Respiratory rhythm generation in vivo

Physiology

Volumn 29, Issue 1, 2014, Pages 58-71

  Richter, Diethelm W ^a,b   Smith, Jeffrey C ^a,b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXIN II; NERVE PROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL; BREATHING; BREATHING MECHANICS; HUMAN; MEMBRANE POTENTIAL; NERVE CELL; PHYSIOLOGY; RESPIRATORY FUNCTION; REVIEW;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; HUMANS; MEMBRANE POTENTIALS; NERVE TISSUE PROTEINS; NEURONS; RESPIRATION; RESPIRATORY MECHANICS; RESPIRATORY PHYSIOLOGICAL PHENOMENA;

EID: 84891551593     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00035.2013     Document Type: Review

References (101)

1. 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, 2009.
2. Abdala AP, Dutschmann M, Bissonnette JM, Paton JF. Correction of respiratory disorders in a mouse model of Rett syndrome. Proc Natl Acad Sci USA 107: 18208-18213, 2010.
3. Alheid GF, Milsom WK, McCrimmon DR. Pontine influences on breathing: an overview. Respir Physiol Neurobiol 143: 105-114, 2004.
4. Alheid GF, McCrimmon DR. The chemical neuroanatomy of breathing. Respir Physiol Neurobiol 164: 3-11, 2008.
5. Backman SB, Anders C, Ballantyne D, Röhrig N, Camerer H, Mifflin S, Jordan D, Dickhaus H, Spyer KM, Richter DW. Evidence for a monosynaptic connection between slowly adapting pulmonary stretch receptor afferents and inspira-tory beta neurones. Pflügers Arch 402: 129-136, 1984.
6. Balis UJ, Morris KF, Koleski J, Lindsey BG. Simulations of a ventrolateral medullary neural network for respiratory rhyth-mogenesis inferred from spike train cross-correlation. Biol Cybern 70: 311-327, 1994.
7. Ballantyne D, Richter DW. Post-synaptic inhibition of bulbar inspiratory neurones in the cat. J Physiol 348: 67-87, 1984.
8. Bianchi AL, Grélot L, Iscoe S, Remmers JE. Electrophysiolog-ical properties of rostral medullary respiratory neurones in the cat: an intracellular study. J Physiol 407: 293-310, 1988.
9. Büsselberg D, Bischoff AM, Paton JF, Richter DW. Reorganisation of respiratory network activity after loss of glycinergic inhibition. Pflügers Arch 441: 444-449, 2001.
10. Büsselberg D, Bischoff AM, Becker K, Becker CM, Richter DW. The respiratory rhythm in mutant oscillator mice. Neu-rosci Lett 316: 99-102, 2001.
11. Busselberg D, Bischoff AM, Richter DW. A combined blockade of glycine and calcium-dependent potassium channels abolishes the respiratory rhythm. Neuroscience 122: 831-841, 2003.
12. Butera RJ Jr, Rinzel J, Smith JC. Models of respiratory rhythm generation in the pre-Botzinger complex. II. Populations of coupled pacemaker neurons. J Neurophysiol 82: 398-415, 1999.
13. Butera, RJ Jr, Rinzel J, Smith JC. Models of respiratory rhythm generation in the pre-Botzinger complex. I. Bursting pacemaker neurons. J Neurophysiol 82: 382-397, 1999.
14. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, Neul JL, Gong S, Lu HC, Heintz N, Ekker M, Rubenstein JL, Noebels JL, Rosenmund C, Zoghbi HY. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468: 263-269, 2010.
15. Connelly CA, Dobbins EG, Feldman JL. Pre-Botzinger complex in cats: respiratory neuronal discharge patterns. Brain Res 590: 337-340, 1992.
16. Dediu D, Levinson SC. On the antiquity of language: the reinterpretation of Neandertal linguistic capacities and its consequences. Front Psychol 4: 397, 2013.
17. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC. Persistent sodium current, membrane properties and bursting behavior of pre-Botzinger complex inspiratory neurons in vitro. J Neu-rophysiol 88: 2242-2250, 2002.
18. Devor A. The great gate: control of sensory information flow to the cerebellum. Cerebellum 1: 27-34, 2002.
19. Dick TE, Bellingham MC, Richter DW. Pontine respiratory neurons in anesthetized cats. Brain Res 636: 259-269, 1994.
20. Dubreuil V, Ramanantsoa N, Trochet D, Vaubourg V, Amiel J, Gallego J, Brunet JF, Goridis C. A human mutation in Phox2b causes lack of CO2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. Proc Natl Acad Sci USA 105: 1067-1072, 2008.
21. Dutschmann M, Paton JF. Trigeminal reflex regulation of the glottis depends on central glycinergic inhibition in the rat. Am J Physiol Regul Integr Comp Physiol 282: R999-R1005, 2002.
22. Ezure K, Tanaka I, Kondo M. Glycine is used as a transmitter by decrementing expiratory neurons of the ventrolateral medulla in the rat. J Neurosci 23: 8941-8948, 2003.
23. Feldman JL. Chapter 14: looking forward to breathing. Prog Brain Res 188: 213-218, 2011.
24. Fluorens P. Note sur le point vital de la moelle allongée. CR Acad Sci 33: 437-439, 1851.
25. Frermann D, Keller BU, Richter DW. Calcium oscillations in rhythmically active respiratory neurones in the brainstem of the mouse. J Physiol 515: 119-131, 1999.
26. Guyenet PG, Mulkey DK. Retrotrapezoid nucleus and parafacial respiratory group. Respir Physiol Neurobiol 173: 244-255, 2010.
27. Herrigel E. Zen in the Art of Archery. New York: Vintage, 1972.
28. Hutchison AA, Wozniak JA, Choi HG, Conlon M, Otto RA, Abrams RM, Kosch PC. Laryngeal and diaphragmatic muscle activities and airflow patterns after birth in premature lambs. J Appl Physiol 75: 121-131, 1993.
29. Jasinski PE, Molkov YI, Shevtsova NA, Smith JC, Rybak IA. Sodium and calcium mechanisms of rhythmic bursting in excitatory neural networks of the pre-Botzinger complex: a computational modelling study. Eur J Neurosci 37: 212-230, 2013.
30. Johnson SM, Koshiya N, Smith JC. Isolation of the kernel for respiratory rhythm generation in a novel preparation: the pre-Botzinger complex "island". J Neurophysiol 85: 1772-1776, 2001.
31. Jonas P, Bischofberger J, Sandkuhler J. Core-lease of two fast neurotransmitters at a central synapse. Science 281: 419-424, 1998.
32. Julu PO, Kerr AM, Apartopoulos F, Al-Rawas S, Engerström IW, Engerström L, Jamal GA, Han-sen S. Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder. Arch Dis Child 85: 29-37, 2001.
33. Kobayashi S, Onimaru H, Inoue M, Inoue T, Sasa R. Localization and properties of respiratory neurons in the rostral pons of the newborn rat. Neu-roscience 134: 317-325, 2005.
34. Koizumi H, Smith JC. Persistent Na+ and K+-dominated leak currents contribute to respiratory rhythm generation in the pre-Botzinger complex in vitro. J Neurosci 28: 1773-1785, 2008.
35. Koizumi H, Smerin SE, Yamanishi T, Moorjani BR, Zhang R, Smith JC. TASK channels contribute to the K+-dominated leak current regulating respiratory rhythm generation in vitro. J Neurosci 30: 4273-4284, 2010.
36. Koizumi H, Koshiya N, Chia JX, Cao F, Nugent J, Zhang R, Smith JC. Structural-functional properties of identified excitatory and inhibitory interneurons within pre-Botzinger complex respiratory microcir-cuits. J Neurosci 33: 2994-3009, 2013.
37. Koshiya N, Smith JC. Neuronal pacemaker for breathing visualized in vitro. Nature 400: 360-363, 1999.
38. Lalley PM, Bischoff AM, Richter DW. Serotonin 1A-receptor activation suppresses respiratory apneusis in the cat. Neurosci Lett 172: 59-62, 1994.
39. Lalley PM, Pierrefiche O, Bischoff AM, Richter DW. cAMP-dependent protein kinase modulates expiratory neurons in vivo. J Neurophysiol 77: 1119-1131, 1997.
40. Lawson EE, Richter DW, Ballantyne D, Lalley PM. Peripheral chemoreceptor inputs to medullary in-spiratory and postinspiratory neurons of cats. Pflügers Arch 414: 523-533, 1989.
41. Lawson EE, Richter DW, Bischoff A. Intracellular recordings of respiratory neurons in the lateral medulla of piglets. J Appl Physiol 66: 983-988, 1989.
42. Lawson EE, Richter DW, Czyzyk-Krzeska MF, Bischoff A, Rudesill RC. Respiratory neuronal activity during apnea and other breathing patterns induced by laryngeal stimulation. J Appl Physiol 70: 2742-2749, 1991.
43. Lipski J, McAllen RM, Spyer KM. The carotid chemoreceptor input to the respiratory neurones of the nucleus of tractus solitarus. J Physiol 269: 797-810, 1977.
44. Liss B, Roeper J. A role for neuronal K(ATP) channels in metabolic control of the seizure gate. Trends Pharmacol Sci 22: 599-601; discussion 601-602, 2001.
45. Mandala M, Rufa A, Cerase A, Bracco S, Galluzzi P, Venturi C, Nuti D. Lateral medullary ischemia presenting with persistent hiccups and vertigo. Int J Neurosci 120: 226-230, 2010.
46. Manzke T, Preusse S, Hülsmann S, Richter DW. Developmental changes of serotonin 4(a) receptor expression in the rat pre-Botzinger complex. J Comp Neurol 506: 775-790, 2008.
47. Manzke T, Dutschmann M, Schlaf G, Mörschel M, Koch UR, Ponimaskin E, Bidon O, Lalley PM, Rich-ter DW. Serotonin targets inhibitory synapses to induce modulation of network functions. Philos Trans R Soc Lond B Biol Sci 364: 2589-2602, 2009.
48. Manzke T, Niebert M, Koch UR, Caley A, Vogel-gesang S, Hülsmann S, Ponimaskin E, Müller U, Smart TG, Harvey RJ, Richter DW. Serotonin receptor 1A-modulated phosphorylation of glycine receptor alpha3 controls breathing in mice. J Clin Invest 120: 4118-4128, 2010.
49. Markstahler U, Kremer E, Kimmina S, Becker K, Richter DW. Effects of functional knock-out of alpha 1 glycine-receptors on breathing movements in oscillator mice. Respir Physiol Neurobiol 130: 33-42, 2002.
50. McCrimmon DR, Alheid GF, Jiang M, Calandriello T, Topgi A. Converging functional and anatomical evidence for novel brainstem respiratory compartments in the rat. Adv Exp Med Biol 551: 101-105, 2004.
51. Medrihan L, Tantalaki E, Aramuni G, Sargsyan V, Dudanova I, Missler M, Zhang W. Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J Neu-rophysiol 99: 112-121, 2008.
52. Merrill EG. Where are the real respiratory neurons? Fed Proc 40: 2389-2394, 1981.
53. Mironov SL, Langohr K, Richter DW. A1 adeno-sine receptors modulate respiratory activity of the neonatal mouse via the cAMP-mediated signaling pathway. J Neurophysiol 81: 247-255, 1999.
54. Mironov SL. Metabotropic glutamate receptors activate dendritic calcium waves and TRPM channels which drive rhythmic respiratory patterns in mice. J Physiol 586: 2277-2291, 2008.
55. Morgado-Valle C, Baca SM, Feldman JL. Glycin-ergic pacemaker neurons in preBotzinger complex of neonatal mouse. J Neurosci 30: 3634-3639, 2010.
56. Morschel M, Dutschmann M. Pontine respiratory activity involved in inspiratory/expiratory phase transition. Philos Trans R Soc Lond B Biol Sci 364: 2517-2526, 2009.
57. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA, Guyenet PG. Respiratory control by ventral surface chemoreceptor neurons in rats. Nature Neurosci 7: 1360-1369, 2004.
58. Ogilvie MD, Gottschalk A, Anders K, Richter DW, Pack AI. A network model of respiratory rhyth-mogenesis. Am J Physiol Regul Integr Comp Physiol 263: R962-R975, 1992.
59. Pace RW, Mackay DD, Feldman JL, Del Negro CA. Inspiratory bursts in the preBotzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. J Physiol 582: 113-125, 2007.
60. Paton JF. A working heart-brainstem preparation of the mouse. J Neurosci Meth 65: 63-68, 1996.
61. Paton JF, Abdala AP, Koizumi H, Smith JC, St-John WM. Respiratory rhythm generation during gasping depends on persistent sodium current. Nat Neurosci 9: 311-313, 2006.
62. Peña F, Parkis MA, Tryba AK, Ramirez JM. Differential contribution of pacemaker properties to the generation of respiratory rhythms during nor-moxia and hypoxia. Neuron 43: 105-117, 2004.
63. Pierrefiche O, Champagnat J, Richter DW. Calcium-dependent conductances control neurones involved in termination of inspiration in cats. Neurosci Lett 184: 101-104, 1995.
64. Pierrefiche O, Haji A, Bischoff A, Richter DW. Calcium currents in respiratory neurons of the cat in vivo. Pflügers Arch 438: 817-826, 1999.
65. Ramirez JM, Richter DW. The neuronal mechanisms of respiratory rhythm generation. Curr Opin Neurobiol 6: 817-825, 1996.
66. Ramirez JM, Telgkamp P, Elsen FP, Quellmalz UJ, Richter DW. Respiratory rhythm generation in mammals: synaptic and membrane properties. Respir Physiol 110: 71-85, 1997.
67. Ramirez JM, Koch H, Garcia AJ 3rd, Doi A, Zanella S. The role of spiking and bursting pacemakers in the neuronal control of breathing. J Biol Phys 37: 241-261, 2011.
68. Rekling JC, Feldman JL. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60: 385-405, 1998.
69. Remmers JE, Richter DW, Ballantyne D, Bainton CR, Klein JP. Reflex prolongation of stage I of expiration. Pflügers Arch 407: 190-198, 1986.
70. Rett A. On a unusual brain atrophy syndrome in hyperammonemia in childhood. Wien Med Wochenschr 116: 723-726, 1966.
71. Richter DW, Camerer H, Meesmann M, Röhrig N. Studies on the synaptic interconnection between bulbar respiratory neurones of cats. Pflügers Arch 380: 245-257, 1979.
72. Richter DW. Generation and maintenance of the respiratory rhythm. J Exp Biol 100: 93-107, 1982.
73. Richter DW, Ballantyne D, Remmers JE. The differential organization of medullary post-inspira-tory activities. Pflügers Arch 410: 420-427, 1987.
74. Richter DW, Bischoff A, Anders K, Bellingham M, Windhorst U. Response of the medullary respiratory network of the cat to hypoxia. J Physiol 443: 231-256, 1991.
75. Richter DW. Neural regulation of respiration: rhythmogenesis and afferent control. In: Comprehensive Human Physiology: From Cellular Mechanism to Integration, edited by Gregore R, Windhorts U. Berlin: Springer Verlag, 1996, p. 2079-2095.
76. Richter DW, Pierrefiche O, Lalley PM, Polder HR. Voltage-clamp analysis of neurons within deep layers of the brain. J Neurosci Meth 67: 121-123, 1996.
77. Richter DW, Spyer KM. Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci 24: 464-472, 2001.
78. Richter DW, Manzke T, Wilken B, Ponimaskin E. Serotonin receptors: guardians of stable breathing. Trends Mol Med 9: 542-548, 2003.
79. Richter DW, Ballantyne D, Remmers JE. How is the respiratory rhythm generated? A model. News Physiol Sci 1: 109-112, 1986.
80. 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.
81. Rubin JE, Bacak BJ, Molkov YI, Shevtsova NA, Smith JC, Rybak IA. Interacting oscillations in neural control of breathing: modeling and qualitative analysis. J Comput Neurosci 30: 607-632, 2011.
82. Schmid K, Foutz AS, Denavit-Saubie M. Inhibitions mediated by glycine and GABAA receptors shape the discharge pattern of bulbar respiratory neurons. Brain Res 710: 150-160, 1996.
83. Schwarzacher SW, Wilhelm Z, Anders K, Richter DW. The medullary respiratory network in the rat. J Physiol 435: 631-644, 1991.
84. Schwarzacher SW, Smith JC, Richter DW. Pre-Botzinger complex in the cat. J Neurophysiol 73: 1452-1461, 1995.
85. Sears T. Some Neural and Mechanical Aspects of Singing. Music and the Brain, edited by Critchley M, Henson RA. London: Heineman, 1977.
86. Smeets E, Schollen E, Moog U, Matthijs G, Her-bergs J, Smeets H, Curfs L, Schrander-Stumpel C, Fryns JP. Rett syndrome in adolescent and adult females: clinical and molecular genetic findings. Am J Med Genet A 122A: 227-233, 2003.
87. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. Pre-Botzinger complex: a brain-stem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
88. 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.
89. 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 Neu-rophysiol 98: 3370-3387, 2007.
90. Smith JC, Abdala AP, Rybak IA, Paton JF. Structural and functional architecture of respiratory networks in the mammalian brainstem. Philos Trans R Soc Lond B Biol Sci 364: 2577-2587, 2009.
91. Smith JC, Abdala AP, Borgmann A, Rybak IA, Paton JF. Brainstem respiratory networks: building blocks and microcircuits. Trends Neurosci 36: 152-162, 2012.
92. St-John WM, Stornetta RL, Guyenet PG, Paton JF. Location and properties of respiratory neurones with putative intrinsic bursting properties in the rat in situ. J Physiol 587: 3175-3188, 2009.
93. Stettner GM, Huppke P, Brendel C, Richter DW, Gärtner J, Dutschmann M. Breathing dysfunctions associated with impaired control of postin-spiratory activity in Mecp2-/y knockout mice. J Physiol 579: 863-876, 2007.
94. Stettner GM, Huppke P, Gärtner J, Richter DW, Dutschmann M. Disturbances of breathing in Rett syndrome: results from patients and animal models. Adv Exp Med Biol 605: 503-507, 2008.
95. Wall PD. The gate control theory of pain mechanisms. A re-examination and re-statement. Brain 101: 1-18, 1978.
96. Wang S, Shi Y, Shu S, Guyenet PG, Bayliss DA. Phox2b-expressing retrotrapezoid neurons are intrinsically responsive to H and CO2. J Neurosci 33: 7756-7761, 2013.
97. Wilken B, Lalley P, Bischoff AM, Christen HJ, Behnke J, Hanefeld F, Richter DW. Treatment of apneustic respiratory disturbance with a serotonin-receptor agonist. J Pediatr 130: 89-94, 1997.
98. Winter SM, Fresemann J, Schnell C, Oku Y, Hir-rlinger J, Hülsmann S. Glycinergic interneurons are functionally integrated into the inspiratory network of mouse medullary slices. Pflügers Arch 458: 459-469, 2009.
99. Zhao MG, Hülsmann S, Winter SM, Dutschmann M, Richter DW. Calcium-regulated potassium currents secure respiratory rhythm generation after loss of glycinergic inhibition. Eur J Neurosci 24: 145-154, 2006.
100. Zheng Y, Barillot JC, Bianchi AL Patterns of membrane potentials and distributions of the medullary respiratory neurons in the decerebrate rat. Brain Res 546: 261-270, 1991.
101. Zoghbi HY. Rett syndrome: what do we know for sure? Nat Neurosci 12: 239-240, 2009.