The rat: A laboratory model for studies of the diving response

Journal of Applied Physiology

Volumn 108, Issue 4, 2010, Pages 811-820

  Michael Panneton, W ^a   Gan, Qi ^a   Juric, Rajko ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Blood pressure; Bradycardia; Nasopharyngeal reflex; Pulse pressure

Indexed keywords

AMMONIA;

ANIMAL; ANIMAL MODEL; ARTICLE; CHOLINERGIC SYSTEM; DECEREBRATION; DIVING; DRUG EFFECT; HEART RATE; HEMODYNAMICS; INHALATIONAL DRUG ADMINISTRATION; MALE; NOSE MUCOSA; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; SWIMMING; VASOCONSTRICTION;

ADMINISTRATION, INHALATION; AMMONIA; ANIMALS; DECEREBRATE STATE; DIVING; HEART RATE; HEMODYNAMICS; MALE; MODELS, ANIMAL; NASAL MUCOSA; OXYGEN CONSUMPTION; PARASYMPATHETIC NERVOUS SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; SWIMMING; VASOCONSTRICTION;

EID: 77950577610     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00600.2009     Document Type: Article

References (105)

1. Baker MA, Horvath SM. Influence of water temperature on heart rate and rectal temperature of swimming rats. Am J Physiol, 207: 1073-1076, 1964.
2. Beidenbach MA, Beuerman RW, Brown AC. Graphic-digitizer analysis of axon spectra in ethmoidal and lingual branches of the trigeminal nerve. Cell Tissue Res 157: 341-352, 1975.
3. Blake DW, Blombery PA, Korner PI. Effects of ketamine, althesin, and thiopentone on the Valsalva-contrictor and heart rate reflexes of the rabbit. J Auton Nerv Syst 5: 291-301, 1982.
4. Blake DW, Korner PI. Role of baroreceptor reflexes in the hemodynamic and heart rate responses to althesin, ketamine, and thiopentone anesthesia. J Auton Nerv Syst 3: 55-70, 1981.
5. Blake DW, Korner PI. Effects of ketamine and althesin anesthesia on baroreceptor-heart rate reflex and hemodynamics of intact and pontine rabbits. J Auton Nerv Syst 5: 145-154, 1982.
6. Blix AS, Folkow B. Cardiovascular adjustments to diving in mammals and birds. In: Handbook of Physiology. The Cardiovascular System. Peripheral Circulation and Organ Blood Flow. Bethesda, MD: Am Physiol Soc, 1983, sect. 2, vol.III, p. 917-945.
7. Butler PJ. Diving beyond the limits. News Physiol Sci 16: 222-227, 2001.
8. Butler PJ, Jones DR. The comparative physiology of diving in vertebrates. Adv Comp Physiol Biochem 8: 179-364, 1982.
9. Butler PJ, Jones DR. Physiology of diving of birds and mammals. Physiol Rev 77: 837-899, 1997.
10. Byku M, Gan Q, Panneton WM. A physiological and neuroanatomical comparison of rats after either voluntary or forced dives (Abstract). FASEB J 18: A1102, 2004.
11. Campbell JN, Raja SN, Meyer RA. Halothane sensitizes cutaneous nociceptors in monkeys. J Neurophysiol 52: 762-770, 1984.
12. Cauna N, Hinderer KH, Wentges RT. Sensory receptor organs of the human nasal respiratory mucosa. Am J Anat 124: 187-210, 1969.
13. 13. Davis RW, Polasek L, Watson R, Fuson A, Williams TM, Kanatous SB. The diving paradox: new insights into the role of the dive response in air-breathing vertebrates. Comp Biochem Physiol A Mol Integr Physiol 138: 263-268, 2004. (Pubitemid 39094652)
14. de Burgh Daly M. Breath-hold diving: mechanisms of cardiovascular adjustments in the mammal. Recent Adv Physiol 10: 201-245, 1984.
15. Doyle RE, Panneton WM, Vogler GA, Romeo JP, Watson BJ, Higgins B. The muskrat in biomedical research. Lab Anim Sci 38: 667-674, 1988.
16. Drummond PC, Jones DR. The initiation and maintenance of bradycardia in a diving mammal, the muskrat, Ondatra zibethica. J Physiol, 290: 253-271, 1979.
17. Dykes RW. Factors related to the dive reflex in harbor seals: respiration, immersion, bradycardia, and lability of the heart rate. Can J Physiol Pharmacol 52: 248-257, 1974.
18. Dykes RW. Factors related to the dive reflex in harbor seals: sensory contributions from the trigeminal region. Can J Physiol Pharmacol 52: 259-265, 1974.
19. Eisner R, Franklin DL, Van Citters RL, Kenney DW. Cardiovascular defense against asphyxia. Science 153: 941-949, 1966.
20. Eisner R, Gooden B. Diving and Asphyxia: A Comparative Study of Animals and Man. New York: Cambridge Univ. Press, 1983, p. 1-168.
21. Faber JE. Effects of althesin and urethan-chloralose on neurohumoral cardiovascular regulation. Am J Physiol Regul Integr Comp Physiol 256: R757-R765, 1989.
22. Ferretti G. Extreme human breath-hold diving. Eur J Appl Physiol 84: 254-271, 2001.
23. Finger TE, St. Jeor VL, Kinnamon JC, Silver WL. Ultrastructure of substance P- and CGRP-immunoreactive nerve fibers in the nasal epithelium of rodents. J Comp Neurol 294: 293-305, 1990.
24. 24. Foster GE, Sheel AW. The human diving response, its function, and its control. Scand J Med Sci Sports 15: 3-12, 2005. (Pubitemid 40269616)
25. Gabbott GRJ, Jones DR. The effect of brain transection on the response to forced submergence in ducks. J Auton Nerv Syst 36: 65-74, 1991.
26. Gieroba ZJ, Yu YH, Blessing WW. Vasoconstriction induced by inhalation of irritant vapour is associated with appearance of Fos protein in Cl catecholamine neurons in rabbit medulla oblongata. Brain Res 636: 157-161, 1994.
27. 27. Goksör E, Rosengren L, Wennergren G. Bradycardic response during submersion in infant swimming. Acta Paediatr 91: 307-312, 2002. (Pubitemid 34270870)
28. Greaves DK, Schreer JF, Hammill MO, Burns JM. Diving heart rate development in postnatal harbour seals, Phoca vitulina. Physiol Biochem Zool 78: 9-17, 2005.
29. Halliwill JR, Billman GE. Effect of general anesthesia on cardiac vagal tone. Am J Physiol Heart Circ Physiol 262: H1719-H1724, 1992.
30. Hanney PW. Rodents: Their Lives and Habits. Vancouver: David and Charles, 1975.
31. 31. Hill RD, Schneider RC, Liggins GC, Schuette AH, Elliott RL, Guppy M, Hochachka PW, Qvist J, Falke KJ, Zapol WM. Heart rate and body temperature during free diving of Weddell seals. Am J Physiol Regul Integr Comp Physiol 253: R344-R351, 1987. (Pubitemid 17155287)
32. Ho CY, Kou YR. Protective and defensive airway reflexes evoked by nasal exposure to wood smoke in anesthetized rats. J Appl Physiol 88: 863-870, 2000.
33. Hochachka PW, Liggins GC, Guyton GP, Schneider RC, Stanek KS, Hurford WE, Creasy RK, Zapol DG, Zapol WM. Hormonal regulatory adjustments during voluntary diving in. Weddell seals. Comp Biochem Physiol 112B: 361-375, 1995.
34. Inagaki H, Kuwahara M, Tsubone H. Effects of psychological stress on autonomic control of heart in rats. Exp Anim 53: 373-378, 2004. (Pubitemid 41349905)
35. Jobsis PD, Ponganis PJ, Kooyman GL. Effects of training on forced submersion responses in harbor seals. J Exp Biol 204: 3877-3885, 2001.
36. Jones DR, Furilla RA, Heieis MR, Cabbott A, Smith FM. The effect of the stress of forcible submergence on the diving response in muskrats (Ondatra zibethica). Can J Zool 60: 187-193, 1982.
37. 37. Jorgensen C, Lydersen C, Brix O, Kovacs KA. Diving development in nursing harbour seal pups. J Exp Biol 204: 3993-4004, 2001. (Pubitemid 34861319)
38. Kaufman MP, Forster HV. Reflexes controlling circulatory, ventilatory and airway responses to exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am Physiol Soc, 1996, sect. 12, p. 381-447.
39. Kooyman GL. Physiology without restraint in diving mammals. Mar Mamm Sci 1: 166-178, 1985.
40. Kooyman GL. Diverse Divers: Physiology and Behavior. Berlin: Springer, 1989.
41. Kooyman GL, Castellini MA, Davis RW. Physiology of diving in marine mammals. Annu Rev Physiol, 43: 343-356, 1981.
42. Kooyman GL, Ponganis PJ. The physiological basis of diving to depth.: birds and mammals. Annu Rev Physiol 60: 19-32, 1998.
43. Koppányi T, Dooley MS. Submergence and postural apnea in the muskrat. Am J Physiol 88: 592-595, 1929.
44. Korner PI, Langsford G, Starr D, Uther JB, Ward W, White SW. The effects of chloralose-urethane and sodium pentobarbitone anesthesia on the local and autonomic components of the circulatory response to arterial hypoxia. J Physiol 199: 283-302, 1968.
45. Korner PI, Uther JB, White SW. Circulatory effects of chloraloseurethane and sodium pentobarbitone anesthesia in the rabbit. J Physiol, 199: 253-265, 1968.
46. Lacombe AMA, Jones DR. Neural and humoral effects on hindlimb vascular resistance of ducks during forced submergence. Am J Physiol Regul Integr Comp Physiol 261: R1579-R1586, 1991.
47. Lacombe AMA, Jones DR. Role of adrenal catecholamines during forced submergence in ducks. Am J Physiol Regul Integr Comp Physiol 261: R1364-R1372, 1991.
48. 48. Leiter JC, Böhm I. Mechanisms of pathogenesis in the Sudden Infant Death. Syndrome. Respir Physiol Neurobiol 159: 127-138, 2007. (Pubitemid 47562905)
49. Lin YC. Autonomic nervous control of cardiovascular response during diving in the rat. Am J Physiol 227: 601-605, 1974.
50. Lin YC, Baker DG. Cardiac output and its distribution during diving in the rat. Am J Physiol 228: 733-737, 1975.
51. Lobban CDR. The human dive reflex as a primary cause of SIDS: a review of the literature. Med J Aust 155: 561-563, 1991.
52. MacArthur RA. Aquatic thermoregulation in the muskrat (Ondatra zibethicus): energy demands of swimming and diving. Can J Zool 62: 241-248, 1984.
53. Martner J, Wadenvik H, Lisander B. Apnoea and bradycardia from submersion in "chronically" decerebrated cats. Acta Physiol Scand 101: 476-480, 1977.
54. McCulloch PF, Faber KM, Panneton WM. Electrical stimulation of the anterior ethmoidal nerve produces the diving response. Brain Res 830: 24-31, 1999.
55. McCulloch PF, Jones DR. Cortical influences on diving bradycardia in muskrats (Ondatra zibethicus). Physiol Zool 63: 1098-1117, 1990.
56. 56. McCulloch PF, Ollenberger GP, Bekar LK, West NH. Trigeminal and chemoreceptor contributions to bradycardia during voluntary dives in rats. Am J Physiol Regul Integr Comp Physiol 273: R814-R822, 1997. (Pubitemid 27428101)
57. McCulloch PF, Panneton WM. Fos immunohistochemical determination of brainstem neuronal activation in the muskrat after nasal stimulation. Neuroscience 78: 913-925, 1997.
58. McCulloch PF, Panneton WM. Activation of brainstem catecholaminergic neurons during voluntary diving in rats. Brain Res 984: 42-53, 2003.
59. McCulloch PF, Panneton WM, Guyenet PG. The rostral ventrolateral medulla mediates the sympathoactivation produced by chemical stimulation of the nasal mucosa. J Physiol 516: 471-484, 1999.
60. McRitchie RJ, White SW. Role of trigeminal olfactory, carotid sinus and aortic nerves in the respiratory and circulatory response to nasal inhalation of cigarette smoke and other irritants in the rabbit. Aust J Exp Biol Med Sci 52: 127-140, 1974.
61. 61. Mutoh T, Kanamaru A, Tsubone H, Nishimura R, Sasaki N. Respiratory reflexes in response to nasal administration of halothane to anesthetized, spontaneously breathing dogs. Am J Vet Res 61: 260-267, 2000. (Pubitemid 30121148)
62. Mutoh T, Nishimura R, Kim H, Matsunaga S, Sasaki N. Cardiopulmonary effects of sevoflurane, compared with halothane, enflurane, and isoflurane, in dogs. Am J Vet Res 58: 885-890, 1997.
63. 63. Mutoh T, Tsubone H, Nishimura R, Sasaki N. Effects of volatile anesthetics on vagal C-fiber activities and their reflexes in anesthetized dogs. Respir Physiol 112: 253-264, 1998. (Pubitemid 28356824)
64. 64. Nagasaki G, Tanaka M, Nishikawa T. The recovery profile of baroreflex control of heart rate after isoflurane or sevoflurane anesthesia in humans. Anesth Analg 93: 1127-1131, 2001. (Pubitemid 33021001)
65. Noren SR, Cuccurullo V, Williams TM. The development of diving bradycardia in bottlenose dolphins (Tursiops truncatus). J Comp Physiol, [B] 174: 139-147, 2004.
66. Noren SR, Williams TM, Pabst DA, McLellan WA, Dearolf JL. The development of diving in marine endotherme: preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence. J Comp Physiol [B] 171: 127-134, 2001.
67. 67. Ollenberger GP, Matte G, Wilkinson AA, West NH. Relative distribution of blood flow in rats during surface and submerged swimming. Comp Biochem Physiol 119A: 271-277, 1998. (Pubitemid 28162394)
68. 68. Ollenberger GP, West NH. Contribution of hypercapnia and trigeminal stimulation to cerebrovascular dilation during simulated diving. Am J Physiol Regul Integr Comp Physiol 274: R921-R930, 1998. (Pubitemid 28217741)
69. 69. Ollenberger GP, West NH. Distribution of regional cerebral blood flow in voluntarily diving rats. J Exp Biol 201: 549-558, 1998. (Pubitemid 28107175)
70. Panneton M, Watson BJ. Stereotaxic atlas of the brainstem of the muskrat, Ondatra zibethicus. Brain Res Bull 26: 479-509, 1991.
71. Panneton WM. Controlled bradycardia induced by nasal stimulation in the muskrat, Ondatra zibethicus. J Auton Nerv Syst 30: 253-264, 1990.
72. Panneton WM. Primary afferent projections from the upper respiratory tract in the muskrat. J Comp Neurol 308: 51-65, 1991.
73. Panneton WM. Trigeminal mediation of the diving response in the muskrat. Brain Res 560: 321-325, 1991.
74. Panneton WM, Gan Q. Cardiovascular changes induced in freely diving, swimming and nasally stimulated rats (Abstract). Soc Neurosci Abstr 28: 923.2, 2003.
75. 75. Panneton WM, Gan Q, Juric R. Brainstem projections from recipient zones of the anterior ethmoidal nerve in the medullary dorsal horn. Neuroscience 141: 889-906, 2006. (Pubitemid 44066667)
76. Panneton WM, Gan Q, Sun W. Pressor responses to nasal stimulation are unaltered after disrupting the CPA. Auton Neurosci 144: 13-21, 2008.
77. 77. Panneton WM, McCulloch PF, Sun W. Trigemino-autonomic connections in the muskrat: the neural substrate for the diving response. Brain Res 874: 48-65, 2000. (Pubitemid 30599494)
78. Panneton WM, Sun W. Cardiorespiratory changes after nasal stimulation persist after partial pontine transection (Abstract). Soc. Neurosci Abstr 27: 170.14, 2001.
79. Panneton WM, Yavari P. A medullary dorsal horn relay for the cardiorespiratory responses evoked by stimulation of the nasal mucosa in the muskrat, Ondatra zibethicus: evidence for excitatory amino acid transmission. Brain Res 691: 37-45, 1995.
80. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1998.
81. Peterson DF, Coote JH, Gilbey MP, Futuro-Neto HA. Differential pattern of sympathetic outflow during upper airway stimulation with smoke. Am J Physiol Regul Integr Comp Physiol 245: R433-R437, 1983.
82. 82. Picker O, Schwarte LA, Roth HJ, Greve J, Scheeren TW. Comparison of the role of endothelin, vasopressin and angiotensin in arterial pressure regulation during sevoflurane anaesthesia in dogs. Br J Anaesth 92: 102-108, 2004. (Pubitemid 38054657)
83. Rozloznik M, Paton JFR, Dutschmann M. Repetitive paired stimulation of nasotrigeminal and peripheral chemoreceptor afferents cause progressive potentiation of the diving bradycardia. Am J Physiol Regul Integr Comp Physiol 296: R80-R87, 2009.
84. Rybka EJ, McCulloch PF. The anterior ethmoidal nerve is necessary for the initiation of the nasopharyngeal response in the rat. Brain Res 1075: 122-132, 2006.
85. Schagatay E, Van Kampen M. Apneic snout immersion in trained pigs elicits a "diving response". Adv Exp Med Biol 393: 73-76, 1995.
86. Scholander PF. The master switch of life. Sci Am 209: 92-106, 1963.
87. Sgoifo A, Koolhaas JM, Musso E, De Boer SF. Different sympathovagal modulation of heart rate during social and nonsocial stress episodes in wild-type rats. Physiol Behav 67: 733-738, 1999.
88. 88. Singer D. Neonatal tolerance to hypoxia: a comparative-physiological approach. Comp Biochem Physiol A 123: 221-234, 1999. (Pubitemid 29395567)
89. Stephenson R, Butler PJ, Dunstone N, Woakes AJ. Heart rate and gas exchange in freely diving American mink (Mustela vison). J Exp Biol 134: 435-442, 1988.
90. Sun MK, Reis DJ. Urethane directly inhibits chemoreflex excitation of medullary vasomotor neurons in rats. Eur J Pharmacol 293: 237-243, 1995.
91. Sun MK, Spyer KM. Reticulospinal vasomotor neurones in decerebrate rats: effect of pentobarbitone. J Auton Nerv Syst 33: 85-90, 1991.
92. Swain UG, Gilbert FF, Robinette JD. Heart rates in the captive, free-ranging beaver. Comp Biochem Physiol A Comp Physiol 91: 431-435, 1988.
93. Swanson LW. Brain Maps: Structure of the Rat Brain. A. Laboratory Guide with Printed and Electronic Templates for Data, Models and Schematics. Amsterdam: Elsevier, 2004.
94. Tanelian DL, Maclver MB. Differential excitatory and depressant anesthetic effects on mammalian A-delta and C fiber sensory afferents. Ann NY Acad Sci 625: 273-275, 1991.
95. Tchobroutsky C, Merlet C, Rey P. The diving reflex in rabbit, sheep and newborn lamb and its afferent pathways. Respir Physiol 8: 108-117, 1969.
96. 96. Wallois F, Gros F, Condamin M, Macron M. Postnatal development of the anterior ethmoidal nerve in cats: unmyelinated and myelinated nerve fiber analysis. Neurosci Lett 160: 221-224, 1993. (Pubitemid 23294745)
97. Wallois F, Larnicol N, Rose D, Duron B. A comparative HRP study of the neuronal supply to the inferior and superior nasal meatus in the cat. Neurosci Lett 139: 234-238, 1992.
98. Whishaw IQ, Schallert T. Hippocampal RSA (theta), apnea, bradycardia, and effects of atropine during underwater swimming in the rat. Electroencephalogr Clin Neurophysiol 42: 389-396, 1977.
99. White S, McRitchie RJ, Korner PI. Central nervous system control of cardiorespiratory nasopharyngeal reflexes in the rabbit. Am J Physiol 228: 404-409, 1975.
100. White SW, McRitchie RJ, Franklin DL. Autonomic cardiovascular effects of nasal inhalation of cigarette smoke in the rabbit. Aust J Exp Biol Med Sci 52: 111-126, 1974.
101. Whyane TF, Smith NT, Eger EI, Stoelting RK, Whitcher CE. The effects of halothane anesthesia on reflex cardiovascular responses to simulated diving and the Valsalva maneuver. Anesthesiology 34: 262-270, 1971.
102. Wood SK, Verhoeven RE, Savit AZ, Kenner CR, Fishbach PS, Woods JH. Facilitation of cardiac vagal activity by CRF-R1 antagonists during swim stress in rats. Neuropsychopharmacology 31: 2580-2590, 2006.
103. 103. Yavari P, McCulloch PF, Panneton WM. Trigeminally-mediated alteration of cardiorespiratory rhythms during nasal application of carbon dioxide in the rat. J Auton Nerv Syst 61: 195-200, 1996. (Pubitemid 26384346)
104. 104. Zapol WM, Liggins GC, Schneider RC, Qvist J, Snider MT, Creasy RK, Hochachka PW. Regional blood flow during simulated diving in the conscious Weddell seal. J Appl Physiol 47: 968-973, 1979. (Pubitemid 10187511)
105. 105. Zimpfer M, Sit SP, Vatner SF. Effects of anesthesia on the canine carotid chemoreceptor reflex. Circ Res 48: 400-406, 1981. (Pubitemid 11102704)