Late-expiratory activity: Emergence and interactions with the respiratory CPG

Journal of Neurophysiology

Volumn 104, Issue 5, 2010, Pages 2713-2729

  Molkov, Yaroslav I ^a   Abdala, Ana P L ^b   Bacak, Bartholomew J ^a   Smith, Jeffrey C ^c   Paton, Julian F R ^b   Rybak, Ilya A ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN STEM; BREATHING; CONTROLLED STUDY; HYPERCAPNIA; HYPOXIA; MOLECULAR INTERACTION; NERVE CELL NETWORK; NERVE EXCITABILITY; NONBIOLOGICAL MODEL; NONHUMAN; OSCILLATION; PHRENIC NERVE; PRIORITY JOURNAL; RAT; RESPIRATION CENTER; RESPIRATION CONTROL;

ANIMALS; BRAIN STEM; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; EXHALATION; MODELS, NEUROLOGICAL; NEURONS; RATS; RESPIRATION; RILUZOLE; SPINAL CORD;

EID: 78049507151     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00334.2010     Document Type: Article

References (73)

1. Abdala AP, Rybak IA, Smith JC, Paton JF. Abdominal expiratory activity in the rat brain stem-spinal cord in situ: patterns, origins and implications for respiratory rhythm generation. J Physiol 587: 3539-3559, 2009a.
2. Abdala AP, Rybak IA, Smith JC, Zoccal DB, Machado BH, St-John WM, Paton JF. Multiple pontomedullary mechanisms of respiratory rhythmogenesis. Respir Physiol Neurobiol 168: 19-25, 2009b.
3. Abu-Shaweesh JM, Dreshaj IA, Thomas AJ, Haxhiu MA, Strohl KP, Martin RJ. Changes in respiratory timing induced by hypercapnia in maturing rats. J Appl Physiol 87: 484-490, 1999.
4. Baker SN, Kilner JM, Pinches EM, Lemon RN. The role of synchrony and oscillations in the motor output. Exp Brain Res 128: 109-117, 1999.
5. Ballanyi K, Onimaru H, Homma I. Respiratory network function in the isolated brainstem-spinal cord of newborn rats. Prog Neurobiol 59: 583-634, 1999.
6. Bauer M, Oostenveld R, Peeters M, Fries P. Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26: 490-501, 2006.
7. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nat Neurosci 2: 168-174, 1999.
8. Bianchi AL, Denavitsaubie M, Champagnat J. Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol Rev 75: 1-45, 1995.
9. Bongianni F, Mutolo D, Cinelli E, Pantalleo T. Respiratory responses induced by blockades of GABA and glycine receptors within the Bötzinger complex and the pre-Bötzinger complex of the rabbit. Brain Res 1344: 134-147, 2010.
10. Butera RJ, Rinzel JR, Smith JC. Models of respiratory rhythm generation in the pre-Bötzinger complex: II. Populations of coupled pacemaker neurons. J Neurophysiol 82: 398-415, 1999.
11. Cohen MI. Neurogenesis of respiratory rhythm in the mammal. Physiol Rev 59: 1105-1173, 1979.
12. Del Negro CA, Kam K, Hayes JA, Feldman JL. Asymmetric control of inspiratory and expiratory phases by excitability in the respiratory network of neonatal mice in vitro. J Physiol 587: 1217-1231, 2009.
13. Dutschmann M, 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: 1071-1084, 2006.
14. Elsen FP, Ramirez JM. Calcium currents of rhythmic neurons recorded in the isolated respiratory network of neonatal mice. J Neurosci 18: 10652-10662, 1998.
15. Ezure K. Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog Neurobiol 35: 429-450, 1990.
16. Ezure K, Tanaka I, Saito Y. Brain stem and spinal projections of augmenting expiratory neurons in the rat. Neurosci Res 45: 41-51, 2003.
17. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7: 232-242, 2006.
18. Feldman JL, Janczewski WA. Point:Counterpoint: the parafacial respiratory group (pFRG)/pre-Bötzinger complex (pre-BötC) is the primary site of respiratory rhythm generation in the mammal. Counterpoint: the pre-BötC is the primary site of respiratory rhythm generation in the mammal. J Appl Physiol 100: 2096-2097, 2006.
19. Feldman JL, Kam K, Janczewski WA. Practice makes perfect, even for breathing. Nat Neurosci 12: 961-963, 2009.
20. Fortin G, Thoby-Brisson M. Embryonic emergence of the respiratory rhythm generator. Respir Physiol Neurobiol 168: 86-91, 2009.
21. Fortuna MG, West GH, Stornetta RL, Guyenet PG. Bötzinger expiratory augmenting neurons and the parafacial respiratory group. J Neurosci 28: 2506-2515, 2008.
22. Frermann D, Keller BU, Richter DW. Calcium oscillations in rhythmically active respiratory neurons in the brain stem of the mouse. J Physiol 515: 119-131, 1999.
23. Fukuda Y, Honda Y. Modification by chemical stimuli of temporal difference in the onset of inspiratory activity between vagal (superior laryngeal) or hypoglossal and phrenic nerves of the rat. Jpn J Physiol 38: 309-319, 1988.
24. Grillner S, Markram H, DeSchutter E, Silberberg G, LeBeau FEN. Microcircuits in action: from CPGs to neocortex. Trends Neurosci 28: 525-533, 2005.
25. Guyenet PG. Carl Ludwig Lecture: retrotrapezoid nucleus, CO2 homeostasis, and breathing automaticity. J Appl Physiol 105: 404-416, 2008.
26. Guyenet PG, Bayliss DA, Stornetta RL, Fortuna MG, Abbott SB, DePuy SD. Retrotrapezoid nucleus, respiratory chemosensitivity and breathing automaticity. Respir Physiol Neurobiol 168: 59-68, 2009.
27. Guyenet PG, Mulkey DK. Retrotrapezoid nucleus and parafacial respiratory group. Respir Physiol Neurobiol 173: 244-255, 2010.
28. Guyenet PG, Mulkey DK, Stornetta RL, Bayliss DA. Regulation of ventral surface chemoreceptors by the central respiratory pattern generator. J Neurosci 25: 8938-8947, 2005.
29. Hegger R, Kantz H, Schreiber T. Practical implementation of nonlinear time series methods: The TISEAN package. Chaos 9: 413-435, 1999.
30. Iizuka M, Fregosi RF. Influence of hypercapnic acidosis and hypoxia on abdominal expiratory nerve activity in the rat. Respir Physiol Neurobiol 157: 196-205, 2007.
31. Janczewski WA, Feldman JL. Distinct rhythm generators for inspiration and expiration in the juvenile rat. J Physiol 570: 407-420, 2006.
32. Janczewski WA, Onimaru H, Homma I, Feldman JL. Opioid-resistant respiratory pathway from the preinspiratory neurones to abdominal muscles: in vivo and in vitro study in the newborn rat J Physiol 545: 1017-1026, 2002.
33. Jiang C, Lipski J. Extensive monosynaptic inhibition of ventral respiratory group neurons by augmenting neurons in the Bötzinger complex in the cat. Exp Brain Res 81: 639-648, 1990.
34. Joseph IM, Butera RJ. A simple model of dynamic interactions between respiratory centers. Conf Proc IEEE Eng Med Biol Soc 6: 5840-5842, 2005.
35. Kay LM, Beshel J, Brea J, Martin C, Rojas-Libano D, Kopell N. Olfactory oscillations: the what, how and what for. Trends Neurosci 32: 207-214, 2009.
36. Koshiya N, Smith JC. Neuronal pacemaker for breathing visualized in vitro. Nature 400: 360-363, 1999.
37. Leiter JC, St. -John WM. Phrenic, vagal and hypoglossal activities in rat: pre-inspiratory, inspiratory, expiratory components. Respir Physiol Neurobiol 142: 115-125, 2004.
38. Li A, Randall M, Nattie EE. CO2 microdialysis in retrotrapezoid nucleus of the rat increases breathing in wakefulness but not in sleep. J Appl Physiol 87: 910-919, 1999.
39. Marder E, Calabrese RL. Principles of rhythmic motor pattern generation. Physiol Rev 76: 687-717, 1996.
40. Mellen NM, Janczewski WA, Bocchiaro CM, Feldman JL. Opioid-induced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron 37: 821-826, 2003.
41. Morgado-Valle C, Baca SM, Feldman JL. Glycinergic pacemaker neurons in preBötzinger Complex of neonatal mouse. J Neurosci 30: 3634-3639, 2010.
42. Onimaru H, Arata A, Homma I. Primary respiratory rhythm generator in the medulla of brain stem-spinal cord preparation from newborn rat. Brain Res 445: 314-324, 1988.
43. Onimaru H, Arata A, Homma I. Intrinsic burst generation of preinspiratory neurons in the medulla of brain stem-spinal cord preparations isolated from newborn rats. Exp Brain Res 106: 57-68, 1995.
44. Onimaru H, Homma I. Respiratory rhythm generator neurons in medulla of brain stem-spinal cord preparation from newborn rat. Brain Res 403: 380-384, 1987.
45. Onimaru H, Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23: 1478-1486, 2003.
46. Onimaru H, Ikeda K, Kawakami K. Phox2b, RTN/pFRG neurons and respiratory rhythmogenesis. Respir Physiol Neurobiol 168: 13-18, 2009.
47. Onimaru H, Kumagawa Y, Homma I. Respiration-related rhythmic activity in the rostral medulla of newborn rats. J Neurophysiol 96: 55-61, 2006.
48. Pagliardini S, Tan W, Janczewski WA, Feldman JL. Excitation and disinhibition of RTN/pFRG neurons induce active expiration in adult rats. In: The XI-th Oxford Conference on Modeling and Control of Breathing: New Frontiers in Respiratory Control, Program and Abstracts. Nara, Japan: 2009, p. 101.
49. Paton JFR, Abdala APL, Koizumi H, Smith JC, St-John WM. Respiratory rhythm generation during gasping depends on persistent sodium current. Nat Neurosci 9: 311-313, 2006.
50. Peever JH, Shen L, Duffin J. Respiratory pre-motor control of hypoglossal motoneurons in the rat. Neurosci 110: 711-712, 2002.
51. Rekling JC, Feldman JL. PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60: 385-405, 1998.
52. Richter DW. Neural regulation of respiration: rhythmogenesis and afferent control. In: Comprehensive Human Physiology, edited by Gregor R and Windhorst U. Berlin: Springer-Verlag, 1996, vol. 2, p. 2079-2095.
53. Richter DW, Spyer KM. Studying rhythmogenesis of breathing: comparison of in vitro and in vivo models. Trends Neurosci 24: 464-472, 2001.
54. Rubin JE, Shevtsova NA, Ermentrout GB, Smith JC, Rybak IA. Multiple rhythmic states in a model of the respiratory central pattern generator. J Neurophysiol 101: 2146-2165, 2009.
55. Rybak IA, Abdala AP, Markin SN, Paton JF, Smith JC. Spatial organization and state-dependent mechanisms for respiratory rhythm and pattern generation. Prog Brain Res 165: 201-220, 2007.
56. Rybak IA, O'Connor R, Ross A, Shevtsova NA, Nuding SC, Segers LS, Shannon R, Dick TE, Dunin-Barkowski WL, Orem JM, Solomon IC, Morris KF, Lindsey BG. Reconfiguration of the pontomedullary respiratory network: a computational modeling study with coordinated in vivo experiments. J Neurophysiol 100: 1770-1799, 2008.
57. Rybak IA, Ptak K, Shevtsova NA, McCrimmon DR. Sodium currents in neurons from the rostroventrolateral medulla of the rat. J Neurophysiol 90: 1635-1642, 2003a.
58. Rybak IA, Shevtsova NA, Paton JF, Dick TE, St-John WM, Morschel M, Dutschmann M. Modeling the ponto-medullary respiratory network. Respir Physiol Neurobiol 143: 307-319, 2004.
59. Rybak IA, Shevtsova NA, St-John WM, Paton JF, Pierrefiche O. Endogenous rhythm generation in the pre-Bötzinger complex and ionic currents: modelling and in vitro studies. Eur J Neurosci 18: 239-257, 2003b.
60. Schwarzacher S, Wilhelm Z, Anders K, Richter D. The medullary respiratory network in the rat. J Physiol 435: 631-644, 1991.
61. Singer W. Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55: 349-374, 1993.
62. Smith JC, Abdala AP, Koizumi H, Rybak IA, Paton JF. Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol 98: 3370-3387, 2007.
63. Smith JC, Abdala AP, Rybak IA, Paton JF. Structural and functional architecture of respiratory networks in the mammalian brain stem. Philos Trans R Soc Lond B 364: 2577-2587, 2009.
64. Smith JC, Butera RJ, Koshiya N, Del Negro C, Wilson CG, Johnson SM. Respiratory rhythm generation in neonatal and adult mammals: the hybrid pacemaker-network model. Respir Physiol 122: 131-147, 2000.
65. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. Pre-Bötzinger complex: a brain stem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
66. St-John WM, Paton JF. Characterizations of eupnea, apneusis and gasping in a perfused rat preparation. Respir Physiol 123: 201-213, 2000.
67. Strohl KP, Thomas AJ, St Jean P, Schlenker EH, Koletsky RJ, Schork NJ. Ventilation and metabolism among rat strains. J Appl Physiol 82: 317-323, 1997.
68. Thoby-Brisson M, Karlen M, Wu N, Charnay P, Champagnat J, Fortin G. Genetic identification of an embryonic parafacial oscillator coupling to the preBötzinger complex. Nat Neurosci 12: 1028-1100, 2009.
69. Tian GF, Peever JH, Duffin J. Bötzinger-complex, bulbospinal expiratory neurones monosynaptically inhibit ventral-group respiratory neurones in the decerebrate rat. Exp Brain Res 124: 173-180, 1999.
70. Tort AB, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a t-maze task. Proc Natl Acad Sci USA 105: 20517-20522, 2008.
71. Winter SM, Fresemann J, Schnell C, Oku Y, Hirrlinger J, Hülsmann S. Glycinergic interneurons are functionally integrated into the inspiratory network of mouse medullary slices. Pfluegers 458: 459-469, 2009.
72. Wittmeier S, Song G, Duffin J, Poon CS. Pacemakers handshake synchronization mechanism of mammalian respiratory rhythmogenesis. Proc Natl Acad Sci USA 105: 18000-18005, 2008.
73. Zhou D, Huang Q, Fung ML, Li A, Darnall RA, Nattie EE, St John WM. Phrenic response to hypercapnia in the unanesthetized, decerbrate, newborn rat. Respir Physiol 104: 11-22, 1996.