The lateral paragigantocellular nucleus modulates parasympathetic cardiac neurons: A mechanism for rapid eye movement sleep-dependent changes in heart rate

Journal of Neurophysiology

Volumn 104, Issue 2, 2010, Pages 685-694

  Dergacheva, Olga ^a   Wang, Xin ^a   Lovett Barr, Mary R ^a   Jameson, Heather ^a   Mendelowitz, David ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BUNGAROTOXIN; NICOTINE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN NUCLEUS; BRAIN STEM; CARDIAC VAGAL NERVE CELL; CONTROLLED STUDY; ELECTROSTIMULATION; GABAERGIC SYSTEM; HEART CONTRACTION; HEART RATE; HYPERCAPNIA; HYPOXIA; LATERAL PARAGIGANTOCELLULAR NUCLEUS; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PARASYMPATHETIC FUNCTION; PRIORITY JOURNAL; RAT; REM SLEEP;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; HEART; HEART RATE; INHIBITORY POSTSYNAPTIC POTENTIALS; MEDULLA OBLONGATA; N-METHYLASPARTATE; NEURONS; NICOTINE; NICOTINIC AGONISTS; PATCH-CLAMP TECHNIQUES; PYRIDAZINES; RATS; RATS, SPRAGUE-DAWLEY; SLEEP, REM; TIME FACTORS; VAGUS NERVE; VALINE;

EID: 77955973923     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00228.2010     Document Type: Article

References (71)

1. Babic T, Ciriello J. Medullary and spinal cord projections from cardiovascular responsive sites in the rostral ventromedial medulla. J Comp Neurol 469: 391-412, 2004.
2. Benedito MA, Camarini R. Rapid eye movement sleep deprivation induces an increase in acetylcholinesterase activity in discrete rat brain regions. Braz J Med Biol Res 34: 103-109, 2001.
3. Berlad II, Shlitner A, Ben-Haim S, Lavie P. Power spectrum analysis and heart rate variability in Stage 4 and REM sleep: evidence for state-specific changes in autonomic dominance. J Sleep Res 2: 88-90, 1993.
4. Bieger D, Hopkins DA. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol 262: 546-562, 1987. (Pubitemid 17130953)
5. Boissard R, Gervasoni D, Schmidt MH, Barbagli B, Fort P, Luppi PH. The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur J Neurosci 16: 1959-1973, 2002.
6. Burlet S, Tyler CJ, Leonard CS. Direct and indirect excitation of laterodorsal tegmental neurons by Hypocretin/Orexin peptides: implications for wakefulness and narcolepsy. J Neurosci 22: 2862-2872, 2002.
7. Cheng Z, Zhang H, Yu J, Wurster RD, Gozal D. Attenuation of baroreflex sensitivity after domoic acid lesion of the nucleus ambiguus of rats. J Appl Physiol 96: 1137-1145, 2004.
8. Christian EP, Dudek FE. Characteristics of local excitatory circuits studied with glutamate microapplication in the CA3 area of rat hippocampal slices. J Neurophysiol 59: 90-109, 1988.
9. Ciriello J, Calaresu FR. Distribution of vagal cardioinhibitory neurons in the medulla of the cat. Am J Physiol 238: R57-R64, 1980. (Pubitemid 10112382)
10. Ciriello J, Li Z, de Oliveira CV. Cardioacceleratory responses to hypocretin- 1 injections into rostral ventromedial medulla. Brain Res 991: 84-95, 2003.
11. Cobb LA, Werner JA, Trobaugh GB. Sudden cardiac death. I. A decade's experience with out-of-hospital resuscitation. Mod Concepts Cardiovasc Dis 49: 31-36, 1980.
12. Dahan L, Astier B, Vautrelle N, Urbain N, Kocsis B, Chouvet G. Prominent burst firing of dopaminergic neurons in the ventral tegmental area during paradoxical sleep. Neuropsychopharmacology 32: 1232-1241, 2007.
13. Dehkordi O, Millis RM, Dennis GC, Jazini E, Williams C, Hussain D, Jayam-Trouth A. Expression of alpha-7 and alpha-4 nicotinic acetylcholine receptors by GABAergic neurons of rostral ventral medulla and caudal pons. Brain Res 1185: 95-102, 2007.
14. del Bo A, Ledoux JE, Tucker LW, Harshkfield GA, Reis DJ. Arterial pressure and heart rate changes during natural sleep in rat. Physiol Behav 28: 425-429, 1982. (Pubitemid 12116568)
15. DeMesquita S, Hale GA. Cardiopulmonary regulation after rapid-eye-movement sleep deprivation. J Appl Physiol 72: 970-976, 1992.
16. Dergacheva O, Kamendi H, Wang X, Pinol RM, Frank J, Jameson H, Gorini C, Mendelowitz D. The role of 5-HT3 and other excitatory receptors in central cardiorespiratory responses to hypoxia: implications for sudden infant death syndrome. Pediatr Res 65: 625-630, 2009.
17. Dickerson LW, Huang AH, Nearing BD, Verrier RL. Primary coronary vasodilation associated with pauses in heart rhythm during sleep. Am J Physiol 264: R186-R196, 1993a.
18. Dickerson LW, Huang AH, Thurnher MM, Nearing BD, Verrier RL. Relationship between coronary hemodynamic changes and the phasic events of rapid eye movement sleep. Sleep 16: 550-557, 1993b.
19. Doyle MW, Andresen MC. Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85: 2213-2223, 2001.
20. 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.
21. Franco P, Szliwowski H, Dramaix M, Kahn A. Decreased autonomic responses to obstructive sleep events in future victims of sudden infant death syndrome. Pediatr Res 46: 33-39, 1999.
22. Frank JG, Jameson HS, Gorini C, Mendelowitz D. Mapping and identification of GABAergic neurons in transgenic mice projecting to cardiac vagal neurons in the nucleus ambiguus using photo-uncaging. J Neurophysiol 101: 1755-1760, 2009.
23. Gabriel M, Albani M. Cardiac slowing and respiratory arrest in preterm infants. Eur J Pediatr 122: 257-261, 1976.
24. Gaultier C. Cardiorespiratory adaptation during sleep in infants and children. Pediatr Pulmonol 19: 105-117, 1995.
25. George CF, Kryger MH. Sleep and control of heart rate. Clin Chest Med 6: 595-601, 1985.
26. Holmes CJ, Jones BE. Importance of cholinergic, GABAergic, serotonergic and other neurons in the medial medullary reticular formation for sleepwake states studied by cytotoxic lesions in the cat. Neuroscience 62: 1179-1200, 1994. (Pubitemid 24335610)
27. Huertas J, McMillin JK. Paradoxical sleep: effect of low partial pressures of atmospheric oxygen. Science 159: 745-746, 1968.
28. Jouvet M. Research on the neural structures and responsible mechanisms in different phases of physiological sleep. Arch Ital Biol 100: 125-206, 1962.
29. Kamendi HW, Cheng Q, Dergacheva O, Frank JG, Gorini C, Jameson HS, Pinol RA, Wang X, Mendelowitz D. Recruitment of excitatory serotonergic neurotransmission to cardiac vagal neurons in the nucleus ambiguus post hypoxia and hypercapnia. J Neurophysiol 99: 1163-1168, 2008.
30. Karayannis T, Huerta-Ocampo I, Capogna M. GABAergic and pyramidal neurons of deep cortical layers directly receive and differently integrate callosal input. Cereb Cortex 17: 1213-1226, 2007.
31. 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.
32. Kodama T, Lai YY, Siegel JM. Enhancement of acetylcholine release during REM sleep in the caudomedial medulla as measured by in vivo microdialysis. Brain Res 580: 348-350, 1992.
33. Koehler U, Fus E, Grimm W, Pankow W, Schafer H, Stammnitz A, Peter JH. Heart block in patients with obstructive sleep apnoea: pathogenetic factors and effects of treatment. Eur Respir J 11: 434-439, 1998.
34. Kuo TB, Yang CC. Scatterplot analysis of EEG slow-wave magnitude and heart rate variability: an integrative exploration of cerebral cortical and autonomic functions. Sleep 27: 648-656, 2004.
35. Laszy J, Sarkadi A. Hypoxia-induced sleep disturbance in rats. Sleep 13: 205-217, 1990.
36. Meny RG, Carroll JL, Carbone MT, Kelly DH. Cardiorespiratory recordings from infants dying suddenly and unexpectedly at home. Pediatrics 93: 44-49, 1994.
37. Metz B. Hypercapnia and acetylcholine release from the cerebral cortex and medulla. J Physiol 186: 321-332, 1966.
38. Mirmiran M. The importance of fetal/neonatal REM sleep. Eur J Obstet Gynecol Reprod Biol 21: 283-291, 1986.
39. Neff RA, Simmens SJ, Evans C, Mendelowitz D. Prenatal nicotine exposure alters central cardiorespiratory responses to hypoxia in rats: implications for sudden infant death syndrome. J Neurosci 24: 9261-9268, 2004. (Pubitemid 39426162)
40. Nelson JP, McCarley RW, Hobson JA. REM sleep burst neurons, PGO waves, and eye movement information. J Neurophysiol 50: 784-797, 1983.
41. Paxinos G. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1997.
42. Rampon C, Peyron C, Gervasoni D, Pow DV, Luppi PH, Fort P. Origins of the glycinergic inputs to the rat locus coeruleus and dorsal raphe nuclei: a study combining retrograde tracing with glycine immunohistochemistry. Eur J Neurosci 11: 1058-1066, 1999.
43. Sakai K. Executive mechanisms of paradoxical sleep. Arch Ital Biol 126: 239-257, 1988.
44. Sandyk R. Melatonin and maturation of REM sleep. Int J Neurosci 63: 105-114, 1992.
45. Sato T, Seto K. Centrally administered ouabain aggravates rapid-eye-movement- sleep-related bradyarrhythmias in freely moving rats. Br J Pharmacol 110: 253-256, 1993.
46. Sei H, Morita Y. Effect of ambient temperature on arterial pressure variability during sleep in the rat. J Sleep Res 5: 37-41, 1996. (Pubitemid 26148966)
47. Sei H, Sano A, Ohno H, Yamabe K, Nishioka Y, Sone S, Morita Y. Age-related changes in control of blood pressure and heart rate during sleep in the rat. Sleep 25: 279-285, 2002.
48. Snyder F, Hobson JA, Morrison DF, Goldfrank F. Changes in respiration, heart rate, and systolic blood pressure in human sleep. J Appl Physiol 19: 417-422, 1964.
49. Song G, Li Q, Shao FZ. GABAergic neurons in Kolliker-Fuse nucleus and Botzinger complex with axons projecting to phrenic nucleus. Sheng Li Xue Bao 52: 167-169, 2000.
50. Standish A, Enquist LW, Escardo JA, Schwaber JS. Central neuronal circuit innervating the rat heart defined by transneuronal transport of pseudorabies virus. J Neurosci 15: 1998-2012, 1995.
51. Steinschneider A. Prolonged apnea and the sudden infant death syndrome: clinical and laboratory observations. Pediatrics 50: 646-654, 1972.
52. Stuesse SL. Origins of cardiac vagal preganglionic fibers: a retrograde transport study. Brain Res 236: 15-25, 1982.
53. Ter Horst GJ, Van den Brink A, Homminga SA, Hautvast RW, Rakhorst G, Mettenleiter TC, De Jongste MJ, Lie KI, Korf J. Transneuronal viral labelling of rat heart left ventricle controlling pathways. Neuroreport 4: 1307-1310, 1993.
54. Toscani L, Gangemi PF, Parigi A, Silipo R, Ragghianti P, Sirabella E, Morelli M, Bagnoli L, Vergassola R, Zaccara G. Human heart rate variability and sleep stages. Ital J Neurol Sci 17: 437-439, 1996.
55. Valladares EM, Eljammal SM, Motivala S, Ehlers CL, Irwin MR. Sex differences in cardiac sympathovagal balance and vagal tone during nocturnal sleep. Sleep Med 9: 310-316, 2008. (Pubitemid 351387089)
56. Varner KJ, Rutherford DS, Vasquez EC, Brody MJ. Identification of cardiovascular neurons in the rostral ventromedial medulla in anesthetized rats. Hypertension 19: II193-II197, 1992.
57. Vazquez J, Baghdoyan HA. GABAA receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation. J Neurophysiol 92: 2198-2206, 2004.
58. Verret L, Fort P, Gervasoni D, Leger L, Luppi PH. Localization of the neurons active during paradoxical (REM) sleep and projecting to the locus coeruleus noradrenergic neurons in the rat. J Comp Neurol 495: 573-586, 2006.
59. 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.
60. Verrier RL, Lau TR, Wallooppillai U, Quattrochi J, Nearing BD, Moreno R, Hobson JA. Primary vagally mediated decelerations in heart rate during tonic rapid eye movement sleep in cats. Am J Physiol 274: R1136-R1141, 1998.
61. Verrier RL, Muller JE, Hobson JA. Sleep, dreams, and sudden death: the case for sleep as an autonomic stress test for the heart. Cardiovasc Res 31: 181-211, 1996.
62. Villa MP, Calcagnini G, Pagani J, Paggi B, Massa F, Ronchetti R. Effects of sleep stage and age on short-term heart rate variability during sleep in healthy infants and children. Chest 117: 460-466, 2000.
63. Wang J, Irnaten M, Neff RA, Venkatesan P, Evans C, Loewy AD, Mettenleiter TC, Mendelowitz D. Synaptic and neurotransmitter activation of cardiac vagal neurons in the nucleus ambiguus. Ann NY Acad Sci 940: 237-246, 2001. (Pubitemid 32623397)
64. Wang J, Irnaten M, Venkatesan P, Evans C, Baxi S, Mendelowitz D. Synaptic activation of hypoglossal respiratory motorneurons during inspiration in rats. Neurosci Lett 332: 195-199, 2002. (Pubitemid 35223480)
65. Wang J, Wang X, Irnaten M, Venkatesan P, Evans C, Baxi S, Mendelowitz D. Endogenous acetylcholine and nicotine activation enhances GABAergic and glycinergic inputs to cardiac vagal neurons. J Neurophysiol 89: 2473-2481, 2003.
66. Wuarin JP, Dudek FE. Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol 85: 1067-1077, 2001.
67. Xi MC, Chase MH. Neuronal mechanisms of active (rapid eye movement) sleep induced by microinjections of hypocretin into the nucleus pontis oralis of the cat. Neuroscience 140: 335-342, 2006.
68. Xi MC, Fung SJ, Yamuy J, Morales FR, Chase MH. Induction of active (REM) sleep and motor inhibition by hypocretin in the nucleus pontis oralis of the cat. J Neurophysiol 87: 2880-2888, 2002. (Pubitemid 34670668)
69. Xi MC, Fung SJ, Yamuy J, Morales FR, Chase MH. Hypocretinergic facilitation of synaptic activity of neurons in the nucleus pontis oralis of the cat. Brain Res 976: 253-258, 2003.
70. Yoshimura M, Nishi S. Primary afferent-evoked glycine- and GABA-mediated IPSPs in substantia gelatinosa neurones in the rat spinal cord in vitro. J Physiol 482: 29-38, 1995.
71. Zhang J, Mifflin SW. Integration of aortic nerve inputs in hypertensive rats. Hypertension 35: 430-436, 2000. (Pubitemid 30054212)