The nitric oxide synthase inhibitor NG-nitro-L-arginine increases basal forebrain acetylcholine release during sleep and wakefulness

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5597-5605

  Vazquez, Jacqueline ^a,b   Lydic, Ralph ^a   Baghdoyan, Helen A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Basal forebrain; In vivo microdialysis; NG nitro L arginine; Nitric oxide; Sleep; Substantia innominata

Indexed keywords

ACETYLCHOLINE; N(G) NITROARGININE; NITRIC OXIDE SYNTHASE INHIBITOR;

ACETYLCHOLINE RELEASE; ANIMAL MODEL; ARTICLE; BRAIN NERVE CELL; BREATHING RATE; CAT; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FOREBRAIN; MALE; MICRODIALYSIS; MICROINJECTION; NEUROTRANSMISSION; NONHUMAN; NONREM SLEEP; PONS; PRIORITY JOURNAL; REM SLEEP; SLEEP; WAKEFULNESS;

EID: 0036662885     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05597.2002     Document Type: Article

References (61)

1. Baghdoyan HA, Lydic R (2002) Neurotransmitters and neuromodulators regulating sleep. In: Sleep and Epilepsy: The Clinical Spectrum (Bazil C, Malow B, Sammaritano M, eds), pp 17-44. New York: Elsevier Science.
2. Baghdoyan HA, Spotts JL, Snyder SG (1993) Simultaneous pontine and basal forebrain microinjections of carbachol suppress REM sleep. J Neurosci 13:229-242.
3. Baghdoyan HA, Lydic R, Fleegal MA (1998) M2 muscarinic autoreceptors modulate acetylcholine release in the medial pontine reticular formation. J Pharmacol Exp Ther 286:1446-1452.
4. Benevento LA, McCleary LB (1992) An immunocytochemical method for marking microelectrode tracks following single-unit recordings in long surviving, awake monkeys. J Neurosci Methods 41:199-204.
5. Berman AL, Jones EG (1982) The Thalamus and Basal Telencephalon of the Cat. Madison: University of Wisconsin.
6. Bickford ME, Günlük AE, Van Horn SC, Sherman SM (1994) GABAergic projection from the basal forebrain to the visual sector of the thalamic reticular nucleus in the cat. J Comp Neurol 348:481-510.
7. Bringmann A, Klingberg F (1989) Electrical stimulations of the basal forebrain and the nucleus cuneiformis differently modulate behavioural activation of freely moving rat. Biomed Biochim Acta 48:781-791.
8. Buccafusco JJ, Terry AV (2000) Multiple central nervous system targets for eliciting beneficial effects on memory and cognition. J Pharmacol Exp Ther 295:438-446.
9. Burlet S, Leger L, Cespuglio R (1999) Nitric oxide and sleep in the rat: A puzzling relationship. Neuroscience 92:627-639.
10. de la Torre JC, Stefano GB (2000) Evidence that Alzheimer's disease is a microvascular disorder: The role of constitutive nitric oxide. Brain Res Brain Res Rev 34:119-136.
11. Dzoljic MR, de Vries R (1994) Nitric oxide synthase inhibition reduces wakefulness. Neuropharmacology 33:1505-1509.
12. Dzoljic MR, de Vries R, van Leeuwen R (1996) Sleep and nitric oxide: Effects of 7-nitro indazole, inhibitor of brain nitric oxide synthase. Brain Res 718:145-150.
13. Felder CC, Bymaster FP, Ward J, DeLapp N (2000) Therapeutic opportunities for muscarinic receptors in the central nervous system. J Med Chem 43:4333-4353.
14. Fukuto JM, Chaudhuri G (1995) Inhibition of constitutive and inducible nitric oxide synthase: Potential selective inhibition. Annu Rev Pharmacol Toxicol 35:165-194.
15. Garthwaite J, Boulton CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706.
16. Gilbert KA, Lydic R (1994) Pontine cholinergic reticular mechanisms cause state-dependent changes in the discharge of parabrachial neurons. Am J Physiol 266:R136-R150.
17. Gritti I, Mainville L, Jones BE (1993) Codistribution of GABA- with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J Comp Neurol 329:438-457.
18. Gritti I, Mariotti M, Mancia M (1998) GABAergic and cholinergic basal forebrain and preoptic-anterior hypothalamic projections to the mediodorsal nucleus of the thalamus in the cat. Neuroscience 85:149-178.
19. Guide for the Care and Use of Laboratory Animals (1996) Washington, DC: National Academy of Sciences.
20. Harper RM, Rector D, Poe G, Frysinger RC, Kristensen M, Gozal D (1996) Rostral brain regions contributing to respiratory control. Prog Brain Res 107:145-156.
21. Ikarashi Y, Takahashi A, Ishimaru H, Shiobara T, Maruyama Y (1998) The role of nitric oxide in striatal acetylcholine release induced by N-methyl-D-aspartate. Neurochem Int 33:255-261.
22. Kapas L, Fang J, Krueger JM (1994a) Inhibition of nitric oxide synthesis inhibits rat sleep. Brain Res 664:189-196.
23. Kapas L, Shibata M, Kimura M, Krueger JM (1994b) Inhibition of nitric oxide synthesis suppresses sleep in rabbits. Am J Physiol 266:R151-R157.
24. Khateb A, Fort P, Williams S, Serafin M, Jones BE, Mühlethaler M (1997) Modulation of cholinergic nucleus basalis neurons by acetylcholine and N-methyl-D-aspartate. Neuroscience 81:47-55.
25. Khateb A, Fort P, Williams S, Serafin M, Muhlethaler M, Jones BE (1998) GABAergic input to cholinergic nucleus basalis neurons. Neuroscience 86:937-947.
26. Kimura H, McGeer PL, Peng JH, McGeer EG (1981) The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 200:151-201.
27. King AB, Menon RS, Hachinski V, Cechetto DF (1999) Human forebrain activation by visceral stimuli. J Comp Neurol 413:527-582.
28. Kitchener PD, Diamond J (1993) Distribution and colocalization of choline acetyltransferase immunoreactivity and NADPH diaphorase reactivity in neurons within the medial septum and diagonal band of Broca in the rat basal forebrain. J Comp Neurol 335:1-15.
29. Law A, Gauthier S, Quirion R (2001) Say NO to Alzheimer's disease: The putative links between nitric oxide and dementia of the Alzheimer's type. Brain Res Brain Res Rev 35:73-96.
30. Leonard TO, Lydic R (1995) Nitric oxide synthase inhibition decreases pontine acetylcholine release. NeuroReport 6:1525-1529.
31. Leonard TO, Lydic R (1997) Pontine nitric oxide modulates acetylcholine release, rapid eye movement sleep generation, and respiratory rate. J Neurosci 17:774-785.
32. Leonard TO, Lydic R (1999) Nitric oxide: A diffusible modulator of physiological traits and behavioral states. In: Rapid Eye Movement Sleep (Mallick BN, Inoue S, eds), pp 167-193. New Delhi: Narosa.
33. Leonard CS, Michaelis EK, Mitchell KM (2001) Activity-dependent nitric oxide concentration dynamics in the laterodorsal tegmental nucleus in vitro. J Neurophysiol 86:2159-2172.
34. Lydic R, Baghdoyan HA (1993) Pedunculopontine stimulation alters respiration and increases ACh release in the pontine reticular formation. Am J Physiol 264:R544-R554.
35. Manning HL, Schwartzstein RM (1995) Pathophysiology of dyspnea. N Engl J Med 333:1547-1553.
36. Manns ID, Alonso A, Jones BE (2000) Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J Neurosci 20:1505-1518.
37. Meng X-W, Ohara PT, Ralston III HJ (1996) Nitric oxide synthase immunoreactivity distinguishes a sub-population of GABA-immunoreactive neurons in the ventrobasal complex of the cat. Brain Res 728:111-115.
38. Mesulam M-M (1996) The systems-level organization of cholinergic innervation in the human cerebral cortex and its alterations in Alzheimer's disease. Prog Brain Res 109:285-297.
39. Miasnikov AA, Webster HH, Dykes RW (1999) Temporally structured impulse activity in spontaneously discharging somatosensory cortical neurons in the awake cat: Recognition and quantitative description of four different patterns of bursts, post-recording GFAP immunohistology and computer reconstruction of the studied cortical surface. Brain Res Brain Res Protoc 4:49-68.
40. Mizukawa K, Vincent SR, McGeer PL, McGeer EG (1989) Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J Comp Neurol 279:281-311.
41. Moore H, Stuckman S, Sarter M, Bruno JP (1995) Stimulation of cortical acetylcholine efflux by FG 7142 measured with repeated microdialysis sampling. Synapse 21:324-331.
42. Nishino S, Tafti M, Reid MS, Shelton J, Siegel JM, Dement WC, Mignot E (1995) Muscle atonia is triggered by cholinergic stimulation of the basal forebrain: Implication for the pathophysiology of canine narcolepsy. J Neurosci 15:4806-4814.
43. Parent A, Pare D, Smith Y, Steriade M (1988) Basal forebrain cholinergic and noncholinergic projections to the thalamus and brainstem in cats and monkeys. J Comp Neurol 277:281-301.
44. Pasqualotto BA, Vincent SR (1991) Galanin and NADPH-diaphorase coexistence in cholinergic neurons of the rat basal forebrain. Brain Res 551:78-86.
45. Pose I, Sampogna S, Chase MH, Morales FR (2000) Cuneiform neurons activated during cholinergically induced active sleep in the cat. J Neurosci 20:3319-3327.
46. Prast H, Philippu A (1992) Nitric oxide releases acetylcholine in the basal forebrain. Eur J Pharmacol 216:139-140.
47. Prast H, Philippu A (2001) Nitric oxide as a modulator of neuronal function. Prog Neurobiol 64:51-68.
48. Sarter M, Bruno JP (2000) Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: Differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents. Neuroscience 95:933-952.
49. Semba K (2000) Multiple output pathways of the basal forebrain: Organization, chemical heterogeneity, and roles in vigilance. Behav Brain Res 115:117-141.
50. Spengler CM, Banzett RB, Systrom DM, Shannon DC, Shea SA (1998) Respiratory sensations during heavy exercise in subjects without respiratory chemosensitivity. Respir Physiol 114:65-74.
51. Steriade M, Parent A, Pare D, Smith Y (1987) Cholinergic and noncholinergic neurons of cat basal forebrain project to reticular and mediodorsal thalamic nuclei. Brain Res 408:372-376.
52. Sugaya K, McKinney M (1994) Nitric oxide synthase gene expression in cholinergic neurons in the rat brain examined by combined immunocytochemistry and in situ hybridization histochemistry. Mol Brain Res 23:111-125.
53. Szymusiak R, Alam N, McGinty D (2000) Discharge patterns of neurons in cholinergic regions of the basal forebrain during waking and sleep. Behav Brain Res 115:171-182.
54. Ursin R, Sterman M (1981) A Manual for Standardized Scoring of Sleep and Waking States in the Adult Cat. Los Angeles: Brain Information Services/Brain Research Institute, University of California.
55. Valtschanoff JG, Weinberg RJ, Kharazia VN, Nakane M, Schmidt HHHW (1993) Neurons in rat hippocampus that synthesize nitric oxide. J Comp Neurol 331:111-121.
56. Vazquez J, Baghdoyan HA (2001) Basal forebrain acetylcholine release during REM sleep is significantly greater than during waking. Am J Physiol 280:R598-R601.
57. Vazquez J, Wilcox M, Lydic R, Baghdoyan HA (2001) A nitric oxide synthase (NOS) inhibitor increases acetylcholine (ACh) release in feline basal forebrain (BF). Soc Neurosci Abstr 27:522.3.
58. Vincent SR, Reiner PB (1987) The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371-415.
59. G-nitro-arginine on endothelium-dependent relaxation of rat aorta. J Pharmacol Exp Ther 265:112-119.
60. Wild JM, Arends JJ, Zeigler HP (1990) Projections of the parabrachial nucleus in the pigeon. J Comp Neurol 293:499-523.
61. Zhang J, Snyder SH (1995) Nitric oxide in the nervous system. Annu Rev Pharmacol Toxicol 35:213-233.