Modulation of the thermoregulatory sweating response to mild hyperthermia during activation of the muscle metaboreflex in humans

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Modulation of the thermoregulatory sweating response to mild hyperthermia during activation of the muscle metaboreflex in humans

Narihiko Kondo, Hirotaka Tominaga, Manabu Shibasaki, Ken Aoki, Shunsaku Koga * and Takeshi Nishiyasu ¹

Laboratory for Applied Human Physiology, Faculty of Human Development, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe 657-8501, * Applied Physiology Laboratory, Kobe Design University, Kobe 651-2129 and ¹ Department of Medical Humanities and Sciences, School of Medicine, Yamaguchi University, Yamaguchi 753-0841, Japan

MS 8382 Received 22 June 1998; accepted after revision 26 November 1998.

ABSTRACT

Top
Abstract
Introduction
Methods
Results
Discussion
References

To investigate the effect of the muscle metaboreflex on the thermoregulatory sweating response in humans, eight healthy male subjects performed sustained isometric handgrip exercise in an environmental chamber (35 �C and 50 % relative humidity) at 30 or 45 % maximal voluntary contraction (MVC), at the end of which the blood circulation to the forearm was occluded for 120 s. The environmental conditions were such as to produce sweating by increase in skin temperature without a marked change in oesophageal temperature.

During circulatory occlusion after handgrip exercise at 30 % MVC for 120 s or at 45 % MVC for 60 s, the sweating rate (SR) on the chest and forearm (hairy regions), and the mean arterial blood pressure were significantly above baseline values (P < 0�05). There were no changes from baseline values in the oesophageal temperature, mean skin temperature, or SR on the palm (hairless regions).

During the occlusion after handgrip exercise at 30 % MVC for 60 s and during the occlusion alone, none of the measured parameters differed from baseline values.

It is concluded that, under mildly hyperthermic conditions, the thermoregulatory sweating response on the hairy regions is modulated by afferent signals from muscle metaboreceptors.

	INTRODUCTION

Top Abstract Introduction Methods Results Discussion References

In humans, increasing the sweating rate is the main way of dissipating excess heat from the body during exercise in a warm environment, since the evaporation of sweat is the only way to lose heat when the ambient temperature is higher than the skin temperature. The main thermal factors associated with regulation of the sweating response are changes in the core and skin temperatures (Nielsen, 1969; Nadel et al. 1971; Kondo et al. 1998). In addition, it has been hypothesized that the sweating response may be modulated by several non-thermal factors: (1) peripheral mechanisms activating the mechanosensitive (Van Beaumont & Bullard, 1963; Gisolfi & Robinson, 1970; Kondo et al. 1997) and metabosensitive receptors in the exercising muscles, (2) central command signals linked with volitional effort (Yamazaki et al. 1994; Kondo et al. 1997; Vissing, 1997), and (3) emotional and mental stimuli (Ogawa, 1975). Since activation of the metabosensitive receptors in the active muscles might be enhanced during moderate to intense exercise, it may be that the sweating response is under the influence of the muscle metaboreflex. However, the effects of the metaboreflex on the sweating response are not known.

Occluding the circulation to the forearm just before the end of isometric handgrip exercise keeps the systemic arterial blood pressure and muscle sympathetic nerve activity above their resting levels, leading to the conclusion that chemosensitive afferents within the muscle are responsible for these increases (Mitchell & Schmidt, 1983; Victor et al. 1988; Rowell & O'Leary, 1990; Saito et al. 1990; Vissing, 1997; Nishiyasu et al. 1998). Vissing (1997) has reported that, during post-exercise muscle ischaemia, skin sympathetic nerve activity (including vasoconstrictor, sudomotor and vasodilator activity) and electrodermal activity (measured as an index of sudomotor changes in the hairy regions of the body) did not vary from resting levels under normothermic conditions. Further, Saito et al. (1990) indicated that in a hairless region (foot) skin sympathetic nerve activity was not influenced by post-exercise muscle ischaemia under normothermic conditions. Recently, however, it was shown that cutaneous vasodilatation, which may be associated with the thermoregulatory sweating response, was only influenced by muscle metaboreceptor activation in hyperthermia and not in normothermia (Crandall et al. 1998). These results suggest that the effect of activation of muscle metaboreceptors on thermoregulatory responses (both sweating and changes in skin blood flow) may differ depending on the thermal conditions. However, there is no actual evidence that the sweating response is modulated during activation of the muscle metaboreflex in hyperthermia (when sweating has already been initiated). Furthermore, although the sweating response in the hairy regions is known to differ from that in hairless regions (palm and foot), where mental and emotional sweating occurs (Kuno, 1956; Ogawa, 1975; Sakakibara et al. 1989), regional differences in the effect of the muscle metaboreflex on the thermoregulatory sweating response have not previously been studied.

The purpose of this study was to examine whether the thermoregulatory sweating response can be modulated by the muscle metaboreflex and if so, whether there are any regional differences in the modulation of the response. To this end, we measured the sweating response in three regions (palm, chest and forearm) during post-exercise ischaemia (circulatory occlusion after sustained isometric exercise) under environmental conditions in which sudomotor activity was enhanced by thermal stimulation without a marked change in core body temperature.

METHODS

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Abstract
Introduction
Methods
Results
Discussion
References

Subjects

The experiments were performed on eight healthy male subjects with the following morphometric characteristics (means � S.D.): age 23�9 � 2�5 years, height 1�71 � 0�05 m and mass 69�0 � 8�5 kg. Each subject was informed in advance of the purpose of the study and the procedures involved, and their consent was obtained. This study was approved by the Human Subjects Committee of our university.

Procedures

Four experiments were conducted on each subject, with only one individual being tested on a given day. All experiments were conducted in an environmental chamber (SR-3000; Nagano Science Co. Ltd, Osaka, Japan) maintained at an ambient temperature of 35�C and a relative humidity of 50 % with minimal air movement. We selected these environmental conditions (mildly hyperthermic conditions) to produce sudomotor activity by increasing the skin temperature without a marked change in core body temperature. After entering the chamber, each subject rested in the supine position for about 90 min until the sweating rate reached a steady state. During this time, the monitoring instruments were attached. After a 30 min period of rest, each subject twice performed a maximal voluntary contraction (MVC) with his right hand using a handgrip dynamometer. We used the higher value to determine the relative workload (30 and 45 % MVC). After this, the subjects rested again for about 60 min and then baseline data were recorded for 5 min at rest before the isometric handgrip exercise. The subject then maintained an isometric handgrip at either 30 % MVC for 60 s, 30 % MVC for 120 s or 45 % MVC for 60 s. In all cases, a visual feedback system was used so that the subject could maintain the force throughout the exercise period. Starting 5 s before the end of each exercise, a cuff around the right upper arm was inflated to a supersystolic pressure (> 240 mmHg) for 120 s. After the occlusion, the cuff was deflated and recovery data were recorded for 120 s. This protocol makes it possible to investigate the effect of the muscle metaboreflex on the sweating response, since the muscle metaboreceptor afferents are activated during the post-handgrip forearm ischaemia while the muscle relaxation eliminates both central command and stimulation of the muscle mechanoreceptor afferents (Mitchell & Schmidt, 1983; Victor et al. 1988; Rowell & O'Leary, 1990; Saito et al. 1990; Vissing, 1997; Nishiyasu et al. 1998). Since skin sympathetic nerve activity is influenced by respiration (Delius et al. 1972), we asked the subjects to keep their respiratory frequency at 12 breaths min^-1 during the periods of rest, handgrip exercise, post-exercise muscle ischaemia and recovery with the aid of auditory signals. To minimize muscular fatigue, the experiments were done in a random order with at least a 10 min rest between experiments (four experiments were done: the three combinations of exercise intensity and duration, and occlusion alone).

Measurements

In all experiments, measurements were made of oesophageal temperature (T_oes), local skin temperature at eight sites on the body (chest, forearm, palm, forehead, abdomen, thigh, lower leg and foot), local sweating rate (SR) on the chest, forearm and palm, blood flow in the skin (SkBF) of the chest and forearm, heart rate (HR), and arterial blood pressure (systolic and diastolic). HR was measured continuously from an electrocardiogram. The arterial blood pressure was measured in the left middle finger by the Penaz method (Finapres; Ohmeda Co. Ltd, USA). Mean arterial blood pressure (MAP) was calculated as the diastolic pressure plus one-third of the pulse pressure. Temperature parameters were measured using a copper-constantan thermocouple. One thermocouple, with a silicon lubricant on the tip, was inserted through the nose into the oesophagus to a distance equal to one-quarter of the subject's height. Mean skin temperature ( T-bar _sk) was calculated according to the method of Hardy & Dubois (1938).

The SR on the three body sites was measured continuously by the ventilated capsule method (Van Beaumont & Bullard, 1963; Nadel et al. 1971; Ogawa, 1975; Yamazaki et al. 1994; Kondo et al. 1998). Dry nitrogen gas was supplied to three capsules (chest and forearm: 7�06 cm²; palm: 1�53 cm²) at a rate of 1�5 l min^-1 and the humidity of the nitrogen gas flowing out of the capsules was measured using a capacitance hygrometer (HMP 133Y; Vaisala, Finland). The time delay of this system for measuring SR was 1 s and was counted for calculating SR. Changes in SkBF were followed continuously by laser Doppler velocimetry (ALF21; Advance, Japan). Cutaneous vascular conductance (CVC) for each site was calculated from the ratio of skin blood flow to MAP. At each measurement site, the probe for measuring SkBF was located within 1 cm of the ventilated capsule. The various temperatures, SR and SkBF were recorded every second, and the data were stored in a personal computer (PC9801RA; NEC Co. Ltd, Japan) using a data logger (HR2300; Yokogawa Co. Ltd, Japan).

Statistics

Values were calculated for the following periods: a 30 s pre-exercise period (rest), the final 30 s of the handgrip exercise (handgrip), the final 30 s of the post-exercise ischaemia (occlusion) and the final 30 s of the recovery (recovery). The data are presented as means � S.E.M. A two-way analysis of variance was performed (with Sheffe's test being used when F values were significant) to compare the data across the periods of rest, handgrip exercise, post-exercise muscle ischaemia and recovery. The P value for significance was set at 0�05.

RESULTS

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Abstract
Introduction
Methods
Results
Discussion
References

Figure 1A shows the levels of the body temperature parameters (T_oes and T-bar _sk), HR, MAP, SkBF (chest and forearm) and SR (chest, forearm and palm) at rest, during handgrip exercise at 45 % MVC for 60 s, during post-exercise forearm ischaemia and during recovery. During the initial 90 min exposure to the environmental conditions, SR values were 0�10 � 0�02 mg cm^-2 min^-1 on the chest, 0�09 � 0�02 mg cm^-2 min^-1 on the forearm and 0�19 � 0�02 mg cm^-2 min^-1 on the palm in all experiments. T_oes and T-bar _sk were essentially constant during the periods of handgrip exercise, occlusion and recovery. HR and SkBF increased during the handgrip and returned to pre-exercise levels during the occlusion. In contrast, MAP and SR on the chest and forearm increased during the handgrip exercise and subsequently remained above their resting level until the end of the occlusion period. Occlusion alone did not affect any of the parameters monitored (Fig. 1B).

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Figure 1. Responses of measured parameters during a handgrip exercise and occlusion
A, changes in oesophageal temperature (T_oes), mean skin temperature ( T-bar _sk), heart rate (HR), mean arterial blood pressure (MAP), blood flow in the skin (SkBF) of the chest and forearm, and local sweating rate (SR) on the chest, forearm, and palm. The data were obtained at rest, during handgrip exercise for 60 s at 45 % maximal voluntary contraction (MVC), during post-exercise ischaemia (occlusion) for 120 s and during the recovery. Values are means � S.E.M. for 8 subjects. B,the effect of circulatory occlusion alone on the same parameters as in A. Values are means � S.E.M. for 8 subjects.

During the periods of handgrip exercise at 30 % MVC for 120 s and at 45 % MVC for 60 s, HR, MAP and SR on the chest, forearm and palm all increased significantly from resting levels (Figs 2 and 3, P < 0�05). During the muscle ischaemia after handgrip exercise at 30 % MVC for 60 s, MAP and SR did not differ significantly from their resting levels (Figs 2 and 3). On the other hand, during the occlusion after periods of handgrip exercise at either 30 % MVC for 120 s or at 45 % MVC for 60 s, MAP was significantly above its resting level (Fig. 2; from 81�8 � 4�6 to 101 � 6�7 mmHg and from 80�2 � 4�8 to 110�9 � 6�1 mmHg, respectively, P < 0�05). During these occlusions, the SR on the chest and forearm changed in parallel with the MAP, both parameters being significantly above resting levels (P < 0�05), but the SR on the palm did not differ significantly from its resting level (Fig. 3). The MAP was higher during the occlusion after 45 % MVC for 60 s than after 30 % MVC for 120 s (Fig. 2). During the occlusion, HR did not differ from the baseline value in any of these experiments. All the measured parameters returned to near resting levels during the recovery period. T_o_es and T-bar _sk maintained a steady state throughout each experiment (Fig. 2).

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Figure 2. Effect of the muscle metaboreflex on body temperature and cardiovascular parameters
Levels of oesophageal temperature (T_oes), mean skin temperature ( T-bar _sk), heart rate (HR) and mean arterial blood pressure (MAP) at rest, during handgrip exercise for 60 s or 120 s at 30 % maximal voluntary contraction (MVC), or for 120 s at 45 % MVC, during post-exercise ischaemia (occlusion) for 120 s after each of these handgrip exercises and during recovery. Values are means � S.E.M. for 8 subjects. * Significantly different from 'Rest' (P < 0�05).

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Figure 3. Effect of the muscle metaboreflex on sweating response
Local sweating rate (SR) on the chest, forearm and palm at rest, during handgrip exercise for 60 s or 120 s at 30 % maximal voluntary contraction (MVC), or for 120 s at 45 % MVC, during post-exercise ischaemia (occlusion) for 120 s after each of these handgrip exercises and during recovery. Values are means � S.E.M. for 8 subjects. * Significantly different from 'Rest' (P < 0�05).

Figure 4 shows the relationships between the change in MAP and the changes in SR on the chest and forearm during the periods of occlusion after the three levels of exercise (the changes being expressed relative to baseline values). Changes in sweating rate tend to level off at the higher MAP.

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Figure 4. Effect of the intensity of the muscle metaboreflex on the sweating response
Change in sweating rate ( $Delta$ SR) on the chest and forearm plotted against change in mean arterial blood pressure ( $Delta$ MAP; in each case, change from the resting level). Data were collected during occlusion after handgrip exercise at 30 % maximal voluntary contraction (MVC) for 60 s or 120 s, and at 45 % MVC for 60 s. Values are means � S.E.M. for 8 subjects.

Table 1 shows the percentage changes in SkBF and CVC for the chest and forearm during each exercise experiment. During the periods of handgrip exercise, occlusion and recovery, the CVC for the chest and forearm did not change from resting values, and SkBF increased significantly from resting levels at these two sites only during handgrip exercise at 45 % MVC for 60 s.

Table 1. Changes in skin blood flow (SkBF) and cutaneous vascular conductance (CVC) for the chest and forearm during each exercise experiment

	SkBF, chest (%)	SkBF, forearm (%)	CVC, chest (%)	CVC, forearm (%)
30 % MVC, 60 s
Rest	100	100	100	100
Handgrip	110�5 � 6�4	116�2 � 8�2	92�6 � 5�6	97�6 � 7�6
Occlusion	105�8 � 2�0	109�1 � 4�0	106�9 � 4�0	109�7 � 3�8
Recovery	99�0 � 2�8	103�1 � 3�2	101�9 � 3�9	105�8 � 3�2
30 % MVC, 120 s
Rest	100	100	100	100
Handgrip	108�9 � 7�8	105�6 � 10�0	100�9 � 4�8	97�4 � 7�0
Occlusion	103�4 � 3�8	102�4 � 4�7	104�6 � 5�7	103�5 � 6�1
Recovery	110�2 � 4�0	109�3 � 2�6	110�2 � 4�0	109�3 � 2�6
45 % MVC, 60 s
Rest	100	100	100	100
Handgrip	150�7 � 9�8 *	132�2 � 11�9 *	107�4 � 10�0	94�2 � 9�9
Occlusion	105�4 � 7�0	99�5 � 6�5	104�0 � 6�2	98�4 � 6�5
Recovery	92�3 � 5�4	98�5 � 5�8	91�5 � 6�0	97�7 � 6�6

Each result is calculated as the percentage change from rest (means � S.E.M.). MVC, maximal voluntary contraction. * Significantly different from 'Rest' (P < 0�05).

DISCUSSION

Top
Abstract
Introduction
Methods
Results
Discussion
References

In this study, the SR values for the chest and forearm (hairy regions) rose during handgrip exercise at 30 % MVC for 120 s and 45 % MVC for 60 s and remained elevated during the subsequent occlusion (Fig. 3). Since T_oes and T-bar _sk did not change during the occlusion, the increases in SR were not due to changes in these body temperatures. The elevation in MAP that occurs during occlusion is believed to be due to the muscle metaboreflex (Mitchell & Schmidt, 1983; Victor et al. 1988; Rowell & O'Leary, 1990; Saito et al. 1990; Vissing, 1997; Nishiyasu et al. 1998). Therefore, the elevations in SR on the hairy regions that occurred during occlusion following handgrip exercise (at 30 % MVC for 120 s and at 45 % MVC for 60 s) are probably also due to activation of the muscle metaboreflex. To our knowledge, this is the first study to produce evidence that thermoregulatory sweating responses are modulated by the muscle metaboreflex.

To clarify the effect of the muscle metaboreflex on the sweating response, we adopted four experimental conditions: handgrip exercise at 30 % MVC for 60 s (1), at 30 % MVC for 120 s (2) and at 45 % MVC for 60 s (3), and occlusion alone (4). It has been reported that MAP changes in inverse proportion to muscle pH (Nishiyasu et al. 1994). Nishiyasu et al. (1994) also showed that during post-exercise ischaemia after a 60 s handgrip exercise at 50 % MVC (similar to condition 3 above), the muscle pH remained low by at least 0�7 units. Victor et al. (1988) showed that 2 min of a 30 % MVC handgrip exercise (similar to condition 2 above) lowered muscle pH by 0�4 units. Thus, conditions 2 and 3 should both have activated the muscle metaboreflex, and the stimulus to the muscle metaboreflex should have been greater after 45 % MVC for 60 s. In the present study, the increases in MAP during the occlusion after the 45 % MVC exercise for 60 s and after the 30 % MVC exercise for 120 s were by 30�7 � 6�3 and 19�5 � 6�6 mmHg, respectively. This confirms that the intensity of the muscle metaboreflex during the occlusion after the 45 % MVC exercise was the greater, in agreement with previous studies. However, the changes in SR on the hairy regions during post-exercise occlusion did not differ between conditions 2 and 3 (Fig. 4), suggesting the SR change in the hairy regions during the muscle metaboreflex might be levelling off at the greater intensity of the stimulus of metabosensitive receptors.

By contrast, Victor et al. (1988) showed that handgrip exercise at 30 % MVC for 60 s did not lower muscle pH, which suggests that this exercise is not of sufficient magnitude for the muscle metaboreflex to be activated during a subsequent occlusion, and thus we should not expect a raised MAP during the occlusion. In fact, Sinoway et al. (1989) showed that MAP did not differ from baseline during the ischaemia after a 60 s handgrip at 30 % MVC. Similarly, in the present study MAP was not significantly above baseline during the occlusion after exercise at 30 % MVC for 60 s. These results suggest that the muscle metaboreflex was not activated by this level of exercise, or if it was activated, the activation was not great enough to evoke a significant physiological effect. Furthermore, during occlusion alone, there was no significant physiological response (Fig. 1B). In the present study, the finding that elevation in SR on the chest and forearm occurred only during occlusion after exercise either at 30 % MVC for 120 s or at 45 % MVC for 60 s leads to the conclusion that the sweating response in the hairy regions results from activation of muscle metaboreceptors, not from any artifacts or physiological responses related to the procedures used during the isometric exercise or occlusion.

Skin sympathetic nerve activity (which includes vasoconstrictor, sudomotor and vasodilator activity) has been found not to be influenced by post-exercise muscle ischaemia under normothermic conditions (Saito et al. 1990; Vissing, 1997). In addition, no changes in the sweating response were found during muscle ischaemia in these studies. However, the question remains as to whether the experimental conditions employed in the above studies were sufficient to activate the sudomotor pathway, because these studies were performed under normothermic conditions. Indeed, it has recently been reported that the muscle metaboreflex modulates cutaneous vasodilatation (which may be associated with the thermoregulatory sweating response) in hyperthermia but not in normothermia (Crandall et al. 1998). Although it has been reported that the sweating rate during muscle ischaemia is significantly above the resting level (Crandall et al. 1998), the core temperature measured sublingually also increased significantly during the ischaemia in that study. This would have a significant effect on the response (Nielsen, 1969; Nadel et al. 1971; Kondo et al. 1998). Therefore, from the study of Crandall et al. (1998), it is impossible to conclude that the increased sweating rate was solely due to activation of the muscle metaboreflex. By contrast, the increase in the sweating rate during the occlusion in the present study is likely to have resulted from the muscle metaboreflex, because the core and skin temperatures did not change significantly from pre-exercise levels during any of the experiments (Fig. 2). Our conclusion is that the non-thermal increase in the rate of sweating due to the muscle metaboreflex only occurs when sweating has already been initiated.

In the present study, the sweating responses in the hairless (palm) and hairy (chest and forearm) regions during occlusion differed from each other (Fig. 3). Our results suggest that modulation of the sweating response by the muscle metaboreflex only affects the hairy regions, where thermal sweating occurs. Interestingly, Saito et al. (1990) showed that skin sympathetic nerve activity and the sweating rate on the foot (hairless region) decreased to pre-exercise levels during occlusion of the working forearm after a handgrip. Thermoregulatory responses in the hairy regions are mediated by vasoconstrictor, sudomotor and vasodilator fibres (Bini et al. 1980; Okamoto et al. 1994; Sugenoya et al. 1998). By contrast, the thermoregulatory reflexes in the distal glabrous skin areas are mediated mainly via vasoconstrictor fibres (Bini et al. 1980), and palmar skin may not be innervated by vasodilator fibres (Johnson et al. 1995). Raising the ambient temperature suppresses the sudomotor and vasoconstrictor activity in the area of skin innervated by the tibial nerve (hairless region), whereas it increases the sudomotor activity in the area served by the peroneal nerve (hairy region) (Okamoto et al. 1994). These results suggest that the differences between the hairless and hairy regions in the effect on the sweating response of activation of the muscle metaboreflex may be related to differences in the sympathetic innervation of these functionally different types of skin.

In this study, the muscle metaboreflex had no effect on CVC under our mildly hyperthermic conditions. Vissing (1997) indicated that skin sympathetic nerve activity returned to control levels during post-exercise muscle ischaemia under normothermic conditions. By contrast, it has been reported that during post-exercise muscle ischaemia in hyperthermia, CVC is significantly reduced from pre-exercise levels (Crandall et al. 1998). The difference between these results may be attributable to the thermal conditions. Sympathetic vasoconstrictor and sympathetic active vasodilator systems both regulate skin blood flow (Johnson & Proppe, 1996), the active vasodilator system being activated in hyperthermia, especially when the core temperature is increased (Kellogg et al. 1991). In the study by Crandall et al. (1998), CVC decreased during muscle ischaemia in hyperthermia even though adrenergic vasoconstrictor function had been blocked by bretylium iontophoresis, suggesting that the reduction was due to inhibition of the cutaneous active vasodilator system. Taken together, the above results seem to indicate that muscle metaboreceptors primarily inhibit the active vasodilator system. In our study, since T_oes did not increase markedly during the mild hyperthermia, we assumed that the active vasodilator system was not activated. This is presumably why we saw no occlusion-induced changes in CVC.

In conclusion, during circulatory occlusion after handgrip exercise at 30 % MVC for 120 s or at 45 % MVC for 60 s (but not at 30 % MVC for 60 s), the MAP and the SR on the chest and forearm (hairy regions) were significantly above their resting levels, whereas the SR on the palm (hairless region) was not, nor T_oes, nor T-bar _sk. These results suggest that the thermoregulatory sweating response in hairy regions is modulated by afferent signals from muscle metaboreceptors in mild hyperthermic conditions.

We should like to sincerely thank our volunteer subjects. We would also like to acknowledge the critical reading of the English manuscript by Dr Robert J. Timms. We also thank S. Okada, Faculty of Human Development, Kobe University, for supporting our experiments.

Corresponding author

N. Kondo: Laboratory for Applied Human Physiology, Faculty of Human Development, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe 657-8501, Japan.

Email: kondo{at}kobe-u.ac.jp

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