Perinatal maturation of the respiratory rhythm generator in mammals: From experimental results to computational simulation

Respiratory Physiology and Neurobiology

Volumn 149, Issue 1-3, 2005, Pages 17-27

  Achard, Pablo ^a,b,c   Zanella, Sébastien ^b   Rodriguez, Roger ^a   Hilaire, Gérard ^b  

^a CENTRE DE PHYSIQUE THÉORIQUE   (France)

^b CNRS   (France)

^c UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Pacemaker neurones; PreB tzinger complex; Respiratory network; Synaptic noise

Indexed keywords

AMINE;

ARTICLE; BIOLOGICAL RHYTHM; BRAIN REGION; CENTRAL NERVOUS SYSTEM FUNCTION; CHEMOSENSITIVITY; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; FETUS BREATHING; GESTATIONAL AGE; HUMAN; HYPOTHALAMUS; HYPOXIA; LAMB; MAMMAL; MODEL; NERVE CELL; NEUROMODULATION; NOISE; NONHUMAN; PACEMAKER; PERINATAL DEVELOPMENT; POSTNATAL DEVELOPMENT; PREGNANCY; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; RESPIRATION CENTER; RESPIRATION CONTROL; SIMULATION; SODIUM CONDUCTANCE;

ANIMALS; ANIMALS, NEWBORN; COMPUTER SIMULATION; HUMANS; INFANT, NEWBORN; PERIODICITY; RESPIRATORY CENTER; RESPIRATORY PHYSIOLOGY;

EID: 26044474487     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2005.01.015     Document Type: Article

References (65)

1. O.S. Bamford, G.S. Dawes, and R.A. Ward Effects of apomorphine and haloperidol in fetal lambs J. Physiol. 377 1986 37 47
2. B. Blanchi, L.M. Kelly, J.C. Viemari, I. Lafon, H. Burnet, M. Bevengut, S. Tillmanns, L. Daniel, T. Graf, G. Hilaire, and M.H. Sieweke MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth Nat. Neurosci. 6 2003 1091 1100
3. C.E. Blanco Maturation of fetal breathing activity Biol. Neonate 65 1994 182 188
4. R.J. Butera Jr., J. Rinzel, and J.C. Smith Models of respiratory rhythm generation in the pre-Botzinger complex. II. Populations of coupled pacemaker neurons J. Neurophysiol. 82 1999 398 415
5. R.J. Butera Jr., J. Rinzel, and J.C. Smith Models of respiratory rhythm generation in the pre-Botzinger complex. I. Bursting pacemaker neurons J. Neurophysiol. 82 1999 382 397
6. I.R. Cooke, and P.J. Berger Precursor of respiratory pattern in the early gestation mammalian fetus Brain Res. 522 1990 333 336
7. I.R. Cooke, and P.J. Berger Development of patterns of activity in diaphragm of fetal lamb early in gestation J. Neurobiol. 30 1996 385 396
8. E.V. Cosmi, E. Cosmi, and R. La Torre The effects of fetal breathing movements on the utero-fetal-placental circulation Early Pregnancy 5 2001 51 52
9. E.V. Cosmi, M.M. Anceschi, E. Cosmi, J.J. Piazze, and R. La Torre Ultrasonographic patterns of fetal breathing movements in normal pregnancy Int. J. Gynaecol. Obstet. 80 2003 285 290
10. K.J. Dalton, G.S. Dawes, and J.E. Patrick Diurnal, respiratory, and other rhythms of fetal heart rate in lambs Am. J. Obstet. Gynecol. 127 1977 414 424
11. G.S. Dawes, W.N. Gardner, B.M. Johnston, and D.W. Walker Breathing in fetal lambs: the effect of brain stem section J. Physiol. 335 1983 535 553
12. G. De Vries, and Sherman A Channel sharing in pancreatic beta-cells revisited: enhancement of emergent bursting by noise J. Theor. Biol. 207 2000 513 530
13. C.A. Del Negro, C. Morgado-Valle, and J.L. Feldman Respiratory rhythm: an emergent network property? Neuron 34 2002 821 830
14. C.A. Del Negro, S.M. Johnson, R.J. Butera, and J.C. Smith Models of respiratory rhythm generation in the pre-Botzinger complex. III. Experimental tests of model predictions J. Neurophysiol. 86 2001 59 74
15. C.A. Del Negro, N. Koshiya, R.J. Butera Jr., and J.C. Smith Persistent sodium current, membrane properties and bursting behavior of pre-botzinger complex inspiratory neurons in vitro J. Neurophysiol. 88 2002 2242 2250
16. E. Di Pasquale, R. Monteau, and G. Hilaire In vitro study of central respiratory-like activity of the fetal rat Exp. Brain Res. 89 1992 459 464
17. E. Di Pasquale, R. Monteau, and G. Hilaire Endogenous serotonin modulates the fetal respiratory rhythm: an in vitro study in the rat Brain Res. Dev. Brain Res. 80 1994 222 232
18. E. Di Pasquale, R. Monteau, and G. Hilaire Involvement of the rostral ventro-lateral medulla in respiratory rhythm genesis during the peri-natal period: an in vitro study in newborn and fetal rats Brain Res. Dev. Brain Res. 78 1994 243 252
19. C. Endo, K. Fujimori, A. Takanashi, T. Ishida, J. Yamada, A. Sato, and Y. Murata Endocrinological and biophysical responses to further reduction in oxygenation following sustained hypoxemia in fetal goats J. Matern. Fetal. Med. 8 1999 184 189
20. J.L. Feldman, and J.C. Smith Cellular mechanisms underlying modulation of breathing pattern in mammals Ann. N. Y. Acad. Sci. 563 1989 114 130
21. J.L. Feldman, J.C. Smith, and G. Liu Respiratory pattern generation in mammals: in vitro en bloc analyses Curr. Opin. Neurobiol. 1 1991 590 594
22. J.J. Greer, J.C. Smith, and J.L. Feldman Respiratory and locomotor patterns generated in the fetal rat brain stem-spinal cord in vitro J. Neurophysiol. 67 1992 996 999
23. Harding R Sustained alterations in postnatal respiratory function following sub-optimal intrauterine conditions Reprod. Fertil. Dev. 7 1995 431 441
24. S.U. Hasan, C. Pinsky, D.B. Cates, B.J. Nowaczyk, D.A. Gibson, and H. Rigatto The effects of naloxone on the changes in breathing and behaviour induced by morphine in the foetal sheep J. Dev. Physiol. 14 1990 171 179
25. G. Hilaire, and B. Duron Maturation of the mammalian respiratory system Physiol. Rev. 79 1999 325 360
26. G. Hilaire, J.C. Viemari, P. Coulon, M. Simonneau, and M. Bevengut Modulation of the respiratory rhythm generator by the pontine noradrenergic A5 and A6 groups in rodents Respir. Physiol. Neurobiol. 143 2004 187 197
27. A.H. Jansen, and V. Chernick Fetal breathing and development of control of breathing J. Appl. Physiol. 70 1991 1431 1446
28. S.M. Johnson, J.C. Smith, G.D. Funk, and J.L. Feldman Pacemaker behavior of respiratory neurons in medullary slices from neonatal rat J. Neurophysiol. 72 1994 2598 2608
29. S.A. Joseph, and D.W. Walker Catecholamine neurons in fetal brain: effects on breathing movements and electrocorticogram J. Appl. Physiol. 69 1990 1903 1911
30. S.A. Joseph, and D.W. Walker Effects of intracisternal monoamines on breathing movements in fetal sheep Am. J. Physiol. 264 1993 1139 1149
31. K. Kobayashi, R.P. Lemke, and J.J. Greer Ultrasound measurements of fetal breathing movements in the rat J. Appl. Physiol. 91 2001 316 320
32. B.J. Koos, Y. Kawasaki, A. Hari, F. Bohorquez, C. Jan, J. Roostaeian, C.L. Wilson, and L. Kruger Electrical stimulation of the posteromedial thalamus modulates breathing in unanesthetized fetal sheep J. Appl. Physiol. 96 2004 115 123
33. N. Koshiya, and J.C. Smith Neuronal pacemaker for breathing visualized in vitro Nature 400 1999 360 363
34. E.K. Kosmidis, O. Pierrefiche, and J.F. Vibert Respiratory-like rhythmic activity can be produced by an excitatory network of non-pacemaker neuron models J. Neurophysiol. 92 2004 686 699
35. P.I. Macfarlane, S. Wood, and J. Bennett Non-viable delivery at 20-23 weeks gestation: observations and signs of life after birth Arch. Dis. Child. Fetal Neonatal Ed. 88 2003 199 202
36. K. Mizuno, and A. Ueda The maturation and coordination of sucking, swallowing, and respiration in preterm infants J. Pediatr. 142 2003 36 40
37. R. Monteau, and G. Hilaire Spinal respiratory motoneurons Prog. Neurobiol. 37 1991 83 144
38. H. Onimaru, and I. Homma Development of the rat respiratory neuron network during the late fetal period Neurosci. Res. 42 2002 209 218
39. H. Onimaru, A. Arata, and I. Homma Firing properties of respiratory rhythm generating neurons in the absence of synaptic transmission in rat medulla in vitro Exp. Brain Res. 76 3 1989 530 536
40. H. Onimaru, A. Arata, and I. Homma Inhibitory synaptic inputs to the respiratory rhythm generator in the medulla isolated from newborn rats Pflugers Arch. 417 1990 425 432
41. Y. Ozawa, and N. Okado Alteration of serotonergic receptors in the brain stems of human patients with respiratory disorders Neuropediatrics 33 2002 142 149
42. S. Pagliardini, J. Ren, and J.J. Greer Ontogeny of the pre-Botzinger complex in perinatal rats J. Neurosci. 23 2003 9575 9584
43. J.F. Paton, and D.W. Richter Role of fast inhibitory synaptic mechanisms in respiratory rhythm generation in the maturing mouse J. Physiol. 484 Pt 2 1995 505 521
44. F. Pena, and J.M. Ramirez Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro J. Neurosci. 22 2002 11055 11064
45. M.R. Pereira, F.C. Reis, L. Landriault, D.B. Cates, and H. Rigatto Profile of alveolar gases during periodic and regular breathing in preterm infants Biol. Neonate 67 1995 322 329
46. K. Ptak, H. Burnet, B. Blanchi, M. Sieweke, C. De Felipe, S.P. Hunt, R. Monteau, and G. Hilaire The murine neurokinin NK1 receptor gene contributes to the adult hypoxic facilitation of ventilation Eur. J. Neurosci. 16 2002 2245 2252
47. J.M. Ramirez, U.J. Quellmalz, and D.W. Richter Postnatal changes in the mammalian respiratory network as revealed by the transverse brainstem slice of mice J. Physiol. 491 Pt 3 1996 799 812
48. J.C. Rekling, and J.L. Feldman PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation Annu. Rev. Physiol. 60 1998 385 405
49. H. Rigatto Maturation of breathing Clin. Perinatol. 19 1992 739 756
50. H. Rigatto Regulation of fetal breathing Reprod. Fertil. Dev. 8 1996 23 33
51. A.B. Roberts, D. Little, D. Cooper, and S. Campbell Normal patterns of fetal activity in the third trimester Br. J. Obstet. Gynaecol. 86 1979 4 9
52. P.F. Rowat, and R.C. Elson State-dependent effects of Na channel noise on neuronal burst generation J. Comput. Neurosci. 16 2004 87 112
53. I.A. Rybak, K. Ptak, N.A. Shevtsova, and D.R. McCrimmon Sodium currents in neurons from the rostroventrolateral medulla of the rat J. Neurophysiol. 90 2003 1635 1642
54. I.A. Rybak, N.A. Shevtsova, J.F. Paton, T.E. Dick, W.M. St.-John, M. Morschel, and M. Dutschmann Modeling the ponto-medullary respiratory network Respir. Physiol. Neurobiol. 143 2004 307 319
55. S. Shirasawa, A. Arata, H. Onimaru, K.A. Roth, G.A. Brown, S. Horning, S. Arata, K. Okumura, T. Sasazuki, and S.J. Korsmeyer Rnx deficiency results in congenital central hypoventilation Nat. Genet. 24 2000 287 290
56. J.C. Smith, H.H. Ellenberger, K. Ballanyi, D.W. Richter, and J.L. Feldman Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals Science 254 1991 726 729
57. J.C. Smith, R.J. Butera, N. Koshiya, C. Del Negro, C.G. Wilson, and S.M. Johnson Respiratory rhythm generation in neonatal and adult mammals: the hybrid pacemaker-network model Respir. Physiol. 122 2000 131 147
58. T. Suzue Respiratory rhythm generation in the in vitro brain stem-spinal cord preparation of the neonatal rat J. Physiol. 354 1984 173 183
59. J.C. Viemari, H. Burnet, M. Bevengut, and G. Hilaire Perinatal maturation of the mouse respiratory rhythm-generator: in vivo and in vitro studies Eur. J. Neurosci. 17 2003 1233 1244
60. J.C. Viemari, M. Bevengut, H. Burnet, P. Coulon, J.M. Pequignot, M.C. Tiveron, and Hilaire G Phox2a gene, A6 neurons, and noradrenaline are essential for development of normal respiratory rhythm in mice J. Neurosci. 24 2004 928 937
61. D.W. Walker Inhibition of breathing movements in fetal life: relevance to the sudden infant death syndrome Aust. Paediatr. J. 22 Suppl. 1 1986 67 69
62. D.W. Walker Hypoxic inhibition of breathing and motor activity in the foetus and newborn Clin. Exp. Pharmacol. Physiol. 22 1995 533 536
63. K.A. Waters, and D Gozal Responses to hypoxia during early development Respir. Physiol. Neurobiol. 136 2003 115 129
64. Z. Weintraub, R.E. Alvaro, R.J. Baier, D.B. Cates, B. Nowaczyk, C. Martino, and H. Rigatto Effect of norepinephrine on fetal breathing in sheep Biol. Neonate 73 1998 60 68
65. D. Worthington, W.N. Piercy, and B.T. Smith Modification of ovine fetal respiratory-like activity by chronic diazepam administration Am. J. Obstet. Gynecol. 131 1978 749 754