Central CO2 chemoreception and integrated neural mechanisms of cardiovascular and respiratory control

Journal of Applied Physiology

Volumn 108, Issue 4, 2010, Pages 995-1002

  Guyenet, Patrice G ^a   Stornetta, Ruth L ^a   Abbott, Stephen B G ^b   Depuy, Seth D ^a   Fortuna, Michal G ^a   Kanbar, Roy ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

Cardiorespiratory integration; Central chemoreceptors

Indexed keywords

CARBON DIOXIDE; CARBON DIOXIDE RECEPTOR; CELL SURFACE RECEPTOR;

ANIMAL; BREATHING MECHANICS; CENTRAL NERVOUS SYSTEM; CHEMORECEPTOR; DISEASE MODEL; HEMODYNAMICS; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; CARBON DIOXIDE; CENTRAL NERVOUS SYSTEM; CHEMORECEPTOR CELLS; DISEASE MODELS, ANIMAL; HEMODYNAMICS; HUMANS; RECEPTORS, CELL SURFACE; RESPIRATORY MECHANICS;

EID: 77950588339     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00712.2009     Document Type: Review

References (113)

1. Abbott SBG, Stornetta RL, Fortuna MG, Depuy SD, West GH, Harris TE, Guyenet PG. Photostimulation of retrotrapezoid nucleus Phox2b-expressing neurons in vivo produces long-lasting activation of breathing in rats. J Neurosci 29: 5806-5819, 2009.
2. 2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measure- ment, and interpretation. Am J Physiol, Regul Integr Comp Physiol 296: R1473-R1495, 2009.
3. Alheid GF, McCrimmon DR. The chemical neuroanatomy of breathing. Respir Physiol Neurobiol 164: 3-11, 2008.
4. Antunes VR, Brailoiu GC, Kwok EH, Scruggs P, Dun NJ. Orexins/ hypocretins excite rat sympathetic preganglionic neurons in vivo and in vitro. Am J Physiol Regul Integr Comp Physiol 281: R1801-R1807, 2001. (Pubitemid 33776657)
5. Aston-Jones G, Chen S, Zhu Y, Oshinsky ML. A neural circuit for circadian regulation of arousal. Nat Neurosci 4: 732-738, 2001. (Pubitemid 32595412)
6. Aston-Jones G, Ennis M, Pieribone VA, Nickell WT, Shipley MT. The brain nucleus locus coeruleus: restricted afferent control of a broad efferent network. Science 234: 734-737, 1986.
7. Baekey DM, Dick TE, Paton JF. Pontomedullary transection attenuates central respiratory modulation of sympathetic discharge, heart rate and the baroreceptor reflex in the in situ rat preparation. Exp Physiol 93: 803-816, 2008.
8. Bailey TW, Hermes SM, Andresen MC, Aicher SA. Cranial visceral afferent pathways through the nucleus of the solitary tract to caudal ventrolateral medulla or paraventricular hypothalamus: target-specific synaptic reliability and convergence patterns. J Neurosci 26: 11893-11902, 2006.
9. Berthon-Jones M, Sullivan CE. Ventilation and arousal responses to hypercapnia in normal sleeping humans. J Appl Physiol 57: 59-67, 1984.
10. Bodineau L, Frugiere A, Marlot D, Wallois F. Effect of hypoxia on the activity of respiratory and non-respiratory modulated retrotrapezoid neu- rons of the cat. Auton Neurosci 86: 70-77, 2000.
11. Brown DL, Guyenet PG. Electrophysiological study of cardiovascular neurons in the rostral ventrolateral medulla in rats. Circ Res 56: 359-369, 1985. (Pubitemid 15119512)
12. Brown RE, Sergeeva O, Eriksson KS, Haas HL. Orexin A excites serotonergic neurons in the dorsal raphe nucleus of the rat. Neurophar- macology 40: 457-459, 2001. (Pubitemid 32144724)
13. Byrum CE, Guyenet PG. Afferent and efferent connections of the A5 noradrenergic cell group in the rat. J Comp Neurol 261: 529-542, 1987.
14. Chan RKW, Sawchenko PE. Organization and transmitter specificity of medullary neurons activated by sustained hypertension: implications for understanding baroreceptor reflex circuitry. J Neurosci 18: 371-387, 1998.
15. Chen CT, Hwang LL, Chang JK, Dun NJ. Pressor effects of orexins injected intracisternally and to rostral ventrolateral medulla of anesthe- tized rats. Am J Physiol. Regul Integr Comp Physiol 278: R692-R697, 2000. (Pubitemid 30158130)
16. 16. Ciriello J, Li ZH, De Oliveira CVR. Cardioacceleratory responses to hypocretin-1 injections into rostral ventromedial medulla. Brain Res 991: 84-95, 2003. (Pubitemid 37297937)
17. 17. Daly MdB, Ward J, Wood LM. Modification by lung inflation of the vascular responses from the carotid body chemoreceptors and other receptors in dogs. J Physiol 378: 13-30, 1986. (Pubitemid 16003826)
18. Dean JB, Bayliss DA, Erickson JT, Lawing WL, Millhorn DE. Depolarization and stimulation of neurons in nucleus tractus solitarii by carbon dioxide does not require chemical synaptic input. Neuroscience 36: 207-216, 1990.
19. 19. Deng BS, Nakamura A, Zhang W, Yanagisawa M, Fukuda Y, Kuwaki T. Contribution of orexin in hypercapnic chemoreflex: evidence from, genetic and pharmacological disruption and supplementation studies in mice. J Appl Physiol 103: 1772-1779, 2007. (Pubitemid 350033865)
20. 20. Deuchars J, Li YW, Kasparov S, Paton JFR. Morphological and electrophysiological properties of neurones in the dorsal vagal complex of the rat activated by arterial baroreceptors. J Comp Neurol 417: 233-249, 2000. (Pubitemid 30038267)
21. Dias MB, Li A, Nattie EE. Antagonism of orexin receptor 1 (OXlR) in the retrotrapezoid nucleus (RTN) inhibits the ventilatory response to hypercapnia predominantly in wakefulness. J Physiol 587: 2059-2067, 2009.
22. 22. Duffin J. Modelling the respiratory chemoreflex control of acid-base balance. Conf Proc IEEE Eng Med Biol Soc 6: 5836-5839, 2005. (Pubitemid 46230288)
23. Dun NJ, Le Dun S, Chen CT, Hwang LL, Kwok EH, Chang JK. Orexins: a role in medullary sympathetic outflow. Regul Pept 96: 65-70, 2000.
24. 24. Duprat F, Lauritzen I, Patel A, Honore E. The TASK background K2P channels: chemo- and nutrient sensors. Trends Neurosci 30: 573-580, 2007. (Pubitemid 350051422)
25. 25. Elam M, Yao T, Thoren P, Svensson TH. Hypercapnia and Hypoxia: chemoreceptor-mediated control of locus coeruleus neurons and splanchnic sympathetic nerve. Brain Res 222: 373-381, 1981. (Pubitemid 11000346)
26. 2 in multiple brain stem nuclei determined using a voltage-sensitive dye in brain slices from rats. J Neurophysiol 102: 1577-1590, 2009.
27. Geerling JC, Mettenleiter TC, Loewy AD. Orexin neurons project to diverse sympathetic outflow systems. Neuroscience 122: 541-550, 2003.
28. Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci 7: 335-346, 2006.
29. 29. 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. (Pubitemid 41384462)
30. 30. Guyenet PG, Stornetta RL, Weston MC, McQuiston T, Simmons JR. Detection of amino acid and peptide transmitters in physiologically identified brainstem cardiorespiratory neurons. Auton Neurosci 114: 1-10, 2004. (Pubitemid 39149828)
31. 31. Habler HJ, Janig W, Michaelis M. Respiratory modulation in the activity of sympathetic neurones. Progr Neurobiol 43: 567-606, 1994. (Pubitemid 24274419)
32. Haselton JR, Guyenet PG. Central respiratory modulation of medullary sympathoexcitatory neurons in rat. Am J Physiol Regul Integr Comp Physiol 256: R739-R750, 1989.
33. 33. Haxhiu MA, Yung K, Erokwu B, Cherniack NS. COrinduced c-fos expression in the CNS catecholaminergic neurons. Respir Physiol 105: 35-45, 1996. (Pubitemid 26321092)
34. Hodges MR, Tattersall GJ, Harris MB, McEvoy SD, Richerson DN, Deneris ES, Johnson RL, Chen ZF, Richerson GB. Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28: 2495-2505, 2008.
35. Hokfelt T, Fuxe K, Goldstein M, Johansson O. Immunohistochemical evidence for the existence of adrenaline neurons in the rat brain. Brain Res 66: 235-251, 1974.
36. 36. Horvath TL, Peyron C, Diano S, Ivanov A, Aston-Jones G, Kilduff TS, Van den Pol AN. Hypocretin (Orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J Comp Neurol 415: 145-159, 1999. (Pubitemid 29519873)
37. Inokuchi H, Yoshimura M, Polosa C, Nishi S. The effects of 5-hydroxytryptamine on cat sympathetic preganglionic neurons in vitro. Kurume Med J 37: 309-312, 1990.
38. 38. Inokuchi H, Yoshimura M, Polosa C, Nishi S. Adrenergic receptors (alpha 1 and alpha 2) modulate different potassium conductances in sympathetic preganglionic neurons. Can Journal Physiol Pharmacol 70, Suppl: S92-S97, 1992. (Pubitemid 23091611)
39. Jacobs BL, Fornal CA. Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21: 9S-15S, 1999.
40. 40. Janig W, Habler HJ. Neurophysiological analysis of target-related sympathetic pathways-from animal to human: similarities and differences. Acta Physiol Scand 177: 255-274, 2003. (Pubitemid 36337628)
41. Jansen ASP, Nguyen XV, Karpitskiy V, Mettenleiter TC, Loewy AD. Central command neurons of the sympathetic nervous system: basis of the fight-or-flight response. Science 270: 644-646, 1995.
42. Jansen ASP, Wessendorf MW, Loewy AD. Transneuronal labeling of CNS neuropeptide and monoamine neurons after Pseudorabies virus injections into the stellate ganglion. Brain Res 683: 1-24, 1995.
43. 43. Jeske I, Morrison SF, Cravo SL, Reis DJ. Identification of baroreceptor reflex interneurons in the caudal ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol 264: R169-R178, 1993. (Pubitemid 23053544)
44. 44. Kanamaru M, Homma I. Compensatory airway dilation and additive ventilatory augmentation mediated by dorsomedial medullary 5-hydroxytryptamine 2 receptor activity and hypercapnia. Am J Physiol Regul Integr Comp Physiol 293: R854-R860, 2007. (Pubitemid 47205072)
45. Kangrga IM, Loewy AD. Whole-cell recordings from visualized C1 adrenergic bulbospinal neurons: Ionic mechanisms underlying vasomotor tone. Brain Res 670: 215-232, 1995.
46. 46. Kayaba Y, Nakamura A, Kasuya Y, Ohuchi T, Yanagisawa M, Komuro I, Fukuda Y, Kuwaki T. Attenuated defense response and low basal blood pressure in orexin knockout mice. Am J Physiol Regul Integr Comp Physiol 285: R581-R593, 2003. (Pubitemid 37040566)
47. Kerman IA. Organization of brain somatomotor-sympathetic circuits. Exp Brain Res 187: 1-16, 2008.
48. 48. Koshiya N, Guyenet PG. Tonic sympathetic chemoreflex after blockade of respiratory rhythmogenesis in the rat. J Physiol 491: 859-869, 1996. (Pubitemid 26107255)
49. 49. Koshiya N, Huangfu D, Guyenet PG. Ventrolateral medulla and sympathetic chemoreflex in the rat. Brain Res 609: 174-184, 1993. (Pubitemid 23136817)
50. 50. Krupp J, Bordey A, Feltz P. Electrophysiological evidence for multiple glycinergic inputs to neonatal rat sympathetic preganglionic neurons in vitro. Eur J Neurosci 9: 1711-1719, 1997. (Pubitemid 27348329)
51. 51. Kubin L, Alheid GF, Zuperku EJ, McCrimmon DR. Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol 101: 618-627, 2006. (Pubitemid 44162373)
52. Kukkonen JP, Holmqvist T, Ammoun S, Åkerman KEO. Functions of the exinergic/hypocretinergic system. Am J Physiol Cell Physiol 283: C1567-C1591, 2002.
53. Kuwaki T, Zhang W, Nakamura A, Deng BS. Emotional and statedependent modification of cardiorespiratory function: role of orexinergic neurons. Auton Neurosci 142: 11-16, 2008.
54. Lazarenko RM, Milner TA, Depuy SD, Stornetta RL, West GH, Kievits JA, Bayliss DA, Guyenet PG. Acid-sensitivity and ultrastruc- ture of the retrotrapezoid nucleus in phox2b-eGFP transgenic mice. J Comp Neurol; doi: 10.1152/japplphysiol.00712.2009.
55. Li A, Nattie E. Catecholamine neurones in rats modulate sleep, breathing, central chemoreception and breathing variability. J Physiol 570: 385-396, 2006.
56. 56. Li Q, Goodchild AK, Seyedabadi M, Pilowsky PM. Pre-protachykinin A mRNA is colocalized with tyrosine hydroxylase-immunoreactivity in bulbospinal neurons. Neuroscience 136: 205-216, 2005. (Pubitemid 41483848)
57. 2-adrenergic receptors. Am J Physiol Regul Integr Comp Physiol 269: R1356-R1369, 1995.
58. Lipski J, Kanjhan R, Kruszewska B, Rong WF. Properties of presympathetic neurones in the rostral ventrolateral medulla in the rat: an intracellular study "in vivo". J Physiol, 490: 729-744, 1996.
59. 59. Llewellyn-Smith IJ, Martin CL, Marcus JN, Yanagisawa M, Minson JB, Scammell TE. Orexin-immunoreactive inputs to rat sympathetic preganglionic neurons. Neurosci Lett 35.1: 115-119, 2003. (Pubitemid 37329602)
60. 60. Lu J, Sherman D, Devor M, Saper CB. A putative flip-flop switch for control of REM sleep. Nature 441: 589-594, 2006. (Pubitemid 43927285)
61. Mandel DA, Schreihofer AM. Central respiratory modulation of barosensitive neurones in rat caudal ventrolateral medulla. J Physiol 572: 881-896, 2006.
62. 62. Matsushita N, Okada H, Yasoshima Y, Takahashi K, Kiuchi K, Kobayashi K. Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J Neurochem 82: 295-304, 2002. (Pubitemid 34774620)
63. McAllen RM. Central respiratory modulation of subretrofacial bulbospinal neurons in the cat. J Physiol 388: 533-545, 1987.
64. McAllen RM. Actions of carotid chemoreceptors on subretrofacial bulbospinal neurons in the cat. J Auton Nerv Syst 40: 181-188, 1992.
65. McAllen RM, May CN, Shafton AD. Functional anatomy of sympathetic premotor cell groups in the medulla. Clin Exp Hypertens 17: 209-221, 1995.
66. Mifflin SW, Spyer KM, Withington-Wray DJ. Baroreceptor inputs to the nucleus tractus solitarius in the cat: postsynaptic actions and the influence of respiration. J Physiol 399: 349-367, 1988.
67. Millhorn DE. Neural respiratory and circulatory interaction during chemoreceptor stimulation and cooling of ventral medulla in cats. J Physiol 370: 217-231, 1986.
68. 68. Milner TA, Abate C, Reis DJ, Pickel VM. Ultrastructural localization of phenylethanolamine N-methyltransferase-like immunoreactivity in the rat locus coeruleus. Brain Res 478: 1-15, 1989. (Pubitemid 19033446)
69. 69. Moosavi SH, Golestanian E, Binks AP, Lansing RW, Brown R, Banzett RB. Hypoxic and hypercapnic drives to breathe generate equivalent levels of air hunger in humans. J Appl Physiol 94: 141-154, 2003. (Pubitemid 36014306)
70. 70. Moreira TS, Takakura AC, Colombari E, Guyenet PG. Central chemoreceptors and sympathetic vasomotor outflow. J Physiol 577: 369-386, 2006. (Pubitemid 44698262)
71. Morrison SF, Callaway J, Milner TA, Reis DJ. Rostral ventrolateral medulla-a source of the glutamatergic innervation of the sympathetic intermediolateral nucleus. Brain Res 562: 126-135, 1991.
72. 72. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA, Guyenet PG. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7: 1360-1369, 2004. (Pubitemid 41057759)
73. 73. Mulkey DK, Talley EM, Stornetta RL, Siegel AR, West GH, Chen X, Sen N, Mistry AM, Guyenet PG, Bayliss DA. TASK channels determine pH sensitivity in select respiratory neurons but do not contribute to central respiratory chemosensitivity. J Neurosci 27: 14049-14058, 2007. (Pubitemid 351377868)
74. Nattie E, Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol 106: 1464-1466, 2009.
75. 75. Nattie EE, Fung ML, Li A, St. John WM. Responses of respiratory modulated and tonic units in the retrotrapezoid nucleus to CO2. Respir Physiol 94: 35-50, 1993. (Pubitemid 23316603)
76. Neverova NV, Saywell SA, Nashold LJ, Mitchell GS, Feldman JL. Episodic stimulation of alpha1-adrenoreceptors induces protein kinase C-dependent persistent changes in motoneuronal excitability. J Neuro sci 27: 4435-4442, 2007.
77. Nichols NL, Hartzler LK, Conrad SC, Dean JB, Putnam RW. Intrinsic chemosensitivity of individual nucleus tractus solitarius (NTS) and locus coeruleus (LC) neurons from neonatal rats. Adv Exp Med Biol 605: 348-352, 2008.
78. 78. Numao Y, Koshiya N, Gilbey MP, Spyer KM. Central respiratory drive-related activity in sympathetic nerves of the rat: the regional differences. Neurosci Lett 81: 279-284, 1987. (Pubitemid 17159510)
79. 79. Oikawa S, Hirakawa H, Kusakabe T, Nakashima Y, Hayashida Y.Autonomic cardiovascular responses to hypercapnia in conscious rats:the roles of the chemo- and baroreceptors. Auton Neurosci 117: 105-114, 2005. (Pubitemid 40128591)
80. Paton JFR. Pattern of cardiorespiratory afferent convergence to solitary tract neurons driven by pulmonary vagal C-fiber stimulation in the mouse. J Neurophysiol 79: 2365-2373, 1998.
81. Paton JFR. Nucleus tractus solitarii: Integrating structures. Exp Physiol 84: 815-833, 1999.
82. 2 in sleeping dogs. Am Rev Respir Dis 115: 251-259, 1977.
83. Ptak K, Yamanishi T, Aungst J, Milescu LS, Zhang R, Richerson GB, Smith JC. Raphe neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 29: 3720-3737, 2009.
84. 2 and acid signaling in chemosensitive neurons. Am J Physiol Cell Physiol 287: C1493-C1526, 2004.
85. Richerson GB. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5: 449-461, 2004.
86. 86. Rogers RF, Paton JFR, Schwaber JS. NTS neuronal responses to arterial pressure and pressure changes in the rat. Am J Physiol Regul Integr Comp Physiol 265: R1355-R1368, 1993. (Pubitemid 2034484)
87. 87. Rosin DL, Chang DA, Guyenet PG. Afferent and efferent connections of the rat retrotrapezoid nucleus. J Comp Neurol 499: 64-89, 2006. (Pubitemid 44423696)
88. Ross CA, Ruggiero DA, Park DH, Joh TH, Sved AF, Fernandez Pardal J, Saavedra JM, Reis DJ. Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J Neurosci 4: 474-494, 1984.
89. 89. Scheuer DA, Zhang J, Toney GM, Mifflin SW. Temporal processing of aortic nerve evoked activity in the nucleus of the solitary tract. J Neurophysiol 76: 3750-3757, 1996. (Pubitemid 27009679)
90. Schiltz JC, Sawchenko PE. Specificity and generality of the involvement of catecholaminergic afferents in hypothalamic responses to immune insults. J Comp Neurol 502: 455-467, 2007.
91. Schreihofer AM, Guyenet PG. Baroactivated neurons with pulsemodulated activity in the rat caudal ventrolateral medulla express GA.D67 mRNA. J Neurophysiol 89: 1265-1277, 2003.
92. Shao XM, Tan W, Xiu J, Puskar N, Fonck C, Lester HA, Feldman JL. Alpha4* nicotinic receptors in preBotzinger complex mediate cholinergic/nicotinic modulation of respiratory rhythm. J Neurosci 28: 519-528, 2008.
93. 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.
94. Smith PM, Connolly BC, Ferguson AV. Microinjection of orexin into the rat nucleus tractus solitarius causes increases in blood pressure. Brain Res 950: 261-267, 2002.
95. Somers VK, Mark AL, Abboud FM. Interaction of baroreceptor and chemoreceptor reflex control of sympathetic nerve activity in normal humans. J Clin Invest 87: 1953-1957, 1991.
96. Somers VK, Mark AL, Zavala DC, Abboud FM. Contrasting effects of hypercapnia on ventilation and sympathetic activity in humans. J Appl Physiol 67: 2101-2106, 1989.
97. 97. St Croix CM, Satoh M, Morgan BJ, Skatrud JB, Dempsey JA. Role of respiratory motor output in within-breath modulation of muscle sympathetic nerve activity in humans. Circ Res 85: 457-469, 1999. (Pubitemid 29409622)
98. Stocker SD, Simmons JR, Stornetta RL, Toney GM, Guyenet PG. Water deprivation activates a glutamatergic projection from the hypothalamic paraventricular nucleus to the rostral ventrolateral medulla. J Comp Neurol 494: 673-685, 2006.
99. Stornetta RL, Sevigny CP, Schreihofer AM, Rosin DL, Guyenet PG. Vesicular glutamate transporter DNPI/GLUT2 is expressed by both C1 adrenergic and nonaminergic presympathetic vasomotor neurons of the rat medulla. J Comp Neurol 444: 207-220, 2002.
100. Stunden CE, Filosa JA, Garcia AJ, Dean JB, Putnam RW. Development of in vivo ventilatory and single chemosensitive neuron responses to hypercapnia in rats. Respir Physiol 127: 135-155, 2001.
101. 10.1. Sun MK, Guyenet PG. GABA-mediated baroreceptor inhibition of reticulospinal neurons. Am J Physiol Regul Integr Comp Physiol 249: R672-R680, 1985.
102. 102. Sun QJ, Minson J, Llewellyn-Smith LI, Arnolda L, Chalmers J, Pilowsky P. Botzinger neurons project towards bulbospinal neurons in the rostral ventrolateral medulla of the rat. J Comp Neurol 388: 23-31, 1997. (Pubitemid 27485630)
103. 2 activates orexin-containing neurons in mice. Respir Physiol Neurobiol 166: 184-186, 2009.
104. 104. Sundlof G, Wallin BG. Human muscle nerve sympathetic activity at rest. Relationship to blood pressure and age. J Physiol. 274: 621-637, 1978. (Pubitemid 8284570)
105. Sved AF, Feisten G. Stimulation of the locus coeruleus decreases arterial pressure. Brain Res 414: 119-132, 1987.
106. 2-sensitive neurons in rats. J Physiol 572: 503-523, 2006.
107. 107. Trzebski A, Kubin L. Is the central inspiratory activity responsible for Pc02-dependent drive of the sympathetic discharge? J Auton Nerv Syst 3: 401-420, 1981. (Pubitemid 11069146)
108. Veasey SC, Fornal CA, Metzler CW, Jacobs BL. Response of serotonergic caudal raphe neurons in relation to specific motor activities in freely moving cats. J Neurosci 15: 5346-5359, 1995.
109. 109. Weston M, Wang H, Stornetta RL, Sevigny CP, Guyenet PG. Fos expression by glutamatergic neurons of the solitary tract nucleus after phenylephrine-induced hypertension in rats. J Comp Neurol 460: 525-541, 2003. (Pubitemid 36528660)
110. Willette RN, Barcas PP, Krieger AJ, Sapru HN. Vasopressor and depressor areas in the rat medulla. Identification by microinjection of L-glutamate. Neuropharmacology 22: 1071-1079, 1983.
111. Willette RN, Krieger AJ, Barcas PP, Sapru HN. Medullary gammaaminobutyric acid (GABA) receptors and the regulation of blood pressure in the rat. J Pharmacol Exp Ther 226: 893-899, 1983.
112. 112. Williams RH, Jensen LT, Verkhratsky A, Fugger L, Burdakov D. Control of hypothalamic orexin neurons by acid and CO2. Proc Natl Acad. Sci USA 104: 10685-10690, 2007. (Pubitemid 47185725)
113. 113. Zhang J, Mifflin SW. Responses of aortic depressor nerve-evoked neurones in rat nucleus of the solitary tract to changes in blood pressure. J Physiol 529: 431-443, 2000. (Pubitemid 32007738)