Effects of hypercapnia and hypocapnia on ventilatory variability and the chaotic dynamics of ventilatory flow in humans

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 5, 2007, Pages

  Fiamma, Marie Noëlle ^a   Straus, Christian ^a,b   Thibault, Sylvain ^c   Wysocki, Marc ^a,d   Baconnier, Pierre ^c   Similowski, Thomas ^a,b,e  

^a SORBONNE UNIVERSITÉ   (France)

^b Necker Children s Hospital   (France)

^c UNIV GRENOBLE ALPES   (France)

^d HAMILTON MEDICAL AG   (Switzerland)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Breathing variability; Chaos; Nonlinear analysis; Respiratory control

Indexed keywords

CARBON DIOXIDE;

ADULT; ARTICLE; BREATHING MECHANICS; CHAOTIC DYNAMICS; CHEMORECEPTOR; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPERCAPNIA; HYPERVENTILATION; HYPOCAPNIA; LUNG VENTILATION; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; RESPIRATION CONTROL; SENSITIVITY ANALYSIS; TITRIMETRY;

EID: 34248196454     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00792.2006     Document Type: Article

References (74)

1. Acharya UR, Faust O, Kannathal N, Chua T, Laxminarayan S. Non-linear analysis of EEG signals at various sleep stages. Comput Methods Programs Biomed 80: 37-45, 2005.
2. Akaike H. A new look at the statistical model identification. IEEE Trans Automatic Control 19: 716-723, 1974.
3. Bar M, Hagberg A, Meron E, Thiele U. Front propagation and pattern formation in anisotropic bistable media. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 62: 366-374, 2000.
4. Barahona M, Poon CS. Detection of nonlinear dynamics in short, noisy time series. Nature 381: 215-217, 1996.
5. Briggs K. An improved method for estimating Lyapunov exponents of chaotic time series. Phys Lett 151: 27-32, 1990.
6. Bunn JC, Mead J. Control of ventilation during speech. J Appl Physiol 31: 870-872, 1971.
7. Burioka N, Cornelissen G, Halberg F, Kaplan DT. Relationship between correlation dimension and indices of linear analysis in both respiratory movement and electroencephalogram. Clin Neurophysiol 112: 1147-1153, 2001.
8. Burioka N, Cornelissen G, Halberg F, Kaplan DT, Suyama H, Sako T, Shimizu E. Approximate entropy of human respiratory movement during eye-closed waking and different sleep stages. Chest 123: 80-86, 2003.
9. Burioka N, Suyama H, Sako T, Miyata M, Takeshima T, Endo M, Kurai J, Fukuoka Y, Takata M, Nomura T, Nakashima K, Shimizu E. Non-linear dynamics applied to human respiratory movement during sleep. Biomed Pharmacother 56, Suppl 2: 370s-373s, 2002.
10. BuSha BF, Stella MH. State and chemical drive modulate respiratory variability. J Appl Physiol 93: 685-696, 2002.
11. Calabrese P, Dinh TP, Eberhard A, Bachy JP, Benchetrit G. Effects of resistive loading on the pattern of breathing. Respir Physiol 113: 167-179, 1998.
12. Colebatch JG, Adams L, Murphy K, Martin AJ, Lammertsma AA, Tochon-Danguy HJ, Clark JC, Friston KJ, Guz A. Regional cerebral blood flow during volitional breathing in man. J Physiol 443: 91-103, 1991.
13. Corfield DR, Morrell MJ, Guz A. The nature of breathing during hypocapnia in awake man. Respir Physiol 101: 145-159, 1995.
14. Datta AK, Shea SA, Horner RL, Guz A. The influence of induced hypocapnia and sleep on the endogenous respiratory rhythm in humans. J Physiol 440: 17-33, 1991.
15. Del Negro CA, Wilson CG, Butera RJ, Rigatto H, Smith JC. Periodicity, mixed-mode oscillations, and quasiperiodicity in a rhythm-generating neural network. Biophys J 82: 206-214, 2002.
16. Donaldson GC. The chaotic behaviour of resting human respiration. Respir Physiol 88: 313-321, 1992.
17. El-Khatib M, Jamaleddine G, Soubra R, Muallem M. Pattern of spontaneous breathing: potential marker for weaning outcome. Spontaneous breathing pattern and weaning from mechanical ventilation. Intensive Care Med 27: 52-58, 2001.
18. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7: 232-242, 2006.
19. Ferri R, Pettinato S, Nobili L, Billiard M, Ferrillo F. Correlation dimension of EEG slow-wave activity during sleep in narcoleptic patients under bed rest conditions. Int J Psychophysiol 34: 37-43, 1999.
20. Fiamma MN, Samara Z, Baconnier P, Similowski T, Straus C. Respiratory inductive plethysmography to assess respiratory variability and complexity in humans. Respir Physiol Neurobiol 56: 234-239, 2007.
21. Fink BR. Influence of cerebral activity in wakefulness on regulation of breathing. J Appl Physiol 16: 15-20, 1961.
22. Foerster D. Motorische felder und bahnen. In: Handbuch der Neurologie, Band 6, edited by Bumke A and Foerster O. Berlin: Springer, 1936, p. 50-51.
23. Gandevia SC, Rothwell JC. Activation of the human diaphragm from the motor cortex. J Physiol 384: 109-118, 1987.
24. Garde S, Regalado MG, Schechtman VL, Khoo MC. Nonlinear dynamics of heart rate variability in cocaine-exposed neonates during sleep. Am J Physiol Heart Circ Physiol 280: H2920-H2928, 2001.
25. Grassberger P, Procaccia I. Characterization of strange attractors. Phys Rev Lett 50: 346-349, 1983.
26. Hongre L, Sailhac P, Alexandrescu M, Dubois J. Nonlinear and multifractals approaches of the geomagnetic field. Phys Earth Planetary Interiors 110: 157-190, 1999.
27. 2 responsiveness. A study of the unloaded respiratory pump in humans. Am Rev Respir Dis 144: 1125-1129, 1991.
28. Jubran A, Grant BJ, Tobin MJ. Effect of hyperoxic hypercapnia on variational activity of breathing. Am J Respir Crit Care Med 156: 1129-1139, 1997.
29. Kikuchi A, Shimizu T, Hayashi A, Horikoshi T, Unno N, Kozuma S, Taketani Y. Nonlinear analyses of heart rate variability in normal and growth-restricted fetuses. Early Hum Dev 82: 217-226, 2006.
30. Liebert W, Pawelzik K, Schuster HG. Optimal embeddings of chaotic attractors from topological considerations. Europhys Lett 14: 521-526, 1991.
31. Lin KH, Wu HD, Chang CW, Wang TG, Wang YH. Ventilatory and mouth occlusion pressure responses to hypercapnia in chronic tetraplegia. Arch Phys Med Rehabil 79: 795-799, 1998.
32. Macefield G, Gandevia SC. The cortical drive to human respiratory muscles in the awake state assessed by premotor cerebral potentials. J Physiol 439: 545-558, 1991.
33. Matsugu M, Duffin J, Poon CS. Entrainment, instability, quasi-periodicity, and chaos in a compound neural oscillator. J Comput Neurosci 5: 35-51, 1998.
34. Mehiri S, Straus C, Arnulf I, Attali V, Zelter M, Derenne JP, Similowski T. Responses of the diaphragm to transcranial magnetic stimulation during wake and sleep in humans. Respir Physiol Neurobiol 154: 406-418, 2006.
35. Meyer-Lindenberg A. The evolution of complexity in human brain development: an EEG study. Electroencephalogr Clin Neurophysiol 99: 405-411, 1996.
36. Miyata M, Burioka N, Sako T, Suyama H, Fukuoka Y, Tomita K, Higami S, Shimizu E. A short daytime test using correlation dimension for respiratory movement in OSAHS. Eur Respir J 23: 885-890, 2004.
37. Miyata M, Burioka N, Suyama H, Sako T, Nomura T, Takeshima T, Higami S, Shimizu E. Non-linear behaviour of respiratory movement in obstructive sleep apnoea syndrome. Clin Physiol Funct Imaging 22: 320-327, 2002.
38. Modarreszadeh M, Bruce EN, Gothe B. Nonrandom variability in respiratory cycle parameters of humans during stage 2 sleep. J Appl Physiol 69: 630-639, 1990.
39. Patzak A, Schluter B, Mrowka R, Unbehaun A, Gerhardt D, Persson PB, Barschdorff D, Trowitzsch E. Rhythms and complexity of respiration during sleep in pre-term infants. Clin Physiol 19: 458-466, 1999.
40. Pereda E, Gamundi A, Nicolau MC, Rial R, Gonzalez J. Interhemispheric differences in awake and sleep human EEG: a comparison between non-linear and spectral measures. Neurosci Lett 263: 37-40, 1999.
41. Pilgram B, Schappacher W, Loscher WN, Pfurtscheller G. Application of the correlation integral to respiratory data of infants during REM sleep. Biol Cybern 72: 543-551, 1995.
42. Pincus SM. Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 88: 2297-2301, 1991.
43. Pincus SM, Goldberger AL. Physiological time-series analysis: what does regularity quantify? Am J Physiol Heart Circ Physiol 266: H1643-H1656, 1994.
44. Plum F, Brown HW, Snoep E. Neurologic significance of posthyperventilation apnea. JAMA 181: 1050-1055, 1962.
45. Poon CS, Barahona M. Titration of chaos with added noise. Proc Natl Acad Sci USA 98: 7107-7112, 2001.
46. Priban IP. An analysis of some short-term patterns of breathing in man at rest. J Physiol 166: 425-434, 1963.
47. 2. Bull Eur Physiopathol Respir 15 Suppl: 75-83, 1979.
48. Raux M, Straus C, Redolfi S, Morelot-Panzini C, Couturier A, Hug F, Similowski T. Electroencephalographic evidence for premotor cortex activation during inspiratory loading in humans. J Physiol 578: 569-578, 2007.
49. Rebuck AS, Slutsky AS. Measurement of ventilatory responses to hypercapnia and hypoxia.. In: Regulation of Breathing. Part II, edited by Hornbein TF. New York: Marcel Dekker, 1981.
50. Remmers J. Central control of breathing. In: Control of Breathing in Health and Disease, edited by Altose MD and Kawakami Y. New York: Marcel Dekker, 1999.
51. Rosenstein M, Collins J, De Luca C. A practical method for calculating largest Lyapunov exponents for small data sets. Physica D 65: 117-134, 1993.
52. Rotstein A, Meckel Y, Inbar O. Perceived speech difficulty during exercise and its relation to exercise intensity and physiological responses. Eur J Appl Physiol 92: 431-436, 2004.
53. Sako T, Burioka N, Suyama H, Nomura T, Takeshima T, Shimizu E. Nonlinear behavior of human respiratory movement during different sleep stages. Chronobiol Int 18: 71-83, 2001.
54. Sammon M, Romaniuk JR, Bruce EN. Bifurcations of the respiratory pattern associated with reduced lung volume in the rat. J Appl Physiol 75: 887-901, 1993.
55. Sammon MP, Bruce EN. Vagal afferent activity increases dynamical dimension of respiration in rats. J Appl Physiol 70: 1748-1762, 1991.
56. Savino GV, Romanelli L, Gonzalez DL, Piro O, Valentinuzzi ME. Evidence for chaotic behavior in driven ventricles. Biophys J 56: 273-280, 1989.
57. Sharshar T, Hopkinson NS, Jonville S, Prigent H, Carlier R, Dayer MJ, Swallow EB, Lofaso F, Moxham J, Polkey MI. Demonstration of a second rapidly conducting cortico-diaphragmatic pathway in humans. J Physiol 560: 897-908, 2004.
58. Shea SA. Behavioural and arousal-related influences on breathing in humans. Exp Physiol 81: 1-26, 1996.
59. Similowski T, Catala M, Rancurel G, Derenne JP. Impairment of central motor conduction to the diaphragm in stroke. Am J Respir Crit Care Med 154: 436-441, 1996.
60. Skatrud JB, Dempsey JA. Interaction of sleep state and chemical stimuli in sustaining rhythmic ventilation. J Appl Physiol 55: 813-822, 1983.
61. Small M, Judd K, Lowe M, Stick S. Is breathing in infants chaotic? Dimension estimates for respiratory patterns during quiet sleep. J Appl Physiol 86: 359-376, 1999.
62. Stanley NN, Cunningham EL, Altose MD, Kelsen SG, Levinson RS, Cherniack NS. Evaluation of breath holding in hypercapnia as a simple clinical test of respiratory chemosensitivity. Thorax 30: 337-343, 1975.
63. Storella RJ, Wood HW, Mills KM, Kanters JK, Hojgaard MV, Holstein-Rathlou NH. Approximate entropy and point correlation dimension of heart rate variability in healthy subjects. Integr Physiol Behav Sci 33: 315-320, 1998.
64. Straus C, Locher C, Zelter M, Derenne JP, Similowski T. Facilitation of the diaphragm response to transcranial magnetic stimulation by increases in human respiratory drive. J Appl Physiol 97: 902-912, 2004.
65. Suyama H, Burioka N, Sako T, Miyata M, Shimizu E. Reduction of correlation dimension in human respiration by inhaling a mixture gas of 5% carbon dioxide and 95% oxygen. Biomed Pharmacother 57, Suppl 1: 116s-121s, 2003.
66. Swanson GD, Ward DS, Bellville JW. Posthyperventilation isocapnic hyperpnea. J Appl Physiol 40: 592-596, 1976.
67. Takens F. Detecting strange attractors in turbulence. LS Young Springer: dynamical systems and turbulence. Lecture Notes Math Berlin 898: 366-381, 1980.
68. Thibault S, Calabrese P, Benchetrit G, Baconnier P. Effects of resistive loading on breathing variability non linear analysis and modelling approaches. Adv Exp Med Biol 551: 293-298, 2004.
69. Tobin MJ, Mador MJ, Guenther SM, Lodato RF, Sackner MA. Variability of resting respiratory drive and timing in healthy subjects. J Appl Physiol 65: 309-317, 1988.
70. Wagner CD, Mrowka R, Nafz B, Persson PB. Complexity and "chaos" in blood pressure after baroreceptor denervation of conscious dogs. Am J Physiol Heart Circ Physiol 269: H1760-H1766, 1995.
71. Wolf A, Swift J, Swinney H, Vastano J. Determining Lyapunov exponents from a time series. Physica D 16: 285-317, 1985.
72. Wysocki M, Fiamma M, Straus C, Poon CS, Similowski T. Chaotic dynamics of resting ventilatory flow in humans assessed through noise titration. Respir Physiol Neurobiol 153: 54-65, 2006.
73. Wysocki M, Fiamma MN, Straus C, Sang Poon C, Similowski T. Chaotic dynamics of ventilatory flow in humans. Conf Proc IEEE Eng Med Biol Sci 1: 759-762, 2005.
74. Yeragani VK, Radhakrishna RK, Tancer M, Uhde T. Nonlinear measures of respiration: respiratory irregularity and increased chaos of respiration in patients with panic disorder. Neuropsychobiology 46: 111-120, 2002.