The emerging role of the parabrachial complex in the generation of wakefulness drive and its implication for respiratory control

Respiratory Physiology and Neurobiology

Volumn 188, Issue 3, 2013, Pages 318-323

  Martelli, Davide ^a   Stanić, Davor ^a   Dutschmann, Mathias ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Ascending reticular arousal system; Breathing; Pons; Sleep wake

Indexed keywords

BLOOD GAS; BODY TEMPERATURE; BRAIN REGION; DRIVE; FEEDBACK SYSTEM; FOREBRAIN; HUMAN; HYPOTHALAMUS; LATERAL HYPOTHALAMUS; NEUROANATOMY; PARABRACHIAL COMPLEX; PHASE TRANSITION; PRIORITY JOURNAL; REM SLEEP; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; REVIEW; SLEEP DISORDERED BREATHING; SLEEP WAKING CYCLE; SLOW BRAIN WAVE; UPPER RESPIRATORY TRACT; WAKEFULNESS;

ASCENDING RETICULAR AROUSAL SYSTEM; BREATHING; PONS; SLEEP-WAKE;

ANIMALS; HUMANS; NEURAL PATHWAYS; RESPIRATORY MECHANICS; RETICULAR FORMATION; SLEEP; SLEEP STAGES; SLEEP, REM; WAKEFULNESS;

EID: 84884209419     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2013.06.019     Document Type: Review

References (98)

1. Alam M.N., Szymusiak R., Gong H., King J., McGinty D. Adenosinergic modulation of rat basal forebrain neurons during sleep and waking: neuronal recording with microdialysis. Journal of Physiology 1999, 521:679-690.
2. Anaclet C., Lin J.S., Vetrivelan R., Krenzer M., Vong L., Fuller P.M., Lu J. Identification and characterization of a sleep-active cell group in the rostral medullary brainstem. Journal of Neuroscience 2012, 32:17970-17976.
3. Baker T.L., Netick A., Dement W.C. Sleep-related apneic and apneustic breathing following pneumotaxic lesion and vagotomy. Respiration Physiology 1981, 46:271-294.
4. Berridge C.W., Foote S.L. Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. Journal of Neuroscience 1991, 11:3135-3145.
5. Berridge C.W., España R.A. Hypocretins: waking, arousal, or action?. Neuron 2005, 46:696-698.
6. Blanco-Centurion C., Gerashchenko D., Shiromani P.J. Effects of saporin-induced lesions of three arousal populations on daily levels of sleep and wake. Journal of Neuroscience 2007, 27:14041-14048.
7. Boissard R., Fort P., Gervasoni D., Barbagli B., Luppi P.H. Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. European Journal of Neuroscience 2003, 18:1627-1639.
8. Carter M.E., Yizhar O., Chikahisa S., Nguyen H., Adamantidis A., Nishino S., Deisseroth K., de Lecea L. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nature Neuroscience 2010, 13:1526-1533.
9. Cerri M., Ocampo-Garces A., Amici R., Baracchi F., Capitani P., Jones C.A., Luppi M., Perez E., Parmeggiani P.L., Zamboni G. Cold exposure and sleep in the rat: effects on sleep architecture and the electroencephalogram. Sleep 2005, 28:694-705.
10. Chamberlin N.L. Functional organization of the parabrachial complex and intertrigeminal region in the control of breathing. Respiratory Physiology and Neurobiology 2004, 143:115-125.
11. Chou T.C., Bjorkum A.A., Gaus S.E., Lu J., Scammell T.E., Saper C.B. Afferents to the ventrolateral preoptic nucleus. Journal of Neuroscience 2002, 22:977-990.
12. Clark S.D., Duangdao D.M., Schulz S., Zhang L., Liu X., Xu Y.L., Reinscheid R.K. Anatomical characterization of the neuropeptide S system in the mouse brain by in situ hybridization and immunohistochemistry. Journal of Comparative Neurology 2011, 519:1867-1893.
13. Clément O., Sapin E., Bérod A., Fort P., Luppi P.H. Evidence that neurons of the sublaterodorsal tegmental nucleus triggering paradoxical (REM) sleep are glutamatergic. Sleep 2011, 34:419-423.
14. Clément O., Sapin E., Libourel P.A., Arthaud S., Brischoux F., Fort P., Luppi P.H. The lateral hypothalamic area controls paradoxical (REM) sleep by means of descending projections to brainstem GABAergic neurons. Journal of Neuroscience 2012, 32:16763-16774.
15. Craig A.D. A new view of pain as a homeostatic emotion. Trends in Neurosciences 2002, 26(6):303-307.
16. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience 2002, 3:655-666.
17. Craig A.D. Interoception: the sense of the physiological condition of the body. Current Opinion in Neurobiology 2003, 13(4):500-505.
18. Dempsey J.A., Veasey S.C., Morgan B.J., O'Donnell C.P. Pathophysiology of sleep apnea. Physiological Reviews 2010, 90:47-112.
19. Dentico D., Amici R., Baracchi F., Cerri M., Del Sindaco E., Luppi M., Martelli D., Perez E., Zamboni G. c-Fos expression in preoptic nuclei as a marker of sleep rebound in the rat. European Journal of Neuroscience 2009, 30:651-661.
20. Duangdao D.M., Clark S.D., Okamura N., Reinscheid R.K. Behavioral phenotyping of neuropeptide S receptor knockout mice. Behavioural Brain Research 2009, 205:1-9.
21. Dutschmann M., Mörschel M., Kron M., Herbert H. Development of adaptive behaviour of the respiratory network: implications for the pontine Kolliker-Fuse nucleus. Respiratory Physiology and Neurobiology 2004, 143:155-165.
22. 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. European Journal of Neuroscience 2006, 24:1071-1084.
23. Dutschmann M., Kron M., Mörschel M., Gestreau C. Activation of Orexin B receptors in the pontine Kolliker-Fuse nucleus modulates pre-inspiratory hypoglossal motor activity in rat. Respiratory Physiology and Neurobiology 2007, 159:232-235.
24. Dutschmann M., Morschel M., Reuter J., Zhang W., Gestreau C., Stettner G.M., Kron M. Postnatal emergence of synaptic plasticity associated with dynamic adaptation of the respiratory motor pattern. Respiratory Physiology and Neurobiology 2008, 164:72-79.
25. Dutschmann M., Dick T.E. Pontine mechanisms of respiratory control. Comprehensive Physiology 2012, 2:2443-2469.
26. Fenik V.B., Rukhadze I., Kubin L. Inhibition of pontine noradrenergic A7 cells reduces hypoglossal nerve activity in rats. Neuroscience 2008, 57:473-482.
27. Fraigne J.J., Dunin-Barkowski W.L., Orem J.M. Effect of hypercapnia on sleep and breathing in unanesthetized cats. Sleep 2008, 31:1025-1033.
28. Fuller P.M., Gooley J.J., Saper C.B. Neurobiology of the sleep-wake cycle: sleep architecture, circadian regulation, and regulatory feedback. Journal of Biological Rhythms 2006, 21:482-493.
29. Fuller P.M., Sherman D., Pedersen N.P., Saper C.B., Lu J. Reassessment of the structural basis of the ascending arousal system. Journal of Comparative Neurology 2011, 519:933-956.
30. Fulwiler C.E., Saper C.B. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Research 1984, 319:229-259.
31. Gang S., Sato Y., Kohama I., 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. Journal of the Autonomic Nervous System 1995, 56:1-7.
32. Gauriau C., Bernard J.F. Pain pathways and parabrachial circuits in the rat. Experimental Physiology 2002, 87:251-258.
33. Gautier H., Bertrand F. Respiratory effects of pneumotaxic center lesions and subsequent vagotomy in chronic cats. Respiration Physiology 1975, 23:71-85.
34. Gestreau C., Dutschmann M., Obled S., Bianchi A.L. Activation of XII motoneurons and premotor neurons during various oropharyngeal behaviors. Respiratory Physiology and Neurobiology 2005, 147:159-176.
35. Gilbert K.A., Lydic R. Parabrachial neuron discharge in the cat is altered during the carbachol-induced REM sleep-like state (DCarb). Neuroscience Letters 1990, 120:241-244.
36. Greco M.A., Fuller P.M., Jhou T.C., Martin-Schild S., Zadina J.E., Hu Z., Shiromani P., Lu J. Opioidergic projections to sleep-active neurons in the ventrolateral preoptic nucleus. Brain Research 2008, 1245:96-107.
37. Guyenet P.G., Abbott S.B. Chemoreception and asphyxia-induced arousal. Respiratory Physiology and Neurobiology 2013, pii:S1569-9048(13)00106-7.
38. Hagan J.J., Leslie R.A., Patel S., Evans M.L., Wattam T.A., Holmes S., Benham C.D., Taylor S.G., Routledge C., Hemmati P., Munton R.P., Ashmeade T.E., Shah A.S., Hatcher J.P., Hatcher P.D., Jones D.N., Smith M.I., Piper D.C., Hunter A.J., Porter R.A., Upton N. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:10911-10916.
39. Herbert H., Moga M.M., Saper C.B. Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. Journal of Comparative Neurology 1990, 1293:540-580.
40. Huang Z.L., Qu W.M., Li W.D., Mochizuki T., Eguchi N., Watanabe T., Urade Y., Hayaishi O. Arousal effect of orexin A depends on activation of the histaminergic system. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:9965-9970.
41. Huang Z.L., Sato Y., Mochizuki T., Okada T., Qu W.M., Yamatodani A., Urade Y., Hayaishi O. Prostaglandin E2 activates the histaminergic system via the EP4 receptor to induce wakefulness in rats. Journal of Neuroscience 2003, 23:5975-5983.
42. Jacobs B.L., Wise W.D., Taylor K.M. Differential behavioral and neurochemical effects following lesions of the dorsal or median raphe nuclei in rats. Brain Research 1974, 79:353-361.
43. Johnson A.K., Thunhorst R.L. The neuroendocrinology of thirst and salt appetite: visceral sensory signals and mechanisms of central integration. Frontiers in Neuroendocrinology 1997, 18:292-353.
44. Jones B.E., Harper S.T., Halaris A.E. Effects of locus coeruleus lesions upon cerebral monoamine content, sleep-wakefulness states and the response to amphetamine in the cat. Brain Research 1977, 124:473-496.
45. Kaur S., Pedersen N.P., Yokota S., Hur E.E., Fuller P.M., Lazarus M., Chamberlin N.L., Saper C.B. Glutamatergic signaling from the parabrachial nucleus plays a critical role in hypercapnic arousal. Journal of Neuroscience 2013, 33:7627-7640.
46. Kiyashchenko L.I., Mileykovskiy B.Y., Maidment N., Lam H.A., Wu M.F., John J., Peever J., Siegel J.M. Release of hypocretin (orexin) during waking and sleep states. Journal of Neuroscience 2002, 22:5282-5286.
47. Krukoff T.L., Harris K.H., Jhamandas J.H. Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Research Bulletin 1993, 30:163-172.
48. Kuna S.T., Remmers J.E. Premotor input to hypoglossal motoneurons from Kolliker-Fuse neurons in decerebrate cats. Respiration Physiology 1999, 117:85-95.
49. Lara J.P., Dawid-Milner M.S., Lopez M.V., Montes C., Spyer K.M., Gonzalez-Baron S. Laryngeal effects of stimulation of rostral and ventral pons in the anaesthetized rat. Brain Research 2002, 934:97-106.
50. Lee H.S., Kim M.A., Valentino R.J., Waterhouse B.D. Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Research 2003, 963:57-71.
51. Lee M.G., Hassani O.K., Jones B.E. Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. Journal of Neuroscience 2005, 25:6716-6720.
52. Lovering A.T., Fraigne J.J., Dunin-Barkowski W.L., Vidruk E.H., Orem J.M. Hypocapnia decreases the amount of rapid eye movement sleep in cats. Sleep 2003, 26:961-967.
53. Lu J., Bjorkum A.A., Xu M., Gaus S.E., Shiromani P.J., Saper C.B. Selective activation of the extended ventrolateral preoptic nucleus during rapid eye movement sleep. Journal of Neuroscience 2002, 22:4568-4576.
54. Lu J., Sherman D., Devor M., Saper C.B. A putative flip-flop switch for control of REM sleep. Nature 2006, 441:589-594.
55. Lumsden T. Observations on the respiratory centers in the cat. Journal of Physiology 1923, 57:152-160.
56. Luppi P.H., Clément O., Sapin E., Peyron C., Gervasoni D., Léger L., Fort P. Brainstem mechanisms of paradoxical (REM) sleep generation. Pflugers Archiv 2012, 463:43-52.
57. Lydic R., Orem J. Respiratory neurons of the pneumotaxic center during sleep and wakefulness. Neuroscience Letters 1975, 15:187-192.
58. Marckwald M. Die Athembewegungen und deren Innervation beim Kaninchen. Zeitschrift fur Biologie 1887, 23:149-283.
59. Mileykovskiy B.Y., Kiyashchenko L.I., Siegel J.M. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005, 46:787-798.
60. Monti J.M. The structure of the dorsal raphe nuéeus and its relevance to the regulation of sleep and wakefulness. Sleep Medicine Reviews 2010, 14:307-317.
61. Morrison S.F., Nakamura K. Central neural pathways for thermoregulation. Frontiers in Bioscience 2011, 16:74-104.
62. Mörschel M., Dutschmann M. Pontine respiratory activity involved in inspiratory/expiratory phase transition. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2009, 364:2517-2526.
63. Moruzzi G., Magoun H.W. Brain stem reticular formation and activation of the EEG. Electroencephalography and Clinical Neurophysiology 1949, 1:455-473.
64. Mraovitch S., Kumada M., Reis D.J. Role of the nucleus parabrachialis in cardiovascular regulation in cat. Brain Research 1982, 232:57-75.
65. Nakamura K., Morrison S.F. A thermosensory pathway that controls body temperature. Nature Neuroscience 2008, 11:62-71.
66. Niu J.G., Yokota S., Tsumori T., Qin Y., Yasui Y. Glutamatergic lateral parabrachial neurons innervate orexin-containing hypothalamic neurons in the rat. Brain Research 2010, 1358:110-122.
67. Norgren R., Leonard C.M. Taste pathways in rat brainstem. Science 1971, 173:1136-1139.
68. Parmeggiani P.L. Physiologic regulation in sleep. Principles and Practice of Sleep Medicine 2005, 185-191. W.B. Saunders Company, Philadelphia. 4th ed. M.H. Kryger, T. Roth, W.E. Dement (Eds.).
69. Reinscheid R.K., Xu Y.L. Neuropeptide S and its receptor: a newly deorphanized G protein-coupled receptor system. Neuroscientist 2005, 11:532-538.
70. Saper C.B., Loewy A.D. Efferent connections of the parabrachial nucleus in the rat. Brain Research 1980, 197:291-317.
71. Saper C.B., Chou T.C., Scammell T.E. The sleep switch: hypothalamic control of sleep and wakefulness. Trends in Neurosciences 2001, 24:726-731.
72. Saper C.B., Scammell T.E., Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437:1257-1263.
73. Sarter M., Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 2000, 95:933-952.
74. Sherin J.E., Shiromani P.J., McCarley R.W., Saper C.B. Activation of ventrolateral preoptic neurons during sleep. Science 1996, 271:216-219.
75. Shin J.W., Geerling J.C., Stein M.K., Miller R.L., Loewy A.D. FoxP2 brainstem neurons project to sodium appetite regulatory sites. Journal of Chemical Neuroanatomy 2011, 42:1-23.
76. Sieck G.C., Harper R.M. Pneumotaxic area neuronal discharge during sleep-waking states in the cat. Experimental Neurology 1980, 67:79-102.
77. Song G., Yu Y., Poon C.S. Cytoarchitecture of pneumotaxic integration of respiratory and nonrespiratory information in the rat. Journal of Neuroscience 2006, 26:300-310.
78. Song G., Poon C.S. Lateral parabrachial nucleus mediates shortening of expiration and increase of inspiratory drive during hypercapnia. Respiratory Physiology and Neurobiology 2009, 165:9-12.
79. Song G., Poon C.S. Lateral parabrachial nucleus mediates shortening of expiration during hypoxia. Respiratory Physiology and Neurobiology 2009, 165:1-8.
80. Song G., Wang H., Xu H., Poon C.S. Kölliker-Fuse neurons send collateral projections to multiple hypoxia-activated and nonactivated structures in rat brainstem and spinal cord. Brain Structure and Function 2012, 217:835-858.
81. St-John W.M. Neurogenesis of patterns of automatic ventilatory activity. Progress in Neurobiology 1998, 56:97-117.
82. Suntsova N., Guzman-Marin R., Kumar S., Alam M.N., Szymusiak R., McGinty D. The median preoptic nucleus reciprocally modulates activity of arousal-related and sleep-related neurons in the perifornical lateral hypothalamus. Journal of Neuroscience 2007, 27:1616-1630.
83. Szymusiak R., Alam N., Steininger T.L., McGinty D. Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Research 1998, 803:178-188.
84. Takahashi K., Lin J.S., Sakai K. Neuronal activity of orexin and non-orexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 2008, 153:860-870.
85. Tao R., Auerbach S.B. Influence of inhibitory and excitatory inputs on serotonin efflux differs in the dorsal and median raphe nuclei. Brain Research 2003, 961:109-120.
86. Verret L., Léger L., Fort P., Luppi P.H. Cholinergic and noncholinergic brainstem neurons expressing Fos after paradoxical (REM) sleep deprivation and recovery. European Journal of Neuroscience 2005, 21:2488-2504.
87. Vetrivelan R., Chang C., Lu J. Muscle tone regulation during REM sleep: neural circuitry and clinical significance. Archives Italiennes de Biologie 2011, 149:348-366.
88. von Economo C. Sleep as a problem of localization. Journal of Nervous and Mental Disease 1930, 71:249-259.
89. von Euler C. On the central pattern generator for the basic breathing rhythmicity. Journal of Applied Physiology 1983, 55:1647-1659.
90. Willis W.D., Westlund K.N. Neuroanatomy of the pain system and of the pathways that modulate pain. Journal of Clinical Neurophysiology 1997, 14:2-31.
91. Winsky-Sommerer R., Boutrel B., de Lecea L. Stress and arousal: the corticotrophin-releasing factor/hypocretin circuitry. Molecular Neurobiology 2005, 32:285-294.
92. Wu Q., Clark M.S., Palmiter R.D. Deciphering a neuronal circuit that mediates appetite. Nature 2012, 483:594-597.
93. Xu Y.L., Reinscheid R.K., Huitron-Resendiz S., Clark S.D., Wang Z., Lin S.H., Brucher F.A., Zeng J., Ly N.K., Henriksen S.J., de Lecea L., Civelli O. Neuropeptide S: a neuropeptide promoting arousal and anxiolytic-like effects. Neuron 2004, 43(4):487-497.
94. Xu Y.L., Gall C.M., Jackson V.R., Civelli O., Reinscheid R.K. Distribution of neuropeptide S receptor mRNA and neurochemical characteristics of neuropeptide S-expressing neurons in the rat brain. Journal of Comparative Neurology 2007, 500:84-102.
95. Yamamoto T., Shimura T., Sako N., Yasoshima Y., Sakai N. Neural substrates for conditioned taste aversion in the rat. Behavioural Brain Research 1994, 65:123-137.
96. Yokota S., Oka T., Tsumori T., Nakamura S., Yasui Y. Glutamatergic neurons in the Kölliker-Fuse nucleus project to the rostral ventral respiratory group and phrenic nucleus: a combined retrograde tracing and in situ hybridization study in the rat. Neuroscience Research 2007, 59:341-346.
97. Yokota S., Tsumori T., Oka T., Nakamura S., Yasui Y. GABAergic neurons in the ventrolateral subnucleus of the nucleus tractus solitarius are in contact with Kölliker-Fuse nucleus neurons projecting to the rostral ventral respiratory group and phrenic nucleus in the rat. Brain Research 2008, 1228:113-126.
98. Zant J.C., Rozov S., Wigren H.K., Panula P., Porkka-Heiskanen T. Histamine release in the basal forebrain mediates cortical activation through cholinergic neurons. Journal of Neuroscience 2012, 32:13244-13254.