Journal of Kerman University of Medical Sciences

Current Issue

By Issue

By Author

Author Index

Keyword Index

About Journal

Aims and Scope

JKMU Ethical Policies

Indexing and Abstracting

Related Links

FAQ

Peer Review Process

News

Metric

Editorial Policies

Data Sharing Policy

Central and Peripheral Thermoregulatory Responses to Cold Exposure: Involvement of Sympathetic System, Nitric Oxide, and Orexin

Document Type : Review Article

Authors

1 Department of Biology, Faculty of Biological Sciences, Kharazmi University, Tehran, Iran

2 Department of Physiology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

Abstract

In hypothermia, the core temperature of the body decreases below 35°C. In this situation, the body initiates some thermal regulatory process. Thermal regulation is the balance between heat production (thermogenesis) and heat loss (thermolysis) during thermal changes. Thermoregulation in skin blood flow can maintain body temperature and so homeostasis. A large body of literature has shown that in cold exposure, the hypothalamus contributes to thermoregulation by affecting skin blood flow. Moreover, some peripheral factors contribute to thermoregulation through modification of skin blood flow. Furthermore, the sympathetic nervous system can regulate the body temperature through a noradrenergic vasoconstrictor and a vasodilator system. As orexin receptors are also found in several peripheral mammal tissues, the activation of the orexin may stimulate the autonomic nervous system to increase blood pressure leading to control of heat balance. The present study aimed to evaluate the activity level and involvement of thermal regulators in cold stress. Generally, more experiments should be accomplished to find the regulatory pathways in these situations. Furthermore, this study was focused on the effect of orexin on thermoregulatory functions. This brief review intended to report the studies revealing the prime effects of orexin on the body temperature through influences exerted on the sympathetic nervous system.

Keywords

References
  1. Tansey, E.A. and C.D. Johnson, Recent advances in thermoregulation. Advances in physiology education, 2015.
  2. Boulant, J.A., Role of the preoptic-anterior hypothalamus in thermoregulation and fever. Clinical infectious diseases, 2000. 31(Supplement_5): p. S157-S161.
  3. Boulant, J.A., Hypothalamic neurons regulating body temperature. Handbook of Physiology. Environmental Physiology, 1996: p. 105-126.
  4. Tansey, E.A. and C.D. Johnson, Recent advances in thermoregulation. Adv Physiol Educ, 2015. 39(3): p. 139-48.
  5. Romanovsky, A.A., Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. American journal of Physiology-Regulatory, integrative and comparative Physiology, 2007. 292(1): p. R37-R46.
  6. Stephens, D.P., et al., Neuropeptide Y antagonism reduces reflex cutaneous vasoconstriction in humans. American Journal of Physiology-Heart and Circulatory Physiology, 2004. 287(3): p. H1404-H1409.
  7. Turk, E.E., Hypothermia. Forensic science, medicine, and pathology, 2010. 6(2): p. 106-115.
  8. Khaksarihadad, M., et al., Decrease in blood flow and temperature of rat knee joint by calcium. Hormozgan Medical Journal, 2007. 10(4): p. 311-320.
  9. Tzschentke, B. and I. Halle, Influence of temperature stimulation during the last 4 days of incubation on secondary sex ratio and later performance in male and female broiler chicks. British Poultry Science, 2009. 50(5): p. 634-640.
  10. Arami, M.K., A. Komaki, and S. Gharibzadeh, Contribution of nucleus raphe magnus to thermoregulation. Physiology & Pharmacology, 2020. 24(3).
  11. Zhao, Z.-D., et al., A hypothalamic circuit that controls body temperature. Proceedings of the National Academy of Sciences, 2017. 114(8): p. 2042-2047.
  12. Arami, M.K., et al., The effect of hyperglycemia on nitric oxidergic neurons in nucleus tractus solitarius and blood pressure regulation in rats with induced diabetes. Iranian Journal of Diabetes and Lipid Disorders, 2005. 4(3): p. E2.
  13. Charkoudian, N. Skin blood flow in adult human thermoregulation: how it works, when it does not, and why. in Mayo Clinic Proceedings. 2003. Elsevier.
  14. Dickenson, A.H., Specific responses of rat raphe neurones to skin temperature. J Physiol, 1977. 273(1): p. 277-293.
  15. Asahina, M., et al., Cutaneous sympathetic function in patients with multiple system atrophy. Clinical Autonomic Research, 2003. 13(2): p. 91-95.
  16. Rathner, J.A. and R.M. McAllen, Differential control of sympathetic drive to the rat tail artery and kidney by medullary premotor cell groups. Brain Res, 1999. 834(1): p. 196-199.
  17. Berner, N.J., D.A. Grahn, and H.C. Heller, 8-OH-DPAT-sensitive neurons in the nucleus raphe magnus modulate thermoregulatory output in rats. Brain Res, 1999. 831(1): p. 155-164.
  18. Korsak, A. and M.P. Gilbey, Rostral ventromedial medulla and the control of cutaneous vasoconstrictor activity following icv prostaglandin E 1. Neurosci, 2004. 124(3): p. 709-717.
  19. Malakouti, S.M., et al., Reversible inactivation and excitation of nucleus raphe magnus can modulate tail blood flow of male wistar rats in response to hypothermia. Iranian Biomedical Journal, 2008. 12(4): p. 237-240.
  20. Masoomeh, A., H. Sohrab, and S. Abdorahman, the effect of nitric oxide level of nucleus raphe magnus in hypothermia in male wistar rats. Korean Journal of Physiology & Pharmacology, 2006. 10: p. 164-0.
  21. Blessing, W.W. and E. Nalivaiko, Regional blood flow and nociceptive stimuli in rabbits: patterning by medullary raphe, not ventrolateral medulla. j Physiol, 2000. 524(1): p. 279-292.
  22. Nalivaiko, E. and W.W. Blessing, Potential role of medullary raphe-spinal neurons in cutaneous vasoconstriction: an in vivo electrophysiological study. J Neurophysiol, 2002. 87(2): p. 901-911.
  23. Key, B. and C. Wigfield, Changes in the tail surface temperature of the rat following injection of 5-hydroxytryptamine into the ventrolateral medulla. Neuropharmacology, 1992. 31(8): p. 717-723.
  24. Tanaka, M., et al., Role of the medullary raphe in thermoregulatory vasomotor control in rats. J Physiol, 2002. 540(2): p. 657-664.
  25. Kourosh Arami, M., et al., The Effect of Nucleus Tractus Solitarius Nitric Oxidergic Neurons on Blood Pressure in Diabetic Rats. Iranian Biomedical Journal, 2006. 10(1): p. 15-19.
  26. Nazari, S., et al., Relative contribution of central and peripheral factors in superficial blood flow regulation following cold exposure. Physiology and Pharmacology (Iran), 2020. 24(2): p. 89-100.
  27. Malakouti, S.M., et al., Reversible inactivation and excitation of nucleus raphe magnus can modulate tail blood flow of male Wistar rats in response to hypothermia. Iran Biomed J, 2008. 12(4): p. 203-208.
  28. Arami, M.K., S. Hajizadeh, and S. Semnanian, Postnatal development changes in excitatory synaptic activity in the rat locus coeruleus neurons. Brain research, 2016. 1648: p. 365-371.
  29. Arami, M.K., et al., Postnatal developmental alterations in the locus coeruleus neuronal fast excitatory postsynaptic currents mediated by ionotropic glutamate receptors of rat. Physiology and Pharmacology, 2011. 14(4): p. 337-348.
  30. Kourosh-Arami, M. and S. Hajizadeh, Maturation of NMDA receptor-mediated spontaneous postsynaptic currents in the rat locus coeruleus neurons. Physiology International, 2020.
  31. D'yakonova, T., NO-producing compounds transform neuron responses to glutamate. Neuroscience and behavioral physiology, 2000. 30(2): p. 153-159.
  32. Kourosharami, M., M. Mohsenzadegan, and A. Komaki, A Review of Excitation-Inhibition Balance in the Nucleus Tractus Solitarius as a Gateway to Neural Cardiovascular Regulation. Journal of Advances in Medical and Biomedical Research, 2020. 28(126): p. 47-53.
  33. Arami, M.K., et al., Nitric oxide in the nucleus raphe magnus modulates cutaneous blood flow in rats during hypothermia. Iran J Basic Med Sci, 2015. 18(10): p. 989-92.
  34. Kourosh-Arami, M., et al., Neurophysiologic implications of neuronal nitric oxide synthase. Reviews in the Neurosciences, 2020. 1(ahead-of-print).
  35. Safari, F., et al., Effect of nitric oxide on skin blood flow of intact and morphine-dependent rats. Physiology and Pharmacology, 2007. 10(4): p. 267-274.
  36. Kourosh-Arami, M., A. Komaki, and M.-R. Zarrindast, Dopamine as a potential target for learning and memory: contribution to related neurological disorders. CNS & Neurological Disorders Drug Targets, 2022.
  37. Zheng, X. and H. Hasegawa, Central dopaminergic neurotransmission plays an important role in thermoregulation and performance during endurance exercise. European Journal of Sport Science, 2016. 16(7): p. 818-828.
  38. Taylor, N.A., et al., Hands and feet: physiological insulators, radiators and evaporators. European journal of applied physiology, 2014. 114(10): p. 2037-2060.
  39. Johnson, J.M. and D.W. Proppe, Cardiovascular adjustments to heat stress. Handbook of Physiology. Environmental Physiology, 1996. 1: p. 215.
  40. Johnson, J.M., et al. Regulation of the cutaneous circulation. in Federation proceedings. 1986.
  41. Johnson, J.M., Exercise and the cutaneous circulation. Exercise and sport sciences reviews, 1992. 20: p. 59-97.
  42. Charkoudian, N., Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans. Journal of applied physiology, 2010. 109(4): p. 1221-1228.
  43. Stephenson, L.A. and M.A. Kolka, Menstrual cycle phase and time of day alter reference signal controlling arm blood flow and sweating. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 1985. 249(2): p. R186-R191.
  44. Aoki, K., D.P. Stephens, and J.M. Johnson, Diurnal variation in cutaneous vasodilator and vasoconstrictor systems during heat stress. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 2001. 281(2): p. R591-R595.
  45. Roberts, M.F., et al., Skin blood flow and sweating changes following exercise training and heat acclimation. Journal of Applied Physiology, 1977. 43(1): p. 133-137.
  46. Charkoudian, N. and J.M. Johnson, Reflex control of cutaneous vasoconstrictor system is reset by exogenous female reproductive hormones. Journal of Applied Physiology, 1999. 87(1): p. 381-385.
  47. Johnson, J.M., et al., Laser-Doppler measurement of skin blood flow: comparison with plethysmography. J Appl Physiol Respir Environ Exerc Physiol, 1984. 56(3): p. 798-803.
  48. Oberg, P.A., Laser-Doppler flowmetry. Crit Rev Biomed Eng, 1990. 18(2): p. 125-63.
  49. Edholm, O.G., R.H. Fox, and R.K. Macpherson, Vasomotor control of the cutaneous blood vessels in the human forearm. J Physiol, 1957. 139(3): p. 455-65.
  50. Lossius, K., M. Eriksen, and L. Walloe, Fluctuations in blood flow to acral skin in humans: connection with heart rate and blood pressure variability. J Physiol, 1993. 460: p. 641-55.
  51. Blessing, W. and E. Nalivaiko, Raphe magnus/pallidus neurons regulate tail but not mesenteric arterial blood flow in rats. Neuroscience, 2001. 105(4): p. 923-929.
  52. Stephens, D.P., et al., Sympathetic nonnoradrenergic cutaneous vasoconstriction in women is associated with reproductive hormone status. American Journal of Physiology-Heart and Circulatory Physiology, 2002. 282(1): p. H264-H272.
  53. Stephens, D.P., et al., Nonnoradrenergic mechanism of reflex cutaneous vasoconstriction in men. American Journal of Physiology-Heart and Circulatory Physiology, 2001. 280(4): p. H1496-H1504.
  54. Smith, C.J. and J.M. Johnson, Responses to hyperthermia. Optimizing heat dissipation by convection and evaporation: Neural control of skin blood flow and sweating in humans. Autonomic Neuroscience, 2016. 196: p. 25-36.
  55. MacKenzie, M., et al., Skin blood flow and autonomic reactivity in human poikilothermia. Clinical Autonomic Research, 1996. 6(2): p. 91-97.
  56. Pergola, P.E., et al., Reflex control of active cutaneous vasodilation by skin temperature in humans. American Journal of Physiology-Heart and Circulatory Physiology, 1994. 266(5): p. H1979-H1984.
  57. Leger, L., et al., Comparative distribution of nitric oxide synthase-and serotonin-containing neurons in the raphe nuclei of four mammalian species. Histochem Cell Biol, 1998. 110(5): p. 517-525.
  58. Arami, M.K., Nitric oxide in the nucleus raphe magnus modulates cutaneous blood flow in rats during hypothermia. Iranian journal of basic medical sciences, 2015. 18(10): p. 989.
  59. Dias, M.B., et al., Raphe magnus nucleus is involved in ventilatory but not hypothermic response to CO2. J Appl Physiol, 2007. 103(5): p. 1780-1788.
  60. Dias, A.C.R., et al., Nitric oxide modulation of glutamatergic, baroreflex, and cardiopulmonary transmission in the nucleus of the solitary tract. American Journal of Physiology-Heart and Circulatory Physiology, 2005. 288(1): p. H256-H262.
  61. Mathai, M.L., et al., Central blockade of nitric oxide synthesis induces hyperthermia that is prevented by indomethacin in rats. J Therm Biol, 2004. 29(7): p. 401-405.
  62. Eriksson, S., et al., Central application of a nitric oxide donor activates heat defense in the rabbit. Brain Res, 1997. 774(1): p. 269-273.
  63. Kellogg, D.L., Jr., et al., Role of nitric oxide in the vascular effects of local warming of the skin in humans. J Appl Physiol (1985), 1999. 86(4): p. 1185-90.
  64. Johnson, J.M., et al., Effect of local warming on forearm reactive hyperaemia. Clin Physiol, 1986. 6(4): p. 337-46.
  65. Babasafari, M., et al., Alteration of Phospholipase C Expression in Rat Visual Cortical Neurons by Chronic Blockade of Orexin Receptor 1. International Journal of Peptide Research and Therapeutics, 2019: p. 1-7.
  66. Rezaei, Z., et al., Orexin type-1 receptor inhibition in the rat lateral paragigantocellularis nucleus attenuates development of morphine dependence. Neuroscience Letters, 2020: p. 134875.
  67. Kourosh-Arami, M., et al., Phospholipase Cβ3 in the hippocampus may mediate impairment of memory by long-term blockade of orexin 1 receptors assessed by the Morris water maze. Life Sciences, 2020. 257: p. 118046.
  68. Babaie, F., M. Kourosh-Arami, and M. Farhadi, Administration of Orexin-A into the Rat Thalamic Paraventricular Nucleus Enhances the Naloxone Induced Morphine Withdrawal. Drug Research, 2022. 72(04): p. 209-214.
  69. Kourosh-Arami, M., et al., Neural correlates and potential targets for the contribution of orexin to addiction in cortical and subcortical areas. Neuropeptides, 2022: p. 102259.
  70. Kourosh-Arami, M., M. Javan, and S. Semnanian, Inhibition of orexin receptor 1 contributes to the development of morphine dependence via attenuation of cAMP response element-binding protein and phospholipase Cβ3. Journal of Chemical Neuroanatomy, 2020. 108: p. 101801.
  71. Kourosh-Arami, M., et al., Persistent effects of the orexin-1 receptor antagonist SB-334867 on naloxone precipitated morphine withdrawal symptoms and nociceptive behaviors in morphine dependent rats. International Journal of Neuroscience, 2021. 132(1): p. 67-76.
  72. Samani, F. and M.K. Arami, Repeated Administration of Orexin into the Thalamic Paraventricular Nucleus Inhibits the Development of Morphine-Induced Analgesia. Protein and Peptide Letters, 2022. 29(1): p. 57-63.
  73. Mousavi, Z., et al., An immunohistochemical study of the effects of orexin receptor blockade on phospholipase C-β3 level in rat hippocampal dentate gyrus neurons. Biotechnic & Histochemistry, 2020: p. 1-6.
  74. Martin, T., et al., Dual orexin receptor antagonist induces changes in core body temperature in rats after exercise. Scientific reports, 2019. 9(1): p. 1-9.
  75. Piri, Z., et al., Alteration of Hematologic Parameters in Morphine-Dependent Rats by Long-Term Administration of Orexin Type 1 Receptor Antagonist. International Journal of High Risk Behaviors and Addiction, 2020. 9(3).
  76. Mochizuki, T., et al., Elevated body temperature during sleep in orexin knockout mice. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 2006. 291(3): p. R533-R540.
  77. Kuwaki, T., Thermoregulation under pressure: a role for orexin neurons. Temperature, 2015. 2(3): p. 379-391.
  78. Takahashi, Y., et al., Orexin neurons are indispensable for prostaglandin E2‐induced fever and defence against environmental cooling in mice. The Journal of physiology, 2013. 591(22): p. 5623-5643.
  79. Tan, C.L. and Z.A. Knight, Regulation of body temperature by the nervous system. Neuron, 2018. 98(1): p. 31-48.
  80. Messina, G., S. Chieffi, and M. Monda, Orexin A exerts more thermogenic than orexinergic functions. PeerJ PrePrints, 2014. 2: p. e392v1.

 

 

Journal of Kerman University of Medical Sciences
Volume 29, Issue 4
July and August 2022
Pages 401-410
Files
Share
How to cite
Statistics