Inhibition of the pontine Kölliker-Fuse nucleus reduces genioglossal activity elicited by stimulation of the retrotrapezoid chemoreceptor neurons

Neuroscience

Volumn 328, Issue , 2016, Pages 9-21

  Silva, Josiane N ^a   Lucena, Elvis V ^a   Silva, Talita M ^a   Damasceno, Rosélia S ^a   Takakura, Ana C ^a   Moreira, Thiago S ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Breathing; Chemoreflex; Dorsolateral pons; Genioglossal activity; Ventrolateral medulla

Indexed keywords

GLUTAMATE DECARBOXYLASE 67; MUSCIMOL; N METHYL DEXTRO ASPARTIC ACID; PROTEIN FOS; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 2; 4 AMINOBUTYRIC ACID A RECEPTOR; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYLASPARTIC ACID; SLC17A6 PROTEIN, RAT;

ABDOMINAL WALL MUSCULATURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NUCLEUS; CHEMORECEPTOR CELL; CONTROLLED STUDY; DENERVATION; DIAPHRAGM MUSCLE; GENIOGLOSSUS MUSCLE; HYPERCAPNIA; KOLLIKER FUSE NUCLEUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RETROTRAPEZOID NUCLEUS; SKELETAL MUSCLE; VAGOTOMY; ANIMAL; BREATHING; CYTOLOGY; DIAPHRAGM; DRUG EFFECTS; INNERVATION; MEDULLA OBLONGATA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PONS; TONGUE; WISTAR RAT;

ANIMALS; CHEMORECEPTOR CELLS; DIAPHRAGM; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; HYPERCAPNIA; MALE; MEDULLA OBLONGATA; MUSCIMOL; N-METHYLASPARTATE; NEUROTRANSMITTER AGENTS; PONS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; RESPIRATION; TONGUE; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84965014040     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.04.028     Document Type: Article

References (63)

1. Abbott S.B., Stornetta R.L., Socolovsky C.S., West G.H., Guyenet P.G. Photostimulation of channelrhodopsin-2 expressing ventrolateral medullary neurons increases sympathetic nerve activity and blood pressure in rats. J Physiol 2009, 587:5613-5631.
2. Abbott S.B., DePuy S.D., Nguyen T., Coates M.B., Stornetta R.L., Guyenet P.G. Selective optogenetic activation of rostral ventrolateral medullary catecholaminergic neurons produces cardiorespiratory stimulation in conscious mice. J Neurosci 2013, 33(7):3164-3177.
3. Abdala A.P., Toward M.A., Dutschmann M., Bissonnette J.M., Paton J.F. Deficiency of GABAergic synaptic inhibition in the Kölliker-Fuse area underlies respiratory dysrhythmia in a mouse model of Rett syndrome. J Physiol 2016, 594:223-237.
4. Barna B.F., Takakura A.C., Moreira T.S. Pontomedullary and hypothalamic distribution of Fos-like immunoreactive neurons after acute exercise in rats. Neuroscience 2012, 212:120-130.
5. Barna B.F., Takakura A.C., Moreira T.S. Acute exercise-induced activation of Phox2b-expressing neurons of the retrotrapezoid nucleus in rats may involve the hypothalamus. Neuroscience 2014, 258:355-363.
6. Basting T.M., Burke P.G., Kanbar R., Viar K.E., Stornetta D.S., Stornetta R.L., Guyenet P.G. Hypoxia silences retrotrapezoid nucleus respiratory chemoreceptors via alkalosis. J Neurosci 2015, 35:527-543.
7. Bautista T.G., Dutschmann M. Inhibition of the pontine Kölliker-Fuse nucleus abolishes eupneic inspiratory hypoglossal motor discharge in rat. Neuroscience 2014, 267:22-29.
8. Bautista T.G., Dutschmann M. The role of the Kölliker-Fuse nuclei in the determination of abdominal motor output in a perfused brainstem preparation of juvenile rat. Respir Physiol Neurobiol 2015, (in press).
9. Brancatisano A., Dodd D.S., Engel L.A. Posterior cricoarytenoid activity and glottic size during hyperpnea in humans. J Appl Physiol (1985) 1991, 71:977-982.
10. Chamberlin N.L., Saper C.B. Topographic organization of respiratory responses to glutamate microstimulation of the parabrachial nucleus in the rat. J Neurosci 1994, 14:6500-6510.
11. Damasceno R.S., Takakura A.C., Moreira T.S. Regulation of the chemosensory control of breathing by Kolliker-Fuse neurons. Am J Physiol Regul Integr Comp Physiol 2014, 307:R57-R67.
12. Damasceno R.S., Takakura A.C., Moreira T.S. Respiratory and sympathetic chemoreflex regulation by Kolliker-Fuse neurons in rats. Pflugers Arch 2015, 467:231-239.
13. Dempsey J.A., Veasey S.C., Morgan B.J., O'Donnell C.P. Pathophysiology of sleep apnea. Physiol Rev 2010, 90:47-112.
14. 2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. Proc Natl Acad Sci U S A 2008, 105:1067-1072.
15. Dutschmann M., Dick T.E. Pontine mechanisms of respiratory control. Compr Physiol 2012, 2:2443-2469.
16. Dutschmann M., Herbert H. The Kolliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur J Neurosci 2006, 24:1071-1084.
17. Ezure K., Tanaka I., Saito Y. Brainstem and spinal projections of augmenting expiratory neurons in the rat. Neurosci Res 2003, 45:41-51.
18. Fortuna M.G., Stornetta R.L., West G.H., Guyenet P.G. Activation of the retrotrapezoid nucleus by posterior hypothalamic stimulation. J Physiol 2009, 587:5121-5138.
19. Fulwiler C.E., Saper C.B. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 1984, 319:229-259.
20. Guyenet P.G. Novel two-rhythm generator theory of breathing in mammals. J Physiol 2006, 570:207.
21. Guyenet P.G. Regulation of breathing and autonomic outflows by chemoreceptors. Compr Physiol 2014, 4:1511-1562.
22. 2 homeostasis. Neuron 2015, 87:946-961.
23. Guyenet P.G., Stornetta R.L., Bayliss D.A. Central respiratory chemoreception. J Comp Neurol 2010, 518:3883-3906.
24. Horner R.L. Neural control of the upper airway: integrative physiological mechanisms and relevance for sleep disordered breathing. Compr Physiol 2012, 2:479-535.
25. Huckstepp R.T., Cardoza K.P., Henderson L.E., Feldman J.L. Role of parafacial nuclei in control of breathing in adult rats. J Neurosci 2015, 1052-1067.
26. Jones S.E., Stanić D., Dutschmann M. Dorsal and ventral aspects of the most caudal medullary reticular formation have differential roles in modulation and formation of the respiratory motor pattern in rat. Brain Struct Funct 2015, (in press).
27. Kaufman D.L., Houser C.R., Tobin A.J. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J Neurochem 1991, 56:720-723.
28. Kincaid A.E., Zheng T., Wilson C.J. Connectivity and convergence of single corticostriatal axons. J Neurosci 1998, 18:4722-4731.
29. Marina N., Abdala A.P., Trapp S., Li A., Nattie E.E., Hewinson J., Smith J.C., Paton J.F., Gourine A.V. Essential role of Phox2b-expressing ventrolateral brainstem neurons in the chemosensory control of inspiration and expiration. J Neurosci 2010, 30:12466-12473.
30. Mizusawa A., Ogawa H., Kikuchi Y., Hida W., Shirato K. Role of the parabrachial nucleus in ventilatory responses of awake rats. J Physiol 1995, 489(Pt 3):877-884.
31. Moreira T.S., Takakura A.C., Colombari E., Menani J.V. Antihypertensive effects of central ablations in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 2009, 296:R1797-R1806.
32. Mulkey D.K., Stornetta R.L., Weston M.C., Simmons J.R., Parker A., Bayliss D.A., Guyenet P.G. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 2004, 7:1360-1369.
33. Mulkey D.K., Henderson R.A., Ritucci N.A., Putnam R.W., Dean J.B. Chemical oxidants acidify solitary complex (SC) neurons in the rat. Undersea Hyperb Med 2004, 31:107-111.
34. Nakamura K., Morrison S.F. A thermosensory pathway that controls body temperature. Nat Neurosci 2008, 11:62-71.
35. 2 sensitivity in rats. Respir Physiol 1994, 97:63-77.
36. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol 2002, 64:313-353.
37. Onimaru H., Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 2003, 23:1478-1486.
38. Pagliardini S., Janczewski W.A., Tan W., Dickson C.T., Deisseroth K., Feldman J.L. Active expiration induced by excitation of ventral medulla in adult anesthetized rats. J Neurosci 2011, 31:2895-2905.
39. Paton J.F., Dutschmann M. Central control of upper airway resistance regulating respiratory airflow in mammals. J Anat 2002, 201:319-323.
40. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, vol. 4. Academic Press, San Diego.
41. Pérez Fontán J.J., Velloff C.R. Neuroanatomic organization of the parasympathetic bronchomotor system in developing sheep. Am J Physiol 1997, 273:R121-R133.
42. Ramanantsoa N., Hirsch M.R., Thoby-Brisson M., Dubreuil V., Bouvier J., Ruffault P.L., Matrot B., Fortin G., Brunet J.F., Gallego J., Goridis C. Breathing without CO(2) chemosensitivity in conditional Phox2b mutants. J Neurosci 2011, 31:12880-12888.
43. Richerson G.B. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 2004, 5:449-461.
44. Robertson S.D., Plummer N.W., de Marchena J., Jensen P. Developmental origins of central norepinephrine neuron diversity. Nat Neurosci 2013, 16:1016-1023.
45. Rosin D.L., Chang D.A., Guyenet P.G. Afferent and efferent connections of the rat retrotrapezoid nucleus. J Comp Neurol 2006, 499:64-89.
46. Ruffault P.L., D'Autreaux F., Hayes J.A., Nomaksteinsky M., Autran S., Fujiyama T., Hoshino M., Hagglund M., Kiehn O., Brunet J.F., Fortin G., Goridis C. The retrotrapezoid nucleus neurons expressing Atoh1 and Phox2b are essential for the respiratory response to CO(2). Elife 2015, 4.
47. Schreihofer A.M., Guyenet P.G. Identification of C1 presympathetic neurons in rat rostral ventrolateral medulla by juxtacellular labeling in vivo. J Comp Neurol 1997, 387:524-536.
48. Smith J.C., Morrison D.E., Ellenberger H.H., Otto M.R., Feldman J.L. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 1989, 281:69-96.
49. Song G., Poon C.S. Lateral parabrachial nucleus mediates shortening of expiration and increase of inspiratory drive during hypercapnia. Respir Physiol Neurobiol 2009, 165:9-12.
50. Song G., Yu Y., Poon C.S. Cytoarchitecture of pneumotaxic integration of respiratory and nonrespiratory information in the rat. J Neurosci 2006, 26:300-310.
51. Song G., Tin C., Poon C.S. Bilateral lesions of pontine Kolliker-Fuse nuclei provoke apnea instead of apneusis in anesthetized adult rats. Adv Exp Med Biol 2010, 669:185-188.
52. Stettner G.M., Rukhadze I., Mann G.L., Lei Y., Kubin L. Respiratory modulation of lingual muscle activity across sleep-wake states in rats. Respir Physiol Neurobiol 2013, 188:308-317.
53. Stocker S.D., Simmons J.R., Stornetta R.L., Toney G.M., Guyenet P.G. Water deprivation activates a glutamatergic projection from the hypothalamic paraventricular nucleus to the rostral ventrolateral medulla. J Comp Neurol 2006, 494(4):673-685.
54. Takakura A.C., Moreira T.S. Contribution of excitatory amino acid receptors of the retrotrapezoid nucleus to the sympathetic chemoreflex in rats. Exp Physiol 2011, 96:989-999.
55. 2-sensitive neurons in rats. J Physiol 2006, 572:503-523.
56. Takakura A.C., Moreira T.S., Stornetta R.L., West G.H., Gwilt J.M., Guyenet P.G. Selective lesion of retrotrapezoid Phox2b-expressing neurons raises the apnoeic threshold in rats. J Physiol 2008, 586:2975-2991.
57. Takakura A.C., Colombari E., Menani J.V., Moreira T.S. Ventrolateral medulla mechanisms involved in cardiorespiratory responses to central chemoreceptor activation in rats. Am J Physiol Regul Integr Comp Physiol 2011, 300:R501-510.
58. Takakura A.C., Moreira T.S., De Paula P.M., Menani J.V., Colombari E. Control of breathing and blood pressure by parafacial neurons in conscious rats. Exp Physiol 2013, 98:304-315.
59. Takakura A.C., Barna B.F., Cruz J.C., Colombari E., Moreira T.S. Phox2b-expressing retrotrapezoid neurons and the integration of central and peripheral chemosensory control of breathing in conscious rats. Exp Physiol 2014, 99:571-585.
60. Yokota S., Tsumori T., Ono K., Yasui Y. Phrenic motoneurons receive monosynaptic inputs from the Kolliker-Fuse nucleus: a light- and electron-microscopic study in the rat. Brain Res 2001, 888:330-335.
61. Yokota S., Oka T., Tsumori T., Nakamura S., Yasui Y. Glutamatergic neurons in the Kolliker-Fuse nucleus project to the rostral ventral respiratory group and phrenic nucleus: a combined retrograde tracing and in situ hybridization study in the rat. Neurosci Res 2007, 59:341-346.
62. Yokota S., Niu J.G., Tsumori T., Oka T., Yasui Y. Glutamatergic Kolliker-Fuse nucleus neurons innervate hypoglossal motoneurons whose axons form the medial (protruder) branch of the hypoglossal nerve in the rat. Brain Res 2011, 1404:10-20.
63. Yokota S., Kaur S., VanderHorst V.G., Saper C.B., Chamberlin N.L. Respiratory-related outputs of glutamatergic, hypercapnia-responsive parabrachial neurons in mice. J Comp Neurol 2015, 523:907-920.