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J Appl Physiol 88: 393-400, 2000;
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Vol. 88, Issue 2, 393-400, February 2000

Modulation of arterial baroreflex control of heart rate by skin cooling and heating in humans

Fumio Yamazaki1 and Ryoko Sone2

1 Department of Clinical Pathophysiology, School of Health Sciences, University of Occupational and Environmental Health, Yahatanishi-ku, 807-8555 Kitakyushu; and 2 Department of Exercise and Health Sciences, Faculty of Education, University of Yamaguchi, Yamaguchi City, Yamaguchi 753-0841, Japan


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The purpose of this study was to examine the effects of skin cooling and heating on the heart rate (HR) control by the arterial baroreflex in humans. The subjects were 15 healthy men who underwent whole body thermal stress (esophageal temperatures, ~36.8 and ~37.0°C; mean skin temperatures, ~26.4 and ~37.7°C, in skin cooling and heating, respectively) produced by a cool or hot water-perfused suit during supine rest. The overall arterial baroreflex sensitivity in the HR control was calculated from spontaneous changes in beat-to-beat arterial pressure and HR during normothermic control and thermal stress periods. The carotid baroreflex sensitivity was evaluated from the maximum slope of the HR response to changes in carotid distending pressure, calculated as mean arterial pressure minus neck pressure. The overall arterial baroreflex sensitivity at existing arterial pressure increased during cooling (-1.32 ± 0.25 vs. -2.13 ± 0.20 beats · min-1 · mmHg-1 in the control and cooling periods, respectively, P < 0.05), whereas it did not change significantly during heating (-1.39 ± 0.23 vs. -1.40 ± 0.15 beats · min-1 · mmHg-1 in the control and heating periods, respectively). Neither the cool nor heat loadings altered the carotid baroreflex sensitivity in the HR control. These results suggest that the sensitivity of HR control by the extracarotid (presumably aortic) baroreflex was augumented by whole body skin cooling, whereas the sensitivities of HR control by arterial baroreflex remain unchanged during mild whole body heating in humans.

aortic baroreceptors; carotid sinus baroreceptors; heart rate variability; power spectra; skin blood flow


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

THERMAL STIMULATION of the body surface increases the activity of thermoreceptors in the stimulated skin, and the thermoreceptive information is transmitted to the thermoregulation center, i.e., the hypothalamus (34). In experimental animals, electrical stimulation of the hypothalamus modified the baroreceptor reflex of the heart rate (HR) (13). Acute thermal stimulation of the hypothalamus modulated the arterial pressure and HR responses (22). These findings suggest the potential interaction of thermal and baroreceptor reflexes (13, 22). The possibility of central interaction between thermal and baroreflex control has been also suggested in a human study (6).

Although arterial blood pressure is increased by both local and whole body skin cooling, the HR responses to the two stresses are different. Tachycardia occurs after severe local stimulation, i.e., a cold pressor test (19), and bradycardia occurs after mild whole body stimulation (10, 28). These contrary responses of the HR may be partly due to a sense of pain during the cold pressor test. Severe whole body heating increases the HR without changing the mean arterial pressure (MAP) in the thermal steady state (15, 39). Thus the central interaction between temperature and blood pressure inputs is likely to be modified by the differences of the stimulated skin area and the magnitude and type of stimulation. It has been reported that the reflex response of the HR to changes in arterial pressure was unaffected by a cold pressor test (17), whereas the effect of whole body skin cooling without the induction of a sense of pain on the arterial baroreflex is unknown. We found previously that the sensitivity of the HR control by the carotid baroreflex remained unchanged during severe whole body heating (39), but there is little information about the human baroreflex control of the HR during mild heating. To further clarify the interaction between thermal and baroreflex controls, analyses of cardiac baroreflex responses during cool loading and heat loading are needed.

Changes in arterial blood pressure are sensed by baroreceptors in the aortic arch and carotid sinuses. Stimulation of these baroreceptors increases the afferent input to the cardiovascular centers, i.e., the medulla, and decreases the HR via reduced sympathetic and increased parasympathetic nerve activities. Thus when the responsiveness of the HR to changes in arterial pressure is altered by skin cooling or heating, the changes may be due to the modification in a carotid baroreflex pathway and/or aortic baroreflex pathway. In the present study, therefore, we investigated whether the arterial baroreflex function of the HR is modified by cooling and by mild heating of whole body skin in normal humans. In addition, we investigated whether the modification originates from carotid or extracarotid arterial baroreflex functions.


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Subjects

Fifteen normal healthy male volunteers [age, 22 ± 1 (SE) yr; weight, 65.5 ± 1.7 kg; height, 173 ± 1 cm; and body fat, 19.6 ± 1.1%] participated in this study. The study was approved by the Human Research Committee of the University of Occupational and Environmental Health, and all subjects gave their written consent to participate after being fully informed about the procedures, risks, and protocol.

Protocols

Each subject was tested two times at normothermic conditions followed by the whole body cooling or heating condition. On the experimental day, each subject reported to the laboratory at 0930, and body fat was measured by a body composition analyzer (model HA-2, EM-SCAN, Springfield, IL). In a climatic chamber (25°C ambient temperature, 50% relative humidity), the subject was harnessed with an esophageal temperature (Tes) probe, skin thermocouples, electrocardiogram (ECG) electrodes, blood pressure cuffs, a thermistor for the monitoring of respiratory patterns, and laser-Doppler flow (LDF) probes for forearm and leg skin blood flow measurements. The subject wore a tube-lined water-perfused suit that covered the entire body, except for the head and right arm, and lay supine in this suit on a bed. The mean skin temperature (Tsk) was controlled by changing the water temperature of the suit. The protocol consisted of a 70- to 85-min normothermic control period and a 40- to 65-min cooling or heating period; the duration of these periods varied slightly among the subjects depending on the stabilization time. In the normothermic condition, Tsk was maintained at 34.5-35.5°C, and baseline measurements were made for the last 10 min of the normothermic control period. After the baseline measurements, carotid baroreflex responsiveness was tested in 7 of the 15 subjects. On completion of the measurements at normothermia, the perfusion water temperature was decreased to 10°C or increased to 45°C to change the Tsk. After the Tsk and HR reached their steady states, measurements were made as in the normothermic condition. Each subject was tested in both the heating and cooling conditions; there was an interval of at least 2 days between the cooling and heating experiments, and the order of treatments was randomized.

Measurements and Analysis

Hemodynamics, breathing, and temperature. The HR was determined from the ECG (CM5 lead). Blood pressure was measured noninvasively every 60 s in each thermal condition by a Dynamap automated oscillometric blood pressure device with the cuff on the left upper arm (model 8100, Criticon, Tampa, FL). In addition, continuous blood pressure was determined by means of arterial tonometry (JENTOW-7700, Colin, Komaki, Japan) on the right radial artery for the baroreflex analysis. The reliability and accuracy of arterial tonometry as a continuous measure of blood pressure have been reported elsewhere (18). MAP was calculated as one-third pulse pressure plus diastolic pressure (DBP). LDF was monitored continuously with LDF meters (BPM-403, TSI, St. Paul, MN); glass-fiber sensor probes (P-430, TSI) were placed at the midpoints on the inside of the right forearm and the outside of the right calf. The LDF measures mainly the average blood flow in the outermost cutaneous tissue (depth 0.6-1.5 mm). The respiratory rate was counted from the respiratory waveform by a nose-tip thermistor (TR-762T, Nihon Kohden, Tokyo, Japan). The ECG, blood pressure, and respiratory waveforms were recorded on a data recorder (RD-111T, TEAC, Tokyo, Japan) during baseline measurements in each thermal condition. Tes as an index of core temperature was measured with a polyethylene-sealed (1-mm diameter) thermocouple swallowed in the esophagus to the level of the heart. Skin temperatures were measured by copper-constantan thermocouples on the chest, upper back, lower back, abdomen, thigh, and calf. Tsk was calculated by using the weighting factors of Taylor et al. (36).

To compare the data obtained in the two thermal conditions, values were averaged over 10-min periods when the Tes, Tsk, HR, blood pressure, LDF, and respiratory rate were stabilized in the respective conditions. Changes in LDF were expressed as a percent change in the voltage level from the normothermic level.

Arterial baroreflex analysis. Overall arterial baroreceptor (i.e., baroreceptors in the aorta and carotid sinuses)-HR reflex sensitivity was calculated for the last 5 min of the baseline data period by using a method described by Bertinieri et al. (2, 3) and others (17, 33, 38). The principle of this method is illustrated in Fig. 1 and permits the calculation of baroreceptor-HR reflex sensitivity from the arterial pressure time series. As a result, arterial baroreceptor function can be analyzed within the normal operating range of the baroreceptors. Briefly, spontaneously occurring sequences of three or more consecutive heartbeats were detected during which both arterial pressure and the interbeat interval are simultaneously increased or decreased. The beat-to-beat HR was calculated from the subsequent interbeat interval in which blood pressure was measured, because the cardiac response to baroreceptor stimulation occurred promptly and the peak response occurred about 1.25 s after the onset of baroreceptor stimulation (7, 8). The blood pressure recordings sampled with 1,000 Hz were used to detect these sequences. Only sequences where successive pressure pulses differed by at least 1.0 mmHg and the HR differed by at least 1.0 beats/min were selected (38). From each of these sequences, linear regressions were calculated for the relationship between blood pressure and instantaneous HR. Only sequences with a correlation coefficient (r) >0.85 were included in the analysis. The slope (i.e., regression coefficient) of the linear relationship between systolic pressure (SBP) and HR was used as a measure for arterial baroreceptor-HR reflex sensitivity. Thus 22 ± 2 sequences were identified for a 5-min period in each thermal condition. The average number of heartbeats analyzed in a blood pressure time series was 22 ± 2% of the number of total heartbeats. The SBP changes over which the slopes of the HR-SBP relationship were calculated were in the range of 1-20 mmHg.


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  		Fig. 1.   Example of arterial blood pressure signal for estimation of sensitivity of baroreceptor-heart rate (HR) reflex (top). Interbeat intervals were defined as time (ms) between two diastolic minima and converted into instantaneous HRs (shown in parentheses). Sensitivity of arterial baroreceptor-HR reflex was estimated by mean of slopes of HR-systolic pressure relationships (bottom).

In previous studies (2, 3, 17, 33, 38), the interbeat interval rather than HR was used as an indicator of the effector response of the cardiac baroreflex. Because the relationship between the R-R interval and the HR is a hyperbolic function, an increase in the baseline HR results in a reduction of the cardiac baroreflex sensitivity presented by the R-R interval even when the sensitivity presented by the HR remains unchanged (23, 30, 32). If stroke volume (SV) and peripheral vascular resistance (PVR) are almost constant during brief pressure perturbations, the HR changes relate linearly to the arterial pressure changes (i.e., arterial pressure = HR × SV × PVR). Thus HR responses to baroreceptor stimulation are related directly to the maintenance of arterial pressure even when baseline HR changes considerably. Therefore we used HR in the evaluation of the cardiac baroreflex control under each thermal condition.

Carotid baroreflex analysis. A tightly sealed Silastic neck chamber connected to a computer-controlled bellows (E2000A, Engineering Development Laboratory, Newport News, VA) was strapped to the anterior neck of the subject. During an expiration held for ~15 s, the pressure of the neck chamber was held at 0 mmHg for three heartbeats and then raised to 40 mmHg above ambient pressure, and the pressure was then held for three heartbeats. With each of the next seven consecutive R waves in ECG, the pressure was reduced by 15 mmHg/pulse until it reached -65 mmHg. This procedure was repeated seven times, and the values were averaged for each response.

The beat-to-beat HR was calculated from the subsequent R-R interval in which the neck pressure was applied. The HR was plotted against the carotid distending pressure, which was calculated as MAP minus the chamber pressure. From the relationship between the HR and the carotid distending pressure, we calculated the maximum, minimum, and range (maximum - minimum) of HR responses, the carotid distending pressures at the maximum and minimum HRs, the maximum slope, and a reference point. The maximum slope, an index of the sensitivity of HR control by the carotid baroreflex, was calculated with the linear regression analysis applied to each set of three consecutive data points. The reference point reflected a position of the baseline HR on the stimulus-response curve and was defined as [(HR at 0 mmHg neck pressure - minimum HR)/HR range] × 100%. The reference point is a measure of the relative baroreflex buffering capacity for pressures above and below resting levels.

Power spectral density analyses of cardiac interval variability. A spectral analysis was performed by using a power spectral density analysis computer software program for cardiac variability (VITAL RHYTHM 98 III, NEC Medical Systems, Tokyo, Japan), with the baseline data. A fast Fourier transformation was used to calculate the power spectral density. The time series of R-R intervals were interpolated at 2 Hz by the Lagrange interpolation method. Consecutive data over 256 s were used for the analysis. All analyses were performed between 0.03 and 0.5 Hz. The frequency range between 0.03 and 0.15 Hz was defined as the low-frequency band, and the range between 0.15 and 0.5 Hz as the high-frequency band. The high-frequency power and the ratio of low- and high-frequency power were used as indexes of cardiac parasympathetic and sympathetic activities, respectively (1, 20, 24, 27).

Statistics

Data are expressed as means ± SE. The comparison of the data in the two thermal conditions was made by paired t-tests. P < 0.05 was considered significant.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Physiological responses during thermal stresses. Figure 2 shows the Tes, Tsk, HR, and forearm and calf LDF responses during cooling and heating. The temperature, cardiovascular, and respiratory response data for each thermal condition are presented in Table 1. Tes increased promptly with the beginning of cooling and then decreased from ~20 min of cooling. Tes increased significantly during both types of thermal stress, and the values did not differ significantly between the cooling and heating conditions. Tsk, HR, and forearm and calf LDF decreased during cooling and increased during heating (P < 0.05). SBP increased significantly during both thermal stresses. DBP and MAP increased significantly during cooling, whereas they remained unchanged during heating. The respiratory rate did not change significantly during cooling and heating, but the rate in the heating period was higher than that in the cooling period. The respiratory frequencies in all subjects were always within the range of 0.15-0.5 Hz, i.e., the high-frequency band for each thermal condition.


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  		Fig. 2.   Responses of HR, esophageal temperature (Tes), mean skin temperature (Tsk), and forearm (Forearm LDF) and calf (Calf LDF) laser-Doppler flow during whole body cooling and heating. Values are means ± SE; n = 15 men.


                              
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  		Table 1.   Physiological variables under normothermic control, cooling, and heating conditions

Baroreceptor-HR reflex. Because the slopes of the HR-SBP relationship did not differ significantly between the increasing and decreasing processes of blood pressure in each thermal condition, the slope values were averaged. As shown in Fig. 3, the slope was significantly greater (P < 0.05) during the cooling condition (-2.13 ± 0.20 beats · min-1 · mmHg-1) compared with the normothermic control (-1.32 ± 0.25 beats · min-1 · mmHg-1), whereas it was not changed by whole body skin heating (-1.39 ± 0.23 in control vs. -1.40 ± 0.15 beats · min-1 · mmHg-1 in the heating condition).


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  		Fig. 3.   Sensitivity of overall arterial baroreflex of HR in each thermal condition. Values are means ± SE; n = 15 men. * P < 0.05 compared with control for each experiment; dagger  P < 0.05 compared with cooling condition.

Figure 4 shows the relationships between HR and carotid distending pressure for the two experiments. The baroreflex curves shifted downward and upward during cooling and heating, respectively. The maximum slopes were not changed by the cool and heat loadings (Table 2). The maximum and minimum HRs decreased during cooling and increased during heating (P < 0.05), but the ranges of the response were not significantly different among the thermal conditions (Table 2). The carotid distending pressures at maximum HR were not changed by either thermal loading, whereas those at minimum HR showed a tendency to increase during both thermal stresses, and the values in the heating condition were significantly higher than in the control condition (Table 2). The reference points showed tendencies to decrease during cooling and to increase during heating, and their values in the heating condition were significantly higher than in the cooling condition (Table 2, P < 0.05).


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  		Fig. 4.   Relationships between HR and carotid distending pressure in each thermal condition. Values are means ± SE; n = 7 men.


                              
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  		Table 2.   Carotid baroreflex variables during normothermic control, cooling, and heating conditions

Power spectral analysis. During cooling, the power spectrum of cardiac interval variability revealed a significantly increased power for the total, low-frequency, and high-frequency components (P < 0.05) but an unchanged ratio of low- to high-frequency power (Fig. 5). During the heating period, the total, low-frequency, and high-frequency power decreased significantly (P < 0.05), whereas the ratio of low- to high-frequency power increased significantly (P < 0.05, Fig. 5).


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  		Fig. 5.   Total, low-frequency, and high-frequency powers and ratio of low- to high-frequency power in each thermal condition. Values are means ± SE; n = 15 men. * P < 0.05 compared with control for each experiment. dagger  P < 0.05 compared with cooling condition.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

In the present study, the overall arterial baroreceptor (aortic and carotid baroreceptors) reflex function in the HR control was determined from the spontaneously occurring arterial pressure and heartbeat changes, whereas the carotid baroreflex function alone was analyzed from HR responses to carotid transmural pressure changes produced by neck pressure changes. Two major findings were obtained by using these techniques. First, the sensitivity of the HR control by the overall arterial baroreflex increased, whereas that by the carotid baroreflex did not change during the cooling condition. Second, the sensitivities of the HR control by the overall arterial baroreflex as well as the separated carotid baroreflex were not altered during the heating condition.

Possible mechanisms of the augumented sensitivity of HR control by arterial baroreflex during cooling stress are as follows: 1) the direct effect of temperature (i.e., the Q10 effect) on the activities in the arterial baroreceptors and/or the pacemaker cell in the heart; and 2) the central modification of baroreflex control by thermoreceptor input. Regarding the first mechanism, the contribution would be minimal, because the increases in Tes in the present study were significant but very small (0.14°C on the average). We suspect that the increase in core temperature during cooling was the result of the rapid decrease of heat dissipation induced by the reduced skin blood flow that occurred with the beginning of cooling and the increase of heat production induced by a slight shivering in the latter period of cooling, although we did not observe visible shivering in any subjects throughout the experiment. Thus the acute cooling stress in this study was specific cooling stimulation not to the body core but to the body surface.

Some studies of humans support the second possible mechanism mentioned above. Heistad et al. (16) observed that vasoconstrictor responses in the finger and forearm to lower body negative pressure during the immersion of the other arm in hot (44-46°C) or cool (10-12°C) water were dependent on the water temperature, and the thermal stimuli did not affect the vasoconstrictor responses to an intra-arterial infusion of norepinephrine. They concluded that the interaction of the thermal and baroreceptor reflexes occurs at a central level. In addition, Ebert et al. (6) compared cardiovascular responses such as HR, blood pressure, and total peripheral resistance to lower body negative pressure with and without hand immersion in cool (10°C) water and observed additive responses in cardiovascular variables except HR to combined local thermoreceptor and baroreceptor stimuli; they suggested the possibility of a central interaction between thermal and baroreflex controls of the HR.

In the present study, the sensitivity of HR control by the overall arterial baroreflex was increased only in the skin cooling period, with no significant difference between the core temperatures during the cooling and heating conditions, suggesting that there was a central interaction between the afferent information from arterial baroreceptors and that from skin cold receptors rather than core thermoreceptors. This central interaction may occur predominantly in the aortic baroreflex pathway, because the carotid baroreflex sensitivity in the HR control was not changed by skin cooling in this study. This hypothesis may be supported by the reports that in humans the aortic baroreflex played a more important role than the carotid baroreflex in HR control (11, 21, 32).

The present study, because the slope of the HR-SBP relationship was measured over a narrow range (<20 mmHg) of spontaneous changes of SBP, shows the sensitivity around the operating point in the full stimulus-response curve generated by changes in the wide range of the pressure. Therefore, the increased sensitivity in the cooling period may be due to the shift of the operating point to a steeper portion in the full baroreflex response curve by the skin cooling. However, it is inferred that such a relocation of the operating point would not occur during cooling, because the reference point showed the tendency to leave the near midpoint in the carotid baroreflex-HR response curve during cooling (i.e., 59 ± 14% in the control period; 34 ± 10% in the cooling period). This inference is based on the assumption that the operating points in both the aortic and carotid baroreflex curves will be shifted in similar directions during cooling.

The finding of the unchanged slope of the HR-blood pressure relationship during whole body heating is consistent with the result in experimental animals (14). Gorman and Proppe (14) reported that the maximum slope and the total range of the HR response of the full sigmoid-shaped baroreflex curve in baboons were not changed when the arterial blood temperature was increased to 39.6°C by heat stress. Moreover, they observed a decrease in the tachycardiac response and an increase in the bradycardiac response to changes in MAP during heat stress. Similar findings were observed in the carotid baroreflex function in hyperthermic (Tes, 38°C; Tsk, 39.1°C) humans (39). In addition, Stauss et al. (33) observed in conscious mature rats that the cardiac responses to spontaneous blood pressure changes were augumented with core temperatures of 40°C and over, and they concluded that the increased baroreceptor reflex sensitivity may contribute to the ability of the cardiovascular system to adjust to heat stress. The present results confirmed the notion that in supine resting humans the arterial baroreflex sensitivity in the HR control is maintained during mild hyperthermia (Tes, ~37.0°C; Tsk, ~37.7°C).

Central blood volume and central venous pressure are decreased by whole body heating, but these variables are increased by whole body cooling (29, 30). It is reported that the decrease and increase of central venous pressure result in an increase and decrease, respectively, in gain of the carotid baroreceptor-cardiac reflex (25, 31). Although there is a report that the interrelation between changes in central venous pressure and the arterial baroreflex control of HR is invalid within a physiological range in humans (35), if such an interrelation was maintained during thermal stress in the present conditions, it is possible that the net impacts of temperature enhanced the sensitivity of carotid baroreceptor-cardiac reflex during cooling and inhibited it during heating.

It is apparent that the downward and upward shifts of the HR-carotid distending pressure curve during skin cooling and heating were caused by the decrease and increase of resting HR, respectively. Regarding the tachycardia during heat stress, Gorman and Proppe (15) reported that ~40% of the HR increase during hyperthermia in baboons was accounted for by a temperature rise of the pacemaker tissue and the rest was accounted for by the autonomic nervous system. They also suggested that ~75% of the autonomic influence was accounted for by a decrease in parasympathetic nerve activity and the rest was attributable to the increase in sympathetic nerve activity.

Similar findings were also described regarding the autonomic mechanisms of tachycardia during heat loading in anesthetized rats (37). In the present study, we estimated the modulation of autonomic nerve activities in the human heart by the spectral analyses of cardiac chronotropic variabilities. Our results suggest that the increased HR during mild hyperthermia was due to an increase in cardiac sympathetic activity and a decrease in cardiac vagal activity, whereas the decreased HR during skin cooling was caused merely by an increase in cardiac vagal activity.

There is general agreement that the bradycardia in response to an elevation of arterial blood pressure is primarily mediated through vagal mechanisms. Pickering et al. (26) have shown that atropine blocks the early decrease in HR after phenylephrine-induced increases in arterial pressure. Chiou and Zipes (4) have observed recently that in dogs the efferent vagal denervation of the sinus and arterioventricular nodes and atria decreased the R-R interval variability and eliminated the cardiac baroreflex sensitivity. The reflex cardiac sympathetic responses to baroreceptor activation are slower than the parasympathetic responses (5). We therefore suspect that the cardiac baroreceptor responses in the present study are mediated mainly by vagal mechanisms, inasmuch as the baroreceptors were stimulated with beat-to-beat changes in arterial blood pressure or carotid transmural pressure and the total durations of stimulation were brief (<15 s) (9, 12). On the efferent arm of the baroreflex pathway during skin cooling, therefore, we speculate that the increased vagal activity in the baseline level results in the increase of HR responses to instantaneous blood pressure changes. However, it is thought that the reduced vagal activities during heating did not change the baroreflex sensitivity in the HR control as a contributory factor in the neural regulation of the arterial pressure.

In conclusion, the present findings suggest that the augumented sensitivity of the aortic baroreceptor-cardiac reflex is responsible for the modulation of the HR control by arterial baroreflex during whole body skin cooling without a sense of pain, while the sensitivity of the HR control by arterial baroreflex remains unchanged during mild whole body heating in supine resting humans.


    ACKNOWLEDGEMENTS

The technical help of K. Monji and Y. Sogabe was greatly appreciated.


    FOOTNOTES

This work was supported by funds from the University of Occupational and Environmental Health, Kitakyushu, Japan.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Address for reprint requests and other correspondence: F. Yamazaki, Dept. of Clinical Pathophysiology, School of Health Sciences, Univ. of Occupational and Environmental Health (UOEH), 1-1 Iseigaoka, Yahatanishi-ku, 807-8555 Kitakyushu, Japan (E-mail: yamazaki{at}health.uoeh-u.ac.jp).

Received 28 August 1998; accepted in final form 23 September 1999.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1.   Akselrod, S., D. Gordon, F. A. Ubel, D. C. Shannon, A. C. Barger, and R. J. Cohen. Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 213: 220-222, 1981[Abstract/Free Full Text].

2.   Bertinieri, G., M. Di Rienzo, A. Cavallazzi, A. U. Ferrari, A. Pedotti, and G. Mancia. A new approach to analysis of the arterial baroreflex. J. Hypertens. 3, Suppl.3: S79-S81, 1985[Web of Science].

3.   Bertinieri, G., M. Di Rienzo, A. Cavallazzi, A. U. Ferrari, A. Pedotti, and G. Mancia. Evaluation of baroreceptor reflex by blood pressure monitoring in unanesthetized cats. Am. J. Physiol. Heart Circ. Physiol. 254: H377-H383, 1988[Abstract/Free Full Text].

4.   Chiou, C.-W., and D. P. Zipes. Selective vagal denervation of the atria eliminates heart rate variability and baroreflex sensitivity while preserving ventricular innervation. Circulation 98: 360-368, 1998[Abstract/Free Full Text].

5.   Coleman, T. G. Arterial baroreflex control of heart rate in the conscious rat. Am. J. Physiol. Heart Circ. Physiol. 238: H515-H520, 1980[Abstract/Free Full Text].

6.   Ebert, T. J., D. F. Stowe, J. A. Barney, J. H. Kalbfleisch, and J. J. Smith. Summated circulatory responses of thermal and baroreflexes in humans. J. Appl. Physiol. 52: 184-189, 1982[Abstract/Free Full Text].

7.   Eckberg, D. L. Temporal response patterns of the human sinus node to brief carotid baroreceptor stimuli. J. Physiol. 258: 769-782, 1976[Abstract/Free Full Text].

8.   Eckberg, D. L. Adaptation of the human carotid baroreceptor-cardiac reflex. J. Physiol. 269: 579-589, 1977[Abstract/Free Full Text].

9.   Eckberg, D. L. How should human baroreflexes be tested? News Physiol. Sci. 8: 7-12, 1993[Abstract/Free Full Text].

10.   Fagius, J., and R. Kay. Low ambient temperature increases baroreflex-governed sympathetic outflow to muscle vessels in humans. Acta Physiol. Scand. 142: 201-209, 1991[Web of Science][Medline].

11.   Ferguson, D. W., F. M. Abboud, and A. L. Mark. Relative contribution of aortic and carotid baroreflexes to heart rate control in man during steady state and dynamic increases in arterial pressure. J. Clin. Invest. 76: 2265-2274, 1985.

12.   Fritsch, J. M., M. L. Smith, D. T. F. Simmons, and D. L. Eckberg. Differential baroreflex modulation of human vagal and sympathetic activity. Am. J. Physiol. Regulatory Integrative Comp. Physiol. 260: R635-R641, 1991[Abstract/Free Full Text].

13.   Gebber, G. L., and D. W. Snyder. Hypothalamic control of baroreceptor reflexes. Am. J. Physiol. 218: 124-131, 1970.

14.   Gorman, A. J., and D. W. Proppe. Influence of heat stress on arterial baroreflex control of heart rate in the baboon. Circ. Res. 51: 73-82, 1982[Abstract/Free Full Text].

15.   Gorman, A. J., and D. W. Proppe. Mechanisms producing tachycardia in conscious baboons during environmental heat stress. J. Appl. Physiol. 56: 441-446, 1984[Abstract/Free Full Text].

16.   Heistad, D. D., F. M. Abboud, A. L. Mark, and P. G. Schmid. Interaction of thermal and baroreceptor reflexes in man. J. Appl. Physiol. 35: 581-586, 1973[Free Full Text].

17.   Hughson, R. L., L. Quintin, G. Annat, Y. Yamamoto, and C. Gharib. Spontaneous baroreflex by sequence and power spectral methods in humans. Clin. Physiol. 13: 663-676, 1993[Web of Science][Medline].

18.   Kemmotsu, O., M. Ueda, H. Otsuka, T. Yamamura, D. C. Winter, and J. S. Eckerle. Arterial tonometry for noninvasive, continuous blood pressure monitoring during anesthesia. Anesthesiology 75: 333-340, 1991[Web of Science][Medline].

19.   LeBlanc, J., J. Côté, S. Dulac, and F. Dulong-Turcot. Effects of age, sex, and physical fitness on responses to local cooling. J. Appl. Physiol. 44: 813-817, 1978[Abstract/Free Full Text].

20.   Lombardi, F., G. Sandrone, S. Pernpruner, R. Sala, M. Garimoldi, S. Cerutti, G. Baselli, M. Pagani, and A. Malliani. Heart rate variability as an index of sympathovagal interaction after acute myocardial infarction. Am. J. Cardiol. 60: 1239-1245, 1987[Web of Science][Medline].

21.   Mancia, G., A. Ferrari, L. Gregorini, R. Valentini, J. Ludbrook, and A. Zanchetti. Circulatory reflexes from carotid and extracarotid baroreceptor areas in man. Circ. Res. 41: 309-315, 1977[Abstract/Free Full Text].

22.   Morishima, M. S., and C. C. Gale. Relationship of blood pressure and heart rate to body temperature in baboons. Am. J. Physiol. 223: 387-395, 1972.

23.   O'Leary, D. S. Heart rate control during exercise by baroreceptors and skeletal muscle afferents. Med. Sci. Sports Exerc. 28: 210-217, 1996[Web of Science][Medline].

24.   Pagani, M., F. Lombardi, S. Guzzetti, O. Rimoldi, R. Furlan, P. Pizzinelli, G. Sandrone, G. Malfatto, S. Dell'Orto, E. Piccaluga, M. Turiel, G. Baselli, S. Cerutti, and A. Malliani. Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circ. Res. 59: 178-193, 1986[Abstract/Free Full Text].

25.   Pawelczyk, J. A., and P. B. Raven. Reductions in central venous pressure improve carotid baroreflex responses in conscious men. Am. J. Physiol. Heart Circ. Physiol. 257: H1389-H1395, 1989[Abstract/Free Full Text].

26.   Pickering, T. G., B. Gribbin, E. Strange-Petersen, D. J. C. Cunningham, and P. Sleight. Effects of autonomic blockade on the baroreflex in man at rest and during exercise. Circ. Res. 30: 177-185, 1972[Abstract/Free Full Text].

27.   Pomeranz, B., R. J. B. Macaulay, M. A. Caudill, I. Kutz, D. Adam, D. Gordon, K. M. Kilborn, A. C. Barger, D. C. Shannon, R. J. Cohen, and H. Benson. Assessment of autonomic function in humans by heart rate spectral analysis. Am. J. Physiol. Heart Circ. Physiol. 248: H151-H153, 1985[Abstract/Free Full Text].

28.   Raven, P. B., G. Pape, W. F. Taylor, F. A. Gaffney, and C. G. Blomqvist. Hemodynamic changes during whole body surface cooling and lower body negative pressure. Aviat. Space Environ. Med. 52: 387-391, 1981[Medline].

29.   Rowell, L. B. Thermal stress. In: Human Circulation. New York: Oxford University Press, 1986, p. 174-212.

30.   Rowell, L. B. Orthostatic intolerance. In: Human Cardiovascular Control. New York: Oxford University Press, 1993, p. 118-161.

31.   Shi, X., J. T. Potts, B. H. Foresman, and P. B. Raven. Carotid baroreflex responsiveness to lower body positive pressure-induced increases in central venous pressure. Am. J. Physiol. Heart Circ. Physiol. 265: H918-H922, 1993[Abstract/Free Full Text].

32.   Shi, X., J. T. Potts, P. B. Raven, and B. H. Foresman. Aortic-cardiac reflex during dynamic exercise. J. Appl. Physiol. 78: 1569-1574, 1995[Abstract/Free Full Text].

33.   Stauss, H. M., D. A. Morgan, K. E. Anderson, M. P. Massett, and K. C. Kregal. Modulation of baroreflex sensitivity and spectral power of blood pressure by heat stress and aging. Am. J. Physiol. Heart Circ. Physiol. 272: H776-H784, 1997[Abstract/Free Full Text].

34.   Ström, G. Central nervous regulation of body temperature. In: Handbook of Physiology. Neurophysiology. Washington, DC: Am. Physiol. Soc, 1960, sect. 1, vol. II, chapt. 46, p. 1173-1196.

35.   Takeshita, A., A. L. Mark, D. L. Eckberg, and F. M. Abboud. Effect of central venous pressure on arterial baroreflex control of heart rate. Am. J. Physiol. Heart Circ. Physiol. 236: H42-H47, 1979[Abstract/Free Full Text].

36.   Taylor, W. F., J. M. Johnson, D. O'Leary, and M. K. Park. Effect of high local temperature on reflex cutaneous vasodilation. J. Appl. Physiol. 57: 191-196, 1984[Abstract/Free Full Text].

37.   Walsh, R. R. Heart rate and its neural regulation with rising body temperature in anesthetized rats. Am. J. Physiol. 217: 1139-1143, 1969.

38.   Watkins, L. L., C. Fainman, J. Dimsdale, and M. G. Ziegler. Assessment of baroreflex control from beat-to-beat blood pressure and heart rate changes: a validation study. Psychophysiology 32: 411-414, 1995[Web of Science][Medline].

39.   Yamazaki, F., S. Sagawa, R. Torii, Y. Endo, and K. Shiraki. Effects of acute hyperthermia on the carotid baroreflex control of heart rate in humans. Int. J. Biometeorol. 40: 200-205, 1997[Web of Science][Medline].

J APPL PHYSIOL 88(2):393-400
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