J. therm. Biol. Vol. 15, No. 3/4, pp. 255-258, 1990 0306-4565/90 $3.00 + 0.00 Printed in Great Britain. All rights reserved Copyright © 1990 Pergamon Press pie

IS THERE MODAL OPPONENCY IN THE THERMAL SENSES?

ROBERTO REFINETTI

Department of Psychology, University of Illinois, Champaign, IL 61820, U.S.A.

(Received 1 July 1989; accepted in revised form 27 October 1989)

Abstract--1. The sensations evoked by pairs of distinct thermal stimuli applied to the back of the hand were studied in 17 volunteer subjects. Four stimulus combinations were used; neutral--cold (NC), neutral-neutral (NN), neutral-warm (NW), and cold-warm (CW).

2. The subjects were first asked to estimate the magnitude of the thermal sensations evoked by the thermal stimuli. On average, the four pairs were reported as increasing in magnitude in the following order: NC, CW, NN, and NW, seeming to suggest that the subjects experienced the cold-warm combination as a composite sensation of cold and warmth intermediate between pure cold and pure warmth.

3. When asked only to detect the presence of a cold stimulus, the subjects performed as well for the CW combination as for the CN combination. This second result indicates that the reported composite magnitude of CW does not result from a true opponency of cold and warmth but from a cognitive combination of distinct sensations of cold and warmth.

Key Word Index: Thermal sense; psychophysics; perception; sensory opponency; man

INTRODUCTION

For over half a century, evidence has accumulated that the thermal sense is composed not of a single sensory modality but of two distinct modalities: cold and warmth. First, thermal stimulation of distinct spots on the skin evokes either a warm or a cold sensation, the so-called warm and cold spots (Rein, 1925; Strughold and Porz, 1931). Second, distinct first-order afferent fibres are either myelinated and react with a positive dynamic response only to cold stimulation of the skin (Kenshalo and Duclaux, 1977; Hensel and Boman, 1960) or are non-myelinated and react with a positive dynamic response only to warm stimulation of the skin (Duclaux and Kenshalo, 1980; Konietzny and Hensel, 1975). Third, magnitude esti- mation functions for thermal stimulation of the skin show distinct exponents for warm and cold stimuli (Stevens and Stevens, 1960). Fourth, reaction time to thermal stimuli of equivalent intensity is shorter for cold stimuli than for warm stimuli (Fruhstorfer et al., 1972, 1974). Finally, electroencephalographic evoked potentials have shorter latency for cold than for warm stimulation of the skin (Chatt and Kenshalo, 1977; Fruhstorfer et al., 1976).

In apparent contradiction to the evidence for separate systems of warm and cold sensations, it has been shown that subjects are able to judge cold and warm sensations along a single continuum of thermal sensation if asked to do so (Attia and Engel, 1981; Banks, 1969) and that simultaneous cold and warm stimulation may evoke a sensation that is a composite of the sensations evoked by independent stimulation (Hall and Klemm, 1969; Young, 1987). However, the fact that subjects can integrate simultaneous warm and cold stimulation in their reports along a single dimension of sensory magnitude does not imply that the composite sensations are truly unidimensional. In

other words, a distinction must be made between (1) a situation in which the subjects are able to discrimin- ate the two sensations but are requested to report a composite sensation and (2) a situation in which the two sensations actually cancel one another through an opponency of warmth and cold operating at some level prior to conscious awareness. In the present experiment, the need for such a distinction was obtained by asking the subjects to judge pairs of thermal stimuli both by magnitude estimation and by modal detection.

MATERIALS AND METHODS

Subjects

Ten male and 7 female volunteer subjects were recruited on campus from the undergraduate, gradu- ate, and faculty population. None of the subjects was familiar with the purpose or details of the experiment.

Apparatus

The thermal stimulators consisted of water- perfused thermodes made of copper tubing. Ex- ternally, the base of each thermode was 5 mm dia. In order to control thermode temperature, water from different baths maintained at constant temperatures was circulated through the thermodes. The tempera- ture of the thermode tip was monitored with a Sensortek BAT-12 thermocouple meter and IT-23 probes. Pilot tests showed that thermode temperature was not significantly affected by contact with the skin.

In order to obtain simultaneous contact of both thermodes with the skin, the two thermodes were attached to a solenoid-driven frame. The subject was asked to hold a rubber handle so that the stimulators located above could hit always the same site on the back of the hand. The distance between the two

255

256 ROBERTO REFINETTI

thermodes was kept constant at 10mm centre-to- centre (5 mm between edges), which is well within the area of high spatial summation and low spatial resolution for the thermal senses (Cain, 1973; Stevens et al., 1974). All stimulus presentations had durations of 3 s, as controlled by an electronic timer. Ambient temperature in the room was kept constant at 21°C for the whole experiment.

Procedure

Each session consisted of two parts. The first part consisted of a magnitude estimation task. Stimuli of different temperatures were presented and the subject was asked to estimate their magnitude. Perceived magnitude was reported verbally as a single number at the end of each stimulus presentation. Four combinat ions were presented three times each as follows: (1) neutral-cold (NC), where one stimula- tor was kept at 33°C (which is felt as neutral by most subjects) and the other at 25°C (which is perceived as cold), (2) neutral-neutral (NN), where both stimula- tors were kept at 33°C, (3) neut ra l -warm (NW), where one stimulator was kept at 33°C and the other at 41~C (which is perceived as warm or hot), and (4) co ld-warm (CW), where one stimulator was main- tained at 25°C and the other at 41°C. Before the beginning of data collection, an N C stimulus was presented and the subject was instructed to call it "magni tude 1" and to estimate the magnitude of upcoming stimuli in relation to the reference magni- tude "1" . The subject was, therefore, strongly encour- aged to estimate the magnitude of cold and warm stimuli along a same continuum. In pilot studies, subjects were tested also under conditions of smaller temperature differences (28-33-38°C or 31-33-35°C). Estimates of magnitude were equally accurate for large and medium differences (25-33-41°C and 28-33-38°C) but became erratic for small differences (31-33-35°C).

After an intermission of a few minutes, the second part of the session was initiated. The same stimuli from the first part were presented, but the subject was now asked to pay attention to the fact that there were two distinct stimulators. For each stimulus combina- tion, the subject was asked to try to detect the presence of a cold stimulus (independently of its being on the left or on the right).

In order to confirm the assumed low spatial resolution of the thermal sense, 10 subjects were also tested in a warm localization task. In this task, a combinat ion of 30 and 36°C was presented 20 times, the warmer stimulus being on the right in 10 of the presentations and on the left in the other 10 presentations. The subject was asked to tell which stimulator (left or right) was warmer. After these 20 trials, 20 more trials were conducted with a com- bination of 36 and 42°C. Thus, in both situations the subject was presented with 6°C difference, but in one case the two temperatures were symmetrically placed about the neutral temperature (30 vs 36°C) whereas in the other, the two temperatures were both above the neutral temperature (36 vs 42°C). Pain sensation is evoked by temperatures above 45°C and therefore was not involved in the present study.

6

o

NC CW NN NW

Fig. l. Magnitude estimation of four combinations of thermal stimuli. Each stimulus combination was presented 3 times to each subject. Each bar shows the mean ( + SEM) for 17 subjects. N: neutral (33°C), C: cold (25°C), W: warm

(41~'C).

Statistics

Differences in the mean magnitude estimation for the four stimulus combinations were tested by para- metric analysis of variance (Fisher's F test). Differ- ences in the cold detection task were tested by nonparametric analysis of variance (Friedman's test). Performance in the warm localization task was evalu- ated by means of a binomial test (n = 20, P = 0.5).

RESULTS

The mean magnitude estimation results for the 17 subjects are shown in Fig. 1. The estimates for the different stimuli are clearly distinct [F(3,48)= 16.85, P < 0.01], the warm stimulus (NW) being perceived as the warmest and the cold stimulus (NC) as the least warm (or the coldest). The cold-warm combination (CW) was perceived as an intermediate sensation, slightly less warm than the neutral combinat ion (NN). These mean results (n = 17) represent very well the results of 14 of the subjects. The remaining 3 subjects differed in some respects. One subject per- ceived WC as warmer than NW, another subject perceived CW as colder than NC, and the last subject paradoxically perceived NC as warmer than NW.

The mean results for the cold detection task are shown in Fig. 2. There is a clear effect of stimulus combinat ion on cold detection [X2(3) = 32.94, P < 0.01]. The subjects rarely detected a cold stimu- lus when it was not present (NN and NW) and

o

NC CW NN NW

Fig. 2. Number of detections of a cold stimulus in four combinations of thermal stimuli. Each stimulus combina- tion was presented 3 times to each subject. Each bar shows the mean (+ SEM) for 17 subjects. N: neutral (33°C), C:

cold (25°C), W: warm (41°C).

Thermal opponency 257

Table 1. Warm localization (number of correct answers in 20 trials)

Subject Condition

30 vs 36°c 36 vs 42°c 1 8 10 2 9 9 3 9 8 4 11 11 5 12 8 6 13 10 7 15" 8 8 15. 11 9 16" 10

10 17. 9

*P < 0.05.

detected it most of the time when it was present either alone (NC) or simultaneously with a warm stimulus (CW). Again, the mean results represent well the performance of 14 of the subjects. Three of the subjects (not the same three mentioned above) consis- tently detected cold in N W or did not detect cold in NC.

The performance of 10 subjects in the warm local- ization task is shown in Table 1. In the cold vs warm condition, four subjects were consistently able to tell which of the two stimulators was warmer, whereas the performance of the other subjects could be explained by chance alone. None of the subjects, however, performed better than chance in the 36 vs 42°C condition.

DISCUSSION

Although young children are not fully capable of estimating the magnitude of single thermal stimuli (Refinetti, 1988), adults can make such estimates with ease and precision (Refinetti, 1989; Stevens and Stevens, 1960). In the present study, adult subjects estimated the magnitude of pairs of thermal stimuli presented simultaneously. The W N combinat ion was perceived as warmer than the N N combination, and this was perceived as warmer than the N C combin- ation. In agreement with a previous relevant study (Young, 1987), although in disagreement with an indirect investigation of the same phenomenon (Green, 1977), the simultaneous presentation of warm and cold stimuli evoked a composite sensation. In the particular experimental conditions of the present study, CW was perceived as warmer than NC but cooler than NN. Thus, the combinat ion of two temperatures that were equidistant from neutrality (i.e. 33 - 8 = 25°C, and 33 + 8 = 41°C) produced a sensation predominantly cold. Further studies on stimulus combinations are necessary to confirm this apparent predominance of the cold sensation.

The ability to estimate the magnitude of the CW combinat ion as intermediate between NC and N W was not due to true sensory opponency. Thus, when the subjects were asked to just detect the presence of a cold stimulus, their performance was as good for the CW combination as for the N C combination. This means that the warm stimulus did not disturb at all the perception of the simultaneously presented cold stimulus.

The failure to observe true opponency could be due to a failure in restricting stimulation to the area of

spatial summation on the skin. Previous research on the warmth sense has indicated that the area of spatial summation for warmth sensation is quite large (Cain, 1973; Stevens et al., 1974), but the present experimental conditions might have presented a unique stimulating situation. The results of the warm localization task indicate that 75 mm 2 is indeed within the area of summation and low resolution for the warmth sense (36 vs 42°C condition). It just happens that warm and cold can be distinguished from each other with a much higher spatial acuity. It would seem that warm and cold do not summate spatially at all, and further research should investigate this inference.

In short, the present experimental results strongly suggest that there is no real opponency between warm and cold senses. The composite sensation reported by the subjects for the CW combination is much more likely due to a cognitive integration of distinct sensations of cold and warmth.

Acknowledgements--The author is deeply grateful to Dr Jack M. Loomis for his advice during the design of the experiment and for his comments on an earlier version of the paper. Dr Harry J. Carlisle generously provided lab space and equipment at the University of California, Santa Barbara. This work was partly supported by U.S. Public Health Service Award Institutional Grant No. MH18412.

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