Central control of cardiovascular function during sleep

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 12, 2013, Pages

  Silvani, Alessandro ^a   Dampney, Roger A L ^b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Blood pressure; Central autonomic commands; Heart rate; Hypocretins orexins; Sleep; Sympathetic nerve activity

Indexed keywords

OREXIN;

BLOOD PRESSURE; CARDIOVASCULAR FUNCTION; CHOLINERGIC NERVE CELL; ELECTROENCEPHALOGRAM; HUMAN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; MEDULLARY NUCLEUS; MESENCEPHALON; MUSCLE CONTRACTION; NERVE STIMULATION; NERVE TRACT; NEUROMUSCULAR BLOCKING; NONHUMAN; NONREM SLEEP; NUCLEUS RAPHE OBSCURUS; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PONS; PONTINE NUCLEUS; PREGANGLIONIC NERVE CELL; PREOPTIC AREA; PRESSORECEPTOR; PRESSORECEPTOR REFLEX; PRIORITY JOURNAL; REM SLEEP; REVIEW; SKELETAL MUSCLE; SLEEP WAKING CYCLE; SYMPATHETIC TONE; VASCULAR RESISTANCE; WAKEFULNESS;

EID: 84890424237     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00554.2013     Document Type: Review

References (102)

1. Abbott SBG, Coates MB, Stornetta RL, Guyenet PG. Optogenetic stimulation of C1 and retrotrapezoid nucleus neurons causes sleep statedependent cardiorespiratory stimulation and arousal in rats. Hypertension 61: 835-841, 2013.
2. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450: 420-424, 2007.
3. Alam MN, McGinty D, Szymusiak R. Neuronal discharge of preoptic/ anterior hypothalamic thermosensitive neurons: relation to NREM sleep. Am J Physiol Regul Integr Comp Physiol 269: R1240-R1249, 1995.
4. Alföldi P, Rubicsek G, Cserni G, Obál. FJ. Brain and core temperatures and peripheral vasomotion during sleep and wakefulness at various ambient temperatures in the rat. Pflügers Arch 417: 336-341, 1990.
5. Andresen MC, Kunze DL. Nucleus tractus solitarius-gateway to neural circulatory control. Annu Rev Physiol 56: 93-116, 1994.
6. Bastianini S, Silvani A, Berteotti C, Elghozi JL, Franzini C, Lenzi P, Lo Martire V, Zoccoli G. Sleep related changes in blood pressure in hypocretin-deficient narcoleptic mice. Sleep 34: 213-218, 2011.
7. Bastianini S, Silvani A, Berteotti C, Lo Martire V, Zoccoli G. Mice show circadian rhythms of blood pressure during each wake-sleep state. Chronobiol Int 29: 82-86, 2012.
8. Ben-Dov IZ, Kark JD, Ben-Ishay D, Mekler J, Ben-Arie L, Bursztyn M. Predictors of all-cause mortality in clinical ambulatory monitoring: unique aspects of blood pressure during sleep. Hypertension 49: 1235-1241, 2007.
9. Berteotti C, Franzini C, Lenzi P, Zoccoli G, Silvani A. Surges of arterial pressure during REM sleep in spontaneously hypertensive rats. Sleep 31: 111-117, 2008.
10. Bizzi E, Pompeiano O, Somogyi I. Vestibular nuclei: activity of single neurons during natural sleep and wakefulness. Science 145: 414-415, 1964.
11. Bonnet MH, Doghramji K, Roehrs T, Stepanski EJ, Sheldon SH, Walters AS, Wise M, Chesson AL Jr. The scoring of arousal in sleep: reliability, validity, and alternatives. J Clin Sleep Med 3: 133-145, 2007.
12. Callaway CW, Lydic R, Baghdoyan HA, Hobson JA. Pontogeniculooccipital waves: spontaneous visual system activity during rapid eye movement sleep. Cell Mol Neurobiol 7: 105-149, 1987.
13. Carrington MJ, Barbieri R, Colrain IM, Crowley KE, Kim Y, Trinder J. Changes in cardiovascular function during the sleep onset period in young adults. J Appl Physiol 98: 468-476, 2005.
14. Carrive P, Bandler R. Viscerotopic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal grey: a correlative functional and anatomical study. Brain Res 541: 206-215, 1991.
15. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB, Yanagisawa M. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98: 437-451, 1999.
16. Cirelli C, Tononi G. On the functional significance of c-fos induction during the sleep-waking cycle. Sleep 23: 453-469, 2000.
17. Dampney RA. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 74: 323-364, 1994.
18. Dauvilliers Y, Arnulf I, Mignot E. Narcolepsy with cataplexy. Lancet 369: 499-511, 2007.
19. Dauvilliers Y, Jaussent I, Krams B, Scholz S, Lado S, Levy P, Pepin JL. Non-dipping blood pressure profile in narcolepsy with cataplexy. PLos One 7: e38977, 2012.
20. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS, 2nd Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95: 322-327, 1998.
21. Eguchi K, Satoh T. Convergence of sleep-wakefulness subsystems onto single neurons in the region of cat's solitary tract nucleus. Arch Ital Biol 118: 331-345, 1980.
22. el Mansari M, Sakai K, Jouvet M. Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 76: 519-529, 1989.
23. Eriksson KS, Sergeeva O, Brown RE, Haas HL. Orexin/hypocretin excites the histaminergic neurons of the tuberomammillary nucleus. J Neurosci 21: 9273-9279, 2001.
24. Felder RB, Mifflin SW. Modulation of carotid sinus afferent input to nucleus tractus solitarius by parabrachial nucleus stimulation. Circ Res 63: 35-49, 1988.
25. Fraigne JJ, Orem JM. Phasic motor activity of respiratory and nonrespiratory muscles in REM sleep. Sleep 34: 425-434, 2011.
26. Fronczek R, Overeem S, Lammers GJ, van Dijk JG, Van Someren EJ. Altered skin-temperature regulation in narcolepsy relates to sleep propensity. Sleep 29: 1444-1449, 2006.
27. Fuller PM, Sherman D, Pedersen NP, Saper CB, Lu J. Reassessment of the structural basis of the ascending arousal system. J Comp Neurol 519: 933-956, 2011.
28. Fulwiler CE, Saper CB. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res Rev 7: 229-259, 1984.
29. Futuro-Neto HA, Coote JH. Changes in sympathetic activity to heart and blood vessels during desynchronized sleep. Brain Res 252: 259-268, 1982.
30. Futuro-Neto HA, Coote JH. Desynchronized sleep-like pattern of sympathetic activity elicited by electrical stimulation of sites in the brainstem. Brain Res 252: 269-276, 1982.
31. Garcia-Rill E, Houser CR, Skinner RD, Smith W, Woodward DJ. Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res Bull 18: 731-738, 1987.
32. Gong H, McGinty D, Guzman-Marin R, Chew KT, Stewart D, Szymusiak R. Activation of c-fos in GABAergic neurones in the preoptic area during sleep and in response to sleep deprivation. J Physiol 556: 935-946, 2004.
33. Grillner S. Neurobiological bases of rhythmic motor acts in vertebrates. Science 228: 143-149, 1985.
34. Grimaldi D, Calandra-Buonaura G, Provini F, Agati P, Pierangeli G, Franceschini C, Barletta G, Plazzi G, Montagna P, Cortelli P. Abnormal sleep-cardiovascular system interaction in narcolepsy with cataplexy: effects of hypocretin deficiency in humans. Sleep 35: 519-528, 2012.
35. Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH. The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262: 105-124, 1987.
36. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, Sugiyama F, Yagami K, Goto K, Yanagisawa M, Sakurai T. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 30: 345-354, 2001.
37. Hayward LF, Felder RB. Lateral parabrachial nucleus modulates baroreflex regulation of sympathetic nerve activity. Am J Physiol Regul Integr Comp Physiol 274: R1274-R1282, 1998.
38. Hermida RC, Ayala DE, Mojon A, Fernandez JR. Blunted sleep-time relative blood pressure decline increases cardiovascular risk independent of blood pressure level-the "normotensive non-dipper" paradox. Chronobiol Int 30: 87-98, 2013.
39. Hermida RC, Ayala DE, Mojon A, Fernandez JR. Decreasing sleeptime blood pressure determined by ambulatory monitoring reduces cardiovascular risk. J Am Coll Cardiol 58: 1165-1173, 2011.
40. Horowitz SS, Blanchard J, Morin LP. Medial vestibular connections with the hypocretin (orexin) system. J Comp Neurol 487: 127-146, 2005.
41. Iigaya K, Horiuchi J, McDowall LM, Lam AC, Sediqi Y, Polson JW, Carrive P, Dampney RA. Blockade of orexin receptors with Almorexant reduces cardiorespiratory responses evoked from the hypothalamus but not baro- or chemoreceptor reflex responses. Am J Physiol Regul Integr Comp Physiol 303: R1011-R1022, 2012.
42. Jacobs BL, Fornal CA. Activity of brain serotonergic neurons in the behaving animal. Pharmacol Rev 43: 563-578, 1991.
43. Kiyashchenko LI, Mileykovskiy BY, Maidment N, Lam HA, Wu MF, John J, Peever J, Siegel JM. Release of hypocretin (orexin) during waking and sleep states. J Neurosci 22: 5282-5286, 2002.
44. Kobayashi R, Koike Y, Hirayama M, Ito H, Sobue G. Skin sympathetic nerve function during sleep-a study with effector responses. Auton Neurosci 103: 121-126, 2003.
45. Kolaj M, Coderre E, Renaud LP. Orexin peptides enhance median preoptic nucleus neuronal excitability via postsynaptic membrane depolarization and enhancement of glutamatergic afferents. Neuroscience 155: 1212-1220, 2008.
46. Krauchi K, Gompper B, Hauenstein D, Flammer J, Pfluger M, Studerus E, Schotzau A, Orgul S. Diurnal blood pressure variations are associated with changes in distal-proximal skin temperature gradient. Chronobiol Int 29: 1273-1283, 2012.
47. Krout KE, Mettenleiter TC, Loewy AD. Single CNS neurons link both central motor and cardiosympathetic systems: a double-virus tracing study. Neuroscience 118: 853-866, 2003.
48. Kuwaki T, Zhang W. Orexin neurons as arousal-associated modulators of central cadiorespiratory regulation. Resp Physiol Neurobiol 174: 43-54, 2010.
49. Lara JP, Parkes MJ, Silva-Carvhalo L, Izzo P, Dawid-Milner MS, Spyer KM. Cardiovascular and respiratory effects of stimulation of cell bodies of the parabrachial nuclei in the anaesthetized rat. J Physiol 477: 321-329, 1994.
50. Lo Martire V, Silvani A, Bastianini S, Berteotti C, Zoccoli G. Effects of ambient temperature on sleep and cardiovascular regulation in mice: the role of hypocretin/orexin neurons. PLos One 7: e47032, 2012.
51. Lu J, Bjorkum AA, Xu M, Gaus SE, Shiromani PJ, Saper CB. Selective activation of the extended ventrolateral preoptic nucleus during rapid eye movement sleep. J Neurosci 22: 4568-4576, 2002.
52. Lu J, Greco MA, Shiromani P, Saper CB. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 20: 3830-3842, 2000.
53. Luppi PH, Clement O, Sapin E, Peyron C, Gervasoni D, Léger L, Fort P. Brainstem mechanisms of paradoxical (REM) sleep generation. Pflügers Arch 463: 43-52, 2012.
54. Malpas SC. The rhythmicity of sympathetic nerve activity. Prog Neurobiol 56: 65-96, 1998.
55. Mandel DA, Schreihofer AM. Central respiratory modulation of barosensitive neurones in rat caudal ventrolateral medulla. J Physiol 572: 881-896, 2006.
56. Marder E. Neuromodulation of neuronal circuits: back to the future. Neuron 76: 1-11, 2012.
57. McCall RB, Clement ME. Identification of serotonergic and sympathetic neurons in medullary raphe nuclei. Brain Res 477: 172-182, 1989.
58. Miki K, Yoshimoto M. Sympathetic nerve activity during sleep, exercise, and mental stress. Auton Neurosci 174: 15-20, 2013.
59. Morrison AR, Pompeiano O. Vestibular influences during sleep. VI. Vestibular control of autonomic functions during the rapid eye movements of desynchronized sleep. Arch Ital Biol 108: 154-180, 1970.
60. Morrison SF, Gebber GL. Raphe neurons with sympathetic-related activity: baroreceptor responses and spinal connections. Am J Physiol Regul Integr Comp Physiol 246: R338-R348, 1984.
61. Muller JE, Tofler GH, Stone PH. Circadian variation and triggers of onset of acute cardiovascular disease. Circulation 79: 733-743, 1989.
62. Nagura S, Sakagami T, Kakiichi A, Yoshimoto M, Miki K. Acute shifts in baroreflex control of renal sympathetic nerve activity induced by REM sleep and grooming in rats. J Physiol 558: 975-983, 2004.
63. Nakamura K. Central circuitries for body temperature regulation and fever. Am J Physiol Regul Integr Comp Physiol 301: R1207-R1228, 2011.
64. Nakamura K, Morrison SF. Central efferent pathways for cold-defensive and febrile shivering. J Physiol 589: 3641-3658, 2011.
65. Padley JR, Kumar NN, Li Q, Nguyen TB, Pilowsky PM, Goodchild AK. Central command regulation of circulatory function mediated by descending pontine cholinergic inputs to sympathoexcitatory rostral ventrolateral medulla neurons. Circ Res 100: 284-291, 2007.
66. Peyron C, Faraco J, Rogers W, Ripley B, Overeem S, Charnay Y, Nevsimalova S, Aldrich M, Reynolds D, Albin R, Li R, Hungs M, Pedrazzoli M, Padigaru M, Kucherlapati M, Fan J, Maki R, Lammers GJ, Bouras C, Kucherlapati R, Nishino S, Mignot E. A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 6: 991-997, 2000.
67. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18: 9996-10015, 1998.
68. Pigarev IN, Nothdurft HC, Kastner S. Evidence for asynchronous development of sleep in cortical areas. Neuroreport 8: 2557-2560, 1997.
69. Plowey ED, Kramer JM, Beatty JA, Waldrop TG. In vivo electrophysiological responses of pedunculopontine neurons to static muscle contraction. Am J Physiol Regul Integr Comp Physiol 283: R1008-R1019, 2002.
70. Ribeiro-do-Valle LE, Lucena RL. Behavioral correlates of the activity of serotonergic and non-serotonergic neurons in caudal raphe nuclei. Braz J Med Biol Res 34: 919-937, 2001.
71. Romanovsky AA. Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol 292: R37-R46, 2007.
72. Saito H, Sakai K, Jouvet M. Discharge patterns of the nucleus parabrachialis lateralis neurons of the cat during sleep and waking. Brain Res 134: 59-72, 1977.
73. Sakai K. Sleep-waking discharge profiles of median preoptic and surrounding neurons in mice. Neuroscience 182: 144-161, 2011.
74. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585, 1998.
75. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. Sleep state switching. Neuron 68: 1023-1042, 2010.
76. Sforza E, Jouny C, Ibanez V. Cardiac activation during arousal in humans: further evidence for hierarchy in the arousal response. Clin Neurophysiol 111: 1611-1619, 2000.
77. Shea SA, Hilton MF, Hu K, Scheer FA. Existence of an endogenous circadian blood pressure rhythm in humans that peaks in the evening. Circ Res 108: 980-984, 2011.
78. Sherin JE, Elmquist JK, Torrealba F, Saper CB. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18: 4705-4721, 1998.
79. Siegel JM. Sleep viewed as a state of adaptive inactivity. Nat Rev Neurosci 10: 747-753, 2009.
80. Silber MH, Ancoli-Israel S, Bonnet MH, Chokroverty S, Grigg-Damberger MM, Hirshkowitz M, Kapen S, Keenan SA, Kryger MH, Penzel T, Pressman MR, Iber C. The visual scoring of sleep in adults. J Clin Sleep Med 3: 121-131, 2007.
81. Silvani A. Physiological sleep-dependent changes in arterial blood pressure: central autonomic commands and baroreflex control. Clin Exp Pharmacol Physiol 35: 987-994, 2008.
82. Silvani A, Bastianini S, Berteotti C, Lo Martire V, Zoccoli G. Control of cardiovascular variability during undisturbed wake-sleep behavior in hypocretin-deficient mice. Am J Physiol Regul Integr Comp Physiol 302: R958-R964, 2012.
83. Silvani A, Grimaldi D, Barletta G, Bastianini S, Vandi S, Pierangeli G, Plazzi G, Cortelli P. Cardiovascular variability as a function of sleep-wake behaviour in narcolepsy with cataplexy. J Sleep Res 22: 178-184, 2013.
84. Silvani A, Grimaldi D, Vandi S, Barletta G, Vetrugno R, Provini F, Pierangeli G, Berteotti C, Montagna P, Zoccoli G, Cortelli P. Sleepdependent changes in the coupling between heart period and blood pressure in human subjects. Am J Physiol Regul Integr Comp Physiol 294: R1686-R1692, 2008.
85. Silvani A, Magosso E, Bastianini S, Lenzi P, Ursino M. Mathematical modeling of cardiovascular coupling: central autonomic commands and baroreflex control. Auton Neurosci 162: 66-71, 2011.
86. Sirieix C, Gervasoni D, Luppi PH, Leger L. Role of the lateral paragigantocellular nucleus in the network of paradoxical (REM) sleep: an electrophysiological and anatomical study in the rat. PLos One 7: e28724, 2012.
87. Sorensen GL, Knudsen S, Petersen ER, Kempfner J, Gammeltoft S, Sorensen HB, Jennum P. Attenuated heart rate response is associated with hypocretin deficiency in patients with narcolepsy. Sleep 36: 91-98, 2013.
88. Staessen JA, Bieniaszewski L, OBrien E, Gosse P, Hayashi H, Imai Y, Kawasaki T, Otsuka K, Palatini P, Thijs L, Fagard R. Nocturnal blood pressure fall on ambulatory monitoring in a large international database. The "Ad Hoc" Working Group. Hypertension 29: 30-39, 1997.
89. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi RC. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10: 2541-2559, 1990.
90. Takahashi K, Kayama Y, Lin JS, Sakai K. Locus coeruleus neuronal activity during the sleep-waking cycle in mice. Neuroscience 169: 1115-1126, 2010.
91. Takahashi K, Lin JS, Sakai K. Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse. J Neurosci 26: 10292-10298, 2006.
92. Takahashi K, Lin JS, Sakai K. Neuronal activity of orexin and non-orexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 153: 860-870, 2008.
93. Takeuchi S, Iwase S, Mano T, Okada H, Sugiyama Y, Watanabe T. Sleep-related changes in human muscle and skin sympathetic nerve activities. J Auton Nerv Syst 47: 121-129, 1994.
94. Tang X, Dworkin BR. Baroreflexes of the rat. VI Sleep and responses to aortic nerve stimulation in the dmNTS. Am J Physiol Regul Integr Comp Physiol 298: R1428-R1434, 2010.
95. Thakkar MM. Histamine in the regulation of wakefulness. Sleep Med Rev 15: 65-74, 2011.
96. Torterolo P, Sampogna S, Chase MH. A restricted parabrachial pontine region is active during non-rapid eye movement sleep. Neuroscience 190: 184-193, 2011.
97. Trinder J, Waloszek J, Woods MJ, Jordan AS. Sleep and cardiovascular regulation. Pflügers Arch 463: 161-168, 2012.
98. Uschakov A, Gong H, McGinty D, Szymusiak R. Sleep-active neurons in the preoptic area project to the hypothalamic paraventricular nucleus and perifornical lateral hypothalamus. Eur J Neurosci 23: 3284-3296, 2006.
99. Vanni-Mercier G, Debilly G. A key role for the caudoventral pontine tegmentum in the simultaneous generation of eye saccades in bursts and associated ponto-geniculo-occipital waves during paradoxical sleep in the cat. Neuroscience 86: 571-585, 1998.
100. Verret L, Leger L, Fort P, Luppi PH. Cholinergic and noncholinergic brainstem neurons expressing Fos after paradoxical (REM) sleep deprivation and recovery. Eur J Neurosci 21: 2488-2504, 2005.
101. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G. Local sleep in awake rats. Nature 472: 443-447, 2011.
102. Yoshimoto M, Yoshida I, Miki K. Functional role of diverse changes in sympathetic nerve activity in regulating arterial pressure during REM sleep. Sleep 34: 1093-1101, 2011.