Thermogenic control during exercise in a cold environment.

Thermogenic control in a cold environment

during

exercise

SUNG-IL HONG AND ETHAN R. NADEL John B. Pierce Foundation Laboratory and Departments of Epidemiology and Public and Physiology, Yale University School of Medicine, New Haven, Connecticut 06519

HONG, SUNG-IL, AND ETHAN R. NADEL. Thermogenic controZ during exercise in a coZd environment. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 47(5): 1084-1089,1979.To determine whether the voluntary contractions of exercise interfere with involuntary shivering contractions, four male subjects were each exposed to a 10°C environment for 60 min of rest followed by either another rest period or 30 min of cycleergometer exercise. On different days exercise was performed at zero load, light load, and moderate load. Each experiment was performed twice, resulting in a minimum of eight experiments for each subj_ect. Esophageal temperature (T,,), eight skin temperatures (T&, oxygen uptake (Vo,), and the integrated electrical activity from a neck muscle (EMG) were continuously monitored. Pedaling flushed cold blood into the body core, causing T, to fall. The rate and absolute magnitude of the decrease in T, was .proportional to the intensity of exercise. Thermoregulatory VO:! (attributable to shivering) and EMG were inversely related both to ijs‘,k during rest, prior to any changes in T,,, and to T,, during exercise, when TSk was constant, once shivering thresholds were surpassed. The slope of the thermoregulatory %&to-Tes relation was significantly suppressed by increasing exercise intensity. The slope of the EMG-to-T, relation was similarly suppressed; since the neck muscles are not involved in the additional activity of exercise, we concluded that the graded inhibition of shivering during exercise was of central origin rather than from the rhythmic contractions required to sustain exercise. shivering;

temperature

regulation;

electromyogram

TO THE LARGE NUMBER of studies investigating temperature regulation in man during exercise and heat stress (see for instance Ref. 15)) relatively few studies have examined the characteristics of human temperature regulation during cold exposure. Most of the latter have described the temporal pattern of change of specific variables (e.g., rectal temperature, metabolic rate) during cold exposure and have developed and refined definitions of cold tolerance. Although defining cold tolerance is useful for characterizing population differences, insights into the physiological mechanisms that defend against hypothermia can be obtained by manipulating separately the primary sites of thermal sensation, those on the skin and in the body core, while monitoring the primary regulatory output, the heat production response. The few investigations that have attempted selective manipulation of the body temperatures in human subjects have of necessity imposed relatively uncomfortable conditions so as to obtain body core cooling. Nadel et al. (11) asked their subjects to rapidly ingest around

IN CONTRAST

1084

Health

500 g of ice cream and Benzinger et al. (1) and Hayward et al. (7) had their subjects sit in cold water for extended periods. Considering that central cold reception has been generally thought to have a minimal role in the control of shivering in man (l), it is important to develop different means for lowering body core temperature without the attendant discomfort, to evaluate its role in the control of shivering metabolism. The degree to which the heat production of voluntary exercise can replace that of involuntary shivering contractions during cold exposure has not been precisely determined. Increased bodily movement during exercise has the effect of increasing the convective and evaporative heat transfer coefficients (12), thereby increasing the rate of heat loss from skin to environment. During cycleergometer exercise in a 10°C environment the elevated heat transfer coefficients account for an increase in rate of heat loss of at least 60 W em-‘, or the equivalent of more than 1 met, as compared to resting in still air. Shivering can occur during exercise (lo), but it is now recognized that the integrated arousal response interferes with ongoing thermoregulation (13). It is also clear that the heat production of moderately heavy exercise is sufficient to raise internal body temperature to a level at which shivering is no longer required. The question remains as to the extent of the inhibition of shivering brought about by inputs other than increased body temperatures accompanying exercise. METHODS

Four healthy male subjects volunteered to participate in the present experiments. Each subject was fully informed and was introduced to the laboratory procedures on several occasions prior to the initial experimental run. Each experimental condition was performed in duplicate and all experiments were performed at the same time of day for each subject and in the same season. Subjects dressed in shorts and athletic shoes entered an antechamber for attachment of probes and then entered the environmental chamber, where temperature was maintained at either 10 or 25OC depending on the day’s protocol. Ambient humidity was always less than 10 Torr and air movement was always less than 0.1 ma s? On entering the chamber the subject was seated for a 60-min rest period, during which he was instructed to resist any voluntary movement. After the rest period the subject mounted a cycle ergometer adjacent to the seat and either sat at rest for an additional 30-60 min or

0161-7567/79/0000-0000$01.25

Copyright

0 1979 the American

Physiological

Society

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THERMOREGULATION

DURING

EXERCISE

IN

1085

COLD

began pedaling at the prescribed exercise intensity for the next 30 min. Pedaling frequency was 60 rpm and the exercise intensities employed were free pedaling (no load), a light intensity (30 W for 2 subj and 60 W for the other 2) and a moderate intensity (60 and 120 W, respectively). Sitting at rest in the environmental room allowed the mean skin temperature (Tsk) to arrive at a new steady level without affecting internal temperature. Exercising at different intensities after 60 min of rest provided a range of internal temperature, as well as different rates of metabolic heat production, at a given Tsk. Internal temperature was recorded continuously from a thermocouple whose tip was in the esophagus at the level of the left atrium. Tsk was calculated each minute from thermocouple recordings at eight skin sites, as previously described (5). Oxygen uptake (Voz) was calculated from continuous records of the fractions of 02 and CO2 in mixed expired air (electronic analyzers, calibrated against gases analyzed by manometric technique) and continuous recording of the expired ventilatory volume. Values were corrected to STPD. Thermoregulatory ~oZ was computed from total Vo2 by subtracting that component attributable to the maintenance of ongoing activity (rest or exercise) from the total. For each subject the resting ~oZ and the Voe at each exercise intensity were obtained in the 25OC environment. Thermoregulatory v02 was then defined as the excess Voz in comparable activities in the 10°C environment. In each case data were accumulated and averaged over lo-min intervals during rest and 5min intervals during exercise. Shivering activity was estimated from the electromyogram (EMG) obtained from silver-silver chloride surface electrodes positioned over the middle of the long axis of the sternocleidomastoides muscle of the neck. Raw unrectified EMG signals were fed directly into a high-gain preamplifier, which smoothed and rectified these signals. Areas under each curve were integrated and summed electronically and these data were simultaneously displayed on a second channel of the same recorder. The sternocleidomastoides muscle is known to be active during shivering and provides easy access for consistent placement of electrodes. Although this muscle group may serve as an accessory muscle in forced inspiration, any additional electrical activity due to exercise per se should be minimal, since the exercise intensities employed were light, and should increase with the increased exercise intensities if forced inspiration were present. Because our hypothesis involved the determination of the degree of shivering inhibition by the integrated arousal response, any decrease in the integrated EMG from the sternocleidomastoides muscle would be over and above any increase accompanying exercise. Such increases were not evident in pilot experiments at 25°C. Integrated EMG records were averaged over intervals similar to those for Voz and data are reported as relative activity in this study. No attempt was made to differentiate activity from any of the individual components of this muscle. RESULTS

Thermal and metabolic data were reproducible in any subject in duplicate experiments and the pattern of re-

sponse was similar in all subjects. Figure 1 illustrates thermal and metabolic data of one subject during the different protocols at 10°C. Data from the 60-min rest periods of eight exposures were averaged. Data from each of the four protocols following the rest period are averages of the duplicate exposures. When the subject entered the environmental chamber, Tsk fell in an approximately exponential manner toward a steady-state value, which was achieved around the end of the 60 min of rest. The rate of decrease of ?&k was nearly 0.3”C min-’ in the first 10 min and the total decrease in 60 min was around 5OC from the level at which the subject entered the chamber. In exposures lasting 120 min, there was no appreciable fall in Tsk from the 60-min value. Esophageal temperature (T,,) remained relatively constant during the 60-min rest period, tending to increase slightly (up to 0.2”C), in the initial 30 min and to decrease to a similar extent in the second 30 min of rest. In the control exposure (no exercise), T,, was essentially unchanged over the entire 120 min. Once the shivering threshold was surpassed, thermoregulatory v02 and shivering activity (EMG) increased with time until a steady state was achieved. Figure 1 shows the data of our leanest subject, who began to shiver almost immediately upon entering the chamber. Thermoregulatory v02 increased steadily between the 10th and 60th min of exposure, after which it remained around 250 ml 02 emin-’ above resting (an absolute value of 2 met) for the duration of the 120-min exposure. Figure 2 illustrates the relation between thermoregulatory ~oZ and Tsk in this same subject. As Tsk decreased l

oyl

lo

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20

A L

30

40

’

50

I L !

;O

70

A”

80

90

IO0

II0

TIME (MIN.) 1. Relative changes in Txk and T,, and 002 attributable to shivering as a function of time. Data points during first 60 min are averaged from 8 exposures and after 60 min are averaged from duplicate exr>osures. Data are from a remesentative subiect. FIG.


1086

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S.-I.

37.6

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Large increases in thermoregulatory ~oZ and EMG activity (the latter not shown in Fig. 1) accompanied the decrease in T,,. However, although there appeared to be a direct correspondence between lowered T,, and increased thermoregulatory voz, closer inspection revealed that the intensity of exercise also interacted with this relation. Because of the variation in T,, induced by this technique, we were able to plot the change in thermoregulatory Voz against T,,, at a fixed level of TSk,at the different exercise intensities. Such a plot from one subject is shown as Fig. 4. At any given exercise intensity there was a proportional relation between increasing thermoregulatory Vo2 and decreasing T,,, below a T,, threshold for shivering. The effect of increasing exercise intensity was to decrease thermoregulatory ~oZ at a given T,, and, more importantly, to decrease the sensitivity of the con-

l EXERCISE

(MIN.)

0 r:

d

26

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I

27

28 f,,

1 29

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2. Thermoregulatory v02 and T,, as functions of T,k during the skin cooling period (first 60 min). Data are from a representative subject. For this subject, thermoregulatory Vo2 = 3454 - 121 T,k (r = FIG.

-0.88).

rapidly toward 28°C there was an elevation in Vo2 that could not be attributed to the absolute Tsk in a proportional control model; rather, in this subject the heightened metabolic response during rapid skin cooling suggests a rate response characteristic in the control of shivering. Below a TSk of 28”C, however, there was a proportional increase in ~oZ with decreasing TSk. Throughout the period of skin cooling, there waskssentially no change in T,,, as shown in the top of Fig. 2. When exercise was begun after the 60 min of rest at lO”C, T,, decreased rapidly. The rate and magnitude of this decrease were related to the intensity of the exercise. Characteristic data from duplicate experiments in a single subject are shown in Fig. 3. In this subject freepedaling induced a decrease in T,, of around 0.3”C within 5 min of beginning exercise. Pedaling at an intensity of 60 W induced a decrease in T,, of 0.6”C within 3 min. Presumably, the decrease in internal temperature with exercise was the result of flushing cold blood from the legs back into the body core. Recovery of T,, also was related to the intensity of exercise. Although the greatest decrease in T,, accompanied the heaviest intensity of exercise, the greater absolute heat production in this condition served to drive T,, up at a steady rate over the final 25 min of exercise. With free-pedaling, the lowest intensity of exercise, the rate of heat production was insufficient to drive T,, back to preexercise levels (Fig. 1). Figure 1 also shows that the changes in TSkat the onset of exercise were minimal with small decreases the result of leg cooling caused by the increased convective heat transfer accompanying . , * ” v leg v exercise (12).

-0.2 9 . $0.4

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-0.8' FIG. 3. Change in T,, with time during duplicate exposures to different intensities of exercise. Prior to exercise, subjects had been seated for 60 min.

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to 7

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SUBJECT

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(‘C)

FIG. 4. Thermoregulatory To2 as a function of T,, at three different exercise intensities. Data points are from a representative subject. During free-pedaling thermoregulatory (th) Vo, = 32461 - 863 T,, (T = -0.85). During . exercise at 30 W, th Voz = 28506 - 764 T,, (r = -0.94) and at 60 W, th VOW = 16720 - 447 T, (r = -0.98).


THERMOREGULATION

DURING

EXERCISE

IN

1087

COLD

trolling system. For the three subjects who underwent a decrease in T,, during free-pedaling, the average slope of the thermoregulatory &to-T,, relation was nearly 1800 ml 02.min-’ OC-l reduction in T,,. Since decreases in T,, averaged 0.6OC during this transition, the peak thermoregulatory To2 averaged slightly over 1 1. min. During the heaviest exercise intensity tested, the slope of this relation averaged 355 ml 02.min-‘. ‘C-l, around 20% of the free-pedaling slope. During the intermediate exercise the slope averaged 605 ml 02 min-’ ‘C-l (for 3 subj), around 34% of the free-pedaling relation. For reference, the sensitivity of the metabolic response to decreases in Tsk averaged only 110 ml 02 min-’ ‘C-l reduction in ?&k, around 6% of the free-pedaling response per unit decrease in T,,. Individual data are shown in Table 1. The integrated EMG data were practically identical in form to the results from the measurement of thermoregulatory vo2 at the different exercise intensities, supporting the notion that increasing voluntary muscular activity per se was not the cause for the suppression of the shivering response at a given T,, (Fig. 5). l

l

l

l

SUBJ.

S H

DISCUSSION

The data of the present study confirmed our previous but preliminary observations (10) that, when internal body temperature was reduced below the shivering threshold, shivering and associated elevations in heat production were superimposed upon the rhythmic muscle contractions and heat production of cycle-ergometer exercise. Also as seen previously (lo), the v02 attributable to shivering was proportional to the decrease of internal temperature at a given intensity of exercise. Although shivering was able to coexist with exercise, the present study demonstrates that shivering is increasingly suppressed at any level of internal body temperature with increasing exercise intensity. This suppression is pronounced, amounting to an 80% decrease in the slope of the thermoregulatory \joZ-to-Tes relation at the heaviest intensity of exercise studied. Although we did not determine the subjects’ maximal aerobic power (vo2 max),the heaviest exercise intensity performed in the present study was certainly not greater than 50% 002 max.Thus, the effect of mild-to-moderate exercise is a graded inhibition of the shivering response. More than 20 yr ago Birzis and Hemingway (2) identified a neuronal pathway that descended from the posterior hypothalamus and whose activity correlated well with shivering activity in the intact cat. If the animal was curarized, nervous activity could still be increased by 1. Characteristics of metabolic response to skin and body core cooling

TABLE

Subj

JF DK RS SH

Rest, AvoJAillgk, d.“C-1

Exercise,

AvoJAT,,

Free pedal

26

Low

1,800

l

ex

Moderate

769

181 105

2,020

t

121

1,563

196 850

* No change in T,, was induced. plete this experiment.

ml OC-’

*

t Subject

was unable

ex

360 455 94 510 to com-

I

36.7

I

37.1

37.5

1

Te*, (‘Cl FIG. 5. Integrated EMG values as a function of T,, at three different exercise intensities. Data points are from the same experiments as shown in Fig. 4. During free-pedaling thermoregulatory (th) Vo, = 376 - 10.0 T,, (r = -0.81). During exercise at 30 W, th J?oz = 488 - 13.1 T,, (r = -0.95) and at 60 W, th VOW = 294 - 7.9 T,, (r = -0.97).

cooling the skin and abolished by skin warming. Birzis and Hemingway termed this the efferent shivering pathway and inferred that the drive for shivering originated ten trally, as a consequence of peripheral stimuli. A.bout the same time, Boyarsky and Stewart (3) reported that a 1-ms pulse stimulus to the skin caused uniform inhibition of shivering over the body. They concluded that activity of a central region was being inhibited. Previously, Hemingway et al. (8) had suppressed shivering by hypothalamic stimulation, and somewhat more recently Stuart et al. (14) were able to suppress bilateral shivering by unilateral stimulation of forebrain septum or caudal hypothalamus. Our data on human subjects are compatible with these early findings that suppression of shivering is of central origin. Inasmuch as the neck muscles themselves are not directly involved in the additional activity of exercise, and suppression of the neck muscle EMG occurred in a manner similar to that of thermoregulatory J?oz,it is safe to conclude that the graded suppression of the shivering response during exercise of increasing intensities was centrally mediated rather than the result of competition at the local (muscle) level. These data also support recent observations of Stitt (13) that, in the rabbit, either electrical or chemical stimulation of the defense area produced an integrated arousal response and a sustained inhibition of shivering in a cold environment, causing rectal temperature to fall. In human subjects the arousal accompanying increased muscular activity presumably


1088 was responsible for the increased suppression of the heat production response. Curiously, inhibition of temperature regulation may not be limited to th at accompanying arousal during cold exposure. Stitt (13) also showed that stimul .ation of the defense area in animals exposed to warm conditions and in .creased rectal tempercaused ear vasoconstriction atures. Recently, we (9) showed that, in conditions of multiple demand (heavy exercise in the heat), circulatory regulation has precedence over temperature regulation in humans and internal temperature is driven steadily upward. These data suggest that the less critical regulatory system, th .at which defends internal body temperature, is temporarily inactivated so as to maintain the more immediate potentially life-saving reflexes of the integrated arousal response. Benzinger et al. (l), Brown and Brengelmann (4)) and more recently Hayward et al. (7) used the water bath to obtain a great many combinations of internal and skin temperatures in human subjects. They measured the ~oZ at the different levels of body temperatures and related the heat produc tion response to these temperatures. Benzinger et al. (1) maintained that the control of shivering metabolism originated from cold reception at the skin, with sensors in the body core responsible only for warmth reception and control against overheating. Brown and Brengelmann (4) developed different driving functions for skin temperature to identify both transient and steady-state relationships between the body temperatures and the rate of shivering thermogenesis. They concluded that the control of shivering metabolism was best described by a multiplication of temperature signals from the skin and core, with a given decrease in the core temperature eliciting nearly 20 times the increase in metabolic rate as the same decrease in mean skin temperature in the region where Tsk was around 28°C. Hayward et al. (7) assumed a multiplicative model and forcefit their data to such a model. Their conto ur plot shows a given change in in .ternal temperature having only around 3-5 times the metabolic effect as a given than 4F in mean skin temperature when Tsk was around 26” C . Differences in the relative importance of the body temperatures between these three studies can be partially attributed to differences in technique and m .aY also be a function of the way temperature changes were achieved in the water bath 9w phereskin temperatures are all fixed at the same level. In air, regional skin temperatures may be quite disparate in the cold and may not produce the sensory information that would be predicted from temperature and surface area alone (5). In both of these latter two studies, however, it is clear that cold reception within the body core is the more important determinant

S.-I.

HONG

AND

E. R. NADEL

of the shivering response. Experiments that have manipulated the average skin and body core temperatures in an air environment have also found a heightened heat production response to body core cooling. Nadel et al. (11) found that, when the core was suddenly cooled by rapid ingestion of ice cream, the increase in metabolic response was around 12 times that stimulated by the same-change in T,k during cold exposure. In the present study the flushing of cold blood from the leg muscles to the body core by leg movement alone produced around 16 times the metabolic increase per unit of internal temperature change as did similar changes in Tsk. This observation supports earlier findings that internal temperature changes are indeed important in the integrated defense against hypothermia. The decrements in body core temperature induced by pedaling reflect a redistribution of the body heat content, by increased mixing of blood between the cooled limbs and warmer viscera, rather than a sudden decrease in mean body temperature. This is similar to the findings of Glaser and Holmes-Jones (6) that shivering could be induced in humans by exercising precooled limbs. This interpretation is counter to the claim that heat content or heat flow rather than internal temperature is the regulated variable in providing for thermal homeostasis, as there is a large increase in the heat production response with minimal change in heat flow from the body. In conclusion several findings are evident. Shivering metabolism is proportional to decreased body core temperature when T,k is constant and to Tsk when internal temperature is constant, below the respective shivering thresholds. Shivering thresholds tended to be at higher body temperatures in leaner individuals. There appears to be a rate effect in the control system, as a rate of ’ stimula tes a higher change of ijT‘,k around 0.3”Cminmetabolic response than would be predicted by a proportional control system. Decreases in body core temperature have a much greater effect than do similar decreases in Tsk in inducing metabolic responses. Finally, although shivering can coexist with exercise, increasing exercise intensities have the effect of increasingly suppressing the shivering response. This may be the consequence of the integrated aro usal response having precedence over thermoregulatory activities. We gratefully acknowledge advice and technical assistance provided by M. F. Roberts, C. B. Wenger and L. I. Crawshaw. This study was supported in part by National Institutes of Health Grant ES-00354. Present address of S.-I. Hong: Dept. of Anesthesiology, New York University Medical Center, New York, NY 10016. Received

26 February

1979; accepted

in final

form

19 June

1979.

REFERENCES 1. BENZINGER, T. H., C. KITZINGER, AND A. W. PRATT. The human thermostat. In: Temperature, Its Measurement and Control in Science and Industry, edited by J. D. Hardy. New York: Reinhold, 1963, vol. 3, part 3, p. 637-665. 2. BIRZIS, L., AND A. HEMINGWAY. Efferent brain discharge during shivering. J. Neurophysiol. 20: 156-166, 1956. 3. BOYARSKY, L. L., AND L. STEWART. Neurogenic inhibition of shivering. Science 125: 649-650, 1957. 4. BROWN, A. C., AND G. L. BRENGELMANN. The interaction of

peripheral and central inputs in the temperature regulation system. In: Physiological and Behavioral Temperature Regulation, edited by J. D. Hardy, A. P. Gagge, and J. A. J. Stolwijk. Springfield, IL: Thomas, 1970, p. 684-702. 5. CRAWSHAW, L. I., E. R. NADEL, J. A. J. STOLWIJK, AND B. A. STAMFORD. Effect of local cooling on sweating rate and cold sensation. Pfluegers Arch. 354: 19-27, 1975. 6. GLASER, E. M., AND R. V. HOLMES-JONES. The initiation of shivering by cooled blood returning from the lower limbs. J. Physiol.


THERMOREGULATION

DURING

EXERCISE

IN

COLD

London 114: 277-282,195l. 7. HAYWARD, J. S., J. D. ECKERSON, AND M. L. COLLIS. Thermoregulatory heat production in man: prediction equation based on skin and core temperatures. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 42: 377-384, 1977. 8. HEMINGWAY, A., P. FORGRAVE, AND L. BIRZIS. Shivering suppression by hypothalamic stimulation. J. Neurophysiol. 17: 375-386, 1954. 9. NADEL, E. R., E. CAFARELLI, M. F. ROBERTS, AND C. B. WENGER. Circulatory regulation during exercise in different ambient temperatures. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 46: 430-437, 1979. 10. NADEL, E. R., I. HOLMI?R, U. BERGH, P.-O. ASTRAND, AND J. A. J. STOLWIJK. Thermoregulatory shivering during exercise. Life Sci. 13: 983-989, 1973.

1089 11. NADEL, E. R., S. M. HORVATH, C. A. DAWSON, AND A. TUCKER. Sensitivity to central and peripheral thermal stimulation in man. J. Appl. Physiol. 29: 603-609, 1970. 12. NISHI, Y., AND A. P. GAGGE. Direct evaluation of convective heat transfer coefficient by naphthalend sublimation. J. Appl. PhysioZ. 29: 830-838, 1970. 13. STITT, J. T. Inhibition of thermoregulatory outflow in conscious rabbits during periods of sustained arousal. J. Physiol. London 260: 32P-33P, 1976. 14. STUART, D. G., Y. KAWAMURA, AND A. HEMINGWAY. Activation and suppression of shivering during septal and hypothalamic stimulation. Exp. Neural. 4: 485-506, 1961. 15. WYNDHAM, C. H. The physiology of exercise under heat stress. Annu. Rev. Physiol. 35: 193-220, 1973.


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