Endogenous GABA levels in the pontine reticular formation are greater during wakefulness than during rapid eye movement sleep

Journal of Neuroscience

Volumn 31, Issue 7, 2011, Pages 2649-2656

  Vanini, Giancarlo ^a   Wathen, Bradley L ^a   Lydic, Ralph ^a   Baghdoyan, Helen A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; NEOSTIGMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTROENCEPHALOGRAM; EXPERIMENTAL CAT; GABAERGIC TRANSMISSION; HISTOLOGY; MALE; MICRODIALYSIS; MICROINJECTION; NONHUMAN; NONREM SLEEP; PONS RETICULAR FORMATION; PRIORITY JOURNAL; REM SLEEP; WAKEFULNESS;

ACETYLCHOLINE; ANIMALS; CATS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROENCEPHALOGRAPHY; GAMMA-AMINOBUTYRIC ACID; MALE; MICRODIALYSIS; RETICULAR FORMATION; SLEEP, REM; TIME FACTORS; WAKEFULNESS;

EID: 79951848552     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5674-10.2011     Document Type: Article

References (60)

1. Baghdoyan HA, Lydic R (1999) M2 muscarinic receptor subtype in the feline medial pontine reticular formation modulates the amount of rapid eye movement sleep. Sleep 22:835-847. (Pubitemid 29526504)
2. Baghdoyan HA, Monaco AP, Rodrigo-Angulo ML, Assens F, McCarley RW, Hobson JA (1984) Microinjection of neostigmine into the pontine reticular formation of cats enhances desynchronized sleep signs. J Pharmacol Exp Ther 231:173-180. (Pubitemid 14023131)
3. Belelli D, Peden DR, Rosahl TW, Wafford KA, Lambert JJ (2005) Extrasynaptic GABAA receptors of thalamocortical neurons: a molecular target for hypnotics. J Neurosci 25:11513-11520. (Pubitemid 43098444)
4. Berman AL (1968) The brain stem of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. Madison, WI: University of Wisconsin.
5. Bourgin P, Escourrou P, Gaultier C, Adrien J (1995) Induction of rapid eye movement sleep by carbachol infusion into the pontine reticular formation. Neuroreport 6:532-536.
6. Brevig HN, Watson CJ, Lydic R, Baghdoyan HA (2010) Hypocretin and GABA interact in the pontine reticular formation to increase wakefulness. Sleep 33:1285-1293.
7. Brischoux F, Mainville L, Jones BE (2008) Muscarinic-2 and orexin-2 receptors on GABAergic and other neurons in the rat mesopontine regmentum and their potential role in sleep-wake control. J Comp Neurol 510:607-630.
8. Brown RE, McKenna JT, Winston S, Basheer R, Yanagawa Y, Thakkar MM, McCarley RW (2008) Characterization of GABAergic neurons in rapid-eye-movement sleep controlling regions of the brainstem reticular formation in GAD67-green fluorescent protein knock-in mice. Eur J Neurosci 27:352-363.
9. Camacho-Arroyo I, Alvarado R, Manjarrez J, Tapia R (1991) Microinjections of muscimol and bicuculline into the pontine reticular formation modify the sleep-waking cycle in the rat. Neurosci Lett 129:95-97.
10. B receptor activation-mediated rapid eye movement sleep suppression in the freely moving rat. J Neurophysiol 97:3841-3850.
11. Datta S (2010) Cellular and chemical neuroscience of mammalian sleep. Sleep Med 11:431-440.
12. Datta S, Quattrochi JJ, Hobson JA (1993) Effect of specific muscarinic M2 receptor antagonist on carbachol induced long-term REM sleep. Sleep 16:8-14. (Pubitemid 23024690)
13. Datta S, Siwek DF, Stack EC (2009) Identification of cholinergic and noncholinergic neurons in the pons expressing phosphorylated cyclic adenosine monophosphate response element-binding protein as a function of rapid eye movement sleep. Neuroscience 163:397-414.
14. de la Roza C, Reinoso-Suárez F (2006) GABAergic structures in the ventral part of the oral pontine reticular nucleus: an ultrastructural immunogold analysis. Neuroscience 142:1183-1193. (Pubitemid 44636049)
15. A receptors in the pontine reticular formation of C57BL/6J mouse modulate neurochemical, electrographic, and behavioral phenotypes of wakefulness. J Neurosci 30:12301-12309.
16. Garzón M, de Andrés I, Reinoso-Suárez F (1997) Neocortical and hippocampal electrical activities are similar in spontaneous and cholinergicinduced REM sleep. Brain Res 766:266-270.
17. Hambrecht-Wiedbusch VS, Gauthier EA, Baghdoyan HA, Lydic R (2010) Benzodiazepine receptor agonists cause drug-specific and state-specific alterations in EEG power and acetylcholine release in rat pontine reticular formation. Sleep 33:909-918.
18. A receptor agonists. J Clin Psychiatry 68 [Suppl 5]:6-12.
19. A receptor subunits in the adult C57 mouse as assessed with in situ hybridization. Neuroscience 150:370-385.
20. Heister DS, Hayar A, Garcia-Rill E (2009) Cholinergic modulation of GABAergic and glutamatergic transmission in the dorsal subcoeruleus: mechanisms for REM sleep control. Sleep 32:1135-1147.
21. Keifer JC, Baghdoyan HA, Lydic R (1996) Pontine cholinergic mechanisms modulate the cortical electroencephalographic spindles of halothane anesthesia. Anesthesiology 84:945-954. (Pubitemid 26105256)
22. Kohlmeier KA, Kristiansen U (2010) GABAergic actions on cholinergic and laterodorsal tegmental neurons: implications for control of behavioral state. Neuroscience 171:812-829.
23. Kubin L (2001) Carbachol models of REM sleep: recent developments and new directions. Arch Ital Biol 139:147-168.
24. Leonard TO, Lydic R (1997) Pontine nitric oxide modulates acetylcholine release, rapid eye movement sleep generation, and respiratory rate. J Neurosci 17:774-785. (Pubitemid 27024589)
25. Liang CL, Marks GA (2009) A novel GABAergic afferent input to the pontine reticular formation: the mesopontine GABAergic column. Brain Res 1297:32-40.
26. Lydic R, Baghdoyan HA (1993) Pedunculopontine stimulation alters respiration and increases ACh release in the pontine reticular formation. Am J Physiol 264:544-554.
27. Lydic R, Baghdoyan HA (2005) Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103:1268-1295. (Pubitemid 41692513)
28. Lydic R, Baghdoyan HA (2008) Acetylcholine modulates sleep and wakefulness: a synaptic perspective. In: Sleep and wakefulness (Monti JM, Pandi-Perumal SR, Sinton CM, eds), pp 109-143. Cambridge, UK: Cambridge UP.
29. Lydic R, Douglas CL, Baghdoyan HA (2002) Microinjection of neostigmine into the pontine reticular formation of C57BL/6J mouse enhances rapid eye movement sleep and depresses breathing. Sleep 25:835-841. (Pubitemid 35424525)
30. Lydic R, Garza-Grande R, Struthers R, Baghdoyan HA (2006) Nitric oxide in B6 mouse and nitric oxide-sensitive soluble guanylate cyclase in cat modulate acetylcholine release in pontine reticular formation. J Appl Physiol 100:1666-1673.
31. Marks GA, Sachs OW, Birabil CG (2008) Blockade of GABA, type A, receptors in the rat pontine reticular formation induces rapid eye movement sleep that is dependent upon the cholinergic system. Neuroscience 156:1-10.
32. Márquez-Ruiz J, Escudero M (2009) Eye movements and abducens motoneuron behavior during cholinergically induced REM sleep. Sleep 32:471-481.
33. Mitani A, Ito K, Hallanger AE, Wainer BH, Kataoka K, McCarley RW (1988) Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res 451:397-402.
34. A receptors responsible for tonic and phasic conductances. Neurochem Res 26:907-913.
35. Morales FR, Engelhardt JK, Soja PJ, Pereda AE, Chase MH (1987) Motoneuron properties during motor inhibition produced by microinjection of carbachol into the pontine reticular formation of the decerebrate cat. J Neurophysiol 57:1118-1129. (Pubitemid 17059750)
36. Nitz D, Siegel JM (1997a) GABA release in the locus coeruleus as a function of sleep/wake state. Neuroscience 78:795-801. (Pubitemid 27179659)
37. Nitz D, Siegel J (1997b) GABA release in the dorsal raphe nucleus: role in the control of REM sleep. Am J Physiol 273:R451-R455.
38. A receptors in freely moving rats. Neurosci Lett 365:200-204.
39. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32:421-431.
40. A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
41. Rodrigo-Angulo ML, Heredero S, Rodríguez-Veiga E, Reinoso-Suárez F (2008) GABAergic and non-GABAergic thalamic, hypothalamic and basal forebrain projections to the ventral oral pontine reticular nucleus: Their implication in REM sleep modulation. Brain Res 1210:116-125.
42. Sanford LD, Tang X, Xiao J, Ross RJ, Morrison AR (2003) GABAergic regulation of REM sleep in reticularis pontis oralis and caudalis in rats. J Neurophysiol 90:938-945. (Pubitemid 37092579)
43. Sitaram N, Wyatt RJ, Dawson S, Gillin JC (1976) REM sleep induction by physostigmine infusion during sleep. Science 191:1281-1283.
44. Sitaram N, Moore AM, Gillin JC (1978) Induction and resetting of REM sleep rhythm in normal man by arecoline: blockade by scopolamine. Sleep 1:83-90. (Pubitemid 9167400)
45. Steriade M, McCarley RW (2005) Brain Control of Wakefulness and Sleep. New York: Kluwer Academic/Plenum.
46. Steriade M, Datta S, Paré D, Oakson G, Curró Dossi RC (1990) Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10:2541-2559.
47. Thakkar M, Portas C, McCarley RW (1996) Chronic low-amplitude electrical stimulation of the laterodorsal tegmental nucleus of freely moving cats increases REM sleep. Brain Res 723:223-227. (Pubitemid 26197820)
48. Torterolo P, Yamuy J, Sampogna S, Morales FR, Chase MH (2001) GABAergic neurons of the laterodorsal and pedunculopontine tegmental nuclei of the cat express c-fos during carbachol-induced active sleep. Brain Res 892:309-319. (Pubitemid 32141217)
49. Torterolo P, Morales FR, Chase MH (2002) GABAergic mechanisms in the pedunculopontine tegmental nucleus of the cat promote active (REM) sleep. Brain Res 944:1-9. (Pubitemid 34775003)
50. B receptors in the freely moving rat. J Neurophysiol 91:1822-1831.
51. Ursin R, Sterman M (1981) Manual for Standardized Scoring of Sleep and Waking States in Adult Cats. Los Angeles: BIS/BRI, University of California.
52. Vanini G, Watson CJ, Lydic R, Baghdoyan HA (2008) Gamma-aminobutyric acid-mediated neurotransmission in the pontine reticular formation modulates hypnosis, immobility, and breathing during isoflurane anesthesia. Anesthesiology 109:978-988.
53. A receptors modulate acetylcholine release in feline basal forebrain. Eur J Neurosci 17:249-259.
54. A receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation. J Neurophysiol 92:2198-2206.
55. Watson CJ, Venton BJ, Kennedy RT (2006) In vivo measurements of neurotransmitters using microdialysis sampling. Anal Chem 78:1391-1399.
56. Watson CJ, Lydic R, Baghdoyan HA (2007) Sleep and GABA levels in the oral part of rat pontine reticular formation are decreased by local and systemic administration of morphine. Neuroscience 144:375-386. (Pubitemid 44841996)
57. Watson CJ, Soto-Calderon H, Lydic R, Baghdoyan HA (2008) Pontine reticular formation (PnO) administration of hypocretin-1 increases PnO GABA levels and wakefulness. Sleep 31:453-464. (Pubitemid 351694267)
58. Westerink BHC, Rea K, Oldenziel WH, Cremers TIFH (2007) Microdialysis of glutamate and GABA in the brain: analysis and interpretation. In: Handbook of Microdialysis (Westerink BHC, Cremers TIFH, eds), pp 17-31. The Netherlands: Elsevier.
59. Xi MC, Morales FR, Chase MH (1999) Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J Neurophysiol 82:2015-2019. (Pubitemid 29471292)
60. Xi MC, Morales FR, Chase MH (2001) Induction of wakefulness and inhibition of active (REM) sleep by GABAergic processes in the nucleus pontis oralis. Arch Ital Biol 139:125-145. (Pubitemid 32158406)