Structure-function analysis of rhythmogenic inspiratory pre-Bötzinger complex networks in "calibrated" newborn rat brainstem slices

Respiratory Physiology and Neurobiology

Volumn 168, Issue 1-2, 2009, Pages 158-178

  Ballanyi, Klaus ^a   Ruangkittisakul, Araya ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Breathing; Fictive eupnea; Fictive sigh; Inspiratory; pre B tzinger complex; Respiratory center

Indexed keywords

CALCIUM ION; POTASSIUM ION;

ARTICLE; BRAIN STEM; CALIBRATION; EVOKED BRAIN STEM RESPONSE; INSPIRATORY BURST PATTERN; INSPIRATORY PREBOTZINGER COMPLEX NETWORK; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RESPIRATION CENTER; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANIMALS, NEWBORN; CALIBRATION; CATIONS; DOSE-RESPONSE RELATIONSHIP, DRUG; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; PERIODICITY; RATS; RESPIRATION; RESPIRATORY CENTER; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 68949191032     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2009.04.020     Document Type: Article

References (149)

1. Alheid G.F., Milsom W.K., and McCrimmon D.R. Pontine influences on breathing: an overview. Respir. Physiol. Neurobiol. 143 (2004) 105-114
2. Al-Zubaidy Z.A., Erickson R.L., and Greer J.J. Serotonergic and noradrenergic effects on respiratory neural discharge in the medullary slice preparation of neonatal rats. Eur. J. Physiol. (Pflügers Archiv) 431 (1996) 942-949
3. Ballanyi K. Isolated tissues. In: Windhorst U., and Johansson H. (Eds). Vitro Preparations, in Modern Techniques in Neuroscience Research (1999), Heidelberg, Springer 307-326
4. Ballanyi K. Neuromodulation of the perinatal respiratory network. Curr. Neuropharm. 2 (2004) 221-243
5. Ballanyi K. Protective role of neuronal KATP channels in brain hypoxia. J. Exp. Biol. 207 (2004) 3201-3212
6. Ballanyi K., Lalley P.M., Hoch B., and Richter D.W. cAMP-dependent reversal of opioid- and prostaglandin-mediated depression of the isolated respiratory network in newborn rats. J. Physiol. 504 (1997) 127-134
7. Ballanyi K., and Onimaru H. Respiratory network analysis, isolated respiratory center functions. In: Binder M., Hirsch M., Hirokawa N., and Windhorst U. (Eds). Encyclopedic Reference of Neuroscience (2009), Springer, Heidelberg, New York, Tokyo 3453-3458 (part 18)
8. Ballanyi K., Onimaru H., and Homma I. Respiratory network function in the isolated brainstem-spinal cord of newborn rats. Prog. Neurobiol. 59 (1999) 583-634
9. Ballanyi K., Onimaru H., and Keller B. Respiratory network analysis, functional imaging. In: Binder M., Hirsch M., Hirokawa N., and Windhorst U. (Eds). Encyclopedic Reference of Neuroscience (2009), Springer, Heidelberg, New York, Tokyo 3447-3453 (part 18)
10. Ballanyi K., and Ruangkittisakul A. Brain slices. In: Binder M., Hirsch M., Hirokawa N., and Windhorst U. (Eds). Encyclopedic Reference of Neuroscience (2009), Springer, Heidelberg, New York, Tokyo 483-490
11. Ballanyi K., Ruangkittisakul A., and Onimaru H. Opioids prolong and anoxia shortens delay between onset of pre-inspiratory (pFRG) and inspiratory (pBötC) network bursting in newborn rat brainstems. Eur. J. Physiol. (Pflüger's Archiv) 458 (2009) 571-587
12. Barnes B.J., Tuong C.M., and Mellen N.M. Functional imaging reveals respiratory network activity during hypoxic and opioid challenge in the neonate rat tilted sagittal slab preparation. J. Neurophysiol. 97 (2007) 2283-2292
13. Bianchi A.L., Denavit-Saubié M., and Champagnat J. Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol. Rev. 75 (1995) 1-45
14. Borday C., Wrobel L., Fortin G., Champagnat J., Thaëron-Antôno C., and Thoby-Brisson M. Developmental gene control of brainstem function: views from the embryo. Prog. Biophys. Mol. Biol. 84 (2004) 89-106
15. Bradley P.M., Murphy D., Kasparov S., Croker J., and Paton J.F. A micro-optrode for simultaneous extracellular electrical and intracellular optical recording from neurons in an intact oscillatory neuronal network. J. Neurosci. Methods 168 (2008) 383-395
16. Brockhaus J., and Ballanyi K. Synaptic inhibition in the isolated respiratory network of neonatal rats. Eur. J. Neurosci. 10 (1998) 3823-3839
17. Brockhaus J., and Ballanyi K. Anticonvulsant A(1) receptor-mediated adenosine action on neuronal networks in the brainstem-spinal cord of newborn rats. Neuroscience 96 (2000) 359-371
18. Brockhaus J., Ballanyi K., Smith J.C., and Richter D.W. Microenvironment of respiratory neurons in the in vitro brainstem-spinal cord of neonatal rats. J. Physiol. 462 (1993) 421-445
19. Büsselberg D., Bischoff A.M., and Richter D.W. A combined blockade of glycine and calcium-dependent potassium channels abolishes the respiratory rhythm. Neuroscience 122 (2003) pp. 831-541
20. Chamberlin N.L., and Dingledine R. Control of epileptiform burst rate by CA3 hippocampal cell afterhyperpolarizations in vitro. Brain Res. 492 (1989) 337-346
21. Connelly C.A., Dobbins E.G., and Feldman J.L. Pre-Bötzinger complex in cats: respiratory neuronal discharge patterns. Brain Res. 590 (1992) 337-340
22. Crowder E.A., Saha M.S., Pace R.W., Zhang H., Prestwich G.D., and Del Negro C.A. Phosphatidylinositol 4,5-bisphosphate regulates inspiratory burst activity in the neonatal mouse preBötzinger complex. J. Physiol. 582 (2007) 1047-1058
23. Del Negro C.A., Morgado-Valle C., and Feldman J.L. Respiratory rhythm: an emergent network property?. Neuron 34 (2002) 821-830
24. 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
25. Dutschmann M., and Herbert H. 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 (2006) 1071-1084
26. Dutschmann M., and Paton J.F. Glycinergic inhibition is essential for co-ordinating cranial and spinal respiratory motor outputs in the neonatal rat. J. Physiol. 543 (2002) 643-653
27. Dutschmann M., Wilson R.J., and Paton J.F. Respiratory activity in neonatal rats. Auton. Neurosci. 84 (2000) 19-29
28. Ellenberger H.H., and Feldman J.L. Brainstem connections of the rostral ventral respiratory group of the rat. Brain Res. 513 (1990) 35-42
29. Eugenin J., Nicholls J.G., Cohen L.B., and Muller K.J. Optical recording from respiratory pattern generator of fetal mouse brainstem reveals a distributed network. Neuroscience 137 (2006) 1221-1227
30. Feldman J.L. Neurophysiology of breathing in mammals. In: Bloom F.E. (Ed). Handbook of Physiology. The Nervous System. Intrinsic Regulatory System in the Brain (1986), Am. Physiol. Soc., Washington, DC pp. 463-524
31. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
32. Feldman J.L., Mitchell G.S., and Nattie E.E. Breathing: rhythmicity, plasticity, chemosensitivity. Annu. Rev. Neurosci. 26 (2003) 239-266
33. Feldman J.L., and Smith J.C. Cellular mechanisms underlying modulation of breathing pattern in mammals. Ann. N. Y. Acad. Sci. 563 (1989) 114-130
34. Fisher J.A., Marchenko V.A., Yodh A.G., and Rogers R.F. Spatiotemporal activity patterns during respiratory rhythmogenesis in the rat ventrolateral medulla. J. Neurophysiol. 95 (2006) 1982-1991
35. 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
36. Funk G.D., Smith J.C., and Feldman J.L. Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J. Neurophysiol. 70 (1993) 1497-1515
37. Funke F., Dutschmann M., and Müller M. Imaging of respiratory-related population activity with single-cell resolution. Am. J. Physiol. Cell. Physiol. 292 (2007) C508-C516
38. Funke F., Müller M., and Dutschmann M. Reconfiguration of respiratory-related population activity in a rostrally tilted transversal slice preparation following blockade of inhibitory neurotransmission in neonatal rats. Eur. J. Physiol. (Pflügers Archiv) 457 (2008) 185-195
39. Gaultier C., and Gallego J. Neural control of breathing: insights from genetic mouse models. J. Appl. Physiol. 104 (2008) 1522-1530
40. Gray P.A. Transcription factors and the genetic organization of brain stem respiratory neurons. J. Appl. Physiol. 104 (2008) 1513-1521
41. Gray P.A., Janczewski W.A., Mellen N., McCrimmon D.R., and Feldman J.L. Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons. Nat. Neurosci. 4 (2001) 927-930
42. 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
43. Greer J.J., Carter J.E., and Allan D.W. Respiratory rhythm generation in a precocial rodent in vitro preparation. Respir. Physiol. 103 (1996) 105-112
44. Greer J.J., and Funk G.D. Perinatal development of respiratory motoneurons. Respir. Physiol. Neurobiol. 149 (2005) 43-61
45. 2 homeostasis, and breathing automaticity. J. Appl. Physiol. 105 (2008) 404-416
46. Härtel K., Schnell C., and Hülsmann S. Astrocytic calcium signals induced by neuromodulators via functional metabotropic receptors in the ventral respiratory group of neonatal mice. Glia 57 (2008) 815-827
47. (ATP) channels in rhythmically active neurons. J. Physiol. 537 (2001) 69-81
48. Hayes J.A., and Del Negro C.A. Neurokinin receptor-expressing pre-Bötzinger complex neurons in neonatal mice studied in vitro. J. Neurophysiol. 97 (2007) 4215-4224
49. Herlenius E., Aden U., Tang L.Q., and Lagercrantz H. Perinatal respiratory control and its modulation by adenosine and caffeine in the rat. Pediatr. Res. 51 (2002) 4-12
50. Hille B. Ion Channels of Excitable Membranes (2001), Sinauer Associates, Sunderland, MA
51. Holtman Jr. J.R., and Speck D.F. Substance P immunoreactive projections to the ventral respiratory group in the rat. Peptides 15 (1994) 803-808
52. Homma R., Baker B.J., Jin L., Garaschuk O., Konnerth A., Cohen L.B., Bleau C.X., Canepari M., Djurisic M., and Zecevic D. Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Methods Mol. Biol. 489 (2009) 43-79
53. Horner R.L. Neuromodulation of hypoglossal motoneurons during sleep. Respir. Physiol. Neurobiol. 164 (2008) 179-196
54. Hülsmann S., Oku Y., Zhang W., and Richter D.W. Metabolic coupling between glia and neurons is necessary for maintaining respiratory activity in transverse medullary slices of neonatal mouse. Eur. J. Neurosci. 12 (2000) 856-862
55. Iizuka M. Rostrocaudal distribution of spinal respiratory motor activity in an in vitro neonatal rat preparation. Neurosci. Res. 50 (2004) 263-269
56. Jacobs B.L., and Azmitia E.C. Structure and function of the brain serotonin system. Physiol. Rev. 72 (1992) 165-229
57. Jacquin T.D., Borday V., Schneider-Maunoury S., Topilko P., Ghilini G., Kato F., Charnay P., and Champagnat J. Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 17 (1996) 747-758
58. Janczewski W.A., and Feldman J.L. Distinct rhythm generators for inspiration and expiration in the juvenile rat. J. Physiol. 570 (2006) 407-420
59. 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
60. 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
61. i/o protein-mediated mechanisms. J. Appl. Physiol. 80 (1996) 2120-2133
62. Johnson S.M., Smith J.C., Funk G.D., and Feldman J.L. Pacemaker behavior of respiratory neurons in medullary slices from neonatal rat. J. Neurophysiol. 72 (1994) 2598-2608
63. Kachidian P., Poulat P., Marlier L., and Privat A. Immunohistochemical evidence for the coexistence of substance P, thyrotropin-releasing hormone, GABA, methionine-enkephalin, and leucin-enkephalin in the serotonergic neurons of the caudal raphe nuclei: a dual labeling in the rat. J. Neurosci. Res. 30 (1991) 521-530
64. Konnerth A., Heinemann U., and Yaari Y. Nonsynaptic epileptogenesis in the mammalian hippocampus in vitro. I. Development of seizurelike activity in low extracellular calcium. J. Neurophysiol. 56 (1986) 409-423
65. Koizumi H., Wilson C.G., Wong S., Yamanishi T., Koshiya N., and Smith J.C. Functional imaging, spatial reconstruction, and biophysical analysis of a respiratory motor circuit isolated in vitro. J. Neurosci. 28 (2008) 2353-2365
66. Koshiya N., and Smith J.C. Neuronal pacemaker for breathing visualized in vitro. Nature 400 (1999) 360-363
67. Krause K.L., Forster H.V., Kiner T., Davis S.E., Bonis J.M., Qian B., and Pan L.G. Normal breathing pattern and arterial blood gases in awake and sleeping goats after near total destruction of the presumed pre-Botzinger complex and the surrounding region. J. Appl. Physiol. 106 (2009) 605-619
68. Kuwana S., Okada Y., and Natsui T. Effects of extracellular calcium and magnesium on central respiratory control in the brainstem-spinal cord of neonatal rat. Brain Res. 786 (1998) 194-204
69. Kuwana S., Tsunekawa N., Yanagawa Y., Okada Y., Kuribayashi J., and Obata K. Electrophysiological and morphological characteristics of GABAergic respiratory neurons in the mouse pre-Bötzinger complex. Eur. J. Neurosci. 23 (2006) 667-674
70. Lalley P.M. Opiate slowing of feline respiratory rhythm and effects on putative medullary phase-regulating neurons. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290 (2006) R1387-R1396
71. Lieske S.P., Thoby-Brisson M., Telgkamp P., and Ramirez J.M. Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat. Neurosci. 3 (2000) 600-607
72. Lipski J., and Merril E.G. Electrophysiological demonstration of the projection from expiratory neurones in rostral medulla to contralateral dorsal respiratory group. Brain Res. 197 (1980) 521-524
73. Long S., and Duffin J. The neuronal determinants of respiratory rhythm. Prog. Neurobiol. 27 (1986) 101-182
74. Lorier A.R., Huxtable A.G., Robinson D.M., Lipski J., Housley G.D., and Funk G.D. P2Y1 receptor modulation of the pre-Bötzinger complex inspiratory rhythm generating network in vitro. J. Neurosci. 27 (2007) 993-1005
75. Lorier A.R., Lipski J., Housley G.D., Greer J.J., and Funk G.D. ATP sensitivity of preBötzinger complex neurones in neonatal rat in vitro: mechanism underlying a P2 receptor-mediated increase in inspiratory frequency. J. Physiol. 586 (2008) 1429-1446
76. Leusen I. Regulation of cerebrospinal fluid composition with reference to breathing. Physiol. Rev. 52 (1972) 1-56
77. Manzke T., Guenther U., Ponimaskin E.G., Haller M., Dutschmann M., Schwarzacher S., and Richter D.W. 5-HT4(a) receptors avert opioid-induced breathing depression without loss of analgesia. Science 301 (2003) 226-229
78. McKay L.C., Janczewski W.A., and Feldman J.L. Sleep-disordered breathing after targeted ablation of preBotzinger complex neurons. Nat. Neurosci. 8 (2005) 1142-1144
79. McLean H.A., and Remmers J.E. Respiratory motor output of the sectioned medulla of the neonatal rat. Respir. Physiol. 96 (1994) 49-60
80. 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
81. Mironov S.L. Metabotropic glutamate receptors activate dendritic calcium waves and TRPM channels which drive rhythmic respiratory patterns in mice. J. Physiol. 586 (2008) 2277-2291
82. Mironov S.L., and Richter D.W. Hypoxic modulation of L-type Ca(2+) channels in inspiratory brainstem neurones: intracellular signalling pathways and metabotropic glutamate receptors. Brain Res. 869 (2000) 166-177
83. Oku Y., Masumiya H., and Okada Y. Postnatal developmental changes in activation profiles of the respiratory neuronal network in the rat ventral medulla. J. Physiol. 585 (2007) 175-186
84. 2+-dependent conductances to membrane potential fluctuations of medullary respiratory neurons of newborn rats in vitro. J. Physiol. 552 (2003) 727-741
85. Onimaru H., and Homma I. Respiratory rhythm generator neurons in medulla of brainstem-spinal cord preparation from newborn rat. Brain Res. 403 (1987) 380-384
86. Onimaru H., and Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J. Neurosci. 23 (2003) 1478-1486
87. 2-sensitive preinspiratory neurons of the parafacial respiratory group express Phox2b in the neonatal rat. J. Neurosci. 28 (2008) 12845-12850
88. Onimaru H., Kumagawa Y., and Homma I. Respiration-related rhythmic activity in the rostral medulla of newborn rats. J. Neurophysiol. 96 (2006) 55-61
89. Oshima N., Kumagai H., Kawai A., Sakata K., Matsuura T., and Saruta T. Three types of putative presympathetic neurons in the rostral ventrolateral medulla studied with rat brainstem-spinal cord preparation. Auton. Neurosci. 84 (2000) 40-49
90. Pace R.W., Mackay D.D., Feldman J.L., and Del Negro C.A. Role of persistent sodium current in mouse preBötzinger complex neurons and respiratory rhythm generation. J. Physiol. 580 (2007) 485-496
91. Pace R.W., Mackay D.D., Feldman J.L., and Del Negro C.A. Inspiratory bursts in the preBötzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. J. Physiol. 582 (2007) 113-125
92. Pagliardini S., Adachi T., Ren J., Funk G.D., and Greer J.J. Fluorescent tagging of rhythmically active respiratory neurons within the pre-Bötzinger complex of rat medullary slice preparations. J. Neurosci. 25 (2005) 2591-2596
93. Pagliardini S., Ren J., and Greer J.J. Ontogeny of the pre-Bötzinger complex in perinatal rats. J. Neurosci. 23 (2003) 9575-9584
94. 2+ of pre-Botzinger complex neurons in newborn rat brainstem slices without change of membrane potential or input resistance. Neurosci. Lett. 456 (2009) 25-29
95. Paton J.F. A working heart-brainstem preparation of the mouse. J. Neurosci. Methods 65 (1996) 63-68
96. Paton J.F., and St-John W.M. Long-term intracellular recordings of respiratory neuronal activities in situ during eupnea, gasping and blockade of synaptic transmission. J. Neurosci. Methods 147 (2005) 138-145
97. Paton J.F., and St-John W.M. Counterpoint: medullary pacemaker neurons are essential for gasping, but not eupnea, in mammals. J. Appl. Physiol. 103 (2007) 718-720 discussion 721-2
98. Peever J.H., Necakov A., and Duffin J. Nucleus raphé obscurus modulates hypoglossal output of neonatal rat in vitro transverse brain stem slices. J. Appl. Physiol. 90 (2001) 269-279
99. Perea G., and Araque A. Glial calcium signaling and neuron-glia communication. Cell Calcium 38 (2005) 375-382
100. Pierrefiche O., Schwarzacher S.W., Bischoff A.M., and Richter D.W. Blockade of synaptic inhibition within the pre-Bötzinger complex in the cat suppresses respiratory rhythm generation in vivo. J. Physiol. 509 (1998) 245-254
101. Ptak K., Yamanishi T., Aungst J., Milescu L.S., Zhang R., Richerson G.B., and Smith J.C. Raphé neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J. Neurosci. 29 (2009) 3720-3737
102. Ramirez J.M., and Garcia III A. Point: medullary pacemaker neurons are essential for both eupnea and gasping in mammals. J. Appl. Physiol. 103 (2007) 717-718 (discussion 722)
103. Ramirez J.M., Schwarzacher S.W., Pierrefiche O., Olivera B.M., and Richter D.W. Selective lesioning of the cat pre-Botzinger complex in vivo eliminates breathing but not gasping. J. Physiol. 507 (1998) 895-907
104. Rekling J.C., Champagnat J., and Denavit-Saubi M. Electroresponsive properties and membrane potential trajectories of three types of inspiratory neurons in the newborn mouse brain stem in vitro. J. Neurophysiol. 75 (1996) 795-810
105. Rekling J.C., Champagnat J., and Denavit-Saubié M. Thyrotropin-releasing hormone (TRH) depolarizes a subset of inspiratory neurons in the newborn mouse brain stem in vitro. J. Neurophysiol. 75 (1996) 811-819
106. Rekling J.C., Shao X.M., and Feldman J.L. Electrical coupling and excitatory synaptic transmission between rhythmogenic respiratory neurons in the preBötzinger complex. J. Neurosci. 20 (2000) RC113
107. Ren J., and Greer J.J. Modulation of respiratory rhythmogenesis by chloride-mediated conductances during the perinatal period. J. Neurosci. 26 (2006) 3721-3730
108. Richerson G.B. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat. Rev. Neurosci. 5 (2004) 449-461
109. Richter D.W., Ballanyi K., and Schwarzacher S. Mechanisms of respiratory rhythm generation. Curr. Opin. Neurobiol. 2 (1992) 788-793
110. Richter D.W., Lalley P.M., Pierrefiche O., Haji A., Bischoff A.M., Wilken B., and Hanefeld F. Intracellular signal pathways controlling respiratory neurons. Respir. Physiol. 110 (1997) 113-123
111. Ruangkittisakul A., and Ballanyi K. Reversal by phosphodiesterase-4 blockers of in vitro apnea in the isolated brainstem-spinal cord preparation from newborn rats. Neurosci. Lett. 401 (2006) 194-198
112. Ruangkittisakul A., Okada Y., Oku Y., Koshiya N., and Ballanyi K. Fluorescence Imaging of active respiratory networks. Respir. Physiol. Neurobiol. 168 (2009) 26-38
113. +] of confocally-imaged respiratory centre neurons in online-calibrated newborn rat brainstem slices. J. Neurosci. 26 (2006) 11870-11880
114. Ruangkittisakul A., Schwarzacher S.W., Secchia L., Ma Y., Bobocea N., Poon B.Y., Funk G.D., and Ballanyi K. Generation of eupnea and sighs by a spatiochemically organized inspiratory network. J. Neurosci. 28 (2008) 2447-2458
115. + antagonism of inspiratory centre rhythms in slices and en bloc preparations of newborn rat brainstem. J. Physiol. 584 (2007) 489-508
116. 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. U.S.A. 106 (2009) 2939-2944
117. Schwarzacher S.W., Smith J.C., and Richter D.W. Pre-Bötzinger complex in the cat. J. Neurophysiol. 73 (1995) 1452-1461
118. Shao X.M., and Feldman J.L. Respiratory rhythm generation and synaptic inhibition of expiratory neurons in pre-Bötzinger complex: differential roles of glycinergic and GABAergic neural transmission. J. Neurophysiol. 77 (1997) 1853-1860
119. Shvarev Y.N., Lagercrantz H., and Yamamoto Y. Two types of rhythm in the respiratory network output in the isolated ventrolateral medulla in the neonatal rats. Neurosci. Lett. 347 (2003) 53-56
120. 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
121. Smith J.C., Ballanyi K., and Richter D.W. Whole-cell patch-clamp recordings from respiratory neurons in neonatal rat brainstem in vitro. Neurosci. Lett. 134 (1992) 153-156
122. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., and Feldman J.L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254 (1991) 726-729
123. Smith J.C., Greer J.J., Liu G.S., and Feldman J.L. Neural mechanisms generating respiratory pattern in mammalian brain stem-spinal cord in vitro. I. Spatiotemporal patterns of motor and medullary neuron activity. J. Neurophysiol. 64 (1990) 1149-1169
124. + alters phrenic motor output response to chemical stimulation of cat pre-Botzinger complex in vivo. J. Appl. Physiol. 94 (2003) 2151-2157
125. Solomon I.C., Edelman N.H., and Neubauer J.A. Patterns of phrenic motor output evoked by chemical stimulation of neurons located in the pre-Bötzinger complex in vivo. J. Neurophysiol. 81 (1999) 1150-1161
126. Solomon I.C., Edelman N.H., and Neubauer J.A. Pre-Bötzinger complex functions as a central hypoxia chemosensor for respiration in vivo. J. Neurophysiol. 83 (2000) 2854-2868
127. Somjen G.G. Ion regulation in the brain: implications for pathophysiology. Neuroscientist 8 (2002) 254-267
128. Speck D.F., and Feldman J.L. The effects of microstimulation and microlesions in the ventral and dorsal respiratory groups in medulla of cat. J. Neurosci. 2 (1982) 744-757
129. St-John W.M., Rudkin A.H., Harris M.R., Leiter J.C., and Paton J.F. Maintenance of eupnea and gasping following alterations in potassium ion concentration of perfusates of in situ rat preparation. J. Neurosci. Methods 142 (2005) 125-129
130. Stornetta R.L. Identification of neurotransmitters and co-localization of transmitters in brainstem respiratory neurons. Respir. Physiol. Neurobiol. 164 (2008) 18-27
131. Stornetta R.L., Sevigny C.P., and Guyenet P.G. Inspiratory augmenting bulbospinal neurons express both glutamatergic and enkephalinergic phenotypes. J. Comp. Neurol. 455 (2003) 113-124
132. Sun Q.J., Goodchild A.K., Chalmers J.P., and Pilowsky P.M. The pre-Bötzinger complex and phase-spanning neurons in the adult rat. Brain Res. 809 (1998) 204-213
133. Suzue T. Respiratory rhythm generation in the in vitro brain stem-spinal cord preparation of the neonatal rat. J. Physiol. 354 (1984) 173-183
134. Szoke K., Härtel K., Grass D., Hirrlinger P.G., Hirrlinger J., and Hülsmann S. Glycine transporter 1 expression in the ventral respiratory group is restricted to protoplasmic astrocytes. Brain Res. 1119 (2006) 182-189
135. Taccola G., Secchia L., and Ballanyi K. Anoxic persistence of lumbar respiratory bursts and block of lumbar locomotion in newborn rat brainstem spinal cords. J. Physiol. 585 (2007) 507-524
136. Tan W., Janczewski W.A., Yang P., Shao X.M., Callaway E.M., and Feldman J.L. Silencing preBötzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat. Neurosci. 11 (2008) 538-540
137. Thoby-Brisson M., Trinh J.B., Champagnat J., and Fortin G. Emergence of the pre-Bötzinger respiratory rhythm generator in the mouse embryo. J. Neurosci. 25 (2005) 4307-4318
138. Tryba A.K., Peña F., Lieske S.P., Viemari J.C., Thoby-Brisson M., and Ramirez J.M. Differential modulation of neural network and pacemaker activity underlying eupnea and sigh-breathing activities. J. Neurophysiol. 99 (2008) 2114-2125
139. Tryba A.K., Peña F., and Ramirez J.M. Stabilization of bursting in respiratory pacemaker neurons. J. Neurosci. 23 (2003) 3538-3546
140. Tryba A.K., and Ramirez J.M. Response of the respiratory network of mice to hyperthermia. J. Neurophysiol. 89 (2003) 2975-2983
141. Tryba A.K., and Ramirez J.M. Hyperthermia modulates respiratory pacemaker bursting properties. J. Neurophysiol. 92 (2004) 2844-2852
142. Völker A., Ballanyi K., and Richter D.W. Anoxic disturbance of the isolated respiratory network of neonatal rats. Exp. Brain Res. 103 (1995) 9-19
143. CO2 and pH and their role as chemo-stimulants in the isolated respiratory network of neonatal rats. J. Physiol. 499 (1997) 527-542
144. Wang H., Stornetta R.L., Rosin D.L., and Guyenet P.G. Neurokinin-1 receptor-immunoreactive neurons of the ventral respiratory group in the rat. J. Comp. Neurol. 434 (2001) 128-146
145. Wenninger J.M., Pan L.G., Klum L., Leekley T., Bastastic J., Hodges M.R., Feroah T.R., Davis S., and Forster H.V. Large lesions in the pre-Botzinger complex area eliminate eupneic respiratory rhythm in awake goats. J. Appl. Physiol. 97 (2004) 1629-1636
146. Wenninger J.M., Pan L.G., Klum L., Leekley T., Bastastic J., Hodges M.R., Feroah T., Davis S., and Forster H.V. Small reduction of neurokinin-1 receptor-expressing neurons in the pre-Bötzinger complex area induces abnormal breathing periods in awake goats. J. Appl. Physiol. 97 (2004) 1620-1628
147. Winter, S.M., Fresemann, J., Schnell, C., Oku, Y., Hirrlinger, J., F., Hülsmann, S., in press. Glycinergic interneurons are functionally integrated into the inspiratory network of mouse medullary slices. Eur. J. Physiol. (Pflüger's Archiv) doi:10.1007/s00424-009-0647-1.
148. Winter S.M., Hirrlinger J., Kirchhoff F., and Hülsmann S. Transgenic expression of fluorescent proteins in respiratory neurons. Respir. Physiol. Neurobiol. 159 (2007) 108-114
149. Zavala-Tecuapetla C., Aguileta M.A., Lopez-Guerrero J.J., González-Marín M.C., and Peña F. Calcium-activated potassium currents differentially modulate respiratory rhythm generation. Eur. J. Neurosci. 27 (2008) 2871-2884