Abstract
The human thermoregulatory system relies primarily on behavioural adaptation and secondarily on autonomic and endocrine responses for thermal homeostasis. This is because autonomic and endocrine responses have a limited capacity in preventing hyper/hypothermia in extreme environments. Until recently, the neuroanatomy of behavioural thermoregulation as well as the neuroanatomic substrate of the various thermoregulatory behaviours remained largely unknown. However, this situation has changed in recent years as behavioural thermoregulation has become a topic of considerable attention. The present review evaluates the current knowledge on behavioural thermoregulation in order to summarize the present state-of-the-art and to point towards future research directions. Findings on the fundamental distinction between thermal (dis)comfort and sensation are reviewed showing that the former drives behaviour while the latter initiates autonomic thermoregulation. Moreover, the thermosensitive neurons and thermoeffector functions of behavioural thermoregulation are presented and analysed in a detailed discussion.
Similar content being viewed by others
References
ASHRAE (1997) Thermal comfort. In: ASHRAE handbook of fundamentals, chapter 8. American Society of Heating, Refrigerating and Air-Conditioning Engineers, Atlanta
Astrup J (1982) Energy-requiring cell functions in the ischemic brain. Their critical supply and possible inhibition in protective therapy. J Neurosurg 56:482–497
Attia M (1984) Thermal pleasantness and temperature regulation in man. Neurosci Biobehav Rev 8:335–342
Attia M, Engel P (1982) Thermal pleasantness sensation: an indicator of thermal stress. Eur J Appl Physiol 50:55–70
Attia M, Engel P, Hildebrandt G (1980) Quantification of thermal comfort parameters using a behavioural indicator. Physiol Behav 24:901–909
Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–208
Becerra LR, Breiter HC, Stojanovic M, Fishman S, Edwards A, Comite AR, Gonzalez RG, Borsook D (1999) Human brain activation under controlled thermal stimulation and habituation to noxious heat: an fMRI study. Magn Reson Med 41:1044–1057
Brink-Elfegoun T, Kaijser L, Gustafsson T, Ekblom B (2007) Maximal oxygen uptake is not limited by a central nervous system governor. J Appl Physiol 102:781–786
Cabanac M (1971) Physiological role of pleasure. Science 173:1103–1107
Cabanac M, Serres P (1976) Peripheral heat as a reward for heart rate response in the curarized rat. J Comp Physiol Psychol 90:435–441
Caputa M, Cabanac M (1980) Muscular work as thermal behavior in humans. J Appl Physiol 48:1020–1023
Caterina MJ (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am J Physiol Regul Integr Comp Physiol 292:R64–R76
Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306–313
Cena K, de Dear R (2001) Thermal comfort and behavioural strategies in office buildings located in a hot-arid climate. J Thermal Biol 26:409–414
Cheng C, Matsukawa T, Sessler DI, Ozaki M, Kurz A, Merrifield B, Lin H, Olofsson P (1995) Increasing mean skin temperature linearly reduces the core-temperature thresholds for vasoconstriction and shivering in humans. Anesthesiology 82:1160–1168
Cheung S, Flouris AD (2009) Maximal oxygen uptake regulation as a behavioral mechanism. J Appl Physiol 106:345
Cheung SS, Mekjavic IB (1995) Human temperature regulation during subanesthetic levels of nitrous oxide-induced narcosis. J Appl Physiol 78:2301–2308
Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D’Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379–386
Collins KJ, Exton-Smith AN (1983) 1983 Henderson award lecture. Thermal homeostasis in old age. J Am Geriatr Soc 31:519–524
Collins KJ, Dore C, Exton-Smith AN, Fox RH, MacDonald IC, Woodward PM (1977) Accidental hypothermia and impaired temperature homoeostasis in the elderly. Br Med J 1:353–356
Collins KJ, Easton JC, Belfield-Smith H, Exton-Smith AN, Pluck RA (1985) Effects of age on body temperature and blood pressure in cold environments. Clin Sci (Lond) 69:465–470
Craig AD, Bushnell MC, Zhang ET, Blomqvist A (1994) A thalamic nucleus specific for pain and temperature sensation. Nature 372:770–773
Davis KD, Kwan CL, Crawley AP, Mikulis DJ (1998) Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. J Neurophysiol 80:1533–1546
Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183–187
Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371–378
Dimicco JA, Zaretsky DV (2007) The dorsomedial hypothalamus: a new player in thermoregulation. Am J Physiol Regul Integr Comp Physiol 292:R47–R63
Drago F, Stanciu M, Salehi S, Scapagnini U (1997) The block of central vasopressin V1 but not V2 receptors suppresses grooming behavior and hypothermia induced by intracerebroventricular vasopressin in male rats. Peptides 18:1389–1392
Ficarra BJ (1996) Diseases and injuries in athletes. A review. J Med 27:241–275
Findlater GS, Cooksey EJ, Anand A, Paintal AS, Iggo A (1987) The effects of hypoxia on slowly adapting type I (SAI) cutaneous mechanoreceptors in the cat and rat. Somatosens Res 5:1–17
Fink GD (2005) Hypothesis: the systemic circulation as a regulated free-market economy. A new approach for understanding the long-term control of blood pressure. Clin Exp Pharmacol Physiol 32:377–383
Flouris AD (2009) Fundamental principles governing behavioral thermoregulation. In: Cisneros AB, Goins BL (eds) Body temperature regulation. Nova Science Publishers, Inc, Hauppauge
Flouris AD, Cheung SS (2006) Design and control optimization of microclimate liquid cooling systems underneath protective clothing. Ann Biomed Eng 34:359–372
Flouris AD, Cheung SS (2008) Human conscious response to thermal input is adjusted to changes in mean body temperature. Br J Sports Med 43:199–203
Flouris AD, Cheung SS, Fowles JR, Kruisselbrink LD, Westwood DA, Carrillo AE, Murphy RJ (2006a) Influence of body heat content on hand function during prolonged cold exposures. J Appl Physiol 101:802–808
Flouris AD, Cheung SS, Fowles JR, Murphy RJ, Westwood DA, Kruisselbrink LD (2006b) A pre-heating approach to preserve manual dexterity and neuromuscular function of the hands during cold exposures. Habitation 10:142–143
Flouris AD, Westwood DA, Cheung SS (2006c) Influence of thermal body state on vigilance during prolonged cold exposures. Appl Physiol Nutr Metab 31:S26
Flouris AD, Westwood DA, Cheung SS (2007) Thermal balance effects on vigilance during 2-hour exposures to −20°C. Aviat Space Environ Med 78:673–679
Frank SM, Raja SN, Bulcao CF, Goldstein DS (1999) Relative contribution of core and cutaneous temperatures to thermal comfort and autonomic responses in humans. J Appl Physiol 86:1588–1593
Gagge AP, Stolwijk JA, Hardy JD (1967) Comfort and thermal sensations and associated physiological responses at various ambient temperatures. Environ Res 1:1–20
Golja P, Mekjavic IB (2003) Effect of hypoxia on preferred hand temperature. Aviat Space Environ Med 74:522–526
Golja P, Kacin A, Tipton MJ, Eiken O, Mekjavic IB (2004) Hypoxia increases the cutaneous threshold for the sensation of cold. Eur J Appl Physiol 92:62–68
Gordon CJ (1997) The role of behavioral thermoregulation as a thermoeffector during prolonged hypoxia in the rat. J Therm Biol 22:315–324
Gordon CJ, Fogelson L (1991) Comparative effects of hypoxia on behavioral thermoregulation in rats, hamsters, and mice. Am J Physiol 260:R120–R125
Grahn D, Brock-Utne JG, Watenpaugh DE, Heller HC (1998) Recovery from mild hypothermia can be accelerated by mechanically distending blood vessels in the hand. J Appl Physiol 85:1643–1648
Guest S, Grabenhorst F, Essick G, Chen Y, Young M, McGlone F, de Araujo I, Rolls ET (2007) Human cortical representation of oral temperature. Physiol Behav 92:975–984
Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22:6408–6414
Hamilton CL, Ciaccia PJ (1971) Hypothalamus, temperature regulation, and feeding in the rat. Am J Physiol 221:800–807
Hicks JW, Wood SC (1985) Temperature regulation in lizards: effects of hypoxia. Am J Physiol 248:R595–R600
Holmes RL, Newman PP, Wolstencroft JH (1960) A heatsensitive region in the medulla. J Physiol 152:93–98
Iggo A, Paintal AS (1977) The metabolic dependence of primate cutaneous cold receptors [proceedings]. J Physiol 272:40P–41P
Johnston CE, White MD, Wu M, Bristow GK, Giesbrecht GG (1996) Eucapnic hypoxia lowers human cold thermoregulatory response thresholds and accelerates core cooling. J Appl Physiol 80:422–429
Kadohisa M, Rolls ET, Verhagen JV (2004) Orbitofrontal cortex: neuronal representation of oral temperature and capsaicin in addition to taste and texture. Neuroscience 127:207–221
Kadohisa M, Rolls ET, Verhagen JV (2005a) Neuronal representations of stimuli in the mouth: the primate insular taste cortex, orbitofrontal cortex and amygdala. Chem Senses 30:401–419
Kadohisa M, Verhagen JV, Rolls ET (2005b) The primate amygdala: neuronal representations of the viscosity, fat texture, temperature, grittiness and taste of foods. Neuroscience 132:33–48
Kanosue K, Sadato N, Okada T, Yoda T, Nakai S, Yoshida K, Hosono T, Nagashima K, Yagishita T, Inoue O, Kobayashi K, Yonekura Y (2002) Brain activation during whole body cooling in humans studied with functional magnetic resonance imaging. Neurosci Lett 329:157–160
Kleitman N, Doktorsky A (1933) The effect of the position of the body and sleep on rectal temperature in man. Am J Physiol 104:340–343
Konishi M, Kanosue K, Kano M, Kobayashi A, Nagashima K (2007) The median preoptic nucleus is involved in the facilitation of heat-escape/cold-seeking behavior during systemic salt loading in rats. Am J Physiol Regul Integr Comp Physiol 292:R150–R159
Kuno S, Ohno H, Nakahara N (1987) A two-dimensional model expressing thermal sensation in transitional conditions. ASHRAE Trans 93:396–406
Liedtke W, Friedman JM (2003) Abnormal osmotic regulation in trpv4−/− mice. Proc Natl Acad Sci USA 100:13698–13703
Malanda UL, Reulen JP, Saris WH, van Marken Lichtenbelt WD (2008) Hypoxia induces no change in cutaneous thresholds for warmth and cold sensation. Eur J Appl Physiol 104:375–381
Mekjavic IB, Savic SA, Eiken O (1995) Nitrogen narcosis attenuates shivering thermogenesis. J Appl Physiol 78:2241–2244
Mercer JB, Simon E (2001) Lessons from the past—human and animal thermal physiology. J Therm Biol 26:249–253
Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, Andahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468–1472
Nagashima K (2006) Central mechanisms for thermoregulation in a hot environment. Ind Health 44:359–367
Nakamura M, Yoda T, Crawshaw LI, Yasuhara S, Saito Y, Kasuga M, Nagashima K, Kanosue K (2008) Regional differences in temperature sensation and thermal comfort in humans. J Appl Physiol 105:1897–1906
Noakes TD, Marino FE (2009) Point: maximal oxygen uptake is limited by a central nervous system governor. J Appl Physiol 106:338–339 (discussion 341)
Passias TC, Meneilly GS, Mekjavic IB (1996) Effect of hypoglycemia on thermoregulatory responses. J Appl Physiol 80:1021–1032
Pertwee RG, Marshall NR, Macdonald AG (1986) Effects of subanesthetic doses of inert gases on behavioral thermoregulation in mice. J Appl Physiol 61:1623–1633
Pieron H (1913) Le probleme physiologique du sommeil (The physiological problem of the sleep). Masson and Cie, Paris
Riddell MC (2008) The endocrine response and substrate utilization during exercise in children and adolescents. J Appl Physiol 105:725–733
Roberts WW (1988) Differential thermosensor control of thermoregulatory grooming, locomotion, and relaxed postural extension. Ann N Y Acad Sci 525:363–374
Roelands B, Goekint M, Heyman E, Piacentini MF, Watson P, Hasegawa H, Buyse L, Pauwels F, De Schutter G, Meeusen R (2008) Acute norepinephrine reuptake inhibition decreases performance in normal and high ambient temperature. J Appl Physiol 105:206–212
Rolls ET, Grabenhorst F, Parris BA (2008) Warm pleasant feelings in the brain. Neuroimage 41:1504–1513
Romanovsky AA (2007) Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol 292:R37–R46
Sawamoto N, Honda M, Okada T, Hanakawa T, Kanda M, Fukuyama H, Konishi J, Shibasaki H (2000) Expectation of pain enhances responses to nonpainful somatosensory stimulation in the anterior cingulate cortex and parietal operculum/posterior insula: an event-related functional magnetic resonance imaging study. J Neurosci 20:7438–7445
Schlader ZJ, Prange HD, Mickleborough TD, Stager JM (2009) Characteristics of the control of human thermoregulatory behavior. Physiol Behav 98:557–562
Simon E (1974) Temperature regulation: the spinal cord as a site of extrahypothalamic thermoregulatory functions. Rev Physiol Biochem Pharmacol 1–76
Simon C, Gronfier C, Schlienger JL, Brandenberger G (1998) Circadian and ultradian variations of leptin in normal man under continuous enteral nutrition: relationship to sleep and body temperature. J Clin Endocrinol Metab 83:1893–1899
Stehling O, Doring H, Nuesslein-Hildesheim B, Olbort M, Schmidt I (1997) Leptin does not reduce body fat content but augments cold defense abilities in thermoneutrally reared rat pups. Pflugers Arch 434:694–697
Suzuki M, Mizuno A, Kodaira K, Imai M (2003) Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278:22664–22668
Szekely M, Szelenyi Z (2005) Regulation of energy balance by peptides: a review. Curr Protein Pept Sci 6:327–353
Taylor NA, Allsopp NK, Parkes DG (1995) Preferred room temperature of young versus aged males: the influence of thermal sensation, thermal comfort, and affect. J Gerontol A Biol Sci Med Sci 50:M216–M221
Tikuisis P, McLellan TM, Selkirk G (2002) Perceptual versus physiological heat strain during exercise-heat stress. Med Sci Sports Exerc 34:1454–1461
Tucker R, Rauch L, Harley YX, Noakes TD (2004) Impaired exercise performance in the heat is associated with an anticipatory reduction in skeletal muscle recruitment. Pflugers Arch 448:422–430
Tucker R, Marle T, Lambert EV, Noakes TD (2006) The rate of heat storage mediates an anticipatory reduction in exercise intensity during cycling at a fixed rating of perceived exertion. J Physiol 574:905–915
Verhagen JV, Kadohisa M, Rolls ET (2004) Primate insular/opercular taste cortex: neuronal representations of the viscosity, fat texture, grittiness, temperature, and taste of foods. J Neurophysiol 92:1685–1699
Acknowledgments
While preparing this manuscript, the author was supported in part by funding from the Canadian Natural Sciences and Engineering Research Council.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Susan Ward.
Rights and permissions
About this article
Cite this article
Flouris, A.D. Functional architecture of behavioural thermoregulation. Eur J Appl Physiol 111, 1–8 (2011). https://doi.org/10.1007/s00421-010-1602-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-010-1602-8