Thermal physiology of laboratory mice: Defining thermoneutrality

Journal of Thermal Biology

Volumn 37, Issue 8, 2012, Pages 654-685

  Gordon, C J ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Aging; Ambient temperature; Brown adipose tissue; Core temperature; Evaporative water loss; Fever; Growth; Huddling; Metabolic rate; Reproduction; Selected temperature; Telemetry; Thermal conductance

Indexed keywords

AGING; ANIMAL BEHAVIOR; BODY GROWTH; BODY WEIGHT; BROWN ADIPOSE TISSUE; CALORIMETRY; CIRCADIAN RHYTHM; CORE TEMPERATURE; DISEASES; ENERGY EXPENDITURE; ENVIRONMENTAL TEMPERATURE; EVAPORATION; FEVER; HEART HYPERTROPHY; HEAT LOSS; HIGH TEMPERATURE; HUDDLING; KIDNEY HYPERTROPHY; LIVER HYPERTROPHY; LOW TEMPERATURE; MOUSE; NESTING; NONHUMAN; ORGANOGENESIS; REGULATORY MECHANISM; REPRODUCTION; REVIEW; SENESCENCE; TELEMETRY; TEMPERATURE MEASUREMENT; THERMAL CONDUCTIVITY; THERMOGENESIS; THERMOREGULATION; TORPOR;

EID: 84866486099     PISSN: 03064565     EISSN: 18790992     Source Type: Journal    
DOI: 10.1016/j.jtherbio.2012.08.004     Document Type: Review

References (111)

1. Alberts, J.R., Huddling by rat pups: group behavioral mechanisms of temperature regulation and energy conservation. J. Comp. Physiol. Psychol. 92 (1978), 231–245.
2. Al-Hilli, F., Wright, E.A., The effects of changes in the environmental temperature on the growth of tail bones in the mouse. Br. J. Exp. Pathol. 64 (1983), 34–42.
3. Al-Hilli, F., Wright, E.A., The effects of changes in the environmental temperature on the growth of bone in the mouse. Radiological and morphological study. Br. J. Exp. Pathol. 64 (1983), 43–52.
4. Al-Hilli, F., Wright, E.A., The effects of environmental temperature on the hair coat of the mouse. J. Therm. Biol. 13 (1988), 21–24.
5. Al-Hilli, F., Wright, E.A., The effects of environmental temperature on the body temperature and ear morphology of the mouse. J. Therm. Biol. 13 (1988), 197–199.
6. Aschoff, J., Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comput. Biochem. Physiol. 69A (1981), 611–619.
7. Barnett, S.A., Genotype and environment in tail length in mice. Q. J. Exp. Physiol. 50 (1965), 417–429.
8. Barnett, S.A., Widdowson, E.M., Organ-weights and body-composition in mice bred for many generations at -3 °C. Proc. R. Soc. London 162 (1965), 502–516.
9. Batchelder, P., Kinney, R.O., Demlow, L., Lynch, C.B., Effects of temperature and social interaction on huddling behavior in Mus musculus. Physiol. Behav. 31 (1983), 97–102.
10. Bradley, S.R., Deavers, D.R., A re-examination of the relationship between thermal conductance and body weight in mammals. Comput. Biochem. Physiol. 65A (1980), 465–476.
11. Bryant, D.M., Hails, C.J., Mechanisms of heat conservation in the litters of mice (Mus musculus L.). Comput. Biochem. Physiol. 50A (1975), 99–104.
12. Bustamante, D.M., Nespolo, R.F., Rezende, E.L., Bozinovic, F., Dynamic Thermal Balance in the leaf-eared mouse: the interplay among ambient temperature, body size, and behavior. Physiol. Biochem. Zool. 75 (2002), 396–404.
13. Cannon, B., Nedergaard, J., Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 214 (2011), 242–253.
14. Edwards, R.M., Haines, H., Effects of ambient water vapor pressure and temperature on evaporative water loss in Peromyscus maniculatus and Mus musculus. J. Comput. Physiol. 128 (1978), 177–184.
15. Eedy, J.W., Ogilvie, D.M., The effect of age on the thermal preference of white mice (Mus musculus) and gerbils (Meriones unguiculatus). Can. J. Zool. 48 (1970), 1303–1306.
16. Einstein, R., Rowan, C., Billing, R., Lavidis, N., The use of telemetry to refine experimental technique. Balls, M., van Seller, Halder, M.E., (eds.) Progress in the Reduciton, Refinement and Replacemen t of Animal Experimentation, 2000, Elsevier Sciences B.V, 1187–1197.
17. Eliason, H.L., Fewell, J.E., Thermoregulatory control during pregnancy and lactation in rats. J. Appl. Physiol. 83 (1997), 837–844.
18. Erskine, D.J., Hutchison, V.H., Critical thermal maxima in small mammals. J. Mammal. 63 (1982), 267–273.
19. Folk, G.E. Jr., Textbook of Environmental Physiology. 1974, Lea and Febiger, Philadelphia.
20. Gaskill, B.N., Lucas, J.R., Pajor, E.A., Garner, J.P., Working with what you’ve got: changes in thermal preference and behavior in mice with or without nesting material. Journal of Thermal Biology 36 (2011), 1193–1199.
21. Gaskill, B.N., Rohr, S.A., Pajor, E.A., Lucas, J.R., Garner, J.P., Some like it hot: mouse temperature preferences in laboratory housing. Appl. Anim. Behav. Sci. 116 (2009), 279–285.
22. Gaskill, B.N., Gordon, C.J., Pajor, E.A., Lucas, J.R., Davis, J.K., Garner, J.P., Heat or insulation: behavioral titration of mouse preference for warmth or access to a nest. Plos1, 7, 2012, 32799.
23. Gilbert, C., McCafferty, D., Le Maho, Y., Martrette, J.M., Giroud, S., Blanc, S., Ancel, A., One for all and all for one: the energetic benefits of huddling in endotherms. Biol. Rev. Cambridge Philos. Soc. 85 (2010), 545–569.
24. Goodrich, C.A., Measurement of body temperature in neonatal mice. J. Appl. Physiol. 43 (1977), 1102–1105.
25. Gordon, C.J., Ferguson, J.H., The correlation between colonic cooling and survival time in the acute cold-exposed laboratory mouse: influence of cold acclimation. J. Thermal. Biol. 5 (1980), 159–162.
26. Gordon, C.J., A review of terms and proposed nomenclature for regulated vs. forced changes in body temperature. Life Sci. 32 (1983), 1285–1295.
27. Gordon, C.J., Autonomic and behavioral thermoregulation in mice exposed to microwave radiation. J. Appl. Physiol. 55 (1983), 1242–1248.
28. Gordon, C.J., Influence of heating rate on the control of heat loss from tail in mice. Am. J. Physiol. 244 (1983), R778–784.
29. Gordon, C.J., Fogelson, L., Comparative effects of hypoxia on behavioral thermoregulation regulation in rats, hamsters, and mice. Am. J. Physiol. 260 (1991), R120–R125.
30. Gordon C.J. Refinetti, R. Measurement of behavioral thermoregulation. In: Methods in Neuroscience, Vol. 14, Paradigms for the Study of Behavior. pp. 266–280, San Diego, Academic Press, 1993.
31. Gordon, C.J., Effect of cage bedding on temperature regulation and metabolism of group- housed female mice. Comput. Med. 54 (2004), 63–68.
32. Gordon, C.J., Relationship between autonomic and behavioral thermoregulation in the mouse. Physiol. Behav. 34 (1985), 687–690.
33. Gordon, C.J., Thermal biology of the laboratory rat. Physiol. Behav. 47 (1990), 963–991.
34. Gordon, C.J., 24-hour control of body temperature in the rat: I. Integration of behavioral and autonomic effectors. Am. J. Physiol. 267 (1994), R71–R77.
35. Gordon, C.J., Quantifying the instability of core temperature in rodents. J. Thermal. Biol. 34 (2009), 213–219.
36. Gordon, C.J., The mouse: an “average” homeotherm. J. Thermal Biology 37 (2012), 2860–3290.
37. Gordon, C.J., Becker, P., Ali, J.S., Behavioral thermoregulatory responses of single- and group-housed mice. Physiol. Behav. 65 (1998), 255–262.
38. Gordon, C.J., Temperature Regulation in Laboratory Rodents. 1993, Cambridge University Press, New York.
39. Gordon, C.J., Becker, P., Padnos, B., A behavioral device to measure the preferred footpad temperature in mice. J. Therm. Biol. 25 (2000), 211–219.
40. Gordon, C.J., Temperature and Toxicology: An Integrative, Comparative, and Environmental Approach. 2005, CRC Press, Boca Raton, FL.
41. Greenberg, G., The effects of ambient temperature and population density on aggression in two inbredstrains of mice, Mus musculus. Behaviour 42 (1972), 119–130.
42. Harrison, G.A., Morton, R.J., Weiner, J.S., The growth in weight and tail length of inbred and hybrid mice reared at two different temperatures. I. Growth in weight. II. Tail length. Phil. Trans. Roy. Soc. Lond. Series B. Biol. Sciences 242 (1959), 479–516.
43. Hart, J.S., Rodents. Whittow, G.C., (eds.) Comparative Physiology of Thermoregulation, Vol. II, 1971, Academic Press, New York, 1–149.
44. Heldmaier, G., The influence of the social thermoregulation on the cold-adaptive growth of BAT in hairless and furred mice. Pflugers Arch. 355 (1975), 261–266.
45. Heldmaier, G., Temperature adaptation and brown adipose tissue in hairless and albino mice. J. Comput. Physiol. 92 (1974), 281–292.
46. Herrington, L.P., The heat regulation of small laboratory animals at various environmental temperatures. Am. J. Physiol. 129 (1940), 123–139.
47. Himms-Hagen, J., Villemure, C., Number of mice per cage influences uncoupling protein content of brown adipose tissue. Proc. Soc. Exp. Biol. Med. 200 (1992), 502–506.
48. Hoffman-Goetz, L., Keir, R., Body temperature responses of aged mice to ambient temperature and humidity stress. J. Gerontol. 39 (1984), 547–551.
49. Hosek, B., Chlumecky, J., Metabolic reaction and heat loss in hairless and normal mice during short-term adaptation to heat and cold. Plugers. Arch. 296 (1967), 248–255.
50. Hughes, B.G., Hekimi, S., A mild impairment of mitochondrial electron transport has sex-specific effects on lifespan and aging in mice. Plos One, 6, 2011, e26116.
51. IUPS Thermal Commission. (2001) Glossary of terms for thermal physiology. Third ed. Revised by The Commission for Thermal Physiology of the International Union of Physiological Sciences. Jap. J. Physiol. 51, 245–280.
52. Jennings, G., Richard, D., Trayhurn, P., Effect of caging singly or in groups of different sizes on the thermogenic activity of interscapular brown adipose tissue in mice. Comput. Biochem. Physiol. 85A (1986), 583–586.
53. Jhaveri, K.A., Tramel, R.A., Toth, L.A., Effect of environmental temperature on sleep, locomotor activity, core body temperature and immune responses of C57BL/6J mice. Brain Behav. Immun. 21 (2007), 975–987.
54. Kaiyala, K.J., Morton, G.J., Leroux, B.G., Ogimoto, K., Wiese, B., Shwartz, M.W., Identification of body fat as a major determinant of metabolic rate in mice. Diabetes 59 (2010), 1657–1666.
55. Kanizsai, P., Garmi, A., Solymar, M., Szolcanyi, J., Szelenyi, Z., Energetics of fasting heterothermia in TRPV1-KO and wild type mice. Physiol. Behav. 96 (2009), 149–154.
56. Karp, C., Unstressing intemperate models: how cold stress undermines mouse modeling. J. Exp. Med. 209 (2012), 1069–1074.
57. Klaus, S., Munzberg, H., Truloff, C., Heldmaier, G., Physiology of transgenic mice with brown fat ablation: obesity is due to lowered body temperature. Am. J. Physiol. 274 (1998), R287–R293.
58. Kramer, K., Kinter, L.B., Evaluation and applications of radiotelemetry in small laboratory animals. Physiol. Genomics 13 (2003), 197–205.
59. Kleiber, M., The Fire of Life: An Introduction to Animal Energetics. 1975, R. E. Krieger Publ, Huntington, New York.
60. Koizumi, A., Tsukada, M., Wada, Y., Masuda, H., Weindruch, R., Mitotic activity in mice is suppressed by energy restriction-induced torpor. J. Nutr. 122 (1992), 1446–1453.
61. Kort, W.J., Hekking-Weijma, J.M., TenKate, M.T., Sorm, V., VanStrik, R., A microchip implant system as a method to determine body temperature of terminally ill rats and mice. Lab. Anim. 32 (1998), 260–269.
62. Krol, E., Johnson, M.S., Speakman, J.R., Limits to sustained energy intake VIII. Resting Metab. Rate Org. Morpholo. Lab. Mice Lactating at Thermoneutrality 206 (2003), 4283–4291.
63. Lagerspetz, K., The postnatal development of homoiothermy and cold resistance in mice. Experentia 18 (1962), 282–284.
64. Leon, L.R., Wieslaw Kozak, W., Rudolph, K., Kluger, M.J., An antipyretic role for interleukin-10 in LPS fever in mice. Am. J. Physiol. 276, Reg. Int. Comput. Physiol. 45 (1999), R81–R89.
65. Leon, L.R., Gordon, C.J., Helwig, B.G., Rufolo, D.M., Blaha, M.D., Thermoregulatory, behavioral, and metabolic responses to heatstroke in a conscious mouse model. Am. J. Physiol. Regul. Integr. Comput. Physiol. 299 (2010), R241–248.
66. Martin, S.S., Bakken, R.R., Lind, C.M., Reed, D.S., Price, J.L., Koeller, C.A., Parker, M.D., Hart, M.K., Fine, D.L., Telemetric analysis to detect febrile responses in mice following vaccination with a live-atteuated virus vaccine. Vaccine 27 (2009), 6814–6823.
67. Meijer, M.K., Spruijt, B.M., van Zutphen, L.F.M., Baumans, V., Effect of restraint and injection methods on heart rate and body temperature in mice. Lab. Anim. 40 (2006), 382–391.
68. Morrow, J.D., Opp, M.R., Diurnal variation of lipopolysaccharide-induced alterations in sleep and body temperature of interleukin-6-deficient mice. Brain Behav. Immun. 19 (2005), 40–51.
69. Mount, L.E., Willmott, J.V., The relation between spontaneous activity, metabolic rate and the 24 hour cycle in mice at different ambient temperatures. J. Physiol. 190 (1967), 371–380.
70. Mousel, M.R., Stroup, W.W., Nielsen, M.K., Locomotor activity, core body temperature, and circadian rhythms in mice sleected for high or low heat loss. J. Anim. Sci. 79 (2001), 861–868.
71. NRC, Guide for the Care and Use of Laboratory Animals. 8th ed., 2011, Nat. Res. Council of the National Academy of Science, Washington, DC.
72. Ogilvie, D.M., Stinson, R.H., The effect of age on temperature selection by laboratory mice (Mus musculus). Can. J. Zool. 44 (1966), 511–517.
73. Ootsuka, Y., de Menezes, R.C., Zaretsky, D.V., Alimoradian, A., Hunt, J., Stefanidis, A., Oldfield, B.J., Blessing, W.W., Brown adipose tissue thermogenesis heats brain and body as part of the brain-coordinated ultradian basic rest-activity cycle. Neuroscience 164 (2009), 849–861.
74. Oufara, S., Barre, H., Rouanet, J.-L., Chatonnet, J., Adaptation to extreme ambient temperatures in cold-acclimated gerbils and mice. Am. J. Phsiol. 253 (1987), R39–R45.
75. Overton, J.M., Phenotyping small animals as models for the human metabolic syndrome: thermoneutrality matters. Int. J. Obes. 34 (2010), 553–558.
76. Paul, C., Murray, A.A., Spears, N., Saunders, T.K., A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136 (2008), 73–84.
77. Pennycuik, P.R., A comparison of the effects of a variety of factors on the metabolic rate of the mouse. Aust. J. Exp. Med. Sci. 45 (1967), 331–346.
78. Phillips, P.K., Heath, J.E., Dependency of surface temperature regulation on body size in terrestrial mammals. J. Thermal. Biol. 20 (1995), 281–289.
79. Prychodko, W., Effect of aggregation of laboratory mice (Mus musculus) on food intake at different temperatures. Ecology 39 (1958), 500–503.
80. Ramantsoa, N., Vaubourg, V., Matrot, B., Vardon, G., Dauger, S., Gallego, J., Effects of temperature on ventilator response to hypercapnia in newborn mice heterozygous for transcription factor Phox2b. Am. J. Physiol. Regul. Integr. Comput. Physiol. 293 (2007), R2027–R2035.
81. Rudaya, A.Y., Steiner, A.A., Robbins, R.R., Dragic, A.S., Romanovsky, A.A., Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am. J. Physiol. Regul. Integr. Comput. Physiol. 289 (2005), R1244–R1252.
82. Sareh, H., Tulapurkar, M.E., Shah, N.G., Singh, I.S., Hasday, J.D., Response of mice to continuous 5-day passive hyperthermia resembles human heat acclimation. Cell Stress Chaperones. 16 (2011), 297–307.
83. Schmidt-Nielson, K., Animal Physiology. 1975, Cambridge University Press, London.
84. Scholander, P.F., Hock, R., Walters, V., Johnson, F., Irving, L., Heat regulation in some arctic and tropical mammals and birds. Biol. Bull. 99 (1950), 237–258.
85. Selman, C., Korhonen, T.K., Bunger, L., Hill, W.G., Speakman, J.R., Thermoregulatory responses of two mouse Mus musculus strains selectively bred for high and low food intake. J. Comp. Physiol. B. 171 (2001), 661–668.
86. Sen, A., Capitano, M.L., Spernyak, J.A., Schueckler, J.T., Thomas, S., Singh, A.K., Evans, S.S., Hylander, B.L., Repasky, E.A., Mild elevation of body temperature reduces tumor interstitial fluid pressure and hypoxia and enhances efficacy of radiotherapy in murine tumor models. Cancer Res. 71 (2011), 3872–3880. 21.
87. Serrat, M.A., King, D., Lovejoy, C.O., Temperature regulates limb length in homeotherms by directly modulating cartilage growth. PNAS 105 (2008), 19348–19353.
88. Solymar, M., Kanizsai, P., Petervan, E., Garami, A., Szelenyi., Mechanism of fasting heterothermia and re-feeding normothermia in mice. J. Thermal Biol. 35 (2010), 280–283.
89. Speakman, J.R., Mitchell, S.E., Caloric restriction. Mol. Aspects Med. 32 (2011), 159–221.
90. Stanier, M.W., Effect of body weight, ambient temperature, and huddling on oxygen consumption and body temperature of young mice. Comput. Biochem. Physiol. 51A (1975), 79–82.
91. Stiles, B.G., Campbell, Y.G., Castle, R.M., Gove, S.A., Correlation of temperature and toxicity in murine studies of staphylococcal enterotoxins and toxic shock syndrome toxin 1. Infect. Immunol. 67 (1999), 1521–1525.
92. Swoap, S.J., Gutilla, M.J., Cardiovascular changes during daily torpor in the laboratory mouse. Am. J. Physiol. Regul. Integr. Comput. Physiol. 297 (2009), R769–R774.
93. Talan, M.I., Body temperature of C57BL/6J mice with age. Exper. Gerontol. 19 (1984), 25–29.
94. Talan, M.I., Ingram, D.K., Age comparisons of body temperature and cold tolerance among differenct strains of Mus musculus. Mech. Ageing Dev. 33 (1986), 247–256.
95. Tatelman, H.M., Talan, M.I., Metabolic heat production during repeated testing at 24 and 6 °C in adult and aged male C57BL/6J mice. Eff. Physical. Restraint Cold Stress 25 (1990), 459–467.
96. 2+−ATPasae activities in various organs in C57BL/6 female mice in both euthermic and torpor states. Mech. Aging Dev. 68 (1993), 183–189.
97. Turturro, A., Witt, W.W., Lewis, S., Hass, B.S., Lipman, R.D., Hart, R.W., Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. 54 (1999), B492–B501.
98. Van Bogaert, M.J.V., Groenink, L., Oosting, R.S., Westphal, K.G.C., Van der Gugten, J., Olivier, B., Mouse strain differences in autonomic responses to stress. Genes Brain Behav. 5 (2006), 139–149.
99. Van Loo, P.L.P., Kuin, N., Sommer, R., Avsaroglu, H., Pham, T., Baumans, V., Impact of ‘living apart together’ on postoperative recovery of mice compared with social and individual housing. Labor. Animals 41 (2007), 441–455.
100. Vianna, D.M.L., Carrive, P., Stress-induced hyperthermia is not mediated by brown adipose tissue in mice. J. Thermal. Biol. 37 (2012), 125–129.
101. Vinter, J., Huyll, D., Elphick, M.C., Onset of thermogenesis in response to cold in newborn mice. Biol. Neonate 42 (1982), 145–151.
102. Vlach, K.D., Boles, J.W., Stiles, B.G., Telemetric evaluation of body temperature and physical activity as predictors of mortality in a murine model of staphylococcal enterotoxic shock. Comput. Med. 50 (2000), 160–166.
103. Wang, Y., Kimura, K., Inokuma, K., Saito, M., Kontani, Y., Kobayashi, Y., Mori, N., Yamashita, H., Potential contribution of vasoconstriction to suppression of heat loss and homeothermic regulation in UCP1-deficient mice. Pflugers Arch. 452 (2006), 363–369.
104. Webster, W.S., Edwards, M.J., Hyperthermia and the induction of neural tube defects in mice. Teratology 29 (1984), 417–425.
105. Weithe, W.H., The thermoregulation of the nude mouse. Exp. Cell. Biol. 52 (1984), 140–144.
106. Williams, T.D., Chambers, J.B., Henderson, R.P., Rashotte, M.E., Overtone, J.M., Cardiovascular responses to caloric restriction and thermoneutrality in C57BL6/6J mice. Am. J. Physiol. 282 (2002), R1459–R1467.
107. Yamauchi, C., Fujita, S., Obara, T., Ueda, T., Effects of room temperature on reproduction, body and organ weighs, food and water intakes, and hematology in mice. Exp. Anim. 32 (1983), 1–11.
108. Yang, Y., Gordon, C.J., Ambient temperature limits and stability of temperature regulation in telemetered male and female rats. J. Therm. Biol. 21 (1996), 353–363.
109. Young, A.A., Dawson, N.J., Evidence for on-off control of heat dissipation from the tail of the rat. Can. J. Physiol. Pharmacol. 60 (1982), 392–398.
110. Zethof, T.J., van der Heyeden, J.A., Tolboom, J.T., Olivier, B., Stress-induced hyperthermia in mice: a methodological study. Physiol. Behav. 55 (1994), 109–115.
111. Zhao, Z.-J., Chi, Q.-S., Cao, J., Han, Y.-D., The energy budget, thermogenic capacity and behavior in Swiss mice exposed to a consecutive decrease in temperature. J. Exp. Biol. 213 (2010), 3988–3997.