Phylogenetic trends in respiratory rhythmogenesis: Insights from ectothermic vertebrates

Respiratory Physiology and Neurobiology

Volumn 168, Issue 1-2, 2009, Pages 39-48

  Kinkead, Richard ^a  

^a Université Laval   (Canada)

Author keywords

Central pattern generation; Comparative physiology; Control of breathing; Ectotherms; Oscillators

Indexed keywords

4 AMINOBUTYRIC ACID; OPIATE; SOMATOSTATIN; SUBSTANCE P;

AMPHIBIA; ARTICLE; BREATHING MECHANICS; BREATHING PATTERN; CELL FUNCTION; LAMPREY; LUNG VENTILATION; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PHYLOGENY; PRE BOTZINGER COMPLEX; PRIORITY JOURNAL; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; RODENT; SYNAPTIC TRANSMISSION; TIDAL VOLUME; TURTLE;

ANALGESICS, OPIOID; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; HUMANS; NERVE NET; NEURONS; PHYLOGENY; RESPIRATION; RESPIRATORY CENTER; SUBSTANCE P; TEMPERATURE; VERTEBRATES;

EID: 69249222623     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2009.05.011     Document Type: Article

References (92)

1. Adrian E.D., and Buytendijk F.J.J. Potential changes in the isolated brainstem of the goldfish. J. Physiol. Lond. 71 (1931) 121-135
2. Auclair F., Lund J.P., and Dubuc R. Immunohistochemical distribution of tachykinins in the CNS of the lamprey Petromyzon marinus. J. Comp. Neurol. 479 (2004) 328-346
3. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3 (2002) 728-739
4. Ben-Ari Y., Gaiarsa J.-L., Tyzio R., and Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87 (2007) 1215-1284
5. A, NMDA and AMPA receptors: a developmentally regulated 'ménage à trois'. Trends Neurosci. 20 (1997) 523-529
6. Bongianni F., Mutolo D., Nardone F., and Pantaleo T. GABAergic and glycinergic inhibitory mechanisms in the lamprey respiratory control. Brain Res. 1090 (2006) 134-145
7. Borday V., Fortin G., and Champagnat J. Early ontogeny of rhythm generation and control of breathing. Respir. Physiol. 110 (1997) 245-249
8. Brainerd E. The evolution of lung-gill bimodal breathing and the homology of vertebrate respiratory pumps. Am. Zool. 34 (1994) 289-299
9. Brainerd E.L., and Owerkowicz T. Functional morphology and evolution of aspiration breathing in tetrapods. Respir. Physiol. Neurobiol. 154 (2006) 73-88
10. Broch L., Morales R.D., Sandoval A.V., and Hedrick M.S. Regulation of the respiratory central pattern generator by chloride-dependent inhibition during development in the bullfrog (Rana catesbeiana). J. Exp. Biol. 205 (2002) 1161-1169
11. Burggren W.W., and West N.H. Changing respiratory importance of gills, lungs and skin during metamorphosis in the bullfrog Rana catesbeiana. Respir. Physiol. 47 (1982) 151-164
12. Champagnat J., and Fortin G. Primordial respiratory-like rhythm generation in the vertebrate embryo. Trends Neurosci. 20 (1997) 119-124
13. Chatonnet F., Borday C., Wrobel L., Thoby-Brisson M., Fortin G., McLean H., and Champagnat J. Ontogeny of central rhythm generation in chicks and rodents. Respir. Physiol. Neurobiol. 154 (2006) 37-46
14. Chen A.K., and Hedrick M.S. Role of glutamate and substance P in the amphibian respiratory network during development. Respir. Physiol. Neurobiol. 162 (2008) 24-31
15. Davies B., Brundage C., Harris M., and Taylor B. Lung respiratory rhythm and pattern generation in the bullfrog: role of neurokinin-1 and μ-opioid receptors. J. Comp. Physiol. B: Biochem. Syst. Environ. Physiol. 179 (2009) 579-592
16. De Marneffe-Foulon C. Contribution à l'étude du mécanisme et du contrôle des mouvements respiratoire chez Rana. Annales de la Société Royale Zool. de Belgique 92 (1962) 81-132
17. Dejours P. From comparative physiology of respiration to several problems of environmental adaptations and to evolution. J. Physiol. (Lond.) 410 (1989) 1-19
18. Doi A., and Ramirez J.-M. Neuromodulation and the orchestration of the respiratory rhythm. Respir. Physiol. Neurobiol. 164 (2008) 96-104
19. Duchcherer M., and Wilson R.J.A. Respiratory oscillators in lower vertebrates. International symposium on respiratory control (2008), St-Maximin, France P. 13
20. Ellenberger H.H., and Feldman J.L. Monosynaptic transmission of respiratory drive to phrenic motoneurons from brainstem bulbospinal neurons in rats. J. Comp. Neurol. 269 (1988) 47-57
21. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
22. Feldman J.L., and Ellenberger H.H. Central coordination of respiratory and cardiovascular control in mammals. Annu. Rev. Physiol. 50 (1988) 593-606
23. Feldman J.L., Mitchell G.S., and Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 26 (2003) 239-266
24. Feldman J.L., and McCrimmon D.R. Neural control of breathing. In: Squire L.R., Bloom F.E., McConnell S.K., Roberts J.L., Spitzer N.C., and Zigmond M.J. (Eds). Fundamental Neuroscience (2003), Academic Press, Amsterdam/Boston/London/New York/Oxford/Paris/San Diego/San Francisco/Singapore/Sydney/Tokyo 967-990
25. Fishman A.P., Galante R.J., and Pack A.I. Diving Physiology (1989), Dekker, New York
26. Forster H.V., Lalley P.M., Greer J., Nattie E.E., Li A., Negro C.A.D., Gray P.A., Dutschmann M., Rybak I.A., Dick T.E., Johnson S.M., Hedrick M.S., Funk G.D., Vasilakos K., Wilson R.J.A., Ballanyi K., and Mellen N.M. The parafacial respiratory group (pFRG)/pre-Bötzinger complex (preBötC) is the primary site of respiratory rhythm generation in the mammal. J. Appl. Physiol. 100 (2006) 2103-2108
27. Fortuna M.G., West G.H., Stornetta R.L., and Guyenet P.G. Botzinger Expiratory-Augmenting Neurons and the Parafacial Respiratory Group. J. Neurosci. 28 (2008) 2506-2515
28. 2 chemoreflex during development in bullfrogs (Lithobates catesbeiana). Neuroscience 155 (2008) 983-996
29. Galante R.J., Kubin L., Fishman A.P., and Pack A.I. Role of chloride-mediated inhibition in respiratory rhythmogenesis in an in vitro brainstem of tadpole, Rana catesbeiana. J. Physiol. (Lond.) 492 (1996) 545-558
30. Gans C., De Jongh H.J., and Farber J. Bullfrog (Rana catesbeiana) ventilation: how does the frog breathe?. Science 163 (1969) 1223-1225
31. Gdovin M.J., Torgerson C.S., and Remmers J.E. Neurorespiratory pattern of gill and lung ventilation in the decerebrate spontaneously breathing tadpole. Respir. Physiol. 113 (1998) 135-146
32. Gray P.A., Rekling J.C., Bocchiaro C.M., and Feldman J.L. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBötzinger complex. Science 286 (1999) 1566-1568
33. Greer J.J., and Funk G.D. Perinatal development of respiratory motoneurons. Respir. Physiol. Neurobiol. (2005)
34. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 4 (2003) 573-586
35. Guimond J.C., Auclair F., Lund J.P., and Dubuc R. Anatomical and physiological study of respiratory motor innervation in lampreys. Neuroscience 122 (2003) 259-266
36. Hedrick M.S. Development of respiratory rhythm generation in ectothermic vertebrates. Respir. Physiol. Neurobiol. 149 (2005) 29-41
37. Hedrick M.S., Broch L., Martinez M., Powell J.L., and Wade R.E. Is the vertebrate respiratory central pattern generator conserved?. In: Kazemi P.a. (Ed). Frontiers in Modeling and Control of Breathing (2001), Kluwer Academic/Plenum Publishers, NY 127-132
38. Homma S. Velar motoneurons of lamprey larvae. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 104 (1975) 175-183
39. Janczewski W.A., and Feldman J.L. Distinct rhythm generators for inspiration and expiration in the juvenile rat. J. Physiol. 570 (2006) 407-420
40. Johnson S.M., Kinney M.E., and Wiegel L.M. Inhibitory and excitatory effects of μ-, δ-, and κ-opioid receptor activation on breathing in awake turtles, Trachemys scripta. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 (2008) R1599-R1612
41. Johnson S.M., Koshiya N., and Smith J.C. Isolation of the kernel for respiratory rhythm generation in a novel preparation: the pre-Bötzinger complex "island". J. Neurophysiol. 85 (2001) 1772-1776
42. Johnson S.M., Wiegel L.M., and Majewski D.J. Are pacemaker properties required for respiratory rhythm generation in adult turtle brainstems in vitro?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R901-910
43. Johnson S.M., Wilkerson J.E., Wenninger M.R., Henderson D.R., and Mitchell G.S. Role of synaptic inhibition in turtle respiratory rhythm generation. J. Physiol. 544 (2002) 253-265
44. Just J.J., Gatz R.N., and Crawford Jr. E.C. Changes in respiratory functions during metamorphosis of the bullfrog, Rana catesbeiana. Respir. Physiol. 17 (1973) 276-282
45. Kawasaki R. Breathing rhythm-generation mechanism in the adult lamprey (Lampetra japonica). Jpn. J. Physiol. 34 (1984) 319-335
46. Keynes R., and Lumsden A. Segmentation and the origin of regional diversity in the vertebrate central nervous system. Neuron 4 (1990) 1-9
47. Klein W., and Owerkowicz T. Function of intracoelomic septa in lung ventilation of amniotes: lessons from lizards. Physiol. Biochem. Zool. 79 (2006) 1019-1032
48. Lumsden A., and Keynes R. Segmental patterns of neuronal development in the chick hindbrain. Nature 337 (1989) 424-428
49. Majewski D.J., Wiegel L.M., and Johnson S.M. Respiratory pattern in midline-lesioned brainstems and hemibrainstems from adult turtles. Respir. Physiol. Neurobiol. 164 (2008) 338-349
50. Martel B., Guimond J.C., Gariepy J.F., Gravel J., Auclair F., Kolta A., Lund J.P., and Dubuc R. Respiratory rhythms generated in the lamprey rhombencephalon. Neuroscience 148 (2007) 279-293
51. McLean H.A., Perry S.F., and Remmers J.E. Two regions in the isolated brainstem of the frog that modulate respiratory-related activity. J. Comp. Physiol. [A] 177 (1995) 135-144
52. McMahon B.R. A functional analysis of the aquatic and aerial respiratory movements of an African lungfish, Protopterus aethiopicus, with reference to the evolution of the lung-ventilation mechanism in vertebrates. J. Exp. Biol. 51 (1969) 407-430
53. Mellen N.M., Janczewski W.A., Bocchiaro C.M., and Feldman J.L. Opioid-induced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron 37 (2003) 821-826
54. Milsom W.K. Mechanoreceptor modulation of endogenous respiratory rhythms in vertebrates. Am. J. Physiol. 259 (1990) R898-910
55. Milsom W.K. Evolutionary trends in respiratory mechanisms. Integration in Respiratory Control (2008) pp. 293-298
56. Milsom W.K., Chatburn J., and Zimmer M.B. Pontine influences on respiratory control in ectothermic and heterothermic vertebrates. Respir. Physiol. Neurobiol. 143 (2004) 263-280
57. Mutolo D., Bongianni F., Einum J., Dubuc R., and Pantaleo T. Opioid-induced depression in the lamprey respiratory network. Neuroscience 150 (2007) 720-729
58. Mutolo, D., Bongianni, F., Cinelli, E., Pantaleo, T., 2008. Influences of neurokinin receptor activation on respiratory rhythm generation in the lamprey. International symposium on respiratory control, St-Maximin, France. P. 14.
59. Oku Y., Kimura N., Masumiya H., and Okada Y. Spatiotemporal organization of frog respiratory neurons visualized on the ventral medullary surface. Respir. Physiol. Neurobiol. 161 (2008) 281-290
60. Onimaru H., and Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J. Neurosci. 23 (2003) 1478-1486
61. Onimaru H., Homma I., Feldman J.L., and Janczewski W.A. Point:Counterpoint: the parafacial respiratory group (pFRG)/pre-Bötzinger complex (preBötC) is the primary site of respiratory rhythm generation in the mammal. J. Appl. Physiol. 100 (2006) 2094-2098
62. Perry S.F., McLean H.A., Kogo N., Kimura N., Kawasaki H., Sakurai M., Kabotyanski E.A., and Remmers J.E. The frog brainstem preparation as a model for studying the central control of breathing in tetrapods. Braz. J. Med. Biol. Res. 28 (1995) 1339-1346
63. Perry S.F., Wilson R.J., Straus C., Harris M.B., and Remmers J.E. Which came first, the lung or the breath?. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129 (2001) 37-47
64. Ramirez J.-M., and Viemari J.-C. Determinants of inspiratory activity. Respir. Physiol. Neurobiol. 147 (2005) 145
65. Rekling J.C., and Feldman J.L. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 60 (1998) 385-405
66. Ren J., and Greer J.J. Modulation of respiratory rhythmogenesis by chloride-mediated conductances during the perinatal period. J. Neurosci. 26 (2006) 3721-3730
67. Richter D.W. Generation and maintenance of the respiratory rhythm. J. Exp. Biol. 100 (1982) 93-107
68. Richter D.W., Ballantyne D., and Remmers J.E. How is the respiratory rhythm generated? A model. NIPS 1 (1986) 109-112
69. Richter D.W., and Spyer K.M. Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci. 24 (2001) 464-472
70. Rovainen C.M. Neurobiology of lampreys. Physiol. Rev. 59 (1979) 1007-1077
71. Rovainen C.M. Generation of respiratory activity by the lamprey brain exposed to picrotoxin and strychnine, and weak synaptic inhibition in motoneurons. Neuroscience 10 (1983) 875-882
72. Rovainen C.M. Respiratory bursts at the midline of the rostral medulla of the lamprey. J. Comp. Physiol. [A] 157 (1985) 303-309
73. Rovainen C.M., and Schieber M.H. Ventilation of larval lampreys. J. Comp. Physiol. A: Neuroethol. Sens. Neural Behav. Physiol. 104 (1975) 185-203
74. Rybak I.A., Abdala A.P.L., Markin S.N., Paton J.F.R., and Smith J.C. Spatial organization and state-dependent mechanisms for respiratory rhythm and pattern generation. In: Paul Cisek T.D.a.J.F.K. (Ed). Progress in Brain Research vol. 165 (2007), Elsevier 201-220
75. Smatresk N.J. Chemoreceptor modulation of endogenous respiratory rhythms in vertebrates. Am. J. Physiol. 259 (1990) R887-897
76. Smatresk N.J. Respiratory control in the transition from water to air breathing in vertebrates. Am. Zool. 34 (1994) 264-279
77. Smith J.C., Butera R.J., Koshiya N., Del Negro C., Wilson C.G., and Johnson S.M. Respiratory rhythm generation in neonatal and adult mammals: the hybrid pacemaker-network model. Respir. Physiol. 122 (2000) 131-147
78. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., and Feldman J.L. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254 (1991) 726-729
79. Storer T., Usinger R., Stebbins R., and Nybakken J. General Zoology (1979), McGraw-Hill
80. Straus C., Wilson R.J., and Remmers J.E. Developmental disinhibition: turning off inhibition turns on breathing in vertebrates. J. Neurobiol. 45 (2000) 75-83
81. Takeda R., Remmers J.E., Baker J.P., Madden K.P., and Farber J.P. Postsynaptic potentials of bulbar respiratory neurons of the turtle. Respir. Physiol. 64 (1986) 149-160
82. Takeda S., Eriksson L.I., Yamamoto Y., Joensen H., Onimaru H., and Lindahl S.G. Opioid action on respiratory neuron activity of the isolated respiratory network in newborn rats. Anesthesiology 95 (2001) 740-749
83. Taylor A.C., and Kollros J.J. Stages in the normal development of Rana pipiens larvae. Anat. Rec. 94 (1946) 7-24
84. Torgerson C.S., Gdovin M.J., Brandt R., and Remmers J.E. Location of central respiratory chemoreceptors in the developing tadpole. Am. J. Physiol. 280 (2001) R921-928
85. Torgerson C.S., Gdovin M.J., and Remmers J.E. Sites of respiratory rhythmogenesis during development in the tadpole. Am. J. Physiol. 280 (2001) R913-920
86. 2 levels in the dogfish, Scyliorhinus canicula. Respir. Physiol. 41 (1980) 13-28
87. Vasilakos K., Wilson R.J., Kimura N., and Remmers J.E. Ancient gill and lung oscillators may generate the respiratory rhythm of frogs and rats. J. Neurobiol. 62 (2005) 369-385
88. + respiratory chemosensitivity: new insights from an old fish?. J. Exp. Biol. 203 (2000) 3505-3512
89. Wilson R.J., Vasilakos K., Harris M.B., Straus C., and Remmers J.E. Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators. J. Physiol. 540 (2002) 557-570
90. Wilson R.J., Vasilakos K., and Remmers J.E. Phylogeny of vertebrate respiratory rhythm generators: the Oscillator Homology Hypothesis. Respir. Physiol. Neurobiol. 154 (2006) 47-60
91. + in the isolated bullfrog brainstem. J. Neurobiol. 55 (2003) 278-287
92. Zhan W.Z., Ellenberger H.H., and Feldman J.L. Monoaminergic and GABAergic terminations in phrenic nucleus of rat identified by immunohistochemical labeling. Neuroscience 31 (1989) 105-113