Abstract
Herein, the principles of homoeostasis are re-visited, but with an emphasis upon repeated homoeostatic disturbances that give rise to physiological adaptation. The central focus is human heat adaptation, and how, for experimental purposes, one might standardise successive adaptation stimuli, and then evaluate and compare the resulting adaptations. To provide sufficient background for that discussion, the principles of physiological control and regulation have been reviewed. The case is presented that, since it is the regulated variables that drive both the effector organs and the processes of physiological adaptation, then it is those variables (e.g., body temperature) that should be used to set and standardise the adaptation stimuli. Alternatively, some have proposed that the same outcome can be achieved through standardising a controlled variable (e.g., heart rate), and so the merits of that proposition are evaluated. Indeed, it can be an effective approach, although some experimental pitfalls are described to highlight its limitations with regard to between-group (e.g., able-bodied versus spinal-injured participants) and between-treatment comparisons (e.g., hot-water versus hot-air adaptation stimuli). The concept of setting the adaptation stimulus relative to an anaerobic or lactate threshold is also critically evaluated. Finally, an appraisal is offered concerning the merits of three different strategies for using deep-body and mean body temperature changes for evaluating thermoeffector adaptations.
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Abbreviations
- ATP:
-
Adenosine triphosphate
References s
Adolph EF (1956) General and specific characteristics of physiological adaptations. Am J Physiol 184:18–28
Adolph EF (1964) Perspectives of adaptation: some general properties. In: Dill DB, Adolph EF (eds) Handbook of physiology. Section 4. Adaptation to the environment. American Physiological Society, Washington, pp 27–35
Armstrong LE, Pandolf KB (1988) Physical training, cardiorespiratory physical fitness and exercise-heat tolerance. In: Pandolf KB, Sawka MN, Gonzales RR (eds) Human performance physiology and environmental medicine at terrestrial extremes. Benchmark Press, Indianapolis, pp 199–226
Banister EW, Calvert TW (1980) Planning for future performance: implications for long term training. Can J Appl Sport Sci 5:170–176
Barcroft H, Edholm OG (1945) On the vasodilatation in human skeletal muscle during post-haemorrhagic fainting. J Physiol 104:161–175
Barr DP, Himwich HE (1923) Studies in the physiology of muscular exercise: II. Comparison of arterial and venous blood following vigorous exercise. J Biol Chem 55:525–537
Bass DE (1963) Thermoregulatory and circulatory adjustments during acclimatization to heat in man. In: Hardy JD (ed) Temperature: its measurement and control in science and industry. Reinhold, New York, pp 299–305
Bass DE, Kleeman CR, Quinn M, Henschel A, Hegnauer AH (1955) Mechanisms of acclimatization to heat in man. Medicine 34:323–380
Bernard C (1879) Leçons sur les phénomènes de la vie communs aux animaux et aux végétaux. J.-B Baillière et Fils, Paris
Bevegård BS, Shepherd JT (1966) Reaction in man of resistance and capacity vessels in forearm and hand to leg exercise. J Appl Physiol 21:123–132
Blair DA, Glover WE, Roddie IC (1961) Vasomotor responses in the human arm during leg exercise. Circ Res 9:264–274
Bligh J (1973) Temperature regulation in mammals and other vertebrates Frontiers of Biology, vol 30. North-Holland Publishing Company, Amsterdam
Booth FW, Roberts CK, Thyfault JP, Ruegsegger GN, Toedebusch RG (2017) Role of inactivity in chronic diseases: evolutionary insight and pathophysiological mechanisms. Physiol Rev 97:1351–1402
Borg GAV (1962) Physical performance and perceived exertion. Gleerup, Lund
Boulant JA (1996) Hypothalamic neurons regulating body temperature. Comprehensive Physiology, Supplement 14: Handbook of Physiology, Environmental Physiology, pp 105–126. https://doi.org/10.1002/cphy.cp040106]
Boutron I, Ravaud P (2018) Misrepresentation and distortion of research in biomedical literature. Proc Natl Acad Sci USA 115:2613–2619
Cannon WB (1929) Organisation for physiological homeostasis. Physiol Rev 9:399–431
Chakravarthy MV (2008) Physiological penalties of the sedentary lifestyle. In: Taylor NAS, Groeller H (eds) Physiological bases of human performance during work and exercise. Churchill Livingstone Elsevier, Edinburgh, pp 493–504
Convertino VA, Keil LC, Greenleaf JE (1983) Plasma volume, renin, and vasopressin responses to graded exercise after training. J Appl Physiol 54:508–514
Costill DL, Coté R, Fink W (1976) Muscle water and electrolytes following varied levels of dehydration in man. J Appl Physiol 40:6–11
Darwin CR (1859) On the origin of species by means of natural selection. John Murray, London
DeLorme TL, Watkins AL (1951) Progressive resistance exercise Technic and medical application. Appleton-Century-Crofts Inc, New York
Eddy DO, Sparks KL, Adelizi DA (1977) The effects of continuous and interval training in women and men. Eur J Appl Physiol 37:83–92
Eldridge FL, Millhorn DE, Waldrop TG (1981) Exercise hyperpnea and locomotion: parallel activation from the hypothalamus. Science 211:844–846
Eichna LW, Park CR, Nelson N, Horvath SM, Palmes ED (1950) Thermal regulation during acclimatization in a hot, dry (desert type) environment. Am J Physiol 163:585–597
Farhi LE, Linnarsson D (1977) Cardiopulmonary readjustments during graded immersion in water at 35°C. Respir Physiol 30:35–50
Ferguson BS, Rogatzki MJ, Goodwin ML, Kane DA, Rightmire Z, Gladden LB (2018) Lactate metabolism: historical context, prior misinterpretations, and current understanding. Eur J Appl Physiol 118:691–728
Fletcher RH, Black B (2007) “Spin” in scientific writing: scientific mischief and legal jeopardy. Med Law 26:511–525
Fox RH, Goldsmith R, Kidd DJ, Lewis HE (1963) Acclimatization to heat in man by controlled elevation of body temperature. J Physiol 166:530–547
Gros G, Wittenberg BA, Jue T (2010) Myoglobin’s old and new clothes: from molecular structure to function in living cells. J Exp Biol 213:2713–2725
Hafez ESE (1964) Behavioral thermoregulation in mammals and birds. Int J Biometeorol 7:231–240
Hales JRS, Rowell LB, King RB (1979) Regional distribution of blood flow in awake heat-stressed baboons. Am J Physiol 273:H705–H712
Hardy JD, DuBois EF (1938) Basal metabolism, radiation, convection and vaporization at temperatures of 22 to 35°C. J Nutr 15:477–497
Hawley JA, Lundby C, Cotter JD, Burke LM (2018) Maximizing cellular adaptation to endurance exercise in skeletal muscle. Cell Metab 27:962–976
Hellon R (1983) Thermoreceptors. Comprehensive Physiology, Supplement 8: Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow, pp 659–673. https://doi.org/10.1002/cphy.cp020318
Hensel H (1973) Neural processes in thermoregulation. Physiol Rev 53:948–1017
Jessen C (1996) Interaction of body temperatures in control of thermoregulatory effector mechanisms. Comprehensive Physiology, Supplement 14: Handbook of Physiology, Environmental Physiology. pp 127–138. https://doi.org/10.1002/cphy.cp040107
Knox FG, Granger JP (1992) Control of sodium excretion: an integrative approach. Comprehensive Physiology, Supplement 25: Handbook of Physiology, Renal Physiology, pp 927–967. https://doi.org/10.1002/cphy.cp080121
Koroxenidis GT, Shepherd JT, Marshall RJ (1961) Cardiovascular response to acute heat stress. J Appl Physiol 16:869–872
Krogh A, Lindhard L (1913) The regulation of respiration and circulation during the initial stages of muscular work. J Physiol 47:112–136
Larsen EH, Deaton LE, Onken H, O’Donnell M, Grosell M, Dantzler WH, Weihrauch D (2014) Osmoregulation and excretion. Comp Physiology 4:405–573
Levine BD, Stray-Gundersen J (1997) “Living high-training low”: effect of moderate-altitude acclimatization with low-altitude training on performance. J Appl Physiol 83:102–112
Lindinger MI, Whipp BJ (2008) The anaerobic threshold: fact or misinterpretation? In: Taylor NAS, Groeller H (eds) Physiological bases of human performance during work and exercise. Churchill Livingstone Elsevier, Edinburgh, pp 191–199
Linnarsson D (1974) Dynamics of pulmonary gas exchange and heart rate changes at start and end of exercise. Acta Physiol Scand 415(Supplement):1–68
Louhevaara V, Sovijärvi A, Ilmarinen J, Teräslinna P (1990) Differences in cardiorespiratory responses during and after arm crank and cycle exercise. Acta Physiol Scand 138:133–143
Lundby C, Marconi C, Cerretelli P, Levine BD (2008) Human adaptation to altitude and hypoxia: ethnic differences, chronic adaptation and altitude training. In: Taylor NAS, Groeller H (eds) Physiological bases of human performance during work and exercise. Churchill Livingstone Elsevier, Edinburgh, pp 447–457
Machado-Moreira CA, McLennan PL, Lillioja S, van Dijk W, Caldwell JN, Taylor NAS (2012) The cholinergic blockade of both thermally and non-thermally induced human eccrine sweating. Exp Physiol 97:930–942
Mackinnon LT, Halson SL, Hooper SL, Jeukendrup AE (2008) Overreaching and overtraining. In: Taylor NAS, Groeller H (eds) Physiological bases of human performance during work and exercise. Churchill Livingstone Elsevier, Edinburgh, pp 505–520
Mancia G, Mark AL (1983) Arterial baroreflexes in humans. In: Shepherd JT, Abboud FM (eds) Handbook of Physiology Section 2 The cardiovascular system, peripheral circulation and organ blood flow. American Physiological Society, Washington, pp 755–793
Maw GJ, Mackenzie IL, Taylor NAS (1998) Human body-fluid distribution during exercise in hot, temperate and cool environments. Acta Physiol Scand 163:297–304
McGlory C, Devries MC, Phillips SM (2017) Skeletal muscle and resistance exercise training; the role of protein synthesis in recovery and remodeling. J Appl Physiol 122:541–548
Mekjavic IB, Eiken O (2006) Contribution of thermal and nonthermal factors to the regulation of body temperature in humans. J Appl Physiol 100:2065–2072
Miller DA (1984) Heat acclimation procedures developed for use by the US Marine Corps aboard ship en route to hot weather operations. Bethesda, Naval Medical Research Institute
Mrosovsky N (1990) Rheostasis: the physiology of change. Oxford University Press, Oxford
Nielsen B, Hales JR, Strange S, Christensen NJ, Warberg J, Saltin B (1993) Human circulatory and thermoregulatory adaptations with heat acclimation and exercise in a hot, dry environment. J Physiol 460:467–485
Notley SR, Fullagar HHK, Lee DS, Matsuda-Nakamura M, Peoples GE, Taylor NAS (2014) Revisiting ventilatory and cardiovascular predictions of whole-body metabolic rate. J Occup Environ Med 56:214–223
Notley SR, Park J, Tagami K, Ohnishi N, Taylor NAS (2016) Morphological dependency of cutaneous blood flow and sweating during compensable heat stress when heat-loss requirements are matched across participants. J Appl Physiol 121:25–35
Notley SR, Park J, Tagami K, Ohnishi N, Taylor NAS (2017) Variations in body morphology explain sex differences in thermoeffector function during compensable heat stress. Exp Physiol 102:545–562
Notley SR, Taylor EA, Ohnishi N, Taylor NAS (2018) Cutaneous vasomotor adaptation following repeated, isothermal heat exposures: evidence of adaptation specificity. Appl Physiol Nutr Metab 43:415–418
Olschewski H, Brück K (1988) Thermoregulatory, cardiovascular, and muscular factors related to exercise after precooling. J Appl Physiol 64:803–811
Patterson MJ, Stocks JM, Taylor NAS (2004) Sustained and generalised extracellular fluid expansion following heat acclimation. J Physiol 559:327–334
Patterson MJ, Stocks JM, Taylor NAS (2014) Whole-body fluid distribution in humans during dehydration and recovery, before and after humid-heat acclimation induced using controlled hyperthermia. Acta Physiol 210:899–912
Périard JD, Racinais S, Sawka MN (2015) Adaptations and mechanisms of human heat acclimation: applications for competitive athletes and sports. Scand J Med Sci Sports 25(Suppl. 1):20–38
Périard JD, Travers GJS, Racinais S, Sawka MN (2016) Cardiovascular adaptations supporting human exercise-heat acclimation. Autono Neurosci 196:52–62
Pierau F-K (1996) Peripheral thermosensors. Comprehensive Physiology, Supplement 14: Handbook of Physiology, Environmental Physiology. pp 85–104. https://doi.org/10.1002/cphy.cp040105
Poirier MP, Gagnon D, Friesen BJ, Hardcastle SG, Kenny GP (2015) Whole-body heat exchange during heat acclimation and its decay. Med Sci Sports Exerc 47:390–400
Prosser CL (1964) Perspectives of adaptation: theoretical aspects. In: Dill DB, Adolph EF (eds) Handbook of physiology. Section 4. Adaptation to the environment. American Physiological Society, Washington, pp 11–25
Rowell LB, Brengelmann GL, Blackmon JR, Murray JA (1970) Redistribution of blood flow during sustained high skin temperature in resting man. J Appl Physiol 28:415–420
Rowell LB, Kraning KK, Kennedy JW, Evans TO (1967) Central circulatory responses to work in dry heat before and after acclimatization. J Appl Physiol 22:509–518
Savard GK, Cooper KE, Veale WL, Malkinson TJ (1985) Peripheral blood flow during rewarming from mild hypothermia in humans. J Appl Physiol 58:4–13
Selye H (1950) Stress and the general adaptation syndrome. BMJ 1:1383–1392
Selye H (1973) Homeostasis and heterostasis. Perspect Biol Med 16:441–445
Shibasaki M, Secher NH, Johnson JM, Crandall CG (2005) Central command and the cutaneous vascular response to isometric exercise in heated humans. J Physiol 565:667–673
Shibasaki M, Secher NH, Selmer C, Kondo N, Crandall CG (2003) Central command is capable of modulating sweating from non-glabrous human skin. J Physiol 553:999–1004
Simon E (1974) Temperature regulation: the spinal cord as a site of extrahypothalamic thermoregulatory functions. Rev Physiol Biochem Pharmacol 71:1–76
Snellen JW (1966) Mean body temperature and the control of thermal sweating. Acta Physiol Pharmacol Neerl 14:99–174
Stephenson BT, Tolfrey K, Goosey-Tolfrey VL (2019) Mixed active and passive, heart rate-controlled heat acclimation is effective for paralympic and able-bodied triathletes. Front Physiol 10:1214
Taylor NAS (2000) Principles and practices of heat adaptation. J Human-Environ Sys 4:11–22
Taylor NAS (2014) Human heat adaptation. Comp Physiol 4:325–365
Taylor NAS (2015) Overwhelming physiological regulation through personal protection. J Strength Cond Res 29:S111–S118
Taylor NAS, Cotter JD (2006) Heat adaptation: guidelines for the optimisation of human performance. Int SportMed J 7:33–57
Taylor NAS, Gordon CJ (2019) The origin, significance and plasticity of the thermoeffector thresholds: extrapolation between humans and laboratory rodents. J Therm Biol 85:102397
Taylor CR, Heglund NC, McMahon TA, Looney TR (1980) Energetic cost of generating muscular force during running: a comparison of large and small animals. J Exp Biol 86:9–18
Taylor NAS, Tipton MJ, Kenny GP (2014) Considerations for the measurement of core, skin and mean body temperatures. J Therm Biol 46:72–101
Vissing SF, Hjortsø EM (1996) Central motor command activates sympathetic outflow to the cutaneous circulation in humans. J Physiol 492:931–939
Wallin BG, Stjernberg L (1984) Sympathetic activity in man after spinal cord injury. Outflow to skin below the lesion. Brain 107:183–198
Wasserman K, McIlroy MB (1964) Detecting the threshold of anaerobic metabolism in cardiac patients during exercise. Am J Cardiol 14:844–852
Werner J, Mekjavic IB, Taylor NAS (2008) Concepts in physiological regulation: a thermoregulatory perspective. In: Taylor NAS, Groeller H (eds) Physiological Bases of Human Performance During Work and Exercise. Churchill Livingstone Elsevier, Edinburgh, pp 325–340
Whipp BJ, Ward SA (1980) Ventilatory control dynamics during muscular exercise in man. Int J Sports Med 1:146–159
Whitney RJ (1954) Circulatory changes in the forearm and hand of man with repeated exposure to heat. J Physiol 125:1–24
Wyndham CH (1951) Effect of acclimatization on circulatory responses to high environmental temperatures. J Appl Physiol 4:383–395
Yoshimura H (1964) Organ systems in adaptation: the skin. In: Dill DB, Adolph EF (eds) Handbook of physiology. Section 4. Adaptation to the environment. American Physiological Society, Washington, pp 109–131
Acknowledgements
NAST was supported by the Brain Pool Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science and Information, Communication and Technology (Grant number: 2019H1D3A2A01061171). SRN was supported by a postdoctoral fellowship from the Human and Environmental Physiology Research Unit (University of Ottawa, Canada).
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Taylor, N.A.S., Notley, S.R. & Lindinger, M.I. Heat adaptation in humans: the significance of controlled and regulated variables for experimental design and interpretation. Eur J Appl Physiol 120, 2583–2595 (2020). https://doi.org/10.1007/s00421-020-04489-0
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DOI: https://doi.org/10.1007/s00421-020-04489-0