The human ventilatory response to stress: rate or depth?

Journal of Physiology

Volumn 595, Issue 17, 2017, Pages 5729-5752

  Tipton, Michael J ^a   Harper, Abbi ^b   Paton, Julian F R ^c   Costello, Joseph T ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^b SOUTHMEAD HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

cold; heat; neurophysiology; pain; panic; respiratory frequency; tidal volume; ventilation

Indexed keywords

BLOOD GAS; BODY TEMPERATURE; BREATHING DEPTH; BREATHING PATTERN; BREATHING RATE; COLD; ENVIRONMENTAL STRESS; EXERCISE; EXERCISE INTENSITY; EXPIRATORY RESERVE VOLUME; GENDER; HEAT; HUMAN; HYPERTHERMIA; HYPOXIA; INSPIRATORY RESERVE VOLUME; LUNG PERFUSION; NONHUMAN; PAIN; PANIC; PRIORITY JOURNAL; RESPIRATORY FUNCTION; REVIEW; STRESS; THERMAL EXPOSURE; TIDAL VOLUME; ANIMAL; BREATHING; FEVER; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; COLD TEMPERATURE; FEVER; HUMANS; HYPOXIA; PAIN; PANIC; RESPIRATION; STRESS, PHYSIOLOGICAL;

EID: 85026367465     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP274596     Document Type: Review

References (225)

1. Abdala AP, Rybak IA, Smith JC & Paton JF (2009a). Abdominal expiratory activity in the rat brainstem-spinal cord in situ: patterns, origins and implications for respiratory rhythm generation. J Physiol 587, 3539–3559.
2. Abdala AP, RybakH IA, Smith JC, Zoccal DB, Machado BH, St-John WM & Paton JF (2009b). Multiple pontomedullary mechanisms of respiratory rhythmogenesis. Respir Physiol Neurobiol 168, 19–25.
3. Abdala AP, Toward MA, Dutschmann M, Bissonnette JM & Paton JF (2016). Deficiency of GABAergic synaptic inhibition in the Kölliker-Fuse area underlies respiratory dysrhythmia in a mouse model of Rett syndrome. J Physiol 594, 223–237.
4. Aitken ML, Franklin JL, Pierson DJ & Schoene RB (1986). Influence of body size and gender on control of ventilation. J App Physiol 60, 1894–1899.
5. Anand A & Paintal AS (1980) Reflex effects following selective stimulation of J receptors in the cat. J Physiol 299, 553–572.
6. Applegate CD, Kapp BS, Underwood MD & McNall CL (1983). Autonomic and somatomotor effects of amygdala central N. stimulation in awake rabbits. Physiol Behav 31, 353–360.
7. Bailey EF & Hoit JD (2002). Speaking and breathing in high respiratory drive. J Speech Lang Hear Res 45, 89–99.
8. Barwood MJ, Burrows H, Cessford J & Goodall S (2016). "Float first and kick for your life": Psychophysiological basis for safety behaviour on accidental short-term cold water immersion. Physiol Behav 154, 83–89.
9. Barwood MJ, Corbett J, Green R, Smith T, Tomlin P, Weir-Blankenstein L & Tipton MJ (2013). Acute anxiety increases the magnitude of the cold shock response before and after habituation. Eur J Appl Physiol 113, 681–689.
10. Barwood MJ, Corbett J & Wagstaff CR (2014). Habituation of the cold shock response may include a significant perceptual component. Aviat Space Environ Med 85, 167–171.
11. Bechbach RR, Chow HHK, Duffin J, Orsini EC (1979). The effects of hypercapnia, hypoxia, exercise and anxiety on the pattern of breathing in man. J Physiol 293, 285–300.
12. Bell HJ & Duffin J (2006). Rapid increases in ventilation accompany the transition from passive to active movement. Resp Physiol Neurobiol 152, 128–142.
13. Bernardi L, Schneider A, Pomidori L, Paolucci E & Cogo A (2006). Hypoxic ventilatory response in successful extreme altitude climbers. Eur Respir J 27, 165-171.
14. Berssenbrugge A, Dempsey J, Iber C, Skatrud J & Wilson P (1983). Mechanisms of hypoxia-induced periodic breathing during sleep in humans. J Physiol 343, 507–524.
15. Bisgard GE & Neubauer JA (1994). Peripheral and central effects of hypoxia. In Regulation of Breathing (2nd edn), eds Dempsey JA & Pack AI, pp. 617–668. Dekker, New York.
16. Blatteis CM & Lutherer LO (1976). Effect of altitude exposure on thermoregulatory response of man to cold. J Appl Physiol 41, 848–858.
17. Boden AG, Harris MC & Parkes MJ (2000). The preoptic area in the hypothalamus is the source of the additional respiratory drive at raised body temperature in anaesthetised rats. Exp Physiol 85, 527–537.
18. Borgbjerg FM, Nielsen K & Franks J (1995). Experimental pain stimulates respiration and attenuates morphine-induced respiratory depression: a controlled study in human volunteers. Pain 64, 123–128.
19. Boscan P & Paton JF (2001). Role of the solitary tract nucleus in mediating nociceptive evoked cardiorespiratory responses. Auton Neurosci 86, 170–182.
20. Bourke DL (1997). Respiratory effects of regional anesthesia during acute pain. Reg Anesth 18, 361–365.
21. 2 and temperature on the relationship between lung volume and inspiratory duration (Hering-Breuer threshold curve). Acta Physiol Scand 92, 351–363.
22. Braun SR (1990). Respiratory rate and pattern. In Clinical Methods: The History, Physical, and Laboratory Examinations, eds Walker HK, Hall WD & Hurst JW, pp. 226–230, Butterworth Publishers, Stoneham, MA, USA.
23. Button C, Croft JL, Cotter JD, Graham MJ & Lucas SJ (2015). Integrative physiological and behavioural responses to sudden cold-water immersion are similar in skilled and less-skilled swimmers. Physiol Behav 138, 254–259.
24. Cabanac M & White MD (1995). Core temperature thresholds for hyperpnea during passive hyperthermia in humans. Eur J Appl Physiol Occup Physiol 71, 71–76.
25. Cannon WB (1929). Bodily Changes in Pain, Fear and Rage, 2nd edn. Appleton and Company, New York.
26. Carey D, Pliego G & Raymond R (2008). How endurance athletes breathe during incremental exercise to fatigue: interaction of tidal volume and frequency. J Ex Physiol 11, 44–51.
27. Carnevali L, Sgoifo A, Trombini M, Landgraf R, Neumann ID & Nalivaiko E (2013) Different patterns of respiration in rat lines selectively bred for high or low anxiety. PLoS One 8, e64519.
28. Caruana-Montaldo B, Gleeson K & Zwillich CW (2000). The control of breathing in clinical practice. Chest 117, 205–225.
29. Chamberlin NL & Saper CB (1994). Topographic organization of respiratory responses to glutamate microstimulation of the parabrachial nucleus in the rat. J Neurosci 14, 6500–6510.
30. Christensen NJ (1991). The biochemical assessment of sympathoadrenal activity in man. Clin Auton Res 1, 167–172.
31. Chu AL, Jay O & White MD (2007). The effects of hyperthermia and hypoxia on ventilation during low-intensity steady-state exercise. Am J Physiol Regul Integr Comp Physiol 292, R195–R203.
32. Clark FJ & von Euler C (1972). On the regulation of depth and rate of breathing. J Physiol 222, 267–295.
33. Cooper KE, Martin S & Riben P (1976). Respiratory and other responses in subjects immersed in cold water. J Appl Physiol 40, 903–910.
34. Critchley HD, Nicotra A, Chiesa PA, Nagai Y, Gray MA, Minati L & Bernardi L (2015). Slow breathing and hypoxic challenge: cardiorespiratory consequences and their central neural substrate. PLoS One 10, e0127082.
35. Croft JL, Button C, Hodge K, Lucas SJ, Barwood MJ & Cotter JD (2013). Responses to sudden cold-water immersion in inexperienced swimmers following training. Aviat Space Environ Med 84, 850–855.
36. Cunningham DJC (1974). Integrative aspects of the regulation of breathing: a personal view. In MTP Int Rev Sci Physiol, series 1, vol. 2, Respiration, ed. Widdicombe JG, p. 310. Butterworths, London.
37. 2 inhalation in man. J Physiol 227, 50P–51P.
38. 2 inhalation in man, with special emphasis on expiration. J Physiol 272, 613–632.
39. Cunningham DJC, Pearson SB & Gardner WN (1972). Regulation of respiratory frequency and tidal volume at various ventilations. Arch Fisiol 69, 443–446.
40. Curran AK, Rodman JR, Eastwood PR, Henderson KS, Dempsey JA & Smith CA (2000) Ventilation responses to specific CNS hypoxia in sleeping dogs. J Appl Physiol 88, 1840–1852.
41. Curtis AN, Walsh ML & White MD (2007). Influence of passive hyperthermia on human ventilation during rest and isocapnic hypoxia. Appl Physiol Nutr Metab 32, 721–732.
42. 2 sensitivity. PLoS Med 4, e239. https://doi.org/10.1371/journal.pmed.0040239
43. Datta A & Tipton M (2006). Respiratory responses to cold water immersion: neural pathways, interactions, and clinical consequences awake and asleep. J Appl Physiol 100, 2057–2064.
44. Davis M (1992). The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15, 353–375.
45. Davies RC, Rowlands AV & Easton RG (2009). Effect of exercise-induced muscle damage on ventilatory and perceived exertion responses to moderate and severe intensity cycle exercise. Eur J Appl Physiol 107, 11–19.
46. De Morree HM, Klein C & Marcora SM (2012). Perception of effort reflects central motor command during movement execution. Psychophysiology 49, 1242–1253.
47. Dempsey JA, Powell FL, Bisgard GE, Blain GM, Poulin MJ & Smith CA (2014). Role of chemoreception in cardiorespiratory acclimatization to, and deacclimatization from, hypoxia. J Appl Physiol 116, 858–866.
48. Dempsey JA & Smith CA (2014). Pathophysiology of human ventilatory control. Eur Respir J 44, 495–512.
49. Dongelmans DA, Paulus F, Veelo DP, Binnekade JM, Vroom MB & Schultz MJ (2011). Adaptive support ventilation may deliver unwanted respiratory rate-tidal volume combinations in patients with acute lung injury ventilated according to an open lung concept. Anesthesiology 114, 1138–1143.
50. Duffin J (2014). The fast exercise drive to breathe. J Physiol 592, 445–451.
51. Duffin J, Mohan RM, Vasiliou P, Stephenson R & Mahamed S (2000). A model of the chemoreflex control of breathing in humans: Model parameters measurement. Respir Physiol 120, 13–26.
52. Duranti R, Pantaleo T, Bellini F, Bongianni F & Scano G (1991). Respiratory responses induced by the activation of somatic nociceptive afferents in humans, J Appl Physiol 71, 2440–2448.
53. Dutschmann M & Herbert H (2006). The Kölliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur J Neurosci 24, 1071–1084.
54. Easton PA & Anthonisen NR (1988). Carobin diaoxide effects on the ventilatory response to sustained hypoxia. J Appl Physiol 64, 1451–1456.
55. Eger EI, Dolan WM, Stevens WC, Miller RD & Way WL (1972). Surgical stimulation antagonises the respiratory depression produced by forane. Anesthesiology 36, 544–549.
56. Eglin CM, Butt G, Howden S, Nash T & Costello JT (2015). Rapid habituation of the cold shock response. Extrem Physiol Med 4 (Suppl. 1), A38.
57. Eglin CM & Tipton MJ (2005). Repeated cold showers as a method of habituating humans to the initial responses to cold water immersion. Eur J Appl Physiol 93, 624–629.
58. Eyzaguirre C & Zapata P (1984). Perspectives in carotid body research. J Appl Physiol 57, 931–957.
59. Faiss R, Pialoux V, Sartori C, Faes C, Deriaz O & Millet GP (2013). Ventilation, oxidative stress, and nitric oxide in hypobaric versus normobaric hypoxia. Med Sci Sports Exerc 45, 253–260.
60. Fan J-L, Cotter JD, Lucas RA, Thomas K, Wilson L & Ainslie PN (2008). Human cardiorespiratory and cerebrovascular function during severe passive hyperthermia: effects of mild hypohydration. J Appl Physiol 105, 433–445.
61. Faulhaber M, Wille M, Gatterer H, Heinrich D & Burtscher M (2014). Resting arterial oxygen saturation and breathing frequency as predictors for acute mountain sickness development: a prospective cohort study. Sleep Breath 18, 669–674.
62. Feldman JL, Del Negro CA & Gray PA (2013). Understanding the rhythm of breathing: so near, yet so far. Annu Rev Physiol 75, 423–452.
63. 2 and hypoxia. J Appl Physiol 31, 586–592.
64. Forster HV, Haouzi P & Dempsey JA (2012). Control of breathing during exercise. Compr Physiol 2, 743–777.
65. Fowler WS (1950). Lung function studies IV. Postural changes in respiratory dead space and functional residual capacity. J Clin Invest 29, 1437–1438.
66. Frank, SM, Higgins MS., Fleisher LA, Sitzmann JV, Hershel R, & Breslow MJ (1997). Adrenergic, respiratory, and cardiovascular effects of core cooling in humans. Am J Physiol Regulatory Integrative Comp Physiol 41, R557–R562.
67. Fujii N, Honda Y, Hayashi K, Kondo N, Koga S & Nishiyasu T (2008a). Effects of chemoreflexes on hyperthermic hyperventilation and cerebral blood velocity in resting heated humans. Exp Physiol 93, 994–1001.
68. Fujii N, Honda Y, Hayashi K, Kondo N & Nishiyasu T (2008b). Effect of hypohydration on hyperthermic hyperpnea and cutaneous vasodilation during exercise in men. J Appl Physiol 105, 1509–1518.
69. Fujii N, Honda Y, Ogawa T, Tsuji B, Kondo N, Koga S & Nishiyasu T (2012). Short-term exercise-heat acclimation enhances skin vasodilation but not hyperthermic hyperpnea in humans exercising in a hot environment. Eur J Appl Physiol 112, 295–307.
70. Fujii N, Tsuji B, Honda Y, Kondo N & Nishiyasu T (2015). Effect of short-term exercise-heat acclimation on ventilatory and cerebral blood flow responses to passive heating at rest in humans. J Appl Physiol 119, 435–444.
71. Fung ML, Wang W & St-John WM (1994). Medullary loci critical for expression of gasping in adult rats. J Physiol 480, 597–611.
72. Gaitier H, Remmers JE & Bartlett D Jr (1973). Control of the duration of expiration. Resp Physiol 18, 205–221.
73. Gardner WN (1977). The relation between tidal volume and inspiratory and expiratory times during steady-state carbon dioxide inhalation in man. J Physiol 272, 591–611.
74. Gaudio R Jr & Abramson N (1968). Heat-induced hyperventilation. J Appl Physiol 25, 742–746.
75. Gaultier C, Amiel J, Dauger S, Trang H, Lyonnet S, Gallego J & Simonneau M (2004). Genetics and early disturbances of breathing control. Pediatr Res 55, 729–733.
76. Gautier H & Bonora M (1980). Possible alterations in brain monoamine metabolism during hypoxia-induced tachypnea in cats. J Appl Physiol 49, 769–777.
77. 2. J Appl Physiol 35, 903-913.
78. 2 breathing on ventilatory response to sustained hypoxia in normal adults. J Appl Physiol 66, 1071–1078.
79. Gold WM, Kessler GF & Yu DYC (1972). Role of vagus nerves in experimental asthma in allergic dogs. J Appl Physiol 33, 719–725.
80. Goode RC, Duffin J, Miller R, Romet TT, Chant W & Ackles A (1975). Sudden cold water immersion. Respir Physiol 23, 301–310.
81. Gorman JM, Kent J, Martinez J, Browne S, Coplan J & Papp L (2000). Physiological changes during carbon dioxide inhalation in patients with panic disorder, major depression, and premenstrual dysphoric disorder: evidence for a central fear mechanism. Arch Gen Psychiatry 58, 125–131.
82. Grunstein M, Younes M & Milic-Emili J (1973). Control of tidal volume and respiratory frequency in anaesthetized cats. J Appl Physiol 35, 463–476.
83. Guz A, Noble MIM, Eisele JH & Trenchard D (1970). The role of vagal inflation reflexes in man and other animals. In Ciba Foundation Symposium on Breathing: Hering-Breuer Centenary Symposium, ed. Porter R, pp. 17–40. Churchill, London.
84. Guz A & Trenchard D (1971). The role of nonmyelinated vagal afferent fibers from the lungs in the genesis of tachypnea in the rabbit. J Physiol 213, 345–371.
85. Haldane JS (1905). The influence of high air temperatures. J Hyg 5, 494–513.
86. Haldane JS, Meakins JC & Priestley JG (1919). The effects of shallow breathing. J Physiol 52, 433–453.
87. Halgren E, Walter R, Cherlow D & Crandall P (1978). Mental phenomema evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain 101, 83–117.
88. Harper RM, Frysinger RC, Trelease RB & Marks JD (1984). State-dependant alternation of respiratory cycle timing by stimulation of the central nucleus of the amygdala. Brain Res 306, 1–8.
89. Hayashi, K (2015). Ventilatory response to increasing body temperature: characteristics and effect on central fatigue. J Phys Fitness Sports Med 4, 143–149.
90. 2 on the ventilatory sensitivity to rising body temperature during exercise. J Appl Physiol 110, 1334–1341.
91. Hayashi, K, Honda Yasushi, Ogawa Takeshi, Kondo Narihiko & Nishiyasu Takeshi (2006). Relationship between ventilator response and body temperature during prolonged submaximal exercise. J Appl Physiol 100, 414–420.
92. Hayward JS & Eckerson JD (1984). Physiological responses and survival time prediction for humans in ice water. Aviat Space Environ Med 55, 206–212.
93. Hess A, Yu L, Klein I, De Mazancourt M, Jebrak G, Mal H, Brugière O, Fournier M, Courbage M, Dauriat G, Schouman-Clayes E, Clerici C & Mangin L (2013). Neural mechanisms underlying breathing complexity. PLoS One 8, e75740.
94. Hey EN, Lloyd BB, Cunningham DJC, Jukes MGM & Bolton DPG (1966). Effects of various respiratory stimuli on the depth and frequency of breathing in man. Resp Physiol 1, 193–205.
95. Heymans C, Bouckhaert JJ & Dautrebande L (1930). Sinus carotidien et reflexes respiratoires II. Influences respiratoires reflexes de l'acidose, de l'alcalose, de l'anhydride carbonique, de l'ion hydrogene et de l'anoxeme. Sinus carotidiens et echanges respiratores dans les poumons et au dela des poumons. Arch Intern Pharmacodyn 39, 400–448.
96. Hinckel P & Schroder-Rosenstock K (1981). Responses of pontine units to skin-temperature changes in the guinea-pig. J Physiol 314, 89–94.
97. Hoit JD, Lansing RW & Perona KE (2007). Speaking-related dyspnea in healthy adults. J Speech Lang Hear Res 50, 361–374.
98. Homma I & Masaoka Y (2008). Breathing rhythms and emotions. Exp Physiol 93, 1011–1021.
99. Jansen ASP, Nguyen XV, Karpitskiy V, Mettenleiter TC & Loewy AD (1995). Central command neurons of the sympathetic nervous system: basis of the fight-or flight response. Science 270, 644–646.
100. Johnson RL Jr (2000) Gas exchange efficiency in congestive heart failure. Circulation 101, 2774–2776.
101. Joris J, Cigarini M, Legrand M, Jacquet N, De Groote D, Franchimont P & Lamy M (1992). Metabolic and respiratory changes after cholecystectomy performed via laparotomy or laparoscopy. Br J Anaesth 69, 341–345.
102. Kallet RH, Alonso JA, Pittet JF & Matthay MA (2004). Prognostic value of the pulmonary dead-space fraction during the first 6 days of acute respiratory distress syndrome. Respiratory Care 49, 1008–1014.
103. Keatinge WR & Evans M (1961). The respiratory and cardiovascular response to immersion in cold and warm water. Quart J Exp Physiol 46, 83–94.
104. Keatinge WR & Nadel JA (1965). Immediate respiratory response to sudden cooling of the skin. J Appl Physiol 20, 65–69.
105. Koglin L & Kayser B (2013). Control and sensation of breathing during cycling exercise in hypoxia under naloxone: a randomised controlled crossover trial. Extreme Physiol Med 2, 1; http://extremephysiolmed.biomedcentral.com/articles/10.1186/2046-7648-2-1
106. Lahiri S, Mulligan E, Andronikou S, Shirahata M & Mokashi A (1987). Carotid body chemosensory function in prolonged normobaric hyperoxia in the cat. J Appl Physiol 62, 1924–1931.
107. Le Doux JE (1998). The Emotional Brain: The Mysterious Underpinnings of Emotional Life. Simon and Schuster, New York.
108. 2 exposure as translational cross-species experimental model for panic. Transl Psychiatry 6, e885.
109. Levitt ES, Abdala AP, Paton JF, Bissonnette JM & Williams JT (2015). μ Opioid receptor activation hyperpolarizes respiratory-controlling Kölliker-Fuse neurons and suppresses post-inspiratory drive. J Physiol 593, 4453–4469.
110. Lumsden T (1924). Effects of bulbar anaemia on respiratory movements. J Physiol 59, 1vii–1x.
111. Lunt HC, Corbett J, Barwood M & Tipton MJ (2011). Cycling cadence affects heart rate variability. Physiol Measurement 32, 1133–1145.
112. Mantoni T, Belhage B, Pedersen LM & Pott FC (2007). Reduced cerebral perfusion on sudden immersion in ice water: a possible cause of drowning. Aviat Space Environ Med 78, 374–376.
113. Mantoni T, Rasmussen JH, Belhage B & Pott FC (2008). Voluntary respiratory control and cerebral blood flow velocity upon ice-water immersion. Aviat Space Environ Med 79, 765–768.
114. Marcora SM, Bosio A & Morree HM (2008). Locomotor muscle fatigue increases cardiorespiratory responses and reduces performance during intense cycling exercise independently from metabolic stress. Am J Physiol Regul Integr Comp Physiol 294, R874–R883.
115. Martin S & Cooper KE (1978). The relationship of deep and surface skin temperature to the ventilatory responses elicited during cold water immersion. Can J Physiol Pharmacol 56, 999–1004.
116. Masaoka Y & Homma I (1997). Anxiety and respiratory pattern: their relationship during mental stress and physical load. Int J Psychophysiol 27, 153–159.
117. Masaoka Y & Homma I (2000). The source generator of respiratory-related anxiety potential in the human brain. Neurosci Lett 283, 21–24.
118. Masaoka Y & Homma I (2001). The effect of anticipatory anxiety on breathing and metabolism in humans. Respir Physiol 128, 171–177.
119. Masaoka Y & Homma I (2004). Amygdala and emotional breathing. In Post-genomic Perspectives in Modelling and Control of Breathing, ed. Champagnat J, pp. 9–14. Kluwer Academic/Plenum Publishers, New York.
120. Masaoka Y, Koiwa N & Homma I (2005). Inspiratory phase-locked alpha oscillation in human olfaction: source generators estimated by a dipole tracing method. J Physiol 566, 979–997.
121. Mateika JH, Mendello C, Obeid D & Badr MS (2004). Peripheral chemoreflex responsiveness is increased at elevated levels of carbon dioxide after episodic hypoxia in awake humans. J Appl Physiol 96, 1197–1205.
122. Mathias CJ, Low DA, Iodice V, Owens AP, Kirbis M & Grahame R (2011). Postural tachycardia syndrome – current experience and concepts. Nat Rev Neurol 8, 22–34.
123. Mead J (1960). Control of respiratory frequency. J Appl Physiol 15, 325–336.
124. Mekjavic IB, Eiken O, La Prairie A & Banister EW (1987a). The pattern of breathing during hypoxic exercise. Eur J Appl Physiol Occup Physiol 56, 619–622.
125. Mekjavic IB, La Prairie A, Burke W & Lindborg B (1987b). Respiratory drive during sudden cold water immersion. Respiratory Physiology 70, 121–130.
126. 2 in hypoxia and in high oxygen. Resp Physiol 20, 17–31.
127. Miller MJ & Tenney SM (1975). Hypoxia-induced tachypnea in carotid-deafferented cats. Respir Physiol 23, 31–39.
128. Morelli C, Badr MS & Mateika JH (2004). Ventilatory responses to carbon dioxide at low and high levels of oxygen are elevated after episodic hypoxia in men compared with women. J Appl Physiol 97, 1673–1680.
129. Murias G, Blanch L & Lucangelo U (2014). The physiology of ventilation. Respiratory Care 59, 1795–1807.
130. Natalino MR, Zwillich CW & Weil JV (1977). Effects of hyperthermia on hypoxic ventilatory response in normal man. J Lab Clin Med 89, 564–572.
131. Nattie E & Li A (2009). Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol 106, 1464–1466.
132. Nielsen B & Nybo L (2003). Cerebral changes during exercise in the heat. Sports Med 33, 1–11.
133. Nelson MD, Haykowsky MJ, Stickland MK, Altamirano-Diaz LA, Willie CK, Smith KJ, Petersen SR & Ainslie PN (2011). Reductions in cerebral blood flow during passive heat stress in humans: partitioning the mechanisms. J Physiol 589, 4053–4064.
134. Niccolai V, van Duinen M & Griez E (2009). Respiratory patterns in panic disorder reviewed: a focus on biological challenge tests [Review]. Acta Psychiatr Scand 120, 167–177.
135. Nicolo A, Bazzucchi I, Haxhi J, Felici F & Sacchetti M (2014). Comparing continuous and intermittent exercise: an “isoeffort” and “isotime” approach. PLoS One 9, e94990.
136. Nicolo A, Marcora SM & Sacchetti M (2016). Respiratory frequency is strongly associated with perceived exertion during time trials of different duration. J Sports Sci 34, 1199–1206.
137. Noble BJ, Metz KF, Pandolf KB & Cafarelli E (1973). Perceptual response to exercise: a multiple regression study. Med Sci Sports 5, 104–109.
138. Nuckton TJ, Alonso JA, Kallet RH, Daniel BM, Pittet JF, Eisner MD & Matthay MA. (2002). Pulmonary dead-space fraction as a risk factor for death in the acute respiratory distress syndrome. New Eng J Med 346, 1281–1286.
139. Nunn JF, Campbell EJ & Peckett BW (1959). Anatomical subdivisions of the volume of respiratory dead space and effect of position of the jaw. J Appl Physiol 14, 174–176.
140. 2 homeostasis is maintained in conscious humans by regulation of tidal volume, but not of respiratory rhythm. Respir Physiol Neurobiol 186, 155–163.
141. Olson LJ, Arruda-Olson AM, Somers VK, Scott CG & Johnson BD (2008). Exercise oscillatory ventilation: instability of breathing control associated with advanced heart failure. Chest 133, 474–481.
142. Papp LA, Martinez JM, Klein DF, Coplan JD, Norman RG, Cole R & de Jesus MJ (1997). Respiratory psychophysiology of panic disorder: three respiratory challenges in 98 subjects. Am J Psychiatry 154, 1557–1565.
143. Pascoe JP & Kapp BS (1985). Electrophysiological characteristics of amygdaloid central nucleus neurons during Pavlovian fear conditioning in the rabbit. Behav Brain Res 16, 117–133.
144. Paton JF, Abdala AP, Koizumi H, Smith JC & St-John WM (2006). Respiratory rhythm generation during gasping depends on persistent sodium current. Nat Neurosci 9, 311–313.
145. Pearson SB & Cunningham DJC (1973). Some observations on the relation between ventilation, tidal volume and frequency in man in various steady and transient states. Acta Neurobiol 33, 177–188.
146. Perez W & Tobin MJ (1985). Separation of factors responsible for changing breathing pattern induced by instrumentation. J Appl Physiol 59, 1515–1520.
147. Petersen ES & Vejby-Christensen H (1977). Effects of body temperature on ventilatory response to hypoxia and breathing pattern in man. J Appl Physiol 42, 492–500.
148. Phillipson ES (1978). Control of breathing during sleep. Am Rev Respir Dis 118, 909–939.
149. Pine DS, Coplan JD, Papp LA, Klein RG, Martinez JM, Kovalenko P, Tancer N, Moreau D, Dummit ES 3rd, Shaffer D, Klein DF & Gorman JM (1998). Ventilatory physiology of children and adolescents with anxiety disorders. Arch Gen Psychiatry 55, 123–129.
150. Pine DS, Klein, RG, Coplan JD, Papp LA, et al. (2000). Differential carbon dioxide sensitivity in childhood anxiety disorders and non-ill comparison group. Arch Gen Psychiatry 57, 960–967.
151. Ponikowski P, Chua TP, Anker SD, Francis DP, Doehner W, Banasiak W, Poole-Wilson PA, Piepoli MF & Coats AJ (2001). Peripheral chemoreceptor hypersensitivity: an ominous sign in patients with chronic heart failure. Circulation 104, 544–549.
152. Prabhakar NR (2000). Oxygen sensing by the carotid body chemoreceptors. J Appl Physiol 88, 2287–2295.
153. Puthon L, Bouzat P, Rupp T, Robach P, Favre-Juvin A & Verges S (2016). Physiological characteristics of elite high-altitude climbers. Scand J Med Sci Sports. 26, 1052–1059.
154. Raurich JM, Vilar M, Colomar A, Ibanez J, Ayestaran I, Perez-Barcena J & Llompart-Pou JA (2010). Prognostic value of the pulmonary dead-space fraction during the early and intermediate phases of acute respiratory distress syndrome. Respiratory Care 55, 282–287.
155. Rebuck AS, Rigg JRA & Saunders NS (1976). Respiratory frequency response to progressive isocapnic hypoxia. J Physiol 258, 19–31.
156. Reiman EM, Fusselman MJ, Fox PT & Raichle ME (1989). Neuroanatomical correlates of anticipatory anxiety. Science 243, 1071–1074.
157. Richard NA & Koehle MS (2012). Differences in cardio-ventilatory responses to hypobaric and normobaric hypoxia: a review. Aviat Space Environ Med 83, 677–84.
158. Richard NA, Sahota IS, Widmer N, Ferguson S, Sheel AW & Koehle MS (2014). Acute mountain sickness, chemosensitivity, and cardiorespiratory responses in humans exposed to hypobaric and normobaric hypoxia. J Appl Physiol 116, 945–952.
159. Richter DW (1982). Generation and maintenance of the respiratory rhythm. J Exp Biol 100, 93–107.
160. Rigg JR, Inman EM, Saunders NA, Leeder SR & Jones NL (1977). Interaction of mental factors with hypercapnic ventilatory drive in man. Clin Sci Mol Med 52, 269–275.
161. Robertshaw D (2006). Mechanisms for the control of respiratory evaporative heat loss in panting animals. J Appl Physiol 101, 664–668.
162. Rosenberg M, Tobias R, Bourke D & Kamat V (1980). Respiratory responses to surgical stimulation during enflurane anesthesia. Anesthesiology 52, 166–167.
163. Sarton E, Dahan, A, Teppema L, Berkenbosch A, van den Elsen M & van Kleef J (1997). Influence of acute pain induced by activation of cutaneous nociceptors on ventilatory control. Anaesthesiology 87, 289–296.
164. Savourey G, Launay JC, Besnard Y, Guinet-Lebreton A, Alonso A, et al. (2007). Normo or hypobaric hypoxic tests: propositions for the determination of the individual susceptibility to altitude illnesses. Eur J Appl Physiol 100, 193–205.
165. Savourey G, Launay JC, Besnard Y, Guinet A & Travers S (2003). Normo and hypobaric hypoxia: are there any physiological differences? Eur J Appl Physiol 89, 122–6.
166. Schoene RB (2001). Limits of human lung function at high altitude. J Exp Biol 204, 3121–3127.
167. Schoene RB, Lahiri S, Hackett PH, et al. (1984). Relationship of hypoxic ventilatory response to exercise performance on Mount Everest. J Appl Physiol 56, 1478–1483.
168. Schondorf R & Low PA (1993). Idiopathic postural orthostatic tachycardia syndrome: An attenuated form of acute pandysautonomia? Neurology 43, 132–137.
169. Sheel AW & Romer LM (2012). Ventilation and respiratory mechanics. Compr Physiol 2, 1093–1142.
170. Simone DA & Kajander KC (1997). Responses of cutaneous A-fiber nociceptors to noxious cold. J Neurophysiol 77, 2049–2060.
171. Simonova TG & Kozyreva TV (1994). Respiratory response to local skin cooling at artificial modulation of skin thermoreceptors. Proc Sixth Int Conf on Environmental Ergonomics 38–39.
172. Schmidt C, Bellingham MC & Richter DW (1995). Adenosinergic modulation of respiratory neurones and hypoxic responses in the anaesthetized cat. J Physiol 483, 769–781.
173. Smith JC, Abdala AP, Borgmann A, Rybak IA & Paton JF (2013). Brainstem respiratory networks: building blocks and microcircuits. Trends Neurosci 36, 152–162.
174. Smith JC, Abdala AP, Koizumi H, Rybak IA & Paton JF (2007). Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol 98, 3370–3387.
175. Smith JC, Abdala AP, Rybak IA & Paton JF (2009). Structural and functional architecture of respiratory networks in the mammalian brainstem. Philos Trans R Soc Lond B Biol Sci 364, 2577–2587.
176. St-John WM (1998). Neurogenesis of patterns of automatic ventilatory activity. Prog Neurobiol 56, 97–117.
177. St-John WM, Bledsoe TA & Sokol HW (1984). Identification of medullary loci critical for neurogenesis of gasping. J Appl Physiol 59, 1008–1019.
178. St-John WM & Paton JF (2003). Defining eupnoea. Respir Physiol Neurobiol 139, 97–103.
179. St-John WM & Paton JF (2004). Role of pontile mechanisms in the neurogenesis of eupnoea. Respir Physiol Neurobiol 143, 321–332.
180. St-John WM, Stornetta RL, Guyenet PG & Paton JF (2009). Location and properties of respiratory neurones with putative intrinsic bursting properties in the rat in situ. J Physiol 587, 3175–3188.
181. Subramanian HH & Holstege G (2014). The midbrain periaqueductal gray changes the eupneic respiratory rhythm into a breathing pattern necessary for survivial of the individual and of the species. Prog Brain Res 212, 351–384.
182. Suess WM, Alexander AB, Smith DD, Sweeney HW & Marion RJ (1980). The effects of psychological stress on respiration: a preliminary study of anxiety and hyperventilation. Psychophysiology 17, 535–540.
183. 2-sensitive neurons in rats. J Physiol 572, 503–523.
184. Tarbichi AG, Rowley JA, Shkoukani MA, Mahadevan K & Badr MS (2003). Lack of gender difference in ventilatory chemoresponsiveness and post-hypoxic ventilatory decline. Respir Physiol Neurobiol 137, 41–50.
185. Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RA & Updegraff JA (2000). Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 107, 411–429.
186. Teppema LJ & Dahan A (2010). The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiol Rev 90, 675–754.
187. Thornton JM, Guz A, Murphy K, Griffin AR, Pedersen DL, Kardos A, Leff A, Adams L, Casadei B & Paterson DJ (2001). Identification of higher rain centres that may encode the cardiorespiratory response to exercise in humans. J Physiol 533, 823–836.
188. Timmers HJ, Wieling W, Karemaker MJ & Lenders JW (2003). Denervation of carotid baro- and chemoreceptors in humans. J Physiol 553, 3–11.
189. Timms RJ (1981). A study of the amygdaloid defence reaction showing the value of Althesin anaesthesia in studies of the functions of the fore-brain in cats. Pflugers Arch 391, 49–56.
190. Tipton MJ (1989). The initial responses to cold-water immersion in man. Clin Sci 77, 581–588.
191. Tipton MJ & Golden FS (1987). The influence of regional insulation on the initial responses to cold immersion. Aviat Space Environ Med 58, 1192–1196.
192. Tipton MJ, Kadinopoulos P, Roiz de Sa D & Barwood MJ (2017). Changes in lung function during exercise are independently mediated by increases in deep body temperature. BMJ Open Sport & Exercise Medicine, https://doi.org/10.1136/bmjsem-2016-000210
193. Tipton MJ, Stubbs DA & Elliott DH (1991). Human initial responses to immersion in cold water at 3 temperatures and following hyperventilation. J Appl Physiol 70, 317–322.
194. Todd AJ, Spike RC, Young S & Puskar Z (2005). Fos induction in lamina I projection neurons in response to noxious thermal stimuli. Neuroscience 131, 209–217.
195. Tracey I & Dickenson A (2012). SnapShot: pain perception. Cell 148, 1308–1308.
196. Tracey I & Mantyh P (2007). The cerebral signature for pain perception and its modulation [Review]. Neuron 55, 377–391.
197. Trenchard D & Guz A (1972). Role of pulmonary vagal afferent nerve fibers in the development of rapid shallow breathing in lung inflammation. Clin Sci 42, 251–263.
198. Tsuji B, Honda Y, Fujii N, Kondo N & Nishiyasu T (2012a). Effect of initial core temperature on hyperthermic hyperventilation during prolonged submaximal exercise in the heat. Am J Physiol Regul Integr Comp Physiol 302, R94–R102.
199. Tsuji B, Honda Y, Fujii N, Kondo N & Nishiyasu T (2012b). Comparison of hyperthermic hyperventilation during passive heating and prolonged light and moderate exercise in the heat. J Appl Physiol 113, 1388–1397.
200. Tsuji B, Hayashi K, Kondo N & Nishiyashi T (2016). Characteristics of hyperthermia-induced hyperventilation in humans. Temperature 3, 146–160.
201. Van Diest I, Winters W, Devriese S, Vercamst E, Han JN, Van de Woestijne KP & Van den Bergh O (2001). Hyperventilation beyond fight/flight: respiratory responses during emotional imagery. Psychophysiology 38, 961–968.
202. Van Klaveren RJ & Demedts M (1998). Determinants of the hypercapnic and hypoxic response in normal man. Respir Physiol 113, 157–165.
203. 2 response in man. Respir Physiol 19, 322–332.
204. 2 response in man. Bull Physiopathol Respir 9, 672–675.
205. von Euler C (1983). On the central pattern generator for the basic breathing rhythmicity. J Appl Physiol Respir Environ Exerc Physiol 55, 1647–1659
206. von Euler C & Trippenbach T (1976). Excitability changes of the inspiratory “off-switch” mechanism tested by electrical stimulation in nucleus parabrachialis in the cat. Acta Physiol Scand 97, 175–188.
207. von Leupoltd A, Sommer T, Kegat S, Baumann HJ, Klose H, Dahme B & Buchel C (2009). Dyspnea and pain share emotion-related brain network. Neuroimage 48, 200–206.
208. Wagner JA & Horvath SM (1985). Influences of age and gender on human thermoregulatory responses to cold exposures. J Appl Physiol 58, 180–186.
209. Waldrop TG, Millhorn DE, Eldridge FL & Klingler LE (1984). Respiratory responses to noxious and nonnoxious heating of skin in cats. J Appl Physiol 57, 1738–1741.
210. Ward LM (2002). Synchronous neural oscillations and cognitive processes. Trends in cognitive sciences 7, 553–559.
211. Weese-Mayer DE, Berry-Kravis EM, Zhou L, Maher BS, Silvestri JM, Curran ME & Marazita ML (2003). Idiopathic congenital central hypoventilation syndrome: analysis of genes pertinent to early autonomic nervous system embryologic development and identification of mutations in PHOX2b. Am J Med Genet A 123A, 267–278.
212. Weissman C, Askanazi J, Forse RA, Hyman AI, Milic-Emili J & Kinney JM (1986). The metabolic and ventilatory response to the infusion of stress hormones. Ann Surg 203, 408–412.
213. West JB (2012). The physiological legacy of the Fenn, Rahn, and Otis school. Am J Physiol Lung Cell Mol Physiol 303, L845–L851.
214. Whipp BJ (1984). Carotid bodies and breathing in humans. Thorax 49, 1081–1084.
215. White MD (2006). Components and mechanisms of thermal hyperpnea. J Appl Physiol 101, 655–663.
216. Whitelaw WA & Derenne JP (1993). Airway occlusion pressure. J Appl Physiol 74, 1475–1483.
217. Whitelaw WA, Derenne J-P & Milic-Emili J (1975). Occlusion pressure as a measure of respiratory centre output in conscious man. Resp Physiol 23, 181–199.
218. Widdicombe JG (1964). Respiratory reflexes. In Handbook of Physiology, section 2, vol. 1. eds Fenn WO & Rahn H, pp. 585–630. American Physiological Society, Washington DC.
219. Widdicombe JG & Winning A (1974). Effects of hypoxia, hypercapnia and changes in body temperature on the pattern of breathing in cats. Resp Physiol 21, 203–221.
220. Wilhelm FH, Gevirtz R & Roth WT (2001). Respiratory dysregulation in anxiety, functional cardiac, and pain disorders. Assessment, phenomenology, and treatment. Behaviour Modification 25, 513–545.
221. Williamson JW, Fadel PJ & Mitchell JH (2006). New insights into central cardiovascular control during exercise in humans: a central command update. Exp Physiol 91, 51–58.
222. Willer JC (1975). The influence of anticipation of pain on heart and respiratory rates and on the pain reflex in man [in French: Influence de l'anticipation de la douleur sur les frequencies cardiaque et respiratoire et sur le reflexe nociceptive chez l'homme]. Physiology and Behaviour 15, 411–415.
223. Winters PM, McCabe PM, Green EJ & Schneiderman N (2000). Stress responses, coping, and cardiovascular neurobiology: central nervous system circuitry underlying learned and unlearned affective responses to stressful stimuli. In Stress, Coping and Cardiovascular Disease. eds Mccabe P, Schneiderman N, Field TM & Wellens AR.pp. 1–49. Routledge, UK.
224. Younes MK & Remmers JE (1981). Control of tidal volume and respiratory frequency. In Regulation of Breathing, part 1, vol.17, ed. Hornbein TF, pp. 621–671. Marcel Dekker, New York.
225. Zoccal DB, Simms AE, Bonagamba LG, Braga VA, Pickering AE, Paton JF & Machado BH (2008). Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J Physiol 586, 3253–3265.