Ultradian Episodes of Thermogenesis in Mammals: Implications for the Timing of Torpor Entry and Arousal

  • Carola W. Meyer
  • William Blessing
  • Gerhard Heldmaier
Chapter

Abstract

Mammals forage and feed in a periodic manner, and facultative thermogenesis in brown adipose tissue (BAT) contributes to the increases in heat production associated with feeding. Even in the absence of food, BAT thermogenesis occurs in an episodic manner. In the torpid or hibernating state, mammals do not feed and thermogenesis is substantially suppressed. However, periodic peaks and troughs of metabolic rate, ventilation and heart rate continue to occur at reduced amplitude. We hypothesize that the episodic pattern of thermogenesis in the normothermic and torpid state is part of a centrally mediated ultradian rhythm that serves maintenance of neuronal integrity and alertness. Periodic thermogenesis may also provide the neuronal and temporal framework for torpor entry and arousal. Therefore, identifying the central pathways that underlie ultradian fluctuations in energy metabolism may lead towards understanding and predicting torpor behaviour.

Keywords

Brown Adipose Tissue Torpor Bout Daily Torpor Ultradian Rhythm Djungarian Hamster 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abrams R, Hammel HT (1964) Hypothalamic temperature in unanesthetized albino rats during feeding and sleeping. Am J Physiol 206:641–646PubMedGoogle Scholar
  2. Aschoff J, Gerkema M (1985) On diversity and uniformity of ultradian rhythms. Exp Brain Res 12(Suppl):321–334CrossRefGoogle Scholar
  3. Aschoff J, Pohl H (1970) Rhythmic variations in energy metabolism. Fed Proc 29:1541–1552PubMedGoogle Scholar
  4. Bieber C, Ruf T (2009) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften 96:165–171PubMedCrossRefGoogle Scholar
  5. Blessing W, Mohammed M, Ootsuka Y (2011) Heating and eating: brown adipose tissue thermogenesis precedes food ingestion as part of the ultradian basic rest-activity cycle in rats. Physiol Behav 105:966–974PubMedCrossRefGoogle Scholar
  6. Braulke LJ, Heldmaier G (2010) Torpor and ultradian rhythms require an intact signalling of the sympathetic nervous system. Cryobiology 60:198–203PubMedCrossRefGoogle Scholar
  7. Brobeck JR (1948) Food intake as a mechanism of temperature regulation. Yale J Biol Med 20:545–552PubMedGoogle Scholar
  8. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359PubMedCrossRefGoogle Scholar
  9. Clemens LE, Heldmaier G, Exner C (2009) Keep cool: memory is retained during hibernation in Alpine marmots. Physiol Behav 98:78–84PubMedCrossRefGoogle Scholar
  10. Daan S, Aschoff J (1981) Short term rhythms in activity. In: Aschoff J, Daan S, Groos GA (eds) Vertebrate circadian systems: structure and physiology. Springer, Berlin, pp 305–331Google Scholar
  11. De Vries J, Strubbe JH, Wildering WC, Gorter JA, Prins AJ (1993) Patterns of body temperature during feeding in rats under varying ambient temperatures. Physiol Behav 53:229–235PubMedCrossRefGoogle Scholar
  12. von der Ohe CG, Garner CC, Darian-Smith C, Heller HC (2007) Synaptic protein dynamics in hibernation. J Neurosci 27:84–92PubMedCrossRefGoogle Scholar
  13. Elvert R, Heldmaier G (2005) Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis. J Exp Biol 208:1373–1383PubMedCrossRefGoogle Scholar
  14. Gerkema MP, Daan S, Wilbrink M, Van der LF Hop MW (1993) Phase control of ultradian feeding rhythms in the common vole (Microtus arvalis): the roles of light and the circadian system. J Biol Rhythms 8:151–171PubMedCrossRefGoogle Scholar
  15. Hart JS (1971) Rodents. In: Whittow GC (ed) Comparative physiology of thermoregulation. Academic Press, New York, pp 1–149Google Scholar
  16. Heldmaier G, Ortmann S, Elvert R (2004) Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141:317–329PubMedCrossRefGoogle Scholar
  17. Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol 142:429–437Google Scholar
  18. Himms-Hagen J (1995) Role of brown adipose tissue thermogenesis in control of thermoregulatory feeding in rats: a new hypothesis that links thermostatic and glucostatic hypotheses for control of food intake. Proc Soc Exp Biol Med 208:159–169PubMedGoogle Scholar
  19. Honma KI, Hiroshige T (1978) Endogenous ultradian rhythms in rats exposed to prolonged continuous light. Am J Physiol 235:R250–R256PubMedGoogle Scholar
  20. Janssen R (1992) Thermal influences on nervous system function. Neurosci Biobehav Rev 16:399–413PubMedCrossRefGoogle Scholar
  21. Kantor S, Mochizuki T, Janisiewicz AM, Clark E, Nishino S, Scammell TE (2009) Orexin neurons are necessary for the circadian control of REM sleep. Sleep 32:1127–1134PubMedGoogle Scholar
  22. Kleitman N (1982) Basic rest-activity cycle—22 years later. Sleep 5:311–317PubMedGoogle Scholar
  23. Lavie P, Kripke DF (1981) Ultradian circa 11/2 hour rhythms: a multioscillatory system. Life Sci 29:2445–2450PubMedCrossRefGoogle Scholar
  24. Levin BE, Goldstein A, Natelson BH (1978) Ultradian rhythm of plasma noradrenaline in rhesus monkeys. Nature 272:164–166PubMedCrossRefGoogle Scholar
  25. Milsom WK, Burlington RF, Burleson ML (1993) Vagal influence on heart rate in hibernating ground squirrels. J Exp Biol 185:25–32Google Scholar
  26. Milsom WK, Harris MB, Reid SG (1997) Do descending influences alternate to produce episodic breathing? Respir Physiol 110:307–317PubMedCrossRefGoogle Scholar
  27. Milsom WK, Zimmer MB, Harris MB (1999) Regulation of cardiac rhythm in hibernating mammals. Comp Biochem Physiol A Mol Integr Physiol 124:383–391PubMedCrossRefGoogle Scholar
  28. Milsom WK, Zimmer MB, Harris MB (2001) Vagal control of cardiorespiratory function in hibernation. Exp Physiol 86:791–796PubMedCrossRefGoogle Scholar
  29. Morrison SF, Nakamura K, Madden CJ (2008) Central control of thermogenesis in mammals. Exp Physiol 93:773–797PubMedCrossRefGoogle Scholar
  30. Oelkrug R, Heldmaier G, Meyer CW (2011) Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice. J Comp Physiol B 181:137–145PubMedCrossRefGoogle Scholar
  31. Ootsuka Y, de Menezes RC, Zaretsky DV, Alimoradian A, Hunt J, Stefanidis A, Oldfield BJ, Blessing WW (2009) Brown adipose tissue thermogenesis heats brain and body as part of the brain-coordinated ultradian basic rest-activity cycle. Neuroscience 164:849–861PubMedCrossRefGoogle Scholar
  32. Ootsuka Y, Kulasekara K, de Menezes RC, Blessing WW (2011) SR59230A, a beta-3 adrenoceptor antagonist, inhibits ultradian brown adipose tissue thermogenesis and interrupts associated episodic brain and body heating. Am J Physiol Regul Integr Comp Physiol 301:R987–R994PubMedCrossRefGoogle Scholar
  33. Ortmann S, Heldmaier G (2000) Regulation of body temperature and energy requirements of hibernating alpine marmots (Marmota marmota). Am J Physiol Regul Integr Comp Physiol 278:R698–R704PubMedGoogle Scholar
  34. Peyron C, Tighe DK, van den Pol AN, De Lecea L, Heller HC, Sutcliffe JG, Kilduff TS (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996–10015PubMedGoogle Scholar
  35. Rampone AJ, Reynolds PJ (1991) Food intake regulation by diet-induced thermogenesis. Med Hypotheses 34:7–12PubMedCrossRefGoogle Scholar
  36. Refinetti R, Menaker M (1992) The circadian rhythm of body temperature. Physiol Behav 51:613–637PubMedCrossRefGoogle Scholar
  37. Rensing L, Meyer-Grahle U, Ruoff P (2001) Biological timing and the clock metaphor: oscillatory and hourglass mechanisms. Chronobiol Int 18:329–369PubMedCrossRefGoogle Scholar
  38. Richter CP (1927) Animal behaviour and internal drives. Quart Rev Biol 2:307–343CrossRefGoogle Scholar
  39. Robinson EL, Fuller CA (1999) Endogenous thermoregulatory rhythms of squirrel monkeys in thermoneutrality and cold. Am J Physiol 276:R1397–R1407PubMedGoogle Scholar
  40. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richarson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573–585PubMedCrossRefGoogle Scholar
  41. Saper CB, Cano G, Scammell TE (2005) Homeostatic, circadian, and emotional regulation of sleep. J Comp Neurol 493:92–98PubMedCrossRefGoogle Scholar
  42. Schibler U, Naef F (2005) Cellular oscillators: rhythmic gene expression and metabolism. Curr Opin Cell Biol 17:223–229PubMedCrossRefGoogle Scholar
  43. Scholander PF, Hock R, Walters V, Irving L (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature insulation, and basal metabolic rate. Biol Bull 99:259–271PubMedCrossRefGoogle Scholar
  44. Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56PubMedCrossRefGoogle Scholar
  45. Sellayah D, Bharaj P, Sikder D (2011) Orexin is required for brown adipose tissue development, differentiation, and function. Cell Metab 14:478–490PubMedCrossRefGoogle Scholar
  46. Stupfel M, Gourlet V, Court L, Perramon A, Merat P, Lemercerre C (1990a) There are basic rest-activity ultradian rhythms of carbon dioxide emission in small laboratory vertebrates characteristic of each species. Prog Clin Biol Res 341A:179–184PubMedGoogle Scholar
  47. Stupfel M, Gourlet V, Perramon A, Merat P, Court L (1990b) Ultradian and circadian compartmentalization of respiratory and metabolic exchanges in small laboratory vertebrates. Chronobiologia 17:275–304PubMedGoogle Scholar
  48. Swoap SJ, Gutilla MJ, Liles LC, Smith RO, Weinshenker D (2006) The full expression of fasting-induced torpor requires beta 3-adrenergic receptor signaling. J Neurosci 26:241–245PubMedCrossRefGoogle Scholar
  49. Swoap SJ, Weinshenker D (2008) Norepinephrine controls both torpor initiation and emergence via distinct mechanisms in the mouse. PLoS One 3:e4038PubMedCrossRefGoogle Scholar
  50. Tapp WN, Levin BE, Natelson BH (1981) Ultradian rhythm of plasma norepinephrine in rats. Endocrinology 109:1781–1783PubMedCrossRefGoogle Scholar
  51. Wehr TA (1992) A brain-warming function for REM sleep. Neurosci Biobehav Rev 16:379–397PubMedCrossRefGoogle Scholar
  52. Zhang W, Sunanaga J, Takahashi Y, Mori T, Skurai T, Kanmura Y, Kuwaki T (2010) Orexin neurons are indispensable for stress-induced thermogenesis in mice. J Physiol 588(Pt 21): 4117–4125Google Scholar
  53. Zimmer MB, Milsom WK (2002) Ventilatory pattern and chemosensitivity in unanesthetized, hypothermic ground squirrels (Spermophilus lateralis). Respir Physiol Neurobiol 133:49–63PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Carola W. Meyer
    • 1
    • 3
  • William Blessing
    • 2
  • Gerhard Heldmaier
    • 1
  1. 1.Animal PhysiologyPhilipps-Universität MarburgMarburgGermany
  2. 2.Human PhysiologyFlinders Medical CenterAdelaideAustralia
  3. 3.Helmholtz Zentrum MünchenDeutsches Forschungszentrum für Gesundheit und Umwelt (GmbH)NeuherbergGermany

Personalised recommendations