small warm stimuli produced anomalous pricking, stinging sensations at temperatures that evoke pleasant warmth when applied normally to large areas of skin. These difficulties encountered with small warm stimulators underscore the artificiality of our present methods for studying skin sensitivity. More important, however, is the implication that, for warmth at least, the “spot” is not the basic unit of skin sensation. The “punctate” concept presumes that the qudity of sensory experience is independent of stimulus size. The results show that this is not the case; rather, they support the view that the spatial properties of the stimulus play an important role in determining the quality of cutaneous experience ( 17). References 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.
12. 13. 14. 15.
G. H. 1944. The peripheral unit for pain. J. Newophysiol. 7: 71-80. M. 1884. Experimentelle BeitrLge zur Losung der Frage iiber die specifische Energie der Hautnerven. Z. Biol. 20: 141-156. DALLENBACR, K. M. 1927. The temperature spots and end-organs. Am. J. Psychol. 39: 402-427. DONALDSON, H. H. 1885. On the temperature sense. Mind 10: 399-416. FREY, M. VON. 1895. BeitrIge zur Sinnesphysiologie der Haut. Bev. kgl. siichs, Ges. Win., math.-phys. Kl. 47: 166-184. “The human senses.” Wiley, New York. GELDARD, F. A. 1953. GOLDSCHEIDER, A. 1884. Die specifische energie der temperaturnerven. Monatsschr. prakt. Dermatol. 3: 53-76. HEISER, F. 1937. Stimulus-duration and sensations of warmth. tlm. J. Psychol. 49: 58-66. 1934. Stimulus-pressure and thermal sensation. HEISER, F., and W. K. MCNAIR, Am. J. Psychol. 46: 580-589. 1960a. Properties of cutaneous touch HUNT, C. C., and A. K. MCINTYRE. receptors in cat. J. Physiol. London 153: 88-98. HUNT, C. C., and A. K. MCINTYRE. 1960b. An analysis of fiber diameter and receptor characteristics of myelinated cutaneous afferent fibers in * cat. J. Physiol. London 153: 99-112. JENKINS, W. L. 1940. Studies in thermal sensitivity: 14. Part-whole relations in seriatim warm-mapping. J. Exptl. Psychol. 27: 76-80. JENKINS, W. L. 1941a. Studies in thermal sensitivity: 16. Further evidence on the effects of stimulus temperature. J. Ezptl. Psychol. 29: 413-419. JENKINS, W. L. 1941b. Studies in thermal sensitivity: 17. The topographical and functional relations of warm and cold. J. Exptl. Psychol. 29: 511-516. LELE, P. P. 1962. An electrothermal stimulator for sensory tests. Neural. Neurosurg. Psychiat. (in press)
BISHOP, BLIX,
*
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GINTY
16. MARUHASHI, J., K. M~ZUGUCHI, and I. TASAKI. 1952. Action currents in single nerve fibers elecited by stimulation of the skin of the toad and cat. J. Physiol. London 117: 129-151. 17. MELZACK, R., and P. D. WALL. 1962. On the nature of cutaneous sensory mechanisms. Brain 86: 331-356. 18. MOUNTCASTLE, V. B., and T. P. S. POWELL. 1959. Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. Bull. Johns Hopkins Hosp. 186: 201-232. 19. TOWER, S. S. 1943. Pain: definition and properties of the unit for sensory reception. Research Publ. Assoc. Research Nervous Mental Disease 29: 16-43. 20. WALL, P. D. 1960. Cord cells responding to touch, damage and temperature of skin. J. Neurophysiol. 23: 197-210. 21. WATERSTON, D. 1924. The sensory activities of the skin for touch and temperature. Repts. St. Andrews Inst. Clin. Research 2: 123-132. 22. WATERSTON, D. 1933. Observations on sensation: the sensory functions of the skin for touch and pain. J. Physiol. London 77: 251-257.
NEUROLOGY
6,
300-314
(1962)
Skin Sensitivity R. MELZACK, Psychology
Section
to Thermal
G. ROSE,
and Research Laboratory of Technology, Cambridge, Received
June
AND
of
D.
Stimuli
MCGINTY~
Electronics, Massachusetts
Massachusetts
Institute
7, 1962
Distribution patterns of cutaneous thermal sensitivity in human subjects were studied by mapping large areas of skin with stimulators the tip temperatures and diameters of which were controlled. The maps show that skin sensitivity to cold and warm stimuli is distributed in the form of large sensory fields rather than isolated “spots.” These sensory fields have a variety of sizes and shapes. Generally, they consist of highly sensitive areas, ranging in size from 6 cm2 to spot-like peaks, surrounded by larger, less sensitive regions. Moreover, there are persistent fluctuations of thermal sensitivity in successive maps of the same area of skin. Fluctuation usually took two forms: marked changes primarily at the boundaries of the sensory fields; and “fragmentation” and “coalescence” of the fields themselves. It was also observed that small, warm stimuli produce frequent reports of pricking, stinging sensations at temperatures that evoke pleasant warmth when applied normally to large areas of skin. This observation suggests that the spatial properties of warm stimuli play an important role in determining the quality of cutaneous experience. Introduction
The traditional view of thermal sensitivity of the human skin is that it consists of a mosaic of “cold spots” and “warm spots.” This belief, which originated with Blix (2), Goldscheider (7), and Donaldson (4), is the basis of von Frey’s (5) classic theory of cutaneous sensation. It assumes that a single specific receptor lies beneath each sensory “spot” on the skin. It assumes, moreover, that there is a one-to-one relationship between the receptor and the quality of sensation projected by the nervous system onto the “spot” of skin above it (see 17). The “skin spot” thus 1 This work was supported in part by the U.S. Army Signal Corps, the Air Force Office of Scientific Research, and the Office of Naval Research, and in part by the National Institutes of Health (grant M-4235Cl). We wish to thank Mr. H. Rosenthal and Mr. R. Swanson for their assistance in the experiment. Mr. Rose is now at the Psychology Department, University of California at Los Angeles; Mr. McGinty, at the Psychology Department, University of Pennsylvania. 300
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SENSITIVITY
301
plays a fundamental role in current concepts of skin sensory mechanisms since it is widely believed to be the basic unit for cutaneous sensation. Recent studies of skin sensory mechanisms argue strongly against the traditional view. Jenkins (12, 13, 14) has provided convincing psychological evidence that “spots” do not represent a true picture of the distribution of thermal sensitivity. The characteristic feature of his maps are “gradients of sensitivity”-highly sensitive areas surrounded by regions of decreasing sensitivity. Similarly, recent physiological data (1, 10, 11, 16, 19, 20) demonstrate that a given area of skin is innervated by widelybranching nerve endings of numerous fibers, whose receptive fields are of varying size and overlap extensively. Spotlike innervation is the exception rather than the rule (10, 11)) and even then, the spots are embedded in larger receptive fields. The psychological and physiological data thus suggest that the “skin spot,” once believed to represent a single specific receptor lying beneath it, is the result of the ability of the central nervous system to integrate the impulses of many fibers having overlapping receptive fields. This picture of skin sensory mechanisms is complicated still further by the fact that there is never perfect correspondence among maps of thermal sensitivity of the same area: Many spots fail to respond on successive examinations while new spots frequently appear (3). That these fluctuations of thermal sensitivity represent a basic biological phenomenon has been proposed by Waterston (21, 22). He observed that an area of skin made anesthetic by nerve or spinal injury does not have a fixed margin, but a zone of varying width in which sensitivity fluctuates from one examination to the next. He found similar fluctuation at the margin of areas of hyperalgesia. Waterston argued on the basis of the experimental and clinical evidence that there is a constant coming and going of activity of different parts of the skin so that onIy a small portion of the sensory surface is active at any one time. It is astonishing that the work of Jenkins and Waterston has been virtually forgotten during the past quarter-century, while the traditional concept of a static, punctate skin sensitivity has been perpetuated. Indeed, there have been few recent studies of thermal sensitivity of human skin even though the physiological evidence of overlapping receptive fields suggests that thermal sensitivity may be distributed in the form of large sensory fields rather than isolated spots. The purpose of this study is to investigate the distributions of sensitivity to warm and cold stimuli in
302
MELZACK,
ROSE,
AND
MC
GINTY
large areas of skin so that evidence of overlapping receptive fields and their properties might become manifest. Methods
Areas ranging in size from 20 cm2 to approximately a quarter of the back were mapped with stimulators whose tip diameters and temperatures could be varied. Most of the maps of cold sensitivity were made with a copper rod that had a tip diameter of 2.5 mm and which extended into a large test tube containing crushed ice. The test tube was covered with thick asbestos insulation, painted with rubber cement and was closed with a rubber stopper holding the copper rod. Calibration of the tip with a thermocouple and temperature measuring device showed a temperature of 10 & 1 C. Fresh ice was placed in the test tube approximately every 1.5 min to prevent fluctuation of the stimulus temperature. Additional experiments of sensitivity to cold were carried out with a “thermovari-probe” apparatus ( 15)2 which permitted even more precise control over the stimulating temperature. The subjects were twelve male and five female students and technicians between the ages of 18 and 25. Aftera series of preliminary test trials with the cold stimulus, a grid with cross-section lines 5 mm apart was stamped on the back of the hand, on the forearm or on the back. An identical grid was stamped on a sheet of paper and the subjects’ reports of intensity of perceived cold were recorded in the corresponding area. The subjects were asked to report their perceptions by using the following scale: 0 = touch, no cold; I = mild cold; 2 = moderate cold; 3 = strong cold. The stimulus was moved randomly from area to area within the grid and the subjects’ reports were recorded. They were unable to see where the stimulus was being presented. It was applied lightly to the skin for approximately 0.5 set and presentations were separated by about S-set intervals. Pressures and durations varied slightly on a random basis from spot to spot, but were well within the limits found by Heiser (8) and Heiser and McNair (9) to have negligible effects on maps of skin sensitivity. The experiments on fluctuation of skin sensitivity were usually carried out in an air-conditioned room after the subjects had been exposed to 2 We are grateful to Dr. lending us this apparatus.
P. P. Lele
of the Massachusetts
General
Hospital
for
SKIN
SENSITIVITY
303
the room temperature for at least an hour. A grid of 5 X 5 cm was chosen to study fluctuation because it could be mapped in a reasonably short time (about 20 min), yet was large enough to permit the appearance of at least portions of large sensitive fields. Most maps of warmth sensitivity were made with thermal probes connected to the ‘Lthermo-vari-probe” machine. Some were made with a copper rod that extended into a test tube filled with warm water. The procedure was similar to that used for the cold mapping, except that S-mm diameter tips were generally used and the subjects were asked to report perceived warmth intensity on a scale of 0, 1, 2, 3, comparable to that used for cold. In addition to reports of sensory intensity, notes were also made of the subjects’ difficulties with the scale and their description of the perceptions were recorded in detail. Results
Stinging Pain Produced by Small Warm Stimuli. It became clear at the outset that small warm stimuli, ranging in temperature between 42 and 44 C, produce persistent reports of pricking or stinging pain. Tips of l-mm diameter, within this temperature range, frequently elicit sharp pricks. Larger tips of 2.5 and 5 mm often produce stinging pain. Some of the subjects actually objected that they were being jabbed with a pin, although they were being stimulated as gently as possible with the warm flat tip. Even with tips as large as 10 mm, there were reports of burning, stinging sensations, although immersion of the fingers or the whole hand in water within this temperature range was perceived unequivocally as pleasant warmth. For some of the subjects the frequency of reports of sting decreased as the tip diameter increased. Nevertheless, reliable scaling turned out to be a difficult task. Although the subjects scaled their perceptions as 0, f, 2, 3, many of them reported that they used the following criteria: 1 meant sting alone or more sting than warmth, 2 was warmth or more warmth than sting, and 3, stinging warmth or hot. The map of warmth sensitivity presented below is based on these criteria. Taking these limitations into consideration, the general principles of sensitivity distribution for warmth appear to be essentially similar to those for cold. These difficulties were not encountered with the cold stimuli. Cold applied with small-diameter tips were perceived as having a “natural” quality, without any biting, painful concomitants, even with temperatures
304
MELZACK,
ROSE,
AND
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as low as 10 C. With a tip diameter of 2.5 mm, the perceptions varied primarily in intensity and the subjects had little difficulty in making the intensity judgments. There were marked individual differences among observers, however. A few failed to develop the ability to scale their thermal perceptions, while some learned to do so only after a few initial stimulations. Most of the observers acquired confidence in their judgments only after one or more complete maps had been made. The results described below were found in all observers who developed confidence in their ability to scale their perceptions of the cold and warm stimuli. Patterns of Skin Sensitivity to Small Thermal Stimuli. More than a hundred maps of various sizes were made of distributions of cold sensitivity on the back of the hand, on the upper forearm and on the back. Figure 1 shows a map of cold sensitivity made on approximately a quarter of the back. The salient feature of all the maps is that they contain one or more large sensitive areas stimulation of which produce reports of strong cold, surrounded by less sensitive areas that elicit moderate and mild cold. The characteristics of these sensitive areas are observed clearly only when maps are made of sufficiently large areas of skin. They demonstrate that the thermally-sensitive surface of the skin consists of large fields having a definite circumscribed area with distinct boundaries. Since the size of some of these fields is larger than the total areas of the maps made by earlier investigators, it becomes obvious why they have not been found in previous studies. When the relative frequencies of 0, 1, 2, 3 are viewed in the perspective of the whole map, it is seen that the areas that fail to elicit reports of cold are small and few in number. Large insensitive regions are rare (Fig. 3, right). Moreover, isolated sensitive spots are infrequent, although there are pointlike peaks of sensitivity lying within a large sensitive field. Maps of sensitivity to warm stimuli, obtained from the back and other areas of the body (Fig. 2), show large sensitive fields having the same variety of sizes and shapes as those observed for cold. When the same area is mapped for sensitivity to both cold and warm stimuli, however, the two distributions are always found to be different. Portions of the sensitive fields in the two maps often overlap, but there appears to be no systematic relationship between the two distributions.
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FIG. 1. Distribution of cold sensitivity of approximately a quarter of the back. The position and size of the area tested is drawn in the lower right corner. The sensitivity distribution was mapped with a round stimulator tip 2.5 mm in diameter at a temperature of 10 C. The cold intensities reported by the subject are represented by different shades of stipple. 305
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Fluctuation of Thermal Sensitivity Distributions. Fluctuation of sensitivity in successive maps of the same area generally took two forms: (a) marked changes that occurred primarily at the boundaries of the large sensory fields while the central portions remained stable, and (b) “fragmentation” and “coalescence” of sensory fields, forming new distribution patterns that remained in the same general portion of the map.
FIG. 2. Distributions upper left, cold sensitivity; area tested. Tip diameter:
of cold and warm sensitivity in the same area of skin: lower left, warm sensitivity; right, location of the forearm 2.5 mm. for both maps. Intensity scale: see Fig. 1 and text.
(a) Typical maps of fluctuation at the boundaries of sensitive fields are shown in Fig. 3. Figure 3 (left) illustrates the most commonly observed changes. Despite fluctuation, the two successive maps of cold sensitivity remain strikingly similar. An opportunity to observe these changes in greater detail is provided by the maps in Fig. 3 (right) in which a large area of skin that is insensitive to cold permits clear visualization of the boundaries of the sensitive regions. (b) The second major form of change observed in successive maps of the same area is the “fragmentation” and “coalescence” of sensitive areas, shown in Fig. 4. Three maps of cold sensitivity (Fig. 4, left) were
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made in the morning and three (Fig. 4, right) were made 4 hours later. The maps made in each session were separated by lo-min intervals. It is seen that the sensitive fields in the upper right-hand corner fluctuate from map to map, producing continually-changing patterns. Nevertheless,
FIG. 3. Fluctuation of cold sensitivity: changes at the boundaries of sensory fields. Left, two successive maps based on the cold intensity scale shown in Fig. 1. Right, two maps from another subject based on reports of “cold” (stipple) or “no cold” (white areas). Each map was completed in approximately 20min; ZO-min interval between two successive maps.
the distribution of sensitivity to cold remains in the same general area in all the maps. Effects of Adaptation on Thermal Sensitivity Distributions: Intermittent Point Stimulation. The following procedure was carried out to study the
effects of repeated, brief stimulation on the distribution patterns of cold sensitivity: First a cold map was obtained in the usual way; then three
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“simultaneous maps” were made in which each point was stimulated three times at approximately 20-set intervals; a final cold map was then obtained using the normal procedure.
FIG. 4. Fluctuation of cold sensitivity: sensory fields. Left, three successive maps of the same area made 4 hours later. Intensity
“fragmentation” and “coalescence” of made in the morning; right, three maps scale: see Fig. 1.
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Maps obtained with this procedure are shown in Fig. 5. The general effect of brief, intermittent stimulation was to produce a widespread reduction in sensitivity. An examination of the changes in the “simultaneous” maps (Fig, 5, lower) shows the progressive lowering of sensitivity during the test. However, the distribution of cold sensitivity in the final conventional map (Fig. 5, upper right) has some similarities to the first map (Fig. 5, upper left) despite the over-all increase in the reports of mild cold.
FIG. 5. Sensitivity reduction brought about by brief, intermittent stimulation. maps in which each Upper left, conventional cold map. Lower, three “simultaneous” point was stimulated three times in succession at approximately to-set intervals. Upper right, final conventional cold map. Stimulus diameter: 2.5 mm. Intensity scale: see Fig. 1.
Effects of Adaptation on Thermal Sensitivity Distributions: Continuous Whole-Area Stimulation. To study the effects of continuous cold stimulation on sensitivity distributions, two successive maps were obtained, and a cellophane bag of ice and water was placed over the area for ten minutes before a third map was made. A cellophane bag of hot water was similarly used to study the effects of continuous warmth stimulation on the sensitivity distribution to cold stimuli. Figure 6 (left) shows the effects of continuous cold stimulation on the distribution of cold sensitivity. It tended to produce a marked narrowing
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of the sensory fields, together with an over-all reduction in sensitivity. Warming the skin had the opposite effect of increasing its sensitivity to cold. The effect in Fig. 6 (right) is small, but was found consistently in all experiments. The effects of intermittent and continuous stimulation on warm maps produced equivocal results. Eflects of Stimulus Temperature on Thermal Sensitivity Distributions. Figure 7 shows that as stimulus temperature decreases, the regions sensi-
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FIG. 7. Orderly increase in size of cold sensory fields brought about by decreasing stimulus temperature. Left, map obtained with a stimulus temperature of 18 C. Right, map of same area with stimulus temperature of 16 C. Tip diameter: 2.5 mm. Intensity scale: see Fig. 1.
tive to cold tend to increase was obtained with a stimulus stimulus 2 degrees colder. It not appear randomly across already found to be present.
in size in an orderly manner. Map 7 (left) temperature of 18 C, and 7 (right) with a is seen that the newly-responsive areas do the map, but adjacent to sensitive areas
The picture of skin sensitivity suggested by this study stands in marked contrast to the traditional view. The results show (a) that skin sensitivity to cold and warm stimuli is distributed in the form of large fields rather than spots, (b) that there is a persistent fluctuation of sensitivity in successive maps of the same area, and (c) that the spatial properties
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of warm stimuli play an important role in determining the quality of cutaneous experience. The maps of large sensory fields confirm and extend Jenkins’ (12,13, 14) observations of “gradients of sensitivity.” The small area covered by his maps, however, precluded the finding of definite, circumscribed regions. Their presence becomes strikingly clear when maps are made of areas as large as a quarter of the back. Figure 1 exhibits some of the variety of sizes and shapes of the sensitive fields of the skin, ranging from spotlike peaks within larger, less sensitive fields, to regions of peak sensitivity having an area greater than 6 cm2 (which is the entire area of Jenkins’ usual maps). These observations of large sensitive fields, obtained with psychological testing methods, are consistent with the physiological data showing overlapping receptive fields in the skin. It is clear that the sensory fields found in this study do not represent a single receptive field. Successive maps show that these large sensory fields may “fragment” and “coalesce,” producing a number of different patterns of sensitivity distribution. It seems likely that these sensory fields represent many smaller receptive fields overlapping one another. These data provide only indirect evidence regarding cutaneous receptor units; but they demonstrate that the thermally sensitive areas of the human skin tend to consist of large fields such as we would expect from the recent physiological data, but not from the concept of isolated, randomly distributed receptors. The mechanisms underlying the persistent fluctuations in thermal sensitivity are unknown. They may be due to change in transmission capacity’ at one or more relays in the central nervous system, possibly brought about by stimulation of inhibitory areas in the course of mapping (IS), or to continuous changes in receptor sensitivity brought about by a continually changing blood flow in the skin capillary beds (see 6, 21). The results (Figs. 5 and 6). show, however, that the act of stimulation itself, at a given moment, determines the sensitivity of the area to subsequent stimulation. But the cause of this “adaptation,” whether neural or circulatory, is also unknown. Whatever the mechanism, it is clear that continuous changes in the distribution of skin sensitivity could prevent total adaptation in peripheral and central neurons, so that information . would be transmitted from the skin to the central nervous system at all times. Perhaps the most surprising result in this study in the difference in
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effects produced by small cold and warm stimuli. While cold felt “natural” regardless of stimulus size, the small warm stimuli produced anomalous pricking, stinging sensations at temperatures that evoke pleasant warmth when applied normally to large areas of skin. These difficulties encountered with small warm stimulators underscore the artificiality of our present methods for studying skin sensitivity. More important, however, is the implication that, for warmth at least, the “spot” is not the basic unit of skin sensation. The “punctate” concept presumes that the qudity of sensory experience is independent of stimulus size. The results show that this is not the case; rather, they support the view that the spatial properties of the stimulus play an important role in determining the quality of cutaneous experience ( 17). References 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.
12. 13. 14. 15.
G. H. 1944. The peripheral unit for pain. J. Newophysiol. 7: 71-80. M. 1884. Experimentelle BeitrLge zur Losung der Frage iiber die specifische Energie der Hautnerven. Z. Biol. 20: 141-156. DALLENBACR, K. M. 1927. The temperature spots and end-organs. Am. J. Psychol. 39: 402-427. DONALDSON, H. H. 1885. On the temperature sense. Mind 10: 399-416. FREY, M. VON. 1895. BeitrIge zur Sinnesphysiologie der Haut. Bev. kgl. siichs, Ges. Win., math.-phys. Kl. 47: 166-184. “The human senses.” Wiley, New York. GELDARD, F. A. 1953. GOLDSCHEIDER, A. 1884. Die specifische energie der temperaturnerven. Monatsschr. prakt. Dermatol. 3: 53-76. HEISER, F. 1937. Stimulus-duration and sensations of warmth. tlm. J. Psychol. 49: 58-66. 1934. Stimulus-pressure and thermal sensation. HEISER, F., and W. K. MCNAIR, Am. J. Psychol. 46: 580-589. 1960a. Properties of cutaneous touch HUNT, C. C., and A. K. MCINTYRE. receptors in cat. J. Physiol. London 153: 88-98. HUNT, C. C., and A. K. MCINTYRE. 1960b. An analysis of fiber diameter and receptor characteristics of myelinated cutaneous afferent fibers in * cat. J. Physiol. London 153: 99-112. JENKINS, W. L. 1940. Studies in thermal sensitivity: 14. Part-whole relations in seriatim warm-mapping. J. Exptl. Psychol. 27: 76-80. JENKINS, W. L. 1941a. Studies in thermal sensitivity: 16. Further evidence on the effects of stimulus temperature. J. Ezptl. Psychol. 29: 413-419. JENKINS, W. L. 1941b. Studies in thermal sensitivity: 17. The topographical and functional relations of warm and cold. J. Exptl. Psychol. 29: 511-516. LELE, P. P. 1962. An electrothermal stimulator for sensory tests. Neural. Neurosurg. Psychiat. (in press)
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16. MARUHASHI, J., K. M~ZUGUCHI, and I. TASAKI. 1952. Action currents in single nerve fibers elecited by stimulation of the skin of the toad and cat. J. Physiol. London 117: 129-151. 17. MELZACK, R., and P. D. WALL. 1962. On the nature of cutaneous sensory mechanisms. Brain 86: 331-356. 18. MOUNTCASTLE, V. B., and T. P. S. POWELL. 1959. Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. Bull. Johns Hopkins Hosp. 186: 201-232. 19. TOWER, S. S. 1943. Pain: definition and properties of the unit for sensory reception. Research Publ. Assoc. Research Nervous Mental Disease 29: 16-43. 20. WALL, P. D. 1960. Cord cells responding to touch, damage and temperature of skin. J. Neurophysiol. 23: 197-210. 21. WATERSTON, D. 1924. The sensory activities of the skin for touch and temperature. Repts. St. Andrews Inst. Clin. Research 2: 123-132. 22. WATERSTON, D. 1933. Observations on sensation: the sensory functions of the skin for touch and pain. J. Physiol. London 77: 251-257.