The involvement of hypothalamic sleep pathways in general anesthesia: Testing the hypothesis using the GABA A receptor β 3N265M knock-in mouse

Journal of Neuroscience

Volumn 29, Issue 7, 2009, Pages 2177-2187

  Zecharia, Anna Y ^a   Nelson, Laura E ^a,b   Gent, Thomas C ^a   Schumacher, Mark ^a,d   Jurd, Rachel ^c,e   Rudolph, Uwe ^c,f   Brickley, Stephen G ^a   Maze, Mervyn ^a,b   Franks, Nicholas P ^a,b  

^a The Blackett Laboratory   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anesthesia; GABA A receptor; Histamine; Hypothalamus; Sleep; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID A BETA3 RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR; ALFAXALONE; DEXMEDETOMIDINE; KETAMINE; MUSCIMOL; OREXIN A; PENTOBARBITAL; PROPOFOL; PROTEIN C FOS; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN NUCLEUS; BRAIN SLICE; CONTROLLED STUDY; DRUG EFFECT; DRUG SENSITIVITY; DRUG TARGETING; ELECTROPHYSIOLOGY; GABAERGIC TRANSMISSION; GENERAL ANESTHESIA; HYPOTHALAMUS; IN VIVO STUDY; INHIBITION KINETICS; LATERAL BRAIN VENTRICLE; LOCUS CERULEUS; MALE; MOUSE; NEUROMODULATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; RAT; RIGHTING REFLEX; SLEEP; SYNAPSE; SYNAPTIC TRANSMISSION; WILD TYPE;

ANESTHETICS, GENERAL; ANIMALS; GAMMA-AMINOBUTYRIC ACID; GENE KNOCK-IN TECHNIQUES; HYPOTHALAMIC AREA, LATERAL; HYPOTHALAMUS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCUS COERULEUS; MALE; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NEURAL PATHWAYS; NEUROPEPTIDES; ORGAN CULTURE TECHNIQUES; PROPOFOL; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SLEEP;

EID: 60849097577     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4997-08.2009     Document Type: Article

References (61)

1. Abrahamson EE, Moore RY (2001) The posterior hypothalamic area: che-moarchitecture and afferent connections. Brain Res 889:1-22.
2. Alam MN, Kumar S, Bashir T, Suntsova N, Methippara MM, Szymusiak R, McGinty D (2005) GABA-mediated control of hypocretin-but not melanin-concentrating hormone-immunoreactive neurones during sleep in rats. J Physiol 563:569-582.
3. Allen TA, Narayanan NS, Kholodar-Smith DB, Zhao Y, Laubach M, Brown TH (2008) Imaging the spread of reversible brain inactivations using fluorescent muscimol. J Neurosci Methods 171:30-38.
4. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA (2001) Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acid(A) receptors in hippocampal neurons. Mol Pharmacol 59:814-824.
5. Bayer L, Eggermann E, Serafin M, Grivel J, Machard D, Muhlethaler M, Jones BE (2005) Opposite effects of noradrenaline and acetylcholine upon hypocretin/orexin versus melanin concentrating hormone neurons in rat hypothalamic slices. Neuroscience 130:807-811.
6. Bittencourt JC, Presse F, Arias C, Peto C, Vaughan J, Nahon JL, Vale W, Sawchenko PE (1992) The melanin-concentrating hormone system of the rat brain: an immuno-and hybridization histochemical characterization. J Comp Neurol 319:218-245.
7. Broberger C, De Lecea L, Sutcliffe JG, Hökfelt T (1998) Hypocretin/orexin-and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropep-tide Y and agouti gene-related protein systems. J Comp Neurol 402:460-474.
8. Burdakov D, Gerasimenko O, Verkhratsky A (2005) Physiological changes in glucose differentially modulate the excitability of hypothalamic melanin-concentrating hormone and orexin neurons in situ. J Neurosci 25:2429-2433.
9. Chen CL, Yang YR, Chiu TH (1999) Activation of rat locus coeruleus neuron GABA(A) receptors by propofol and its potentiation by pentobarbital or alphaxalone. Eur J Pharmacol 386:201-210.
10. Correa-Sales C, Rabin BC, Maze M (1992a) A hypnotic response to dexme-detomidine, an alpha 2 agonist, is mediated in the locus coeruleus in rats. Anesthesiology 76:948-952.
11. Correa-Sales C, Nacif-Coelho C, Reid K, Maze M (1992b) Inhibition of ad-enylate cyclase in the locus coeruleus mediates the hypnotic response to an alpha 2 agonist in the rat. J Pharmacol Exp Ther 263:1046-1049.
12. Devor M, Zalkind V (2001) Reversible analgesia, atonia, and loss of consciousness on bilateral intracerebral microinjection of pentobarbital. Pain 94:101-112.
13. Drexler B, Jurd R, Rudolph U, Antkowiak B (2006) Dual actions of enflu-rane on postsynaptic currents abolished by the gamma-aminobutyric acid type A receptor beta3(N265M) point mutation. Anesthesiology 105:297-304.
14. Eggermann E, Bayer L, Serafin M, Saint-Mleux B, Bernheim L, Machard D, Jones BE, Mühlethaler M (2003) The wake-promoting hypocretin-orexin neurons are in an intrinsic state of membrane depolarization. J Neurosci 23:1557-1562.
15. Estabrooke IV, McCarthy MT, Ko E, Chou TC, Chemelli RM, Yanagisawa M, Saper CB, Scammell TE (2001) Fos expression in orexin neurons varies with behavioral state. J Neurosci 21:1656-1662.
16. Franks NP (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9:370-386.
17. Franks NP, Lieb WR (1994) Molecular and cellular mechanisms of general anaesthesia. Nature 367:607-614.
18. Gerashchenko D, Kohls MD, Greco M, Waleh NS, Salin-Pascual R, Kilduff TS, Lappi DA, Shiromani PJ (2001) Hypocretin-2-saporin lesions of the lateral hypothalamus produce narcoleptic-like sleep behavior in the rat. J Neurosci 21:7273-7283.
19. Gredell JA, Turnquist PA, Maciver MB, Pearce RA (2004) Determination of diffusion and partition coefficients of propofol in rat brain tissue: implications for studies of drug action in vitro. Br J Anaesth 93:810-817.
20. Hales TG, Lambert JJ (1991) The actions of propofol on inhibitory amino acid receptors of bovine adrenomedullary chromaffin cells and rodent central neurones. Br J Pharmacol 104:619-628.
21. Harrison NL, Vicini S, Barker JL (1987) A steroid anesthetic prolongs inhib-itory postsynaptic currents in cultured rat hippocampal neurons. J Neurosci 7:604-609.
22. Hoffman GE, Smith MS, Verbalis JG (1993) c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front Neuroendocrinol 14:173-213.
23. Huang ZL, Qu WM, Li WD, Mochizuki T, Eguchi N, Watanabe T, Urade Y, Hayaishi O (2001) Arousal effect of orexin A depends on activation of the histaminergic system. Proc Natl Acad Sci U S A 98:9965-9970.
24. Jurd R, Arras M, Lambert S, Drexler B, Siegwart R, Crestani F, Zaugg M, Vogt KE, Ledermann B, Antkowiak B, Rudolph U (2003) General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor beta3 subunit. FASEB J 17:250-252.
25. Kaisti KK, Långsjö JW, Aalto S, Oikonen V, Sipilä H, Teräs M, Hinkka S, Metsähonkala L, Scheinin H (2003) Effects of sevoflurane, propofol, and adjunct nitrous oxide on regional cerebral blood flow, oxygen consumption, and blood volume in humans. Anesthesiology 99:603-613.
26. Kelz MB, Sun Y, Chen J, Cheng Meng Q, Moore JT, Veasey SC, Dixon S, Thornton M, Funato H, Yanagisawa M (2008) An essential role for orexins in emergence from general anesthesia. Proc Natl Acad Sci U S A 105:1309-1314.
27. Kitamura A, Sato R, Marszalec W, Yeh JZ, Ogawa R, Narahashi T (2004) Halothane and propofol modulation of gamma-aminobutyric acidA receptor single-channel currents. Anesth Analg 99:409-415, table of contents.
28. Ko EM, Estabrooke IV, McCarthy M, Scammell TE (2003) Wake-related activity of tuberomammillary neurons in rats. Brain Res 992:220-226.
29. Krasowski MD, Koltchine VV, Rick CE, Ye Q, Finn SE, Harrison NL (1998) Propofol and other intravenous anesthetics have sites of action on the gamma-aminobutyric acid type A receptor distinct from that for isoflu-rane. Mol Pharmacol 53:530-538.
30. Kushikata T, Hirota K, Yoshida H, Kudo M, Lambert DG, Smart D, Jerman JC, Matsuki A (2003) Orexinergic neurons and barbiturate anesthesia. Neuroscience 121:855-863.
31. Långsjö JW, Maksimow A, Salmi E, Kaisti K, Aalto S, Oikonen V, Hinkka S, Aantaa R, Sipila H, Viljanen T, Parkkola R, Scheinin H (2005) S-ketamine anesthesia increases cerebral blood flow in excess ofthe metabolic needs in humans. Anesthesiology 103:258-268.
32. Lu J, Nelson LE, Franks N, Maze M, Chamberlin NL, Saper CB (2008) Role of endogenous sleep-wake and analgesic systems in anesthesia. J Comp Neurol 508:648-662.
33. Lydic R, Baghdoyan HA (2005) Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103:1268-1295.
34. Mammoto T, Yamamoto Y, Kagawa K, Hayashi Y, Mashimo T, Yoshiya I, Yamatodani A (1997) Interactions between neuronal histamine and halothane anesthesia in rats. J Neurochem 69:406-411.
35. McDougall SJ, Bailey TW, Mendelowitz D, Andresen MC (2008) Propofol enhances both tonic and phasic inhibitory currents in second-order neurons of the solitary tract nucleus (NTS). Neuropharmacology 54:552-563.
36. Mignot E, Lammers GJ, Ripley B, Okun M, Nevsimalova S, Overeem S, Vankova J, Black J, Harsh J, Bassetti C, Schrader H, Nishino S (2002) The role of cerebrospinal fluid hypocretin measurement in the diagnosis of narcolepsy and other hypersomnias. Arch Neurol 59:1553-1562.
37. Moore RY, Bloom FE (1979) Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Annu Rev Neurosci 2:113-168.
38. Nelson LE, Guo TZ, Lu J, Saper CB, Franks NP, Maze M (2002) The sedative component ofanesthesiais mediated byGABA(A) receptors in an endogenous sleep pathway. Nat Neurosci 5:979-984.
39. Nelson LE, Lu J, Guo T, Saper CB, Franks NP, Maze M (2003) The alpha2-adrenoceptor agonist dexmedetomidine converges on an endogenous sleep-promoting pathway to exert its sedative effects. Anesthesiology 98:428-436.
40. Orser BA, Wang LY, Pennefather PS, MacDonald JF (1994) Propofol mod-ulates activation and desensitization ofGABAAreceptors in cultured mu-rine hippocampal neurons. J Neurosci 14:7747-7760.
41. Panula P, Yang HY, Costa E (1984) Histamine-containing neurons in the rat hypothalamus. Proc Natl Acad Sci U S A 81:2572-2576. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. San Diego: Academic.
42. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015.
43. Rudolph U, Antkowiak B (2004) Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 5:709-720.
44. Sakurai T (2007) The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8:171-181.
45. Sergeeva OA, Andreeva N, Garret M, Scherer A, Haas HL (2005) Pharmacological properties of GABAA receptors in rat hypothalamic neurons expressing the epsilon-subunit. J Neurosci 25:88-95.
46. Sherin JE, Shiromani PJ, McCarley RW, Saper CB (1996) Activation of ventrolateral preoptic neurons during sleep. Science 271:216-219.
47. Sherin JE, Elmquist JK, Torrealba F, Saper CB (1998) Innervation of hista-minergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18:4705-4721.
48. Siegwart R, Jurd R, Rudolph U (2002) Molecular determinants for the action of general anesthetics at recombinant alpha(2)beta(3)gamma(2)gamma- aminobutyric acid(A) receptors. J Neurochem 80:140-148.
49. Sloan TB (1998) Anesthetic effects on electrophysiologic recordings. J Clin Neurophysiol 15:217-226.
50. Spigelman I, Li Z, Liang J, Cagetti E, Samzadeh S, Mihalek RM, Homanics GE, Olsen RW (2003) Reduced inhibition and sensitivityto neurosteroids in hippocampus of mice lacking the GABA(A) receptor delta subunit. J Neurophysiol 90:903-910.
51. Staines WA, Daddona PE, Nagy JI (1987) The organization and hypotha-lamic projections ofthe tuberomammillarynucleus in the rat: an immu-nohistochemical study of adenosine deaminase-positive neurons and fibers. Neuroscience 23:571-596.
52. Suntsova N, Szymusiak R, Alam MN, Guzman-Marin R, McGinty D (2002) Sleep-waking discharge patterns of median preoptic nucleus neurons in rats. J Physiol 543:665-677.
53. Szymusiak R, Alam N, Steininger TL, McGinty D (1998) Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res 803:178-188.
54. Takahashi K, Lin JS, Sakai K (2006) Neuronal activity of histaminergic tu-beromammillary neurons during wake-sleep states in the mouse. J Neurosci 26:10292-10298.
55. Tomlin SL, Jenkins A, Lieb WR, Franks NP (1998) Stereoselective effects of etomidate optical isomers on gamma-aminobutyric acid type A receptors and animals. Anesthesiology 88:708-717.
56. Tung A, Lynch JP, Mendelson WB (2001) Prolonged sedation with propofol in the rat does not result in sleep deprivation. Anesth Analg 92:1232-1236.
57. Tung A, Szafran MJ, Bluhm B, Mendelson WB (2002) Sleep deprivation potentiates the onset and duration of loss of righting reflex induced by propofol and isoflurane. Anesthesiology 97:906-911.
58. Williams JT, Henderson G, North RA (1985) Characterization of alpha 2-adrenoceptors which increase potassium conductance in rat locus co-eruleus neurones. Neuroscience 14:95-101.
59. Zeller A, Arras M, Lazaris A, Jurd R, Rudolph U (2005) Distinct molecular targets for the central respiratory and cardiac actions ofthe general anesthetics etomidate and propofol. FASEB J 19:1677-1679.
60. Zeller A, Arras M, Jurd R, Rudolph U (2007a) Mapping the contribution of beta3-containing GABAA receptors to volatile and intravenous general anesthetic actions. BMC Pharmacol 7:2.
61. Zeller A, Arras M, Jurd R, Rudolph U (2007b) Identification of a molecular target mediating the general anesthetic actions of pentobarbital. Mol Pharmacol 71:852-859.