The conditional nature of the "Central Rhythm Generator" and the production of episodic breathing

Respiratory Physiology and Neurobiology

Volumn 168, Issue 1-2, 2009, Pages 179-187

  Fong, Angelina Y ^a   Zimmer, M Beth ^a,b   Milsom, William K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b FERRIS STATE UNIVERSITY   (United States)

Author keywords

Brainstem; Breathing pattern; Episodic breathing; Interbreath interval

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GLYCINE; MU OPIATE RECEPTOR; NITRIC OXIDE;

ARTICLE; BLOOD GAS; BREATHING PATTERN; CHEMORECEPTOR; GAS EXCHANGE; HISTOGRAM; HUMAN; LUNG RECEPTOR; MESENCEPHALON; NONHUMAN; PONS; PRIORITY JOURNAL; RESPIRATION CENTER;

ANIMALS; BRAIN CHEMISTRY; CANNABINOIDS; CARBON DIOXIDE; HUMANS; MEDULLA OBLONGATA; NEURONS; PERIODICITY; RESPIRATION; RESPIRATORY CENTER;

EID: 68949178682     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2009.05.012     Document Type: Article

References (81)

1. Abadie V., Champagnat J., and Fortin G. Branchiomotor activities in mouse embryo. Neuroreport 11 (2000) 141-145
2. Bassal M., and Bianchi A.L. Inspiratory onset or termination induced by electrical stimulation of the brain. Respir. Physiol. 50 (1982) 23-40
3. O2 drive in the tortoise Testudo horsfieldi. J. Exp. Biol. 87 (1980) 229-236
4. Bennett A.F. Ventilation in two species of lizards during rest and activity. Comp. Biochem. Physiol. A: Comp. Physiol. 46 (1973) 653-671
5. Berssenbrugge A., Dempsey J., Iber C., Skatrud J., and Wilson P. Mechanisms of hypoxia-induced periodic breathing during sleep in humans. J. Physiol. 343 (1983) 507-524
6. 2. Respir. Physiol. Neurobiol. 154 (2006) 30-36
7. Canet E., Praud J.P., and Bureau M.A. Periodic breathing induced on demand in awake newborn lamb. J. Appl. Physiol. 82 (1997) 607-612
8. Castellini M.A., Milsom W.K., Berger R.J., Costa D.P., Jones D.R., Castellini J.M., Rea L.D., Bharma S., and Harris M. Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups. Am. J. Physiol. 266 (1994) R863-R869
9. Champagnat J., and Fortin G. Primordial respiratory-like rhythm generation in the vertebrate embryo. Trends Neurosci. 20 (1997) 119-124
10. Chatonnet F., Thoby-Brisson M., Abadie V., Dominguez del T.E., Champagnat J., and Fortin G. Early development of respiratory rhythm generation in mouse and chick. Respir. Physiol. Neurobiol. 131 (2002) 5-13
11. Corcoran A.E., and Milsom W.K. Maturational changes in pontine and medullary alpha-adrenoceptor influences on respiratory rhythm generation in neonatal rats. Respir. Physiol. Neurobiol. 165 (2009) 195-201
12. Davies B.L., Brundage C.M., Harris M.B., and Taylor B.E. Lung respiratory rhythm and pattern generation in the bullfrog: role of neurokinin-1 and mu-opioid receptors. J. Comp. Physiol. [B] 179 (2009) 579-592
13. Del Negro C.A., Kam K., Hayes J.A., and Feldman J.L. Asymmetric control of inspiratory and expiratory phases by excitability in the respiratory network of neonatal mice in vitro. J. Physiol. 587 (2009) 1217-1231
14. Del Negro C.A., Morgado-Valle C., Hayes J.A., Mackay D.D., Pace R.W., Crowder E.A., and Feldman J.L. Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J. Neurosci. 25 (2005) 446-453
15. Dmi'el R. Effect of activity and temperature on metabolism and water loss in snakes. Am. J. Physiol. 223 (1972) 510-516
16. Douse M.A., and Mitchell G.S. Episodic respiratory related discharge in turtle cranial motoneurons: in vivo and in vitro studies. Brain Res. 536 (1990) 297-300
17. Errchidi S., Monteau R., and Hilaire G. Noradrenergic modulation of the medullary respiratory rhythm generator in the newborn rat: an in vitro study. J. Physiol. 443 (1991) 477-498
18. Fedde M.R., and Peterson D.F. Intrapulmonary receptor response to changes in airway-gas composition in Gallus domesticus. J. Physiol. 209 (1970) 609-625
19. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
20. Feldman J.L., Smith J.C., Ellenberger H.H., Connelly C.A., Liu G.S., Greer J.J., Lindsay A.D., and Otto M.R. Neurogenesis of respiratory rhythm and pattern: emerging concepts. Am. J. Physiol. 259 (1990) R879-R886
21. Fortin G., Champagnat J., and Lumsden A. Onset and maturation of branchio-motor activities in the chick hindbrain. Neuroreport 5 (1994) 1149-1152
22. Fortin G., Jungbluth S., Lumsden A., and Champagnat J. Segmental specification of GABAergic inhibition during development of hindbrain neural networks. Nat. Neurosci. 2 (1999) 873-877
23. Gargaglioni L.H., and Branco L.G. Nucleus isthmi and control of breathing in amphibians. Respir. Physiol. Neurobiol. 143 (2004) 177-186
24. Gargaglioni L.H., Meier J.T., Branco L.G., and Milsom W.K. Role of midbrain in the control of breathing in anuran amphibians. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R447-R457
25. Gauthier P., Monteau R., and Dussardier M. Inspiratory on-switch evoked by stimulation of mesencephalic structures: a patterned response. Exp. Brain Res. 51 (1983) 261-270
26. Gaytan S.P., Pasaro R., Coulon P., Bevengut M., and Hilaire G. Identification of central nervous system neurons innervating the respiratory muscles of the mouse: a transneuronal tracing study. Brain Res. Bull. 57 (2002) 335-339
27. Glass M.L., and Johansen K. Control of breathing in Acrochordus javanicus, an aquatic snake. Physiol. Zool. 49 (1976) 328-340
28. Glass M.L., Rantin F.T., Verzola R.M.M., Fernandes M.N., and Kalinin A.L. Cardio-respiratory synchronization and myocardial function in hypoxic carp Cyprinus carpio L. J. Fish Biol. 39 (1991) 143-149
29. Greer J.J., Funk G.D., and Ballanyi K. Preparing for the first breath: prenatal maturation of respiratory neural control. J. Physiol. 570 (2006) 437-444
30. Harris M.B., Wilson R.J., Vasilakos K., Taylor B.E., and Remmers J.E. Central respiratory activity of the tadpole in vitro brain stem is modulated diversely by nitric oxide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 (2002) R417-R428
31. Hedrick M.S., Chen A.K., and Jessop K.L. Nitric oxide changes its role as a modulator of respiratory motor activity during development in the bullfrog (Rana catesbeiana). Comp. Biochem. Physiol.-Part A: Mol. Integr. Physiol. 142 (2005) 231-240
32. Hetz S.K., and Bradley T.J. Insects breathe discontinuously to avoid oxygen toxicity. Nature 433 (2005) 516-519
33. Hilaire G., Viemari J.C., Coulon P., Simonneau M., and Bevengut M. Modulation of the respiratory rhythm generator by the pontine noradrenergic A5 and A6 groups in rodents. Respir. Physiol. Neurobiol. 143 (2004) 187-197
34. Jackson D.C., Palmer S.E., and Meadow W.L. The effects of temperature and carbon dioxide breathing on ventilation and acid-base status of turtles. Respir. Physiol. 20 (1974) 131-146
35. Janczewski W.A., Onimaru H., Homma I., and Feldman J.L. Opioid-resistant respiratory pathway from the preinspiratory neurones to abdominal muscles: in vivo and in vitro study in the newborn rat. J. Physiol. 545 (2002) 1017-1026
36. Johnson R.A., Johnson S.M., and Mitchell G.S. Catecholaminergic modulation of respiratory rhythm in an in vitro turtle brain stem preparation. J. Appl. Physiol. 85 (1998) 105-114
37. Johnson S.M., Wiegel L.M., and Majewski D.J. Are pacemaker properties required for respiratory rhythm generation in adult turtle brain stems in vitro?. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R901-R910
38. 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
39. Juch P.J., and Ballintijn C.M. Tegmental neurons controlling medullary respiratory centre activity in the carp. Respir. Physiol. 51 (1983) 95-107
40. 2 in bullfrogs. J. Appl. Physiol. 77 (1994) 2048-2051
41. Kinkead R., and Milsom W.K. Chemoreceptors and control of episodic breathing in the bullfrog (Rana catesbeiana). Respir. Physiol. 95 (1994) 81-98
42. Kinkead R., and Milsom W.K. Role of pulmonary stretch receptor feedback in control of episodic breathing in the bullfrog. Am. J. Physiol. Regul. Integr. Comp. Physiol. 272 (1997) R497-R508
43. +-dominated leak currents contribute to respiratory rhythm generation in the pre-Botzinger complex in vitro. J. Neurosci. 28 (2008) 1773-1785
44. Kupper T., Schoffl V., and Netzer N. Cheyne stokes breathing at high altitude: a helpful response or a troublemaker?. Sleep Breath. 12 (2008) 123-127
45. McLean H.A., Kimura N., Kogo N., Perry S.F., and Remmers J.E. Fictive respiratory rhythm in the isolated brainstem of frogs. J. Comp. Physiol. [A] 176 (1995) 703-713
46. 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
47. Milsom W.K. Intermittent breathing in vertebrates. Annu. Rev. Physiol. 53 (1991) 87-105
48. Milsom W.K., and Chan P. The relationship between lung volume, respiratory drive and breathing pattern in the turtle, Chrysemys picta. J. Exp. Biol. 120 (1986) 233-247
49. Milsom W.K., Harris M.B., and Reid S.G. Do descending influences alternate to produce episodic breathing?. Respir. Physiol. 110 (1997) 307-317
50. Milsom W.K., and Jones D.R. The role of vagal afferent information and hypercapnia in control of the breathing pattern in chelonia. J. Exp. Biol. 87 (1980) 53-63
51. Milsom W.K., McArthur M.D., and Webb C.L. Control of breathing in hibernating ground squirrels. In: Heller H.C., Mussachia L.C., and Wang L.C.H. (Eds). Living in the Cold: Physiological and Biochemical Adaptations (1986), Elsevier, New York 467-475
52. Milsom W.K., Reid S.G., Meier J.T., and Kinkead R. Central respiratory pattern generation in the bullfrog Rana catesbeiana. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 124 (1999) 253-264
53. Naifeh K.H., Huggins S.E., and Hoff H.E. Effects of brain section on respiratory patterns of crocodilian reptiles. Respir. Physiol. 13 (1971) 186-197
54. Oka K. The influence of the transection of the brain upon the respiratory movement of the frog. J. Physiol. Soc. Jpn. 20 (1958) 513-519
55. Pena F., Parkis M.A., Tryba A.K., and Ramirez J.M. Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43 (2004) 105-117
56. Peterson D.F., and Fedde M.R. Receptors sensitive to carbon dioxide in lungs of chicken. Science 162 (1968) 1499-1501
57. O2 load. J. Appl. Physiol. 50 (1981) 45-54
58. Quinlan M.C., and Gibbs A.G. Discontinuous gas exchange in insects. Respir. Physiol. Neurobiol. 154 (2006) 18-29
59. C O2 in the chicken. Respir. Physiol. 6 (1969) 135-143
60. Reid S.G., Meier J.T., and Milsom W.K. The influence of descending inputs on breathing pattern formation in the isolated bullfrog brainstem-spinal cord. Respir. Physiol. 120 (2000) 197-211
61. Reid S.G., and Milsom W.K. Respiratory pattern formation in the isolated bullfrog (Rana catesbeiana) brainstem-spinal cord. Respir. Physiol. 114 (1998) 239-255
62. Reid S.G., Milsom W.K., Meier J.T., Munns S., and West N.H. Pulmonary vagal modulation of ventilation in toads (Bufo marinus). Respir. Physiol. 120 (2000) 213-230
63. Reid S.G., Sundin L., Florindo L.H., Rantin F.T., and Milsom W.K. Effects of afferent input on the breathing pattern continuum in the tambaqui (Colossoma macropomum). Respir. Physiol. Neurobiol. 136 (2003) 39-53
64. Reid S.G., and West N.H. Modulation of breathing by phasic pulmonary stretch receptor feedback in an amphibian, Bufo marinus. Respir. Physiol. Neurobiol. 142 (2004) 165-183
65. Roberts B.L., and Ballintijn C.M. Sensory interaction with central 'generators' during respiration in the dogfish. J. Comp. Physiol. [A] 162 (1988) 695-704
66. Roberts J.L. Active branchial and ram gill ventilation in fishes. Biol. Bull. 148 (1975) 85-105
67. Rubin J.E., Hayes J.A., Mendenhall J.L., and Del Negro C.A. Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations. Proc. Natl. Acad. Sci. 106 (2009) 2939-2944
68. Salmoiraghi G.C., and Burns B.D. Localization and patterns of discharge of respiratory neurones in brain-stem of cat. J. Neurophysiol. 23 (1960) 2-13
69. Sanders C.E., and Milsom W.K. The effects of tonic lung inflation on ventilation in the American bullfrog Rana catesbeiana. J. Exp. Biol. 204 (2001) 2647-2656
70. Skovgaard N., and Wang T. Cost of ventilation and effect of digestive state on the ventilatory response of the tegu lizard. Respir. Physiol. Neurobiol. 141 (2004) 85-97
71. Smith J.C., Abdala A.P., Koizumi H., Rybak I.A., and Paton J.F. Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J. Neurophysiol. 98 (2007) 3370-3387
72. Straus C., Wilson R.J., Tezenas du M.S., and Remmers J.E. Baclofen eliminates cluster lung breathing of the tadpole brainstem, in vitro. Neurosci. Lett. 292 (2000) 13-16
73. Sullivan C.E., Kozar L.F., Murphy E., and Phillipson E.A. Primary role of respiratory afferents in sustaining breathing rhythm. J. Appl. Physiol. 45 (1978) 11-17
74. Tanabe A., Fujii T., and Onimaru H. Facilitation of respiratory rhythm by a μ-opioid agonist in newborn rat pons-medulla-spinal cord preparations. Neurosci. Lett. 375 (2005) 19-22
75. Vasilakos K., Kimura N., Wilson R.J., and Remmers J.E. Lung and buccal ventilation in the frog: uncoupling coupled oscillators. Physiol. Biochem. Zool. 79 (2006) 1010-1018
76. 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
77. West N.H., Topor Z.L., and Van Vliet B.N. Hypoxemic threshold for lung ventilation in the toad. Respir. Physiol. 70 (1987) 377-390
78. Wilkerson J.E.R., Wenninger M.R., Mitchell G.S., and Johnson S.M. Time-dependent changes in spontaneous respiratory activity in turtle brainstems in vitro. Respir. Physiol. Neurobiol. 138 (2003) 253-263
79. Zimmer M.B., and Milsom W.K. Effects of changing ambient temperature on metabolic, heart, and ventilation rates during steady state hibernation in golden-mantled ground squirrels (Spermophilus lateralis). Physiol. Biochem. Zool. 74 (2001) 714-723
80. Zimmer M.B., and Milsom W.K. Ventilatory pattern and chemosensitivity in unanesthetized, hypothermic ground squirrels (Spermophilus lateralis). Respir. Physiol. Neurobiol. 133 (2002) 49-63
81. Zimmer M.B., and Milsom W.K. Effect of hypothermia on respiratory rhythm generation in hamster brainstem-spinal cord preparations. Respir. Physiol. Neurobiol. 142 (2004) 237-249