Journal of Comparative and Physiological Psycholog 1975, Vol. 89, No. 4, 364-370
Skin Potential Activity in Rats, Cats, and Primates (Including Man): A Phylogenetic Point of View Katuo Yamazaki Department of Neuropsychiatry, School of Medicine, Fujita Gakuen University, Aichi, Japan
Tetuo Tajimi Clinical Eleclroencephalography Laboratory, Isogo Hospital, Yokohama, Japan
Ken'ichi Okuda Japan Broadcasting Corporation, Tokyo, Japan
Yosizumi Niimi Tokyo Metropolitan Institute for Neurosciences, Tokyo, Japan
With rats, cats, nonhuman primates, and humans serving as subjects, skin potential activity was measured under waking conditions. In good agreement with the findings of previous workers, skin potential response waveform was always monophasic negative in rats and cats, but in humans it took three forms. By contrast, it was always monophasic positive in simian nonhuman primates, although prosimiae gave monophasic negative waves. A skin potential level-skin potential response relationship could not be observed in any subject except humans. From these results, an attempt was made to relate skin potential activity to the peripheral mechanism involved in these species on the basis of a phylogenetic point of view.
Since the pioneer work of Forbes (1936), many experiments have been concerned with the underlying mechanism of the waveform of the skin potential response (SPR) in humans. Three waveforms (monophasic negative, diphasic, and monophasic positive) have been recognized and described in detail as the typical patterns of the SPR (Wilcott, 1964). In other mammals, some studies, focused on a single species, have been done in primates (Takagi & Nakayama, 1959; Wilcott, Note 1; Yamazaki, Tajimi, Okuda, & Niimi, 1972a), in cats (Wang, 1964), and in rats (Tajimi, Yamazaki, Takci, & Niimi, 1973), but there seems to be a discrepancy among various results concerning the waveform of the SPR in these animals, especially in primates. Moreover, there has been no attempt to compare SPR waveforms in humans with those of other mammals on the phylogenetic scale. This research was performed at the Department of Neurophysiology, Primate Research Institute, Kyoto University, Inuyama. We wish to acknowledge our gratitude to the late T. Tokizane and to K. Kubota for their interest and help. Requests for reprints should be sent to K. Yamazaki, Department of Neuropsychiatry, Fujita Gakuen University, 1-98 Kutukake, Toyoake, Aichi 470-11, Japan.
The purposes of this research were (a) to measure the skin potential (SP) activity in various species—humans, nonhuman primates (primates, for short), cats, and albino rats (rats, for short)—and (b) to discuss the waveform of the SPR from a phylogenetic point of view. EXPERIMENT 1 Using an identical technique, the SP activity was measured precisely to make a systematic comparison across the mammals (rats, cats, primates, and humans) and to elucidate the phylogenetic significance of this electrodermal phenomenon of the sweat gland. Moreover, the SPR waveform in Macaca monkeys was measured for comparison with previous reports. Method Subjects. The subjects were 60 rats, 21 cats, 36 primates (1 Pan troglodytes, 13 Macaca fuscata, 9 Macaca mulatta, 1 Macaca irus, 1 Macaca cyclopis, 1 Macaca nemestrina, 1 Erythrocebus patas, 2 Saimiri sciureus, 1 Ateles geoffroyi, 1 Cebus capucinus, 2 Aotus trivirgatus, 2 Galago crassicaudatus and 1 Nycticebes coucang), and 87 humans of both sexes. All of them were intact, normal adults. Apparatus, The SP activity was measured with equipment having stable dc amplifiers with a high input impedance (San'ei, EG-129, EG-900, or Toa, EPR-3T). Two Ag-AgCl disc electrodes (standing
364
COMPARATIVE STUDY OF SKIN POTENTIAI/ACTIVITY potential of less than ±.2 mV), filled with agaragar .05 M NaCl, were attached by means of an adhesive vinyl tape, one active electrode to the foot pad (for rats and cats) or the palm (for primates and humans) and the reference electrode on a drilled skin area of the ipsilateral ankle (for rats and cats) or of the ipsilateral forearm (for primates and humans). Recording procedure. The SP activity of each subject was measured during the relaxed, motionless waking state for about 30 min. The rats and cats, which had been thoroughly accustomed to handling over the course of several months, were tested in a cage with a wood floor. The recording methods used in this study for rats and cats have been described in detail elsewhere (Tajimi, Yamazaki, & Niimi, 1973; Yamazaki, Tajimi, & Niimi, 1969). The primates were seated on a primate chair. Before recording, both arms of the primate were loosely tied to the chair to eliminate possible movement artifact. Most of the primates had been habituated to a primate chair, and their behavior indicated that they were accustomed to the experimental room. Human subjects were seated in a chair in a soundproof and electrically shielded room. The skin potential level (SPL) readings were made in each case just before the appearance of the SPR in each subject. Physical stimuli, such as a handclap, a burst of white noise, or a light flash, were used to evoke the SPR. Room temperature ranged 22° 0-28° C.
Results A purpose of this study was to compare the SP activity among mammals. Therefore, other kinds of analysis of the SPR, such as the time course or amplitude of a response, are not considered in this article. General patterns of SPR in primates. A sample record of the SPR in each primate species is shown in Figure 1. Classification of primates was based on Kawai, Iwamoto, and Yoshiba (1968). At a glance, one can see that Simiae produce only the monophasic positive wave. On the contrary, Prosimiae (G. crassicaudatus and N. coucang in this study) show only the monophasic negative wave. In any case, the diphasic waveform of the SPR was not recorded in primates in response to any stimulus used. We did not observe any monophasic negative waves from Simiae or monophasic positive waves from Prosimiae. General patterns of SP activities in rats, cats, primates, and humans. The waveform of the SPR in each species is shown in Figure 2. Rats and cats in the waking condition always gave monophasic negative waves to
365
any stimulus. In humans, three types of the SPR waveform (monophasic negative, diphasic, and monophasic positive) were recorded during measurements, which is in good agreement with previous reports (Forbes, 1936; Wilcott, 1964; Yokota, Takahashi, Kondo, & Fujimori, 1959). Primates show two types of the SPR waveform, as described above. Figure 3 is a schematic display of the waveform of the SPR obtained in this experiment. SPL differences among rats, cats, primates, and humans. The mean values of the SPL among species are shown in Table 1. The SPL in each species always maintained negativity during the measurement. No polarity change of the resting SPL from negativity to positivity was observed in any of the subjects. Concerning the SPL-SPR relationship, no species showed SPRs that actually effectively passed zero potential, making the palm or foot pad positive relative to the reference electrode. In human subjects, a low negativity of the SPL was associated with negative waves of the SPR, and high potential level was associated with positive waves; diphasic responses were recorded when the potential level was at an intermediate position, as indicated by Wilcott (1964). These SPL-SPR relationships, however, could not be observed in any subjects except humans. The SPL in rats and cats was less negative compared with primates. The maximum value was obtained in human subjects, as shown in Table 1.
EXPERIMENT 2 It was found that Simiae gave only positive potential waves in Experiment 1. The result was not in accord with previous reports by Takagi and Nakayama (1959) and Wilcott (Note 1) on Macaca monkeys. Additional lines of approach were needed to account for the discrepancy. The appearance of only positive waves has been already confirmed uneer a wide spectrum of alert, resting, and sledping conditions in Macaca monkeys (Yamazaki, Tajimi, Okuda, & Niimi, 1972a, 1972b). Therefore, an attempt was made to see whether variations in room temperature and exsanguination, which would influence factors critical for the waveform of the SPR
YAMAZAKI, TAJIMI, OKUDA, AND NIIMI
366
Pongidae
P. lro(loljtis
M. In still ». mlitti
Cercopithecidae Simiae E. pill!
Primates
». li.llni
Cebidae C. cipucinus
Prosimiae
Lorisidae
6. trmicuditll
5»V
''H^tH1^^
40 IK
FIGURE 1. The waveform of the skin potential response (SPR) in the nonhuman primate. (Spontaneous SPRs are also mixed in each record. Movement artifacts appear after approximately 90 sec and at the end of a record in C. capucinus. Negativity at the active electrode is indicated by an upward deflection.)
in humans (Wilcott, 1962; Yokota et al., 1959), could influence the SPR waveform of Macaca monkeys. Method Subjects. Four monkeys of both sexes (two Macaca mulatto and two Macaca fuscata) were used as subjects. All were intact, normal adults. Apparatus. The recording equipment was the same as that used in Experiment 1. For the study of the effect of temperature on the SPR, an artificial meteorological room was used, in which both temperature and humidity could be regulated. Recording procedure: Temperature effect. Set ting the humidity of the artificial meteorological room at a constant level (60%), the temperature was changed from 15° C to 35° C or vice versa at 5° C steps at about 10-min intervals. Each subject was brought into the room and seated on the primate chair with the electrode system prepared as described in Experiment 1.
Exsanguination effect: By fastening one wrist of a primate to stop the blood supply to the palm, the effect of exsanguination on the SPR waveform was studied under normal temperature. Before exsanguination, SPRs of both palms were recorded for several minutes simultaneously. During this control record, there were scarcely any differences in amplitude and waveform of the SPR between the two palms. During exsanguination of one palm, concurrent recordings were continued with the exsanguinated palm as the experimental and with the intact one as the nontreated control for 20 min. Recordings were also made after releasing exsanguination.
Results Temperature effect. With an increase in the room temperature, the frequency of the spontaneous SPR was enhanced as shown in Figure 4. These temperature-dependent rela-
367
COMPARATIVE STUDY OF SKIN POTENTIAL ACTIVITY
RAT
PRIMATE
HUMAN
I 5 nV
FIGURE 2. General patterns of the skin potential response (SPR) waveform in the rat, cat, nonhuman primate, and human. (Spontaneous SPRs also appear in these measurements.)
tionships with the SPR were observed in all primates. However, neither negative nor diphasic potential waves were observed over a wide range of room temperatures. Obtained SPRs were always positive waves. Temperature variation produced no observable effects on this waveform. Exsanguination effect. Before exsanguination, positive potential waves always appeared in both palms in Macaca monkeys. Although positive waves were reduced in amplitude during the initial course of exsanguination in the experimental palm, no polarity change of the waveform was observed during this phase. With a complete exsanguination of the experimental palm, the potential change almost disappeared, while positive waves were still recorded from the control palm as shown in Figure 5. The SPL increased appreciably in negativity, while the amplitude of the positive wave decreased during exsanguination. Neither negative nor diphasic potential waves appeared in the experimental palm in these periods, but very small positive waves were observed simultaneously with the large positive waves in the control palm. Several minutes after removal of the fastener to allow the blood to return to the palm, positive waves appeared in the experimental palm, which could not be differentiated from those in the control palm. These observations were obtained in all primates tested.
DISCUSSION Various waveforms of the SPR were obtained in the mammals in this experiment, although a fairly constant species-specific waveform was also observed. As to humans, the waveform of the SPR showed patterns similar to those described by previous workers (Forbes, 1936; Wilcott, 1964). The finding of monophasic negative potential waves in the waking rat seems to be a new discovery. On the other hand, a waveform similar to that in the rat was also recorded in the waking cat, which was in good agreement with previous reports by Wang (1964) and others. Takagi and Nakayama (1959) used only one primate (Macaca fuscata) and recorded the SPR in the waking condition. They found that the waveform of the SPR was always a monophasic negative deflection. Using two waking primates (Macaca mulatta) as subjects, Wilcott (Note 1) recorded monophasic negative, diphasic, and monophasic positive waves of the SPR, which appeared to be essentially the same as those recorded from humans. Concerning the diphasic and monophasic positive wave in primates, Wilcott suggested that the heightened arousal produced by the restraint of being tied brought about such an electrical phenomenon. However, all macaques (13 Macaca fuscata and 9 Macaca mulatta) always showed monophasic positive waves in the present experiment even when their RAT
CAT
PRIMATE inme
HUMAN
Simiae
FIGURE 3. Schematic display of the skin potential response (SPR) waveform in mammals. (First row is monophasic negative waves; second, a diphasic; and bottom, monophasic positive. Blank area indicates that the waveform described could not be observed.)
YAMAZAKI, TAJIMI, OKUDA, AND NIIMI
368
TABLE 1 MEAN SKIN POTENTIAL LEVEL (SPL) AMONG MAMMALS SPL (in mV)
Rat Cat
Primate Human
60 21 36 87
M
SD
-8.8
3.49 3.59 5.16 6.72
-8.9 -14.7 -42.7
arousal level was low as judged from their behavior. The animals were so adapted to the restraints that they could be considered in a resting state. Moreover, temperature variation or exsanguination did not affect this potential wave, which was in sharp contrast to previous reports in humans (Wilcott, 1962; Yokota et al., 1959). In addition, in a previous study only the monophasic positive wave could be observed during the natural sleep-wake spectrum in Macaca monkeys (Yamazaki et al., 1972b). Therefore, there is no reason to relate these waveforms to the heightened or lowered arousal in primates. The discrepancy of these findings in Macaca monkeys may be caused by methodological differences such as the treatment of a reference site or preparations of the electrode system. At any rate, Simiae showed only monophasic positive waves, and Prosimiae showed only monophasic negative waves like those recorded from rats and cats. It has been noted that the precursor sweat obtained at the upper part of the sweat duct is isotonic or slightly hypertonic (Cage & Dobson, 1965). Therefore, the reabsorption mechanism in the human sweat duct is thought to be responsible for the hypotonicity of the sweat collected at the sweat pores over the human skin surface (Schulz, Ullrich, Fromter, Holzgreve, Frick, & Hegel, 1965). Sweat secreted in the monkey palm (Macaca fuscata and Macaca mulatto) was found to be hypotonic (Ito, 1968; Sato, 1973). Sweat collected from the sweat gland of the hairless footpad of the cat and of the rat was found to be hypertonic (Brusilow, Ikai, & Gordes, 1968; Munger & Brusilow, 1961). The anatomical comparison of the sweat glands of rats, cats, and humans
reveals that the glands of rats and cats have a short and thin duct segment whose epithelial cells contain very few mitochondria, whereas the duct of humans is long and coiled, and the epithelial cells have abundant mitochondria when examined under the light and the electron microscope. Substantial differences in the ductal part of the sweat gland indicate that sodium reabsorption does not occur in the duct of the cat or rat sweat gland (Brusilow et al., 1968; Munger & Brusilow, 1961). On the basis of this theory, Fowles and Venables (1970) proposed that the mechanism of the ductal reabsorption of sodium from sweat might account for the large negative potentials and also for the large positive waves recorded in humans. Applying their proposed hypothesis to other animals, one can see the SPL differences among species in connection with the degree of sodium reabsorption in the sweat gland. The MJ_
30DC
40 sec FIGURE 4. Effect of temperature on the skin potential response (SPIi) in Macaca monkeys.
COMPARATIVE STUDY OF SKIN POTENTIAL ACTIVITY normal
M.f.f.
, 4min
, 12 min
after 7 min
..: L .
40 sec FIGURE 5. Effect of exsanguination on the skin potential response (SPR) in Macaca monkeys. (Curves show the SPR before exsanguination, A; during course of exsanguination of left, L, palm, B and C; and after recovery, D.)
largo negativity in SPL in humans and primates may be attributed to sodium reabsorption in the sweat gland. By contrast, the small negativity in rats and cats can probably result from the lack of ductal reabsorption of sodium in their sweat glands. This proposal suggests some connection between sodium reabsorption and the positive component of the SPR, since Wang (1964) and others have consistently reported that responses from the cat footpad are always monophasic negative waves (Fowles & Venables, 1970).
369
At present, this sodium pump theory appears to be appropriate for the explanation of the peripheral mechanism involved in this electrical phenomenon of the skin. However, it can not explain why Simiae show only monophasic positive waves in spite of the existence of the SPL values like those of rats and cats rather than of humans, and why Simiae do not show monophasic negative and diphasic waveforms like those of humans. The SPL-SPR relationship observed in humans seems to be inapplicable to other animals under natural conditions. The fact that SPRs immediately disappear after peripheral denervation and the SPL remains at the same negativity level as before (Yamazaki & Tajimi, 1972) suggests the possibility of a different origin for the SP activity. There still remain many problems concerning the precise mechanism of the SP activity in the sweat glands. Further work and another line of evidence; concerning the bioelectrical and biochemical properties of the sweat glands are needed to elucidate the peripheral mechanism responsible for SP activity in mammals. In any event, the observation of SP activity might offer some cue for understanding the evolutionary aspects involved in the sweat gland activity in mammals. REFERENCE NOTE 1. Wilcott, R. C. Observations of skin potential, skin resistance and sweating of two rhesus monkeys. Unpublished manuscript, 1965. (Available from R. C. Wilcott, Department of Psychology, Case Western Reserve University, Cleveland, Ohio 44106.
REFERENCES Brusilow, S. W., Ikai, K., & Gordes, E. Comparative physiological aspects of solute secretion by the eccrine sweat gland of the rat. Proceedings of the Society of Experimental Biology and Medicine, 1968, 129, 731-732. Cage, G. W., & Dobson, R. L. Sodium secretion and reabsorption in the human eccrine sweat gland. Journal of Clinical Investigation, 1965 44, 1270-1276. Forbes, T. W. Skin potential and impedance responses with recurring shock stimulation. American Journal of Physiology, 1936, 117, 189199. Fowles, D. C., & Venables, P. H. The effect of epidermal hydration and sodium reabsorption on palmar skin potential. Psychological Bulletin, 1970, 73, 363-378.
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Ito, O. Palmar sweat electrolyte concentration in monkey: Effect of spironolaetone on the sweat electrolyte concentration and the possibility of reabsorption in the sweat duct. Nagoya Medical Journal, 1968, 19, 178-188. Kawai, M., Iwamoto, M., & Yoshiba, K. Monkeys of the world. Tokyo: Mainichi Press, 1968. Hunger, B. L., & Brusilow, S. W. An electron microscopic study of eccrine sweat glands of the cat foot and toe pads—Evidence for ductal reabsorption in the human. Journal of Biophysical and Biochemical Cytology, 1961, 11, 403-417. Sato, K. Sweat induction from an isolated eccrine sweat gland. American Journal of Physiology, 1973, 8KB, 1147-1152. Schulz, I., Ullrich, K. J., Fromter, E., Holzgreve, H., Frick, A., & Hegel, U. Mikropunktion und elektrische Potentialmessung an Schweissdnisen des Menschen. PflUgers Archiv fur die gesamte Physiologic des Menschen und der Tiere, 1965, 284, 360-372. Tajimi, T., Yamazaki, K., & Nimii, Y. Electrodes for recording the skin potential response in the free moving rat. Japanese Psychological Research, 1973, IB, 99-100. Tajimi, T., Yamazaki, K., Takei, H., & Niimi, Y. Activational and behavioral aspects of spontaneous skin potential responses in rats. Psychological Reports, 1973, 32, 1179-1181. Takagi, K., & Nakayama, T. Peripheral effector
mechanism of galvanic skin reflex. Japanese Journal of Physiology, 1959, 9, 1-7. Wang, G. H. The Neural control of sweating. Madison : University of Wisconsin Press, 1964. Wilcott, R. C. Effects of exsanguination on sweating and skin potential responses. Journal of Comparative and Physiological Psychology, 1962, 55, 1136-1137. Wilcott, R. C. The partial independence of skin potential and skin resistance from sweating. Psychophysiology, 1964 1, 55-66. Yamazaki, K., & Tajimi, T. What is skin potential level? Psychophysiology, 1972, 9, 650-652. Yamazaki, K., Tajimi, T., & Niimi, Y. The ontogeny of spontaneous skin potential responses in kittens during awake rest. Japanese Psychological Research, 1969, 11, 167-173. Yamazaki, K., Tajimi, T., Okuda, K., & Niimi, Y. Psychophysiological significance of skin potential activity in monkeys. Psychophysiology, 1972, 9, 620-623. (a) Yamazaki, K., Tajimi, T., Okuda, K., & Niimi, Y. Spontaneous skin potential responses during natural sleep in monkeys. Journal of Physiological Society of Japan, 1972, 84, 757-758. (b) Yokota, T., Takahashi, T., Kondo, M., & Fujimori, B. Studies of the diphasic wave form of the GSR. Electroencephalography and Clinical Neurophysiology, 1959,11, 687-696. (Received May 8, 1974)
Skin Potential Activity in Rats, Cats, and Primates (Including Man): A Phylogenetic Point of View Katuo Yamazaki Department of Neuropsychiatry, School of Medicine, Fujita Gakuen University, Aichi, Japan
Tetuo Tajimi Clinical Eleclroencephalography Laboratory, Isogo Hospital, Yokohama, Japan
Ken'ichi Okuda Japan Broadcasting Corporation, Tokyo, Japan
Yosizumi Niimi Tokyo Metropolitan Institute for Neurosciences, Tokyo, Japan
With rats, cats, nonhuman primates, and humans serving as subjects, skin potential activity was measured under waking conditions. In good agreement with the findings of previous workers, skin potential response waveform was always monophasic negative in rats and cats, but in humans it took three forms. By contrast, it was always monophasic positive in simian nonhuman primates, although prosimiae gave monophasic negative waves. A skin potential level-skin potential response relationship could not be observed in any subject except humans. From these results, an attempt was made to relate skin potential activity to the peripheral mechanism involved in these species on the basis of a phylogenetic point of view.
Since the pioneer work of Forbes (1936), many experiments have been concerned with the underlying mechanism of the waveform of the skin potential response (SPR) in humans. Three waveforms (monophasic negative, diphasic, and monophasic positive) have been recognized and described in detail as the typical patterns of the SPR (Wilcott, 1964). In other mammals, some studies, focused on a single species, have been done in primates (Takagi & Nakayama, 1959; Wilcott, Note 1; Yamazaki, Tajimi, Okuda, & Niimi, 1972a), in cats (Wang, 1964), and in rats (Tajimi, Yamazaki, Takci, & Niimi, 1973), but there seems to be a discrepancy among various results concerning the waveform of the SPR in these animals, especially in primates. Moreover, there has been no attempt to compare SPR waveforms in humans with those of other mammals on the phylogenetic scale. This research was performed at the Department of Neurophysiology, Primate Research Institute, Kyoto University, Inuyama. We wish to acknowledge our gratitude to the late T. Tokizane and to K. Kubota for their interest and help. Requests for reprints should be sent to K. Yamazaki, Department of Neuropsychiatry, Fujita Gakuen University, 1-98 Kutukake, Toyoake, Aichi 470-11, Japan.
The purposes of this research were (a) to measure the skin potential (SP) activity in various species—humans, nonhuman primates (primates, for short), cats, and albino rats (rats, for short)—and (b) to discuss the waveform of the SPR from a phylogenetic point of view. EXPERIMENT 1 Using an identical technique, the SP activity was measured precisely to make a systematic comparison across the mammals (rats, cats, primates, and humans) and to elucidate the phylogenetic significance of this electrodermal phenomenon of the sweat gland. Moreover, the SPR waveform in Macaca monkeys was measured for comparison with previous reports. Method Subjects. The subjects were 60 rats, 21 cats, 36 primates (1 Pan troglodytes, 13 Macaca fuscata, 9 Macaca mulatta, 1 Macaca irus, 1 Macaca cyclopis, 1 Macaca nemestrina, 1 Erythrocebus patas, 2 Saimiri sciureus, 1 Ateles geoffroyi, 1 Cebus capucinus, 2 Aotus trivirgatus, 2 Galago crassicaudatus and 1 Nycticebes coucang), and 87 humans of both sexes. All of them were intact, normal adults. Apparatus, The SP activity was measured with equipment having stable dc amplifiers with a high input impedance (San'ei, EG-129, EG-900, or Toa, EPR-3T). Two Ag-AgCl disc electrodes (standing
364
COMPARATIVE STUDY OF SKIN POTENTIAI/ACTIVITY potential of less than ±.2 mV), filled with agaragar .05 M NaCl, were attached by means of an adhesive vinyl tape, one active electrode to the foot pad (for rats and cats) or the palm (for primates and humans) and the reference electrode on a drilled skin area of the ipsilateral ankle (for rats and cats) or of the ipsilateral forearm (for primates and humans). Recording procedure. The SP activity of each subject was measured during the relaxed, motionless waking state for about 30 min. The rats and cats, which had been thoroughly accustomed to handling over the course of several months, were tested in a cage with a wood floor. The recording methods used in this study for rats and cats have been described in detail elsewhere (Tajimi, Yamazaki, & Niimi, 1973; Yamazaki, Tajimi, & Niimi, 1969). The primates were seated on a primate chair. Before recording, both arms of the primate were loosely tied to the chair to eliminate possible movement artifact. Most of the primates had been habituated to a primate chair, and their behavior indicated that they were accustomed to the experimental room. Human subjects were seated in a chair in a soundproof and electrically shielded room. The skin potential level (SPL) readings were made in each case just before the appearance of the SPR in each subject. Physical stimuli, such as a handclap, a burst of white noise, or a light flash, were used to evoke the SPR. Room temperature ranged 22° 0-28° C.
Results A purpose of this study was to compare the SP activity among mammals. Therefore, other kinds of analysis of the SPR, such as the time course or amplitude of a response, are not considered in this article. General patterns of SPR in primates. A sample record of the SPR in each primate species is shown in Figure 1. Classification of primates was based on Kawai, Iwamoto, and Yoshiba (1968). At a glance, one can see that Simiae produce only the monophasic positive wave. On the contrary, Prosimiae (G. crassicaudatus and N. coucang in this study) show only the monophasic negative wave. In any case, the diphasic waveform of the SPR was not recorded in primates in response to any stimulus used. We did not observe any monophasic negative waves from Simiae or monophasic positive waves from Prosimiae. General patterns of SP activities in rats, cats, primates, and humans. The waveform of the SPR in each species is shown in Figure 2. Rats and cats in the waking condition always gave monophasic negative waves to
365
any stimulus. In humans, three types of the SPR waveform (monophasic negative, diphasic, and monophasic positive) were recorded during measurements, which is in good agreement with previous reports (Forbes, 1936; Wilcott, 1964; Yokota, Takahashi, Kondo, & Fujimori, 1959). Primates show two types of the SPR waveform, as described above. Figure 3 is a schematic display of the waveform of the SPR obtained in this experiment. SPL differences among rats, cats, primates, and humans. The mean values of the SPL among species are shown in Table 1. The SPL in each species always maintained negativity during the measurement. No polarity change of the resting SPL from negativity to positivity was observed in any of the subjects. Concerning the SPL-SPR relationship, no species showed SPRs that actually effectively passed zero potential, making the palm or foot pad positive relative to the reference electrode. In human subjects, a low negativity of the SPL was associated with negative waves of the SPR, and high potential level was associated with positive waves; diphasic responses were recorded when the potential level was at an intermediate position, as indicated by Wilcott (1964). These SPL-SPR relationships, however, could not be observed in any subjects except humans. The SPL in rats and cats was less negative compared with primates. The maximum value was obtained in human subjects, as shown in Table 1.
EXPERIMENT 2 It was found that Simiae gave only positive potential waves in Experiment 1. The result was not in accord with previous reports by Takagi and Nakayama (1959) and Wilcott (Note 1) on Macaca monkeys. Additional lines of approach were needed to account for the discrepancy. The appearance of only positive waves has been already confirmed uneer a wide spectrum of alert, resting, and sledping conditions in Macaca monkeys (Yamazaki, Tajimi, Okuda, & Niimi, 1972a, 1972b). Therefore, an attempt was made to see whether variations in room temperature and exsanguination, which would influence factors critical for the waveform of the SPR
YAMAZAKI, TAJIMI, OKUDA, AND NIIMI
366
Pongidae
P. lro(loljtis
M. In still ». mlitti
Cercopithecidae Simiae E. pill!
Primates
». li.llni
Cebidae C. cipucinus
Prosimiae
Lorisidae
6. trmicuditll
5»V
''H^tH1^^
40 IK
FIGURE 1. The waveform of the skin potential response (SPR) in the nonhuman primate. (Spontaneous SPRs are also mixed in each record. Movement artifacts appear after approximately 90 sec and at the end of a record in C. capucinus. Negativity at the active electrode is indicated by an upward deflection.)
in humans (Wilcott, 1962; Yokota et al., 1959), could influence the SPR waveform of Macaca monkeys. Method Subjects. Four monkeys of both sexes (two Macaca mulatto and two Macaca fuscata) were used as subjects. All were intact, normal adults. Apparatus. The recording equipment was the same as that used in Experiment 1. For the study of the effect of temperature on the SPR, an artificial meteorological room was used, in which both temperature and humidity could be regulated. Recording procedure: Temperature effect. Set ting the humidity of the artificial meteorological room at a constant level (60%), the temperature was changed from 15° C to 35° C or vice versa at 5° C steps at about 10-min intervals. Each subject was brought into the room and seated on the primate chair with the electrode system prepared as described in Experiment 1.
Exsanguination effect: By fastening one wrist of a primate to stop the blood supply to the palm, the effect of exsanguination on the SPR waveform was studied under normal temperature. Before exsanguination, SPRs of both palms were recorded for several minutes simultaneously. During this control record, there were scarcely any differences in amplitude and waveform of the SPR between the two palms. During exsanguination of one palm, concurrent recordings were continued with the exsanguinated palm as the experimental and with the intact one as the nontreated control for 20 min. Recordings were also made after releasing exsanguination.
Results Temperature effect. With an increase in the room temperature, the frequency of the spontaneous SPR was enhanced as shown in Figure 4. These temperature-dependent rela-
367
COMPARATIVE STUDY OF SKIN POTENTIAL ACTIVITY
RAT
PRIMATE
HUMAN
I 5 nV
FIGURE 2. General patterns of the skin potential response (SPR) waveform in the rat, cat, nonhuman primate, and human. (Spontaneous SPRs also appear in these measurements.)
tionships with the SPR were observed in all primates. However, neither negative nor diphasic potential waves were observed over a wide range of room temperatures. Obtained SPRs were always positive waves. Temperature variation produced no observable effects on this waveform. Exsanguination effect. Before exsanguination, positive potential waves always appeared in both palms in Macaca monkeys. Although positive waves were reduced in amplitude during the initial course of exsanguination in the experimental palm, no polarity change of the waveform was observed during this phase. With a complete exsanguination of the experimental palm, the potential change almost disappeared, while positive waves were still recorded from the control palm as shown in Figure 5. The SPL increased appreciably in negativity, while the amplitude of the positive wave decreased during exsanguination. Neither negative nor diphasic potential waves appeared in the experimental palm in these periods, but very small positive waves were observed simultaneously with the large positive waves in the control palm. Several minutes after removal of the fastener to allow the blood to return to the palm, positive waves appeared in the experimental palm, which could not be differentiated from those in the control palm. These observations were obtained in all primates tested.
DISCUSSION Various waveforms of the SPR were obtained in the mammals in this experiment, although a fairly constant species-specific waveform was also observed. As to humans, the waveform of the SPR showed patterns similar to those described by previous workers (Forbes, 1936; Wilcott, 1964). The finding of monophasic negative potential waves in the waking rat seems to be a new discovery. On the other hand, a waveform similar to that in the rat was also recorded in the waking cat, which was in good agreement with previous reports by Wang (1964) and others. Takagi and Nakayama (1959) used only one primate (Macaca fuscata) and recorded the SPR in the waking condition. They found that the waveform of the SPR was always a monophasic negative deflection. Using two waking primates (Macaca mulatta) as subjects, Wilcott (Note 1) recorded monophasic negative, diphasic, and monophasic positive waves of the SPR, which appeared to be essentially the same as those recorded from humans. Concerning the diphasic and monophasic positive wave in primates, Wilcott suggested that the heightened arousal produced by the restraint of being tied brought about such an electrical phenomenon. However, all macaques (13 Macaca fuscata and 9 Macaca mulatta) always showed monophasic positive waves in the present experiment even when their RAT
CAT
PRIMATE inme
HUMAN
Simiae
FIGURE 3. Schematic display of the skin potential response (SPR) waveform in mammals. (First row is monophasic negative waves; second, a diphasic; and bottom, monophasic positive. Blank area indicates that the waveform described could not be observed.)
YAMAZAKI, TAJIMI, OKUDA, AND NIIMI
368
TABLE 1 MEAN SKIN POTENTIAL LEVEL (SPL) AMONG MAMMALS SPL (in mV)
Rat Cat
Primate Human
60 21 36 87
M
SD
-8.8
3.49 3.59 5.16 6.72
-8.9 -14.7 -42.7
arousal level was low as judged from their behavior. The animals were so adapted to the restraints that they could be considered in a resting state. Moreover, temperature variation or exsanguination did not affect this potential wave, which was in sharp contrast to previous reports in humans (Wilcott, 1962; Yokota et al., 1959). In addition, in a previous study only the monophasic positive wave could be observed during the natural sleep-wake spectrum in Macaca monkeys (Yamazaki et al., 1972b). Therefore, there is no reason to relate these waveforms to the heightened or lowered arousal in primates. The discrepancy of these findings in Macaca monkeys may be caused by methodological differences such as the treatment of a reference site or preparations of the electrode system. At any rate, Simiae showed only monophasic positive waves, and Prosimiae showed only monophasic negative waves like those recorded from rats and cats. It has been noted that the precursor sweat obtained at the upper part of the sweat duct is isotonic or slightly hypertonic (Cage & Dobson, 1965). Therefore, the reabsorption mechanism in the human sweat duct is thought to be responsible for the hypotonicity of the sweat collected at the sweat pores over the human skin surface (Schulz, Ullrich, Fromter, Holzgreve, Frick, & Hegel, 1965). Sweat secreted in the monkey palm (Macaca fuscata and Macaca mulatto) was found to be hypotonic (Ito, 1968; Sato, 1973). Sweat collected from the sweat gland of the hairless footpad of the cat and of the rat was found to be hypertonic (Brusilow, Ikai, & Gordes, 1968; Munger & Brusilow, 1961). The anatomical comparison of the sweat glands of rats, cats, and humans
reveals that the glands of rats and cats have a short and thin duct segment whose epithelial cells contain very few mitochondria, whereas the duct of humans is long and coiled, and the epithelial cells have abundant mitochondria when examined under the light and the electron microscope. Substantial differences in the ductal part of the sweat gland indicate that sodium reabsorption does not occur in the duct of the cat or rat sweat gland (Brusilow et al., 1968; Munger & Brusilow, 1961). On the basis of this theory, Fowles and Venables (1970) proposed that the mechanism of the ductal reabsorption of sodium from sweat might account for the large negative potentials and also for the large positive waves recorded in humans. Applying their proposed hypothesis to other animals, one can see the SPL differences among species in connection with the degree of sodium reabsorption in the sweat gland. The MJ_
30DC
40 sec FIGURE 4. Effect of temperature on the skin potential response (SPIi) in Macaca monkeys.
COMPARATIVE STUDY OF SKIN POTENTIAL ACTIVITY normal
M.f.f.
, 4min
, 12 min
after 7 min
..: L .
40 sec FIGURE 5. Effect of exsanguination on the skin potential response (SPR) in Macaca monkeys. (Curves show the SPR before exsanguination, A; during course of exsanguination of left, L, palm, B and C; and after recovery, D.)
largo negativity in SPL in humans and primates may be attributed to sodium reabsorption in the sweat gland. By contrast, the small negativity in rats and cats can probably result from the lack of ductal reabsorption of sodium in their sweat glands. This proposal suggests some connection between sodium reabsorption and the positive component of the SPR, since Wang (1964) and others have consistently reported that responses from the cat footpad are always monophasic negative waves (Fowles & Venables, 1970).
369
At present, this sodium pump theory appears to be appropriate for the explanation of the peripheral mechanism involved in this electrical phenomenon of the skin. However, it can not explain why Simiae show only monophasic positive waves in spite of the existence of the SPL values like those of rats and cats rather than of humans, and why Simiae do not show monophasic negative and diphasic waveforms like those of humans. The SPL-SPR relationship observed in humans seems to be inapplicable to other animals under natural conditions. The fact that SPRs immediately disappear after peripheral denervation and the SPL remains at the same negativity level as before (Yamazaki & Tajimi, 1972) suggests the possibility of a different origin for the SP activity. There still remain many problems concerning the precise mechanism of the SP activity in the sweat glands. Further work and another line of evidence; concerning the bioelectrical and biochemical properties of the sweat glands are needed to elucidate the peripheral mechanism responsible for SP activity in mammals. In any event, the observation of SP activity might offer some cue for understanding the evolutionary aspects involved in the sweat gland activity in mammals. REFERENCE NOTE 1. Wilcott, R. C. Observations of skin potential, skin resistance and sweating of two rhesus monkeys. Unpublished manuscript, 1965. (Available from R. C. Wilcott, Department of Psychology, Case Western Reserve University, Cleveland, Ohio 44106.
REFERENCES Brusilow, S. W., Ikai, K., & Gordes, E. Comparative physiological aspects of solute secretion by the eccrine sweat gland of the rat. Proceedings of the Society of Experimental Biology and Medicine, 1968, 129, 731-732. Cage, G. W., & Dobson, R. L. Sodium secretion and reabsorption in the human eccrine sweat gland. Journal of Clinical Investigation, 1965 44, 1270-1276. Forbes, T. W. Skin potential and impedance responses with recurring shock stimulation. American Journal of Physiology, 1936, 117, 189199. Fowles, D. C., & Venables, P. H. The effect of epidermal hydration and sodium reabsorption on palmar skin potential. Psychological Bulletin, 1970, 73, 363-378.
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Ito, O. Palmar sweat electrolyte concentration in monkey: Effect of spironolaetone on the sweat electrolyte concentration and the possibility of reabsorption in the sweat duct. Nagoya Medical Journal, 1968, 19, 178-188. Kawai, M., Iwamoto, M., & Yoshiba, K. Monkeys of the world. Tokyo: Mainichi Press, 1968. Hunger, B. L., & Brusilow, S. W. An electron microscopic study of eccrine sweat glands of the cat foot and toe pads—Evidence for ductal reabsorption in the human. Journal of Biophysical and Biochemical Cytology, 1961, 11, 403-417. Sato, K. Sweat induction from an isolated eccrine sweat gland. American Journal of Physiology, 1973, 8KB, 1147-1152. Schulz, I., Ullrich, K. J., Fromter, E., Holzgreve, H., Frick, A., & Hegel, U. Mikropunktion und elektrische Potentialmessung an Schweissdnisen des Menschen. PflUgers Archiv fur die gesamte Physiologic des Menschen und der Tiere, 1965, 284, 360-372. Tajimi, T., Yamazaki, K., & Nimii, Y. Electrodes for recording the skin potential response in the free moving rat. Japanese Psychological Research, 1973, IB, 99-100. Tajimi, T., Yamazaki, K., Takei, H., & Niimi, Y. Activational and behavioral aspects of spontaneous skin potential responses in rats. Psychological Reports, 1973, 32, 1179-1181. Takagi, K., & Nakayama, T. Peripheral effector
mechanism of galvanic skin reflex. Japanese Journal of Physiology, 1959, 9, 1-7. Wang, G. H. The Neural control of sweating. Madison : University of Wisconsin Press, 1964. Wilcott, R. C. Effects of exsanguination on sweating and skin potential responses. Journal of Comparative and Physiological Psychology, 1962, 55, 1136-1137. Wilcott, R. C. The partial independence of skin potential and skin resistance from sweating. Psychophysiology, 1964 1, 55-66. Yamazaki, K., & Tajimi, T. What is skin potential level? Psychophysiology, 1972, 9, 650-652. Yamazaki, K., Tajimi, T., & Niimi, Y. The ontogeny of spontaneous skin potential responses in kittens during awake rest. Japanese Psychological Research, 1969, 11, 167-173. Yamazaki, K., Tajimi, T., Okuda, K., & Niimi, Y. Psychophysiological significance of skin potential activity in monkeys. Psychophysiology, 1972, 9, 620-623. (a) Yamazaki, K., Tajimi, T., Okuda, K., & Niimi, Y. Spontaneous skin potential responses during natural sleep in monkeys. Journal of Physiological Society of Japan, 1972, 84, 757-758. (b) Yokota, T., Takahashi, T., Kondo, M., & Fujimori, B. Studies of the diphasic wave form of the GSR. Electroencephalography and Clinical Neurophysiology, 1959,11, 687-696. (Received May 8, 1974)
