Extrasynaptic GABAA receptors in rat pontine reticular formation increase wakefulness

Sleep

Volumn 36, Issue 3, 2013, Pages 337-343

  Vanini, Giancarlo ^a   Baghdoyan, Helen A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Anesthesia; Gaboxadol; Microinjection; Sedative hypnotics; THIP

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GABOXADOL; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; ISOXAZOLE DERIVATIVE; MUSCIMOL; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; MICROINJECTION; NONHUMAN; NONREM SLEEP; PONS RETICULAR FORMATION; PRIORITY JOURNAL; RAT; REM SLEEP; SLEEP; WAKEFULNESS; ANESTHESIA; ANIMAL; DRUG EFFECT; ELECTROENCEPHALOGRAPHY; MALE; METABOLISM; PHYSIOLOGY; PONS; RETICULAR FORMATION; SEDATIVE-HYPNOTICS; SPRAGUE DAWLEY RAT;

ANESTHESIA; GABOXADOL; MICROINJECTION; SEDATIVE-HYPNOTICS; THIP;

ANIMALS; ELECTROENCEPHALOGRAPHY; GABA AGONISTS; GABA-A RECEPTOR AGONISTS; ISOXAZOLES; MALE; MICROINJECTIONS; MUSCIMOL; PONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RETICULAR FORMATION; SLEEP; SODIUM CHLORIDE; WAKEFULNESS;

EID: 84874599321     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.2444     Document Type: Article

References (70)

1. Baghdoyan HA, Lydic R. The neurochemistry of sleep and wakefulness. In: Brady ST, Albers RW, Price DL, Siegel GJ, eds. Basic Neurochemistry. New York: Elsevier, 2012:982-99.
2. Datta S. Cellular and chemical neuroscience of mammalian sleep. Sleep Med 2010;11:431-40.
3. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiol Rev 2012;92:1087-187.
4. Richey SM, Krystal AD. Pharmacological advances in the treatment of insomnia. Curr Pharm Des 2011;17:1471-5.
5. Alkire MT, Hudetz AG, Tononi G. Consciousness and anesthesia. Science 2008;322:876-80.
6. Saari TI, Uusi-Oukari M, Ahonen J, Olkkola KT. Enhancement of GABAergic activity: neuropharmacological effects of benzodiazepines and therapeutic use in anesthesiology. Pharmacol Rev 2011;63:243-67.
7. Olsen RW, Sieghart W. International Union of Pharmacology. LXX. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol Rev 2008;60:243-60.
8. Harrison NL. Mechanisms of sleep induction by GABAA receptor agonists. J Clin Psychiatry 2007;68:6-12.
9. Brickley SG, Mody I. Extrasynaptic GABAA receptors: their function in the CNS and implications for disease. Neuron 2012;73:23-34.
10. Wafford KA, Ebert B. Gaboxadol - a new awakening in sleep. Curr Opin Pharmacol 2006;6:30-6.
11. Orser BA. Extrasynaptic GABAA receptors are critical targets for sedative-hypnotic drugs. J Clin Sleep Med 2006;2:S12-8.
12. Jia F, Yue M, Chandra D, Homanics GE, Goldstein PA, Harrison NL. Isoflurane is a potent modulator of extrasynaptic GABAA receptors in the thalamus. J Pharmacol Exp Ther 2008;324:1127-35.
13. Belelli D, Lambert JJ. Neurosteroids: endogenous regulators of the GABAA receptor. Nat Rev Neurosci 2005;6:565-75.
14. Houston CM, McGee TP, Mackenzie G, et al. Are extrasynaptic GABAA receptors important targets for sedative/hypnotic drugs? J Neurosci 2012;32:3887-97.
15. Zurek AA, Bridgwater EM, Orser BA. Inhibition of alpha5 gammaaminobutyric acid type A receptors restores recognition memory after general anesthesia. Anesth Analg 2012;114:845-55.
16. Krogsgaard-Larsen P, Frolund B, Liljefors T, Ebert B. GABAA agonists and partial agonists: THIP (Gaboxadol) as a non-opioid analgesic and a novel type of hypnotic. Biochem Pharmacol 2004;68:1573-80.
17. Camacho-Arroyo I, Alvarado R, Manjarrez J, Tapia R. Microinjections of muscimol and bicuculline into the pontine reticular formation modify the sleep-waking cycle in the rat. Neurosci Lett 1991;129:95-7.
18. Marks GA, Sachs OW, Birabil CG. 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 2008;156:1-10.
19. Sanford LD, Tang X, Xiao J, Ross RJ, Morrison AR. GABAergic regulation of REM sleep in reticularis pontis oralis and caudalis in rats. J Neurophysiol 2003;90:938-45.
20. Xi MC, Morales FR, Chase MH. Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J Neurophysiol 1999;82:2015-9.
21. Watson CJ, Lydic R, Baghdoyan HA. Sleep duration varies as a function of glutamate and GABA in rat pontine reticular formation. J Neurochem 2011;118:571-80.
22. Vanini G, Wathen BL, Lydic R, Baghdoyan HA. Endogenous GABA levels in the pontine reticular formation are greater during wakefulness than during rapid eye movement sleep. J Neurosci 2011;31:2649-56.
23. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates 6th ed. Burlington, MA: Academic Press, 2007.
24. Berman AL. The Brain Stem of the Cat. A Cytoarchitectonic Atlas with Stereotaxic Coordinates. Madison, WI: University of Wisconsin, 1968.
25. Moruzzi G, Magoun HW. Brain stem reticular formation and activation of the EEG. Electroencephalog Clin Neurophysiol 1949;1:455-73.
26. Steriade M, McCarley RW. Brain Control of Wakefulness and Sleep. 2nd ed. New York: Kluwer Academic/Plenum Press, 2005.
27. Lydic R. Reticular modulation of breathing during sleep and anesthesia. Curr Opin Pulm Med 1996;2:474-81.
28. Lydic R, Baghdoyan HA. Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 2005;103:1268-95.
29. Vanini G, Watson CJ, Lydic R, Baghdoyan HA. Gamma-aminobutyric acid-mediated neurotransmission in the pontine reticular formation modulates hypnosis, immobility, and breathing during isoflurane anesthesia. Anesthesiology 2008;109:978-88.
30. Brevig HN, Watson CJ, Lydic R, Baghdoyan HA. Hypocretin and GABA interact in the pontine reticular formation to increase wakefulness. Sleep 2010;33:1285-93.
31. Watson CJ, Soto-Calderon H, Lydic R, Baghdoyan HA. Pontine reticular formation (PnO) administration of hypocretin-1 increases PnO GABA levels and wakefulness. Sleep 2008;31:453-64.
32. Flint RR, Chang T, Lydic R, Baghdoyan HA. GABAA receptors in the pontine reticular formation of C57BL/6J mouse modulate neurochemical, electrographic, and behavioral phenotypes of wakefulness. J Neurosci 2010;30:12301-9.
33. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G. GABAA receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 2000;101:815-50.
34. Vanini G, Lydic R, Baghdoyan HA. GABAergic Modulation of REM Sleep. In: Mallick BN, Pandi-Perumal SR, McCarley RW, Morrison AR, eds. Rapid Eye Movement Sleep - Regulation and Function. Cambridge, UK: Cambridge University Press, 2011:206-13.
35. Vanini G, Lydic R, Baghdoyan HA. GABA-to-ACh ratio in basal forebrain and cerebral cortex varies significantly during sleep. Sleep 2012;35:1325-34.
36. Mortensen M, Ebert B, Wafford K, Smart TG. Distinct activities of GABA agonists at synaptic- and extrasynaptic-type GABAA receptors. J Physiol 2010;588:1251-68.
37. Lancel M, Faulhaber J. The GABAA agonist THIP (gaboxadol) increases non-REM sleep and enhances delta activity in the rat. Neuroreport 1996;7:2241-5.
38. Lancel M, Langebartels A. gamma-aminobutyric acidA (GABAA) agonist 4,5,6, 7-tetrahydroisoxazolo[4,5-c]pyridin-3-ol persistently increases sleep maintenance and intensity during chronic administration to rats. J Pharmacol Exp Ther 2000;293:1084-90.
39. Winsky-Sommerer R, Vyazovskiy VV, Homanics GE, Tobler I. The EEG effects of THIP (Gaboxadol) on sleep and waking are mediated by the GABAA delta-subunit-containing receptors. Eur J Neurosci 2007;25:1893-9.
40. Walsh JK, Snyder E, Hall J, et al. Slow wave sleep enhancement with gaboxadol reduces daytime sleepiness during sleep restriction. Sleep 2008;31:659-72.
41. Walsh JK, Deacon S, Dijk DJ, Lundahl J. The selective extrasynaptic GABAA agonist, gaboxadol, improves traditional hypnotic efficacy measures and enhances slow wave activity in a model of transient insomnia. Sleep 2007;30:593-602.
42. Deacon S, Staner L, Staner C, Legters A, Loft H, Lundahl J. Effect of short-term treatment with gaboxadol on sleep maintenance and initiation in patients with primary insomnia. Sleep 2007;30:281-7.
43. Lundahl J, Deacon S, Maurice D, Staner L. EEG spectral power density profiles during NREM sleep for gaboxadol and zolpidem in patients with primary insomnia. J Psychopharmacol 2012;26:1081-7.
44. Roth T, Lines C, Vandormael K, Ceesay P, Anderson D, Snavely D. Effect of gaboxadol on patient-reported measures of sleep and waking function in patients with Primary Insomnia: results from two randomized, controlled, 3-month studies. J Clin Sleep Med 2010;6:30-9.
45. Watson CJ, Lydic R, Baghdoyan HA. Sleep and GABA levels in the oral part of rat pontine reticular formation are decreased by local and systemic administration of morphine. Neuroscience 2007;144:375-86.
46. Opp MR. Rat strain differences suggest a role for corticotropin-releasing hormone in modulating sleep. Physiol Behav 1998;63:67-74.
47. Thakkar MM, Winston S, McCarley RW. Effect of microdialysis perfusion of 4,5,6,7-tetrahydroisoxazolo-[5,4-C]pyridine-3-ol in the perifornical hypothalamus on sleep-wakefulness: role of delta-subunit containing extrasynaptic GABAA receptors. Neuroscience 2008;153:551-5.
48. Lin JS, Sakai K, Vanni-Mercier G, Jouvet M. A critical role of the posterior hypothalamus in the mechanisms of wakefulness determined by microinjection of muscimol in freely moving cats. Brain Res 1989;479:225-40.
49. Manfridi A, Brambilla D, Mancia M. Sleep is differently modulated by basal forebrain GABAA and GABAB receptors. Am J Physiol Regul Integr Comp Physiol 2001;281:R170-5.
50. Vanini G, Torterolo P, McGregor R, Chase MH, Morales FR. GABAergic processes in the mesencephalic tegmentum modulate the occurrence of active (rapid eye movement) sleep in guinea pigs. Neuroscience 2007;145:1157-67.
51. Xi MC, Morales FR, Chase MH. Induction of wakefulness and inhibition of active (REM) sleep by GABAergic processes in the nucleus pontis oralis. Arch Ital Biol 2001;139:125-45.
52. Vazquez J, Baghdoyan HA. GABAA receptors inhibit acetylcholine release in cat pontine reticular formation: implications for REM sleep regulation. J Neurophysiol 2004;92:2198-206.
53. Brischoux F, Mainville L, Jones BE. Muscarinic-2 and orexin-2 receptors on GABAergic and other neurons in the rat mesopontine tegmentum and their potential role in sleep-wake state control. J Comp Neurol 2008;510:607-30.
54. Brown RE, McKenna JT, Winston S, et al. 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 2008;27:352-63.
55. Rodrigo-Angulo ML, Heredero S, Rodriguez-Veiga E, Reinoso-Suarez F. 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 2008;1210:116-25.
56. Boissard R, Fort P, Gervasoni D, Barbagli B, Luppi PH. Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur J Neurosci 2003;18:1627-39.
57. Sapin E, Lapray D, Berod A, et al. Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS One 2009;4:e4272.
58. Liang CL, Marks GA. A novel GABAergic afferent input to the pontine reticular formation: the mesopontine GABAergic column. Brain Res 2009;1297:32-40.
59. Del Arco A, Segovia G, Fuxe K, Mora F. Changes in dialysate concentrations of glutamate and GABA in the brain: an index of volume transmission mediated actions? J Neurochem 2003;85:23-33.
60. Watson CJ, Venton BJ, Kennedy RT. In vivo measurements of neurotransmitters by microdialysis sampling. Anal Chem 2006;78:1391-9.
61. Drew KL, Pehek EA, Rasley BT, Ma YL, Green TK. Sampling glutamate and GABA with microdialysis: suggestions on how to get the dialysis membrane closer to the synapse. J Neurosci Methods 2004;140:127-31.
62. Timmerman W, Westerink BH. Brain microdialysis of GABA and glutamate: what does it signify? Synapse 1997;27:242-61.
63. Olah S, Fule M, Komlosi G, et al. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 2009;461:1278-81.
64. Wei W, Zhang N, Peng Z, Houser CR, Mody I. Perisynaptic localization of delta subunit-containing GABAA receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 2003;23:10650-61.
65. Hamann M, Rossi DJ, Attwell D. Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 2002;33:625-33.
66. Bright DP, Renzi M, Bartram J, et al. Profound desensitization by ambient GABA limits activation of delta-containing GABAA receptors during spillover. J Neurosci 2011;31:753-63.
67. Mitchell SJ, Silver RA. GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J Neurosci 2000;20:8651-8.
68. Halassa MM, Fellin T, Haydon PG. Tripartite synapses: roles for astrocytic purines in the control of synaptic physiology and behavior. Neuropharmacology 2009;57:343-6.
69. Angulo MC, Le Meur K, Kozlov AS, Charpak S, Audinat E. GABA, a forgotten gliotransmitter. Prog Neurobiol 2008;86:297-303.
70. Wall MJ, Usowicz MM. Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 1997;9:533-48.