Home LiteratureArticle Details
PMID: 8987799 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Pontine nitric oxide modulates acetylcholine release, rapid eye movement sleep generation, and respiratory rate.

Leonard TO, Lydic R

Abstract

Pontine cholinergic neurotransmission is known to play a key role in the regulation of rapid eye movement (REM) sleep and to contribute to state-dependent respiratory depression. Nitric oxide (NO) has been shown to alter the release of acetylcholine (ACh) in a number of brain regions, and previous studies indicate that NO may participate in the modulation of sleep/wake states. The present investigation tested the hypothesis that inhibition of NO synthase (NOS) within the medial pontine reticular formation (mPRF) of the unanesthetized cat would decrease ACh release, inhibit REM sleep, and prevent cholinergically mediated respiratory depression. Local NOS inhibition by microdialysis delivery of N(G)-nitro-L-arginine (NLA) significantly reduced ACh release in the cholinergic cell body region of the pedunculopontine tegmental nucleus and in the cholinoceptive mPRF. A second series of experiments demonstrated that mPRF microinjection of NLA significantly reduced the amount of REM sleep and the REM sleep-like state caused by mPRF injection of the acetylcholinesterase inhibitor neostigmine. Duration but not frequency of REM sleep epochs was significantly decreased by mPRF NLA administration. Injection of NLA into the mPRF before neostigmine injection also blocked the ability of neostigmine to decrease respiratory rate during the REM sleep-like state. Taken together, these findings suggest that mPRF NO contributes to the modulation of ACh release, REM sleep, and breathing.

MeSH Terms
Acetylcholine/metabolism Anesthetics, Inhalation/pharmacology Animals Arousal/drug effects Cats Cholinergic Fibers/metabolism Chromatography, High Pressure Liquid Enzyme Inhibitors/pharmacology Halothane/pharmacology Male Microdialysis Microinjections Models, Neurological Neostigmine/pharmacology Nitric Oxide/physiology Nitric Oxide Synthase/antagonists & inhibitors,metabolism Nitroarginine/pharmacology Parasympathomimetics/pharmacology Polysomnography Pons/drug effects,metabolism,physiology Respiration/drug effects,physiology Secretory Rate/drug effects Sleep, REM/drug effects,physiology
Chemicals
Anesthetics, Inhalation Enzyme Inhibitors Parasympathomimetics Nitroarginine Nitric Oxide Neostigmine Nitric Oxide Synthase Acetylcholine Halothane
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Leonard T O
Department of Anesthesia, Pennsylvania State University College of Medicine, Hershey 17033, USA.
Lydic R
References (66)
66 references, click to expand
  1. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. I. Retrograde tracing studies.
    J Comp Neurol. 1992 Jul 22;321(4):515-43 PMID: 1380518
  2. Pontine cholinergic mechanisms modulate the cortical electroencephalographic spindles of halothane anesthesia.
    Anesthesiology. 1996 Apr;84(4):945-54 PMID: 8638850
  3. Respiratory nuclei share synaptic connectivity with pontine reticular regions regulating REM sleep.
    Am J Physiol. 1995 Feb;268(2 Pt 1):L251-62 PMID: 7864146
  4. Modulation of in vivo striatal transmitter release by nitric oxide and cyclic GMP.
    J Neurochem. 1994 Feb;62(2):807-10 PMID: 7905029
  5. Nitric oxide synthase inhibition and extracellular glutamate concentration after cerebral ischemia/reperfusion.
    Stroke. 1995 Feb;26(2):298-304 PMID: 7530389
  6. Pontine cholinergic reticular mechanisms cause state-dependent changes in the discharge of parabrachial neurons.
    Am J Physiol. 1994 Jan;266(1 Pt 2):R136-50 PMID: 8304534
  7. Neuronal NADPH diaphorase is a nitric oxide synthase.
    Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2811-4 PMID: 1707173
  8. Nitric oxide releases acetylcholine in the basal forebrain.
    Eur J Pharmacol. 1992 May 27;216(1):139-40 PMID: 1382021
  9. Nitric oxide synthase inhibitor dose-dependently and reversibly reduces the threshold for halothane anesthesia. A role for nitric oxide in mediating consciousness?
    Anesthesiology. 1992 Oct;77(4):779-84 PMID: 1384399
  10. Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase.
    Neuron. 1991 Oct;7(4):615-24 PMID: 1718335
  11. Inhibition of constitutive and inducible nitric oxide synthase: potential selective inhibition.
    Annu Rev Pharmacol Toxicol. 1995;35:165-94 PMID: 7541188
  12. Evidence that cholinergic axons from the parabrachial region of the brainstem are the exclusive source of nitric oxide in the lateral geniculate nucleus of the cat.
    J Comp Neurol. 1993 Aug 15;334(3):410-30 PMID: 7690785
  13. Responses of presumed cholinergic mesopontine tegmental neurons to carbachol microinjections in freely moving cats.
    Exp Brain Res. 1990;83(1):115-23 PMID: 2073933
  14. Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study.
    Neuroscience. 1994 Mar;59(2):309-30 PMID: 8008195
  15. The organization of central cholinergic systems and their functional importance in sleep-waking states.
    Prog Brain Res. 1993;98:61-71 PMID: 8248538
  16. Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system.
    J Comp Neurol. 1989 Jan 8;279(2):281-311 PMID: 2913070
  17. Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. II. Effects upon sleep-waking states.
    Brain Res. 1988 Aug 23;458(2):285-302 PMID: 2905197
  18. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study.
    J Comp Neurol. 1992 Sep 15;323(3):387-410 PMID: 1281170
  19. Muscle atonia is triggered by cholinergic stimulation of the basal forebrain: implication for the pathophysiology of canine narcolepsy.
    J Neurosci. 1995 Jul;15(7 Pt 1):4806-14 PMID: 7623112
  20. Microinjection of neostigmine into the pontine reticular formation of cats enhances desynchronized sleep signs.
    J Pharmacol Exp Ther. 1984 Oct;231(1):173-80 PMID: 6491973
  21. Pedunculopontine stimulation alters respiration and increases ACh release in the pontine reticular formation.
    Am J Physiol. 1993 Mar;264(3 Pt 2):R544-54 PMID: 8457006
  22. Inhalational anesthetics do not alter nitric oxide synthase activity.
    J Pharmacol Exp Ther. 1995 May;273(2):599-604 PMID: 7538577
  23. Roles of endogenous nitric oxide in cerebellar cortical development in slice cultures.
    Neuroreport. 1994 Oct 27;5(16):2049-52 PMID: 7865742
  24. The quantitative contribution of nitric oxide and sensory nerves to bradykinin-induced inflammation in rat skin microvasculature.
    Brain Res. 1992 Aug 28;589(1):102-8 PMID: 1384924
  25. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7797-801 PMID: 1715581
  26. Pressor effects of L and D enantiomers of NG-nitro-arginine in conscious rats are antagonized by L- but not D-arginine.
    Eur J Pharmacol. 1991 Jul 23;200(1):77-81 PMID: 1769375
  27. The role of endothelium and nitric oxide in rat pial arteriolar dilatory responses to CO2 in vivo.
    J Cereb Blood Flow Metab. 1994 Nov;14(6):944-51 PMID: 7929657
  28. NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation.
    Neurosci Lett. 1983 Dec 23;43(1):31-6 PMID: 6366624
  29. Dissociated states of wakefulness and sleep.
    Neurology. 1992 Jul;42(7 Suppl 6):44-51; discussion 52 PMID: 1630638
  30. Firing of 'possibly' cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness.
    Brain Res. 1992 Jan 13;569(2):210-20 PMID: 1540827
  31. Inhibitory action of muscarinic agonists on neurons in the rat laterodorsal tegmental nucleus in vitro.
    J Neurophysiol. 1993 Nov;70(5):2128-35 PMID: 8294974
  32. Nitric oxide modulates the release of acetylcholine in the ventral striatum of the freely moving rat.
    Naunyn Schmiedebergs Arch Pharmacol. 1995 Jul;352(1):67-73 PMID: 7477427
  33. Microdialysis of cat pons reveals enhanced acetylcholine release during state-dependent respiratory depression.
    Am J Physiol. 1991 Sep;261(3 Pt 2):R766-70 PMID: 1887963
  34. Facilitation of N-methyl-D-aspartate-evoked acetylcholine release by hydroxyl radical scavengers.
    Neuroreport. 1995 Oct 23;6(15):2033-6 PMID: 8580434
  35. Pertussis toxin-sensitive G proteins mediate carbachol-induced REM sleep and respiratory depression.
    Am J Physiol. 1995 Aug;269(2 Pt 2):R308-17 PMID: 7653652
  36. Effects of NG-substituted analogues of L-arginine on NANC relaxation of the rat anococcygeus and bovine retractor penis muscles and the bovine penile artery.
    Br J Pharmacol. 1991 Sep;104(1):53-8 PMID: 1786518
  37. State-dependent hypotonia in posterior cricoarytenoid muscles of the larynx caused by cholinoceptive reticular mechanisms.
    FASEB J. 1989 Mar;3(5):1625-31 PMID: 2920876
  38. The carbachol-induced enhancement of desynchronized sleep signs is dose dependent and antagonized by centrally administered atropine.
    Neuropsychopharmacology. 1989 Mar;2(1):67-79 PMID: 2572234
  39. Evidence that nitric oxide is involved in the control of electrocortical arousal.
    Ann N Y Acad Sci. 1994 Nov 17;738:191-200 PMID: 7832428
  40. In vitro and ex vivo inhibitory effects of L- and D-enantiomers of NG-nitro-arginine on endothelium-dependent relaxation of rat aorta.
    J Pharmacol Exp Ther. 1993 Apr;265(1):112-9 PMID: 8473999
  41. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems.
    J Neurosci. 1990 Aug;10(8):2541-59 PMID: 2388079
  42. Cholinoceptive pontine reticular mechanisms cause state-dependent respiratory changes in the cat.
    Neurosci Lett. 1989 Jul 31;102(2-3):211-6 PMID: 2812500
  43. Cholinergic neurons from the dorsolateral pons project to the medial pons: a WGA-HRP and choline acetyltransferase immunohistochemical study.
    Neurosci Lett. 1988 Dec 19;95(1-3):19-23 PMID: 2465510
  44. Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro.
    Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):743-7 PMID: 1731349
  45. Inhibition of nitric oxide synthesis suppresses sleep in rabbits.
    Am J Physiol. 1994 Jan;266(1 Pt 2):R151-7 PMID: 8304536
  46. Nitric oxide signaling in the central nervous system.
    Annu Rev Physiol. 1995;57:683-706 PMID: 7539993
  47. Nitric oxide participates in the cerebrovasodilation elicited from cerebellar fastigial nucleus.
    Am J Physiol. 1992 Nov;263(5 Pt 2):R1156-61 PMID: 1443234
  48. Halothane decreases pontine acetylcholine release and increases EEG spindles.
    Neuroreport. 1994 Jan 31;5(5):577-80 PMID: 8025247
  49. Inhibition of nitric oxide synthesis inhibits rat sleep.
    Brain Res. 1994 Nov 21;664(1-2):189-96 PMID: 7534601
  50. Pontine regulation of REM sleep components in cats: integrity of the pedunculopontine tegmentum (PPT) is important for phasic events but unnecessary for atonia during REM sleep.
    Brain Res. 1992 Jan 31;571(1):50-63 PMID: 1611494
  51. Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat.
    Arch Ital Biol. 1989 Jun;127(3):133-64 PMID: 2774793
  52. Nitric oxide synthase inhibition decreases pontine acetylcholine release.
    Neuroreport. 1995 Jul 31;6(11):1525-9 PMID: 7579140
  53. Nitric oxide synthases: properties and catalytic mechanism.
    Annu Rev Physiol. 1995;57:707-36 PMID: 7539994
  54. Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat.
    Brain Res. 1988 Jun 7;451(1-2):397-402 PMID: 3251602
  55. Effects of targeted neuronal nitric oxide synthase gene disruption and nitroG-L-arginine methylester on the threshold for isoflurane anesthesia.
    Anesthesiology. 1995 Jul;83(1):101-8 PMID: 7541615
  56. Inhibition of nitric oxide synthesis impairs rapid tolerance to ethanol.
    Brain Res Bull. 1993;32(1):43-7 PMID: 8319102
  57. Simultaneous pontine and basal forebrain microinjections of carbachol suppress REM sleep.
    J Neurosci. 1993 Jan;13(1):229-42 PMID: 8423470
  58. A cholinoceptive desynchronized sleep induction zone in the anterodorsal pontine tegmentum: spontaneous and drug-induced neuronal activity.
    Neuroscience. 1990;39(2):295-304 PMID: 2087261
  59. Selective anesthetic inhibition of brain nitric oxide synthase.
    Anesthesiology. 1994 Nov;81(5):1264-9 PMID: 7526751
  60. Does halothane interfere with the release, action, or stability of endothelium-derived relaxing factor/nitric oxide?
    Anesthesiology. 1994 Feb;80(2):417-26 PMID: 8311324
  61. Localization of muscarinic receptor subtypes in brain stem areas regulating sleep.
    Neuroreport. 1994 Aug 15;5(13):1631-4 PMID: 7819535
  62. State-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis.
    J Neurosci. 1994 Sep;14(9):5236-42 PMID: 8083733
  63. Cholinergic mechanisms in canine narcolepsy--II. Acetylcholine release in the pontine reticular formation is enhanced during cataplexy.
    Neuroscience. 1994 Apr;59(3):523-30 PMID: 8008206
  64. Noradrenaline hyperpolarizes identified rat mesopontine cholinergic neurons in vitro.
    J Neurosci. 1993 Sep;13(9):3878-83 PMID: 8103553
  65. Nitric oxide (NO) is an endogenous anticonvulsant but not a mediator of the increase in cerebral blood flow accompanying bicuculline-induced seizures in rats.
    Brain Res. 1994 Sep 26;658(1-2):192-8 PMID: 7530579
  66. Microdialysis of the pontine reticular formation reveals inhibition of acetylcholine release by morphine.
    Anesthesiology. 1993 Nov;79(5):1003-12 PMID: 8238979
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-01-15
Pages
774-85
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6573244
Subset
IM
Grants
NHLBI NIH HHS · HL-4088 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com