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J Appl Physiol 97: 1367-1370, 2004. First published May 28, 2004; doi:10.1152/japplphysiol.00403.2004
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Effect of thermal stress on the vestibulosympathetic reflexes in humans

Thad E. Wilson1 and Chester A. Ray1,2

1Division of Cardiology, Department of Medicine, and 2Department of Cellular and Molecular Physiology, General Clinical Research Center, Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033

Submitted 14 April 2004 ; accepted in final form 21 May 2004


   ABSTRACT
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METHODS
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Both heat stress and vestibular activation alter autonomic responses; however, the interaction of these two sympathetic activators is unknown. To determine the effect of heat stress on the vestibulosympathetic reflex, eight subjects performed static head-down rotation (HDR) during normothermia and whole body heating. Muscle sympathetic nerve activity (MSNA; peroneal microneurography), mean arterial blood pressure (MAP), heart rate (HR), and internal temperature were measured during the experimental trials. HDR during normothermia caused a significant increase in MSNA ({Delta}5 ± 1 bursts/min; {Delta}53 ± 14 arbitrary units/min), whereas no change was observed in MAP, HR, or internal temperature. Whole body heating significantly increased internal temperature ({Delta}0.9 ± 0.1°C), MSNA ({Delta}10 ± 3 bursts/min; {Delta}152 ± 44 arbitrary units/min), and HR ({Delta}25 ± 6 beats/min), but it did not alter MAP. HDR during whole body heating increased MSNA ({Delta}16 ± 4 bursts/min; {Delta}233 ± 90 arbitrary units/min from normothermic baseline), which was not significantly different from the algebraic sum of HDR during normothermia and whole body heating ({Delta}15 ± 4 bursts/min; {Delta}205 ± 55 arbitrary units/min). These data suggest that heat stress does not modify the vestibulosympathetic reflex and that both the vestibulosympathetic and thermal reflexes are robust, independent sympathetic nervous system activators.

orthostasis; otolith organs; muscle sympathetic nerve activity; microneurography; heat stress

ORTHOSTATIC TOLERANCE IS REDUCED during heat stress compared with normothermia (1, 14, 15, 27). Sympathetic nervous system reflexes are imperative in maintaining blood pressure during orthostatic stress. The role of the baroreflexes during orthostasis and heat stress has been systematically examined (3, 10, 24). Baroreflex responses are largely preserved in the heat, albeit at a higher level of sympathetic activation level relative to normothermia (3, 5). If the baroreflexes are operational during heat stress, another mechanism(s) must be involved to account for the reduced orthostatic tolerance. One potential candidate is the vestibular system, because it is heavily involved in autonomic and cardiovascular responses to postural changes.

Doba and Reis (8) demonstrated the important role of the vestibular system during postural change. This study observed that, on denervation of the vestibular nerve, tilted cats were unable to maintain arterial blood pressure (8). Later studies reported that stimulation of the otolith organs increases sympathetic outflow and vascular resistance in the cat (12, 32, 33). In humans, head-down rotation (HDR), which activates the otolith organs, has been shown to increase muscle sympathetic nerve activity (MSNA) and limb vascular resistance (17, 22). Increases in MSNA have also been observed during off-vertical axis rotation, which engages the otolith organs (11).

The vestibulosympathetic reflex in human experiments is independent of other postural reflexes, such as the baroreflexes (20). Currently, the role of heat stress on the vestibulosympathetic reflex is unknown because only the role of baroreceptors has been adequately investigated during orthostasis and heat stress. Heating also has direct effects on endolymph and vestibular hair cell firing characteristics (19, 28). Therefore, it is possible that elevations in body temperature during heat stress will alter afferent feedback from the vestibular sensory organs, modifying autonomic responses. Thus a diminished sympathetic response and subsequent reduction in peripheral resistance may be elicited by the vestibulosympathetic reflex during heat stress and may contribute to the orthostatic intolerance observed during heat stress. On the basis of the finding that the baroreflexes function adequately during heat stress and that heating may have direct effects on the vestibular system, we hypothesize that the vestibulosympathetic reflex would be attenuated during heat stress.


   METHODS
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Subjects.   Eight healthy subjects (5 men, 3 women) participated in this study. The subjects' physical characteristics were age of 23 ± 1 yr, height of 173 ± 4 cm, and weight of 69 ± 4 kg. Subjects were not taking medications and were free of any known cardiovascular, neurological, or metabolic diseases. All subjects refrained from caffeine, alcohol, and exercise 24 h before the study. Written, informed consent from each subject was obtained before participation, and the study was approved by The Pennsylvania State University College of Medicine Institutional Review Board.

Protocol.   All experiments were performed with the subjects in the prone position in a dimly lit, quiet, normothermic (20–22°C) laboratory to minimize environmental influences on autonomic responses. To determine the role of the otolith organs on MSNA responses, static HDR was performed as previously described (26). Briefly, HDR involves the head being extended and supported in the baseline condition; the support is subsequently removed, and the head is allowed to passively rotate to the point of maximal rotation. Subjects performed this maneuver with their eyes closed. Head rotation was measured by means of an electrogoniometer (13). HDR was completed for 3 min during normothermia and then subsequently during whole body heating. Temperature was controlled in normothermia by perfusing neutral temperature water (34–35°C) through a custom-designed high-density tube-lined suit (Med-Eng Systems, Ottawa, ON, Canada). Whole body heating was accomplished by perfusing warm (44–46°C) water through the suit to increase mean skin temperature. Once sublingual temperature increased ~0.5–0.7°C, the temperature of the water was reduced in an attempt to reduce the rate of rise of internal temperature during the HDR data collection period.

Instrumentation and measurements.   Internal temperature was measured via a thermistor placed in the sublingual sulcus. Skin temperature was measured via the weighted average of three thermocouples attached to the skin (25) and routed through a thermocouple meter (TC-1000, Sabel Systems, Henderson, NV).

Multifiber recordings of MSNA were obtained with a tungsten microelectrode inserted in the common peroneal nerve. A reference electrode was placed subcutaneously 2–3 cm from the recording electrode. The recording electrode was adjusted until a site was found in which MSNA bursts were clearly identified using previously established criteria (7, 29). The nerve signal was amplified, passed through a band-pass filter with a bandwidth of 700–2,000 Hz, and integrated with a time constant of 0.1 s (Iowa Bioengineering, Iowa City, IA). Mean voltage neurograms were visually displayed and recorded on a data acquisition system. The nerve signal was also routed to a loudspeaker for monitoring throughout the study.

Arterial blood pressure and heart rate were measured continuously by a finger cuff (Finapres, Ohmeda, Englewood, CO). Cuff blood pressure was also recorded by auscultation of the brachial artery (Dinamap XL, Critikon/GE Medical Systems, Tampa, FL). Skin blood flow was indexed via laser-Doppler flowmetry (model DRT 4, Moor Instruments, Wilmington, DE) from two areas on the back not directly exposed to the water-perfused suit. Back sweat rate was measured via capacitance hygrometry (model HMP233, Viasala, Woburn, MA) by means of perfusing 100% nitrogen at a flow rate of 500 ml/min through a ventilated capsule (surface area = 3.94 cm2) attached to the surface of the skin. Respiratory frequency was monitored by using piezoelectric pneumograph (pneumotrace II, UFI, Morro Bay, CA) to determine whether respiratory patterns were altered during data collection period.

Data analysis and statistics.   Data were sampled at 40–200 Hz via an analog-to-digital converter and data acquisition system (8S, ADInstruments, New Castle, Australia). MSNA was quantified both as burst frequency (burst/min) and total activity calculated via the sum of the area of all the sympathetic bursts in 1 min (arbitrary units/min). Segments with aberrant electrical noise were excluded from the calculation. Average values during the final 60 s of control, HDR, and recovery were statistically analyzed. Cutaneous vascular conductance (CVC) was calculated from the ratio of skin blood flow to mean arterial blood pressure and normalized to baseline (i.e., normothermic levels).

Temperatures, CVC, and sweat rate during normothermia and heat-stress were compared via dependent t-tests. MSNA and cardiovascular responses were compared between normothermia and heat stress conditions by means of two-within-factor (temperature, intervention) repeated-measures ANOVA. All values are reported as means ± SE. P values of <0.05 were considered statistically significant.


   RESULTS
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Whole body heating significantly increased internal temperature (~0.9°C) and mean skin temperature (~4.4°C) compared with normothermia (Table 1). However, no further increase in internal temperature was observed during the HDR intervention (pre-HDR 37.1 ± 0.1 and post-HDR 37.0 ± 0.1°C; P = 0.403). Whole body heating significantly increased CVC and sweat rate (Table 1).


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  		Table 1. Temperature and thermoregulatory effector responses to whole body heating

 
MSNA expressed as burst frequency and total activity increased during both whole body heating and HDR (Fig. 1). HDR during whole body heating elicited an increase in MSNA of 16 ± 4 bursts/min and 233 ± 90 arbitrary units/min from normothermic baseline. However, these values were not significantly different from the algebraic sum of HDR during normothermia and whole body heating ({Delta}15 ± 4 bursts/min and {Delta}205 ± 55 arbitrary units/min) (Fig. 1). To demonstrate increases in MSNA associated with HDR and whole body heating, representative neurograms from one subject during thermal and vestibular perturbations are presented in Fig. 2.



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  		Fig. 1. Change ({Delta}) in muscle sympathetic nerve activity [in bursts/min (A) and in arbitrary units/min (B)] during 3 min of head-down rotation (HDR) during normothermia and heat stress. Values are means ± SE. NS, not significant. Significant increases in muscle sympathetic nerve activity were observed during HDR and heat stress when performed independently. Sum of HDR and heat stress trials (Sum) were comparable to the combination trial (HDR + Heat). *P < 0.05 compared with baseline. # P < 0.05 compared with either heat stress or HDR.

 


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  		Fig. 2. Representative tracing of 1 individual's mean voltage neurograms of muscle sympathetic nerve activity at baseline and HDR during normothermia and heat stress. HDR increases muscle sympathetic nerve activity during both normothermia and heat stress trials.

 
Whole body heating significantly increased heart rate (~25 beats/min) but did not significantly alter arterial blood pressure (Table 2). HDR did not significantly change heart rate or arterial blood pressure in either thermal condition. The combination of HDR and whole body heating increased heart rate by 29 ± 6 beats/min, and this value was not significantly different from the algebraic sum of HDR during normothermia and during whole body heating ({Delta}25 ± 6 beats/min). Mean arterial blood pressure was also not significantly different between combined trial and algebraic sum of whole body heating and HDR (Table 2).


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  		Table 2. Effect of thermal state on cardiovascular responses to 3 min of head-down rotation

 

   DISCUSSION
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
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 REFERENCES
 
The major finding of the present study is that MSNA increases are similar during HDR in normothermia and heat stress. These findings indicate that heat stress does not modify the vestibulosympathetic reflex in humans and that both the vestibulosympathetic and thermal reflexes are robust independent sympathetic nervous system activators. Thus our results suggest that it is unlikely that a diminished vestibulosympathetic reflex contributes to heat-related decreases in orthostatic tolerance.

Increases in internal and mean skin temperature resulted in increases in MSNA. This is a consistent finding in humans (4, 5, 18). HDR caused similar increases in MSNA during both normothermia and heat stress. Although increases in MSNA with HDR are well established during normothermia (9, 17, 23, 26), this is the first report of MSNA responses during otolithic activation during heat stress.

Comparable increases in MSNA during HDR in both normothermia and heat stress indicate that these sympathetic activators are independent effectors of MSNA. The combination of HDR and heat stress was not significantly different from the algebraic sum of HDR and heat stress, thus suggesting that the vestibulosympathetic reflex when combined with thermal reflexes is additive and not augmented or attenuated. The independent and additive MSNA response during HDR has been observed with other sympathetic maneuvers, such as isometric exercise, mental stress, hypoxia, and baroreceptor unloading (2, 16, 20, 21). Having multiple independent sympathetic reflexes is not surprising and likely contributes to coarse and fine homeostatic adjustments of the regulation of blood pressure during orthostasis.

Orthostatic tolerance is reduced during heat stress compared with normothermia (1, 15, 27). The precise mechanism for this increased intolerance is currently unknown, but the vestibular system could be contributing to this intolerance if heat stress altered autonomic responses to the engagement of the otolith organs. We observed that thermal state did not influence the MSNA responses during HDR. This indicates that, contrary to our hypothesis, the MSNA response during activation of otolith organs is not impaired during heat stress. However, even with maintained sympathetic outflows, it is possible that the vasculature is less responsive to vasoconstriction during heat stress compared with normothermia. Experimental evidence supports this assertion (6, 30). Hence, it is possible that a greater MSNA response is necessary during orthostatic stress to elicit a similar end-organ response during heat stress compared with normothermia. However, this does not appear to be possible through activation of the vestibulosympathetic reflex.

Another factor that must be considered when discussing orthostatic tolerance during heat stress is that activation of the otolith organs does not contribute to skin vascular resistance during normothermia (23) and whole body heating (31). This could be problematic for orthostatic tolerance in the human, because large amounts of blood flow are being directed to the skin and reductions within this vascular space would be important to maintain arterial blood pressure, whereas the further constriction of an already vasoconstricted vascular bed (i.e., muscle) would be less essential.

One potential limitation of this study is not having a direct measure of temperature within the otolith organs (i.e., sacculus and utricle). Previous studies have identified direct effects of temperature on endolymph and vestibular hair cell function (19, 28). These heat-related effects may diminish autonomic responses to the vestibulosympathetic reflex. Our whole body heating protocol significantly increased internal and mean skin temperature, but these increases may have not caused changes in endolymph or vestibular hair cell function. Nonetheless, our whole body heating protocol was clearly sufficient to result in significant physiological changes (e.g., increases in heart rate, CVC, and sweat rate) typically associated with heat stress.

Summary.   Whole body heating does not significantly alter MSNA responses to HDR. The engagement of the otolith organs via HDR increases MSNA during normothermia and heat stress. The algebraic sums of MSNA during whole body heating plus HDR were similar to the combination of whole body heating and HDR performed together. This finding indicates that the vestibulosympathetic reflex is not impaired during heat stress. These results suggest that the vestibulosympathetic and thermal reflexes are independent activators of the sympathetic nervous system.


   GRANTS
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 ABSTRACT
 METHODS
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 GRANTS
ACKNOWLEDGMENTS
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This research project was funded in part by National Institutes of Health (NIH) Grant DC-006459 (to C. A. Ray), American Heart Association Established Investigator Grant (to C. A. Ray), and American Heart Association Beginning Grant-in-aid (to T. E. Wilson). This work was supported by National Space Biomedical Research Institute Grant CA00207 through National Aeronautics and Space Administration Grant NCC 9-58 (to C. A. Ray). Additional support was provided by NIH-sponsored General Clinical Research Center Grants M01 RR-10732 and C06 RR-016499.


   ACKNOWLEDGMENTS
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We thank Erica McHugh and Nathan Kuipers for technical assistance.


   FOOTNOTES
 

Address for reprint requests and other correspondence: T. E. Wilson, Div. of Cardiology, H047, Pennsylvania State College of Medicine, 500 Univ. Dr., Hershey, PA 17033-2390 (E-mail: tew12{at}psu.edu).

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. Section 1734 solely to indicate this fact.


   REFERENCES
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  1. Allan JR and Crossley RJ. Effect of controlled elevation of body temperature on human tolerance to +Gz acceleration. J Appl Physiol 33: 418–420, 1972.[Free Full Text]
  2. Carter JR, Ray CA, and Cooke WH. Vestibulosympathetic reflex during mental stress. J Appl Physiol 93: 1260–1264, 2002.[Abstract/Free Full Text]
  3. Crandall CG, Cui J, and Wilson TE. Effects of heat stress on baroreflex function in humans. Acta Physiol Scand 177: 321–328, 2003.[CrossRef][Web of Science][Medline]
  4. Crandall CG, Etzel RA, and Farr DB. Cardiopulmonary baroreceptor control of muscle sympathetic nerve activity in heat-stressed humans. Am J Physiol Heart Circ Physiol 277: H2348–H2352, 1999.[Abstract/Free Full Text]
  5. Cui J, Wilson TE, and Crandall CG. Baroreflex modulation of sympathetic nerve activity to muscle in heat-stressed humans. Am J Physiol Regul Integr Comp Physiol 282: R252–R258, 2002.[Abstract/Free Full Text]
  6. Cui J, Wilson TE, and Crandall CG. Phenylephrine-induced elevations in arterial blood pressure are attenuated in heat-stressed humans. Am J Physiol Regul Integr Comp Physiol 283: R1221–R1226, 2002.[Abstract/Free Full Text]
  7. Delius W, Hagbarth KE, Hongell A, and Wallin BG. Manoeuvres affecting sympathetic outflow in human muscle nerves. Acta Physiol Scand 84: 82–94, 1972.[Web of Science][Medline]
  8. Doba N and Reis DJ. Role of the cerebellum and the vestibular apparatus in regulation of orthostatic reflexes in the cat. Circ Res 40: 9–18, 1974.[Medline]
  9. Hume KM and Ray CA. Sympathetic responses to head-down rotations in humans. J Appl Physiol 86: 1971–1976, 1999.[Abstract/Free Full Text]
  10. Johnson JM and Proppe DW. Cardiovascular adjustments to heat stress. In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc, 1996, sect. 4, vol. I, chapt. 11, p. 215–243.
  11. Kaufmann H, Biaggioni I, Voustianiouk A, Diedrich A, Costa F, Clarke R, Gizzi M, Raphan T, and Cohen B. Vestibular control of sympathetic activity. An otolith-sympathetic reflex in humans. Exp Brain Res 143: 463–469, 2002.[CrossRef][Web of Science][Medline]
  12. Kerman IA, Emanuel BA, and Yates BJ. Vestibular stimulation leads to distinct hemodynamic patterning. Am J Physiol Regul Integr Comp Physiol 279: R118–R125, 2000.[Abstract/Free Full Text]
  13. Kuipers NT, Sauder CL, and Ray CA. Aging attenuates the vestibulorespiratory reflex in humans. J Physiol 548: 955–961, 2003.[Abstract/Free Full Text]
  14. Leithead CS and Lind AR. Heat Stress and Heat Disorders. Philadelphia, PA: Davis, 1964.
  15. Lind AR, Leithead CS, and McNicol GW. Cardiovascular changes during syncope induced by tilting men in the heat. J Appl Physiol 25: 268–276, 1968.[Free Full Text]
  16. Monahan KD and Ray CA. Interactive effect of hypoxia and otolith organ engagement on cardiovascular regulation in humans. J Appl Physiol 93: 576–580, 2002.[Abstract/Free Full Text]
  17. Monahan KD and Ray CA. Limb neurovascular control during altered otolithic input in humans. J Physiol 538: 303–308, 2002.[Abstract/Free Full Text]
  18. Niimi Y, Matsukawa T, Sugiyama Y, Shamsuzzaman AS, Ito H, Sobue G, and Mano T. Effect of heat stress on muscle sympathetic nerve activity in humans. J Auton Nerv Syst 63: 61–67, 1997.[CrossRef][Web of Science][Medline]
  19. Ohtani M, Yamashita T, Amano H, Kubo N, and Kumazawa T. Thermal influence on intracellular calcium concentration in vestibular hair cells isolated from the guinea pig. A preliminary report. Acta Otolaryngol Suppl (Stockh) 500: 46–49, 1993.
  20. Ray CA. Interaction of the vestibular system and baroreflexes on sympathetic nerve activity in humans. Am J Physiol Heart Circ Physiol 279: H2399–H2404, 2000.[Abstract/Free Full Text]
  21. Ray CA. Interaction between vestibulosympathetic and skeletal muscle reflexes on sympathetic activity in humans. J Appl Physiol 90: 242–247, 2001.[Abstract/Free Full Text]
  22. Ray CA and Carter JR. Vestibular activation of sympathetic nerve activity. Acta Physiol Scand 177: 313–319, 2003.[CrossRef][Web of Science][Medline]
  23. Ray CA, Hume KM, and Shortt TL. Skin sympathetic outflow during head-down neck flexion in humans. Am J Physiol Regul Integr Comp Physiol 273: R1142–R1146, 1997.[Abstract/Free Full Text]
  24. Rowell LB. Human Cardiovascular Control. Oxford, UK: Oxford University Press, 1993.
  25. Sawka MN, Gonzalez RR, Young AJ, Muza SR, Pandolf KB, Latzka WA, Dennis RC, and Valeri CR. Polycythemia and hydration: effects on thermoregulation and blood volume during exercise-heat stress. Am J Physiol Regul Integr Comp Physiol 255: R456–R463, 1988.[Abstract/Free Full Text]
  26. Shortt TL and Ray CA. Sympathetic and vascular responses to head-down neck flexion in humans. Am J Physiol Heart Circ Physiol 272: H1780–H1784, 1997.[Abstract/Free Full Text]
  27. Shvartz E, Strydom NB, and Kotze H. Orthostatism and heat acclimation. J Appl Physiol 39: 590–595, 1975.[Abstract/Free Full Text]
  28. Suzuki M, Kadir A, Hayashi N, and Takamoto M. Direct influence of temperature on the semicircular canal receptor. J Vestib Res 8: 169–173, 1998.[CrossRef][Web of Science][Medline]
  29. Vallbo AB, Hagbarth KE, Torebjork HE, and Wallin BG. Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol Rev 59: 919–957, 1979.[Free Full Text]
  30. Wilson TE, Cui J, and Crandall CG. Effect of whole-body and local heating on cutaneous vasoconstrictor responses in humans. Auton Neurosci 97: 122–128, 2002.[CrossRef][Web of Science][Medline]
  31. Wilson TE, Kuipers NT, McHugh EA, and Ray CA. Vestibular activation does not influence skin sympathetic nerve responses during whole body heating. J Appl Physiol 97: 540–544, 2004.[Abstract/Free Full Text]
  32. Yates BJ. Vestibular influences on the autonomic nervous system. Ann NY Acad Sci 781: 458–473, 1996.[Web of Science][Medline]
  33. Yates BJ and Miller AD. Properties of sympathetic reflexes elicited by natural vestibular stimulation: implications for cardiovascular control. J Neurophysiol 71: 2087–2092, 1994.[Abstract/Free Full Text]



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