Respiratory responses induced by blockades of GABA and glycine receptors within the Bötzinger complex and the pre-Bötzinger complex of the rabbit

Brain Research

Volumn 1344, Issue , 2010, Pages 134-147

  Bongianni, Fulvia ^a   Mutolo, Donatella ^a   Cinelli, Elenia ^a   Pantaleo, Tito ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Bicuculline; Control of respiration; Inhibitory amino acid receptor; Respiratory rhythm generation; Strychnine

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 3 AMINOPROPYL(DIETHOXYMETHYL)PHOSPHINIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; BICUCULLINE; GLYCINE RECEPTOR; STRYCHNINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APNEA; ARTICLE; ARTIFICIAL VENTILATION; BOTZINGER COMPLEX; BREATHING; BREATHING RATE; CONTROLLED STUDY; HYPERCAPNIA; MALE; MEDULLA OBLONGATA; NONHUMAN; PRE BOTZINGER COMPLEX; PRIORITY JOURNAL; RABBIT; RESPIRATION DEPRESSION; RESPIRATORY FUNCTION;

ANIMALS; BICUCULLINE; GABA ANTAGONISTS; GABA-A RECEPTOR AGONISTS; GLYCINE AGENTS; HYPERCAPNIA; MALE; MICROINJECTIONS; MUSCIMOL; ORGANOPHOSPHORUS COMPOUNDS; PYRIDAZINES; RABBITS; RECEPTORS, GABA; RECEPTORS, GLYCINE; RESPIRATORY CENTER; RESPIRATORY PHYSIOLOGICAL PHENOMENA; STRYCHNINE; TIME FACTORS;

ORYCTOLAGUS CUNICULUS; STRYCHNOS TOXIFERA;

EID: 77953915875     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.05.032     Document Type: Article

References (74)

1. Abdala A.P., Rybak I.A., Smith J.C., and Paton J.F. Abdominal expiratory activity in the rat brainstem-spinal cord in situ: patterns, origins and implications for respiratory rhythm generation. J. Physiol. 587 (2009) 3539-3559
2. Alheid G.F., and McCrimmon D.R. The chemical neuroanatomy of breathing. Respir. Physiol. Neurobiol. 164 (2008) 3-11
3. 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
4. Bianchi A.L., Denavit-Saubie M., and Champagnat J. Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol. Rev. 75 (1995) 1-45
5. Blessing W.W. Distribution of glutamate decarboxylase-containing neurons in rabbit medulla oblongata with attention to intramedullary and spinal projections. Neuroscience 37 (1990) 171-185
6. Bongianni F., Mutolo D., and Pantaleo T. Depressant effects on inspiratory and expiratory activity produced by chemical activation of Bötzinger complex neurons in the rabbit. Brain Res. 749 (1997) 1-9
7. Bongianni F., Mutolo D., Cinelli E., and Pantaleo T. Neurokinin receptor modulation of respiratory activity in the rabbit. Eur. J. Neurosci. 27 (2008) 3233-3243
8. Bongianni F., Mutolo D., Cinelli E., and Pantaleo T. Respiratory role of GABA and glycine receptors within the Bötzinger complex of the rabbit. International symposium on respiratory control. St-Maximin, France (2008) P 31
9. Bongianni F., Mutolo D., Cinelli E., and Pantaleo T. Respiratory role of GABA and glycine receptors within the Bötzinger complex of the rabbit. Acta Physiol. 197 Suppl. 672 (2009) 42
10. Busselberg D., Bischoff A.M., Paton J.F., and Richter D.W. Reorganisation of respiratory network activity after loss of glycinergic inhibition. Pflugers Arch. 441 (2001) 444-449
11. Busselberg 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) 831-841
12. Chitravanshi V.C., and Sapru H.N. Microinjections of glycine into the pre-Bötzinger complex inhibit phrenic nerve activity in the rat. Brain Res. 947 (2002) 25-33
13. Cohen M.I. Neurogenesis of respiratory rhythm in the mammal. Physiol. Rev. 59 (1979) 1105-1173
14. 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
15. Debarbieux F., Brunton J., and Charpak S. Effect of bicuculline on thalamic activity: a direct blockade of IAHP in reticularis neurons. J. Neurophysiol. 79 (1998) 2911-2918
16. Dutschmann M., and Herbert H. NMDA and GABAA receptors in the rat Kolliker-Fuse area control cardiorespiratory responses evoked by trigeminal ethmoidal nerve stimulation. J. Physiol. 510 (1998) 793-804
17. 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
18. Ellenberger H.H., and Feldman J.L. Brainstem connections of the rostral ventral respiratory group of the rat. Brain Res. 513 (1990) 35-42
19. Ezure K. Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog. Neurobiol. 35 (1990) 429-450
20. Ezure K., Tanaka I., and Kondo M. Glycine is used as a transmitter by decrementing expiratory neurons of the ventrolateral medulla in the rat. J. Neurosci. 23 (2003) 8941-8948
21. Ezure K., Tanaka I., and Saito Y. Brainstem and spinal projections of augmenting expiratory neurons in the rat. Neurosci. Res. 45 (2003) 41-51
22. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
23. Gang S., Sato Y., Kohama I., and Aoki M. Afferent projections to the Bötzinger complex from the upper cervical cord and other respiratory related structures in the brainstem in cats: retrograde WGA-HRP tracing. J. Auton. Nerv. Syst. 56 (1995) 1-7
24. Gaytan S.P., Calero F., Nunez-Abades P.A., Morillo A.M., and Pasaro R. Pontomedullary efferent projections of the ventral respiratory neuronal subsets of the rat. Brain Res. Bull. 42 (1997) 323-334
25. Haji A., Takeda R., and Okazaki M. Neuropharmacology of control of respiratory rhythm and pattern in mature mammals. Pharmacol. Ther. 86 (2000) 277-304
26. Hayashi F., and Lipski J. The role of inhibitory amino acids in control of respiratory motor output in an arterially perfused rat. Respir. Physiol. 89 (1992) 47-63
27. Jiang C., and Lipski J. Extensive monosynaptic inhibition of ventral respiratory group neurons by augmenting neurons in the Bötzinger complex in the cat. Exp. Brain Res. 81 (1990) 639-648
28. Jiang C., and Shen E. Respiratory neurons in the medulla of the rabbit: distribution, discharge patterns and spinal projections. Brain Res. 541 (1991) 284-292
29. Jonas P., Bischofberger J., and Sandkuhler J. Corelease of two fast neurotransmitters at a central synapse. Science 281 (1998) 419-424
30. 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
31. Liu Y.Y., Ju G., and Wong-Riley M.T. Distribution and colocalization of neurotransmitters and receptors in the pre-Bötzinger complex of rats. J. Appl. Physiol. 91 (2001) 1387-1395
32. Liu Y.Y., Wong-Riley M.T., Liu J.P., Jia Y., Liu H.L., Jiao X.Y., and Ju G. GABAergic and glycinergic synapses onto neurokinin-1 receptor-immunoreactive neurons in the pre-Botzinger complex of rats: light and electron microscopic studies. Eur. J. Neurosci. 16 (2002) 1058-1066
33. Mandel D.A., and Schreihofer A.M. Modulation of the sympathetic response to acute hypoxia by the caudal ventrolateral medulla in rats. J. Physiol. 587 (2009) 461-475
34. Marchenko V., and Rogers R.F. GABAAergic and glycinergic inhibition in the phrenic nucleus organizes and couples fast oscillations in motor output. J. Neurophysiol. 101 (2009) 2134-2145
35. Markstahler U., Kremer E., Kimmina S., Becker K., and Richter D.W. Effects of functional knock-out of alpha 1 glycine-receptors on breathing movements in oscillator mice. Respir. Physiol. Neurobiol. 130 (2002) 33-42
36. Monnier A., Alheid G.F., and McCrimmon D.R. Defining ventral medullary respiratory compartments with a glutamate receptor agonist in the rat. J. Physiol. 548 (2003) 859-874
37. Morgado-Valle C., Baca S.M., and Feldman J.L. Glycinergic pacemaker neurons in preBotzinger complex of neonatal mouse. J. Neurosci. 30 (2010) 3634-3639
38. Mutolo D., Bongianni F., Carfi M., and Pantaleo T. Respiratory responses to chemical stimulation of the parabrachial nuclear complex in the rabbit. Brain Res. 807 (1998) 182-186
39. Mutolo D., Bongianni F., Carfi M., and Pantaleo T. Respiratory changes induced by kainic acid lesions in rostral ventral respiratory group of rabbits. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 (2002) R227-R242
40. Mutolo D., Bongianni F., Nardone F., and Pantaleo T. Respiratory responses evoked by blockades of ionotropic glutamate receptors within the Bötzinger complex and the pre-Bötzinger complex of the rabbit. Eur. J. Neurosci. 21 (2005) 122-134
41. Mutolo D., Bongianni F., Cinelli E., Fontana G.A., and Pantaleo T. Modulation of the cough reflex by antitussive agents within the caudal aspect of the nucleus tractus solitarii in the rabbit. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 (2008) R243-R251
42. Nicholson C. Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res. 333 (1985) 325-329
43. Nicholson C., and Sykova E. Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 21 (1998) 207-215
44. Okazaki M., Takeda R., Haji A., and Yamazaki H. Glutamic acid decarboxylase-immunoreactivity of bulbar respiratory neurons identified by intracellular recording and labeling in rats. Brain Res. 914 (2001) 34-47
45. Patlak C.S., and Fenstermacher J.D. Measurements of dog blood-brain transfer constants by ventriculocisternal perfusion. Am. J. Physiol. 229 (1975) 877-884
46. 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 (Lond) 509 (1998) 245-254
47. Rekling J.C., and Feldman J.L. PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 60 (1998) 385-405
48. 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
49. Rubin J.E., Shevtsova N.A., Ermentrout G.B., Smith J.C., and Rybak I.A. Multiple rhythmic states in a model of the respiratory central pattern generator. J. Neurophysiol. 101 (2009) 2146-2165
50. Rybak I.A., Abdala A.P., Markin S.N., Paton J.F., and Smith J.C. Spatial organization and state-dependent mechanisms for respiratory rhythm and pattern generation. Prog. Brain Res. 165 (2007) 201-220
51. Rybak I.A., O'Connor R., Ross A., Shevtsova N.A., Nuding S.C., Segers L.S., Shannon R., Dick T.E., Dunin-Barkowski W.L., Orem J.M., Solomon I.C., Morris K.F., and Lindsey B.G. Reconfiguration of the pontomedullary respiratory network: a computational modeling study with coordinated in vivo experiments. J. Neurophysiol. 100 (2008) 1770-1799
52. Schmid K., Bohmer G., and Gebauer K. GABAB receptor mediated effects on central respiratory system and their antagonism by phaclofen. Neurosci. Lett. 99 (1989) 305-310
53. Schmid K., Bohmer G., and Gebauer K. GABAA receptor mediated fast synaptic inhibition in the rabbit brain-stem respiratory system. Acta Physiol. Scand. 142 (1991) 411-420
54. Schmid K., Bohmer G., and Gebauer K. Glycine receptor-mediated fast synaptic inhibition in the brainstem respiratory system. Respir. Physiol. 84 (1991) 351-361
55. Schreihofer A.M., Stornetta R.L., and Guyenet P.G. Evidence for glycinergic respiratory neurons: Botzinger neurons express mRNA for glycinergic transporter 2. J. Comp. Neurol. 407 (1999) 583-597
56. Schwarzacher S.W., Smith J.C., and Richter D.W. Pre-Bötzinger complex in the cat. J. Neurophysiol. 73 (1995) 1452-1461
57. Segers L.S., Nuding S.C., Dick T.E., Shannon R., Baekey D.M., Solomon I.C., Morris K.F., and Lindsey B.G. Functional connectivity in the pontomedullary respiratory network. J. Neurophysiol. 100 (2008) 1749-1769
58. Shek J.W., Wen G.Y., and Wisniewski H.M. Atlas of the rabbit brain and spinal cord (1986), Karger, Basel
59. Shen L., Li Y.M., and Duffin J. Inhibitory connections among rostral medullary expiratory neurones detected with cross-correlation in the decerebrate rat. Pflugers Arch. 446 (2003) 365-372
60. Smith J.C., Morrison D.E., Ellenberger H.H., Otto M.R., and Feldman J.L. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J. Comp. Neurol. 281 (1989) 69-96
61. 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
62. 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
63. Smith J.C., Abdala A.P., Rybak I.A., and Paton J.F. Structural and functional architecture of respiratory networks in the mammalian brainstem. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009) 2577-2587
64. Solomon I.C. Excitation of phrenic and sympathetic output during acute hypoxia: contribution of medullary oxygen detectors. Respir. Physiol. 121 (2000) 101-117
65. 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
66. St John W.M. Neurogenesis of patterns of automatic ventilatory activity. Prog. Neurobiol. 56 (1998) 97-117
67. St John W.M. Noeud vital for breathing in the brainstem: gasping-yes, eupnoea-doubtful. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364 (2009) 2625-2633
68. St John W.M., and Paton J.F. Neurogenesis of gasping does not require inhibitory transmission using GABA(A) or glycine receptors. Respir. Physiol. Neurobiol. 132 (2002) 265-277
69. Tian G.F., Peever J.H., and Duffin J. Botzinger-complex, bulbospinal expiratory neurones monosynaptically inhibit ventral-group respiratory neurones in the decerebrate rat. Exp. Brain Res. 124 (1999) 173-180
70. Tian G.F., Peever J.H., and Duffin J. Mutual inhibition between Botzinger-complex bulbospinal expiratory neurons detected with cross-correlation in the decerebrate rat. Exp. Brain Res. 125 (1999) 440-446
71. Tryba A.K., Pena 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
72. Von Euler C. Brain stem mechanisms for generation and control of breathing pattern. In: Cherniack N.S., and Widdicombe J.G. (Eds). Handbook of Physiology. The Respiratory System. Control of Breathing Vol. II (1986), American Physiological Society, Bethesda, Maryland 1-67
73. Winter S.M., Fresemann J., Schnell C., Oku Y., Hirrlinger J., and Hulsmann S. Glycinergic interneurons are functionally integrated into the inspiratory network of mouse medullary slices. Pflugers Arch. 458 (2009) 459-469
74. Zhang W., Barnbrock A., Gajic S., Pfeiffer A., and Ritter B. Differential ontogeny of GABA(B)-receptor-mediated pre- and postsynaptic modulation of GABA and glycine transmission in respiratory rhythm-generating network in mouse. J. Physiol. 540 (2002) 435-446