α2-adrenergic stimulation of the ventrolateral preoptic nucleus destabilizes the anesthetic state

Journal of Neuroscience

Volumn 34, Issue 49, 2014, Pages 16385-16396

  McCarren, Hilary S ^a,b   Chalifoux, Michael R ^a   Han, Bo ^a   Moore, Jason T ^a   Meng, Qing Cheng ^a   Baron Hionis, Nina ^a   Sedigh Sarvestani, Madineh ^a   Contreras, Diego ^a   Beck, Sheryl G ^a,c   Kelz, Max B ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Adrenergic; Anesthesia; Dexmedetomidine; Emergence; Sleep; VLPO

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; ALPHA 2A ADRENERGIC RECEPTOR; ALPHA 2B ADRENERGIC RECEPTOR; ALPHA 2C ADRENERGIC RECEPTOR; DEXMEDETOMIDINE; ISOFLURANE; MESSENGER RNA; NEUROTRANSMITTER; NORADRENALIN; PHENYLEPHRINE; TETRODOTOXIN; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; ANESTHETIC AGENT;

ALPHA ADRENERGIC STIMULATION; ALPHA2 ADRENERGIC STIMULATION; ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN ELECTROPHYSIOLOGY; CANNULA; CONTROLLED STUDY; DEPOLARIZATION; DEPRESSION; ELECTRODE; ELECTROENCEPHALOGRAPHY; EVOKED SOMATOSENSORY RESPONSE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERPOLARIZATION; MALE; MEMBRANE POTENTIAL; MOUSE; NERVE CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PREOPTIC NUCLEUS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIGHTING REFLEX; RNA EXTRACTION; SOMATOSENSORY CORTEX; STEADY STATE; STEREOTACTIC PROCEDURE; ANIMAL; ANTAGONISTS AND INHIBITORS; AROUSAL; DRUG EFFECTS; ELECTROENCEPHALOGRAM; METABOLISM; MICROINJECTION; PHYSIOLOGY; PREOPTIC AREA;

ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ANESTHETICS; ANIMALS; AROUSAL; BRAIN WAVES; DEXMEDETOMIDINE; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, SOMATOSENSORY; ISOFLURANE; MALE; MICE; MICROINJECTIONS; NOREPINEPHRINE; PREOPTIC AREA; RECEPTORS, ADRENERGIC, ALPHA-2;

EID: 84914674449     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1135-14.2014     Document Type: Article

References (71)

1. Alkire MT, McReynolds JR, Hahn EL, Trivedi AN (2007) Thalamic microinjection of nicotine reverses sevoflurane-induced loss of righting reflex in the rat. Anesthesiology 107:264-272. CrossRef Medline
2. Alkire MT, Asher CD, Franciscus AM, Hahn EL (2009) Thalamic microinfusion of antibody to a voltage-gated potassium channel restores consciousness during anesthesia. Anesthesiology 110:766-773. CrossRef Medline
3. Antunes LM, Golledge HDR, Roughan JV, Flecknell PA (2003) Comparison of electroencephalogram activity and auditory evoked responses during isoflurane and halothane anaesthesia in the rat. Vet Anaesth Analg 30:15-23. CrossRef Medline
4. Bai D, Renaud LP (1998) Median preoptic nucleus neurons: an in vitro patch-clamp analysis of their intrinsic properties and noradrenergic receptors in the rat. Neuroscience 83:905-916. CrossRef Medline
5. Banoub M, Tetzlaff JE, Schubert A (2003) Pharmacologic and physiologic influences affecting sensory evoked potentials: implications for perioperative monitoring. Anesthesiology 99:716-737. CrossRef Medline
6. Berridge CW, Schmeichel BE, Espana RA (2012) Noradrenergic modulation of wakefulness/arousal. Sleep Med Rev 16:187-197. CrossRef Medline
7. Brefel-Courbon C, Payoux P, Ory F, Sommet A, Slaoui T, Raboyeau G, Lemesle B, Puel M, Montastruc JL, Demonet JF, Cardebat D (2007) Clinical and imaging evidence of zolpidem effect in hypoxic encephalopathy. Ann Neurol 62:102-105. CrossRef Medline
8. Chou TC, Bjorkum AA, Gaus SE, Lu J, Scammell TE, Saper CB (2002) Afferents to the ventrolateral preoptic nucleus. J Neurosci 22:977-990. Medline
9. Clauss RP, Güldenpfennig WM, Nel HW, Sathekge MM, Venkannagari RR (2000) Extraordinary arousal from semi-comatose state on zolpidem. A case report. South Afr Med J Suid-Afr Tydskr Vir Geneeskd 90:68-72.
10. Cohen L, Chaaban B, Habert MO (2004) Transient improvement of aphasia with zolpidem. N Engl J Med 350:949-950. CrossRef Medline
11. Eckenhoff MF, Eckenhoff RG (1998) Quantitative autoradiography of halothane binding in rat brain. J Pharmacol Exp Ther 285:371-376. Medline
12. Erchova IA, Lebedev MA, Diamond ME (2002) Somatosensory cortical neuronal population activity across states of anaesthesia. Eur J Neurosci 15:744-752. CrossRef Medline
13. Feldman SM, Waller HJ (1962) Dissociation of electrocortical activation and behavioural arousal. Nature 196:1320-1322. CrossRef Medline
14. Franklin KBJ, Paxinos G (2007) The mouse brain in stereotaxic coordinates, Ed 3. San Diego: Elsevier.
15. Franks NP (2008) General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9:370-386. CrossRef Medline
16. Franks NP, Lieb WR (1996) Temperature dependence of the potency of volatile general anesthetics: implications for in vitro experiments. Anesthesiology 84:716-720. CrossRef Medline
17. Frontini A, Giordano A (2010) Leptin-sensitive neurons in mouse preoptic area express_1A-and_2A-adrenergic receptor isoforms. Neurosci Lett 471:83-88. CrossRef Medline
18. Gallopin T, Fort P, Eggermann E, Cauli B, Luppi PH, Rossier J, Audinat E, Mühlethaler M, Serafin M (2000) Identification of sleep-promoting neurons in vitro. Nature 404:992-995. CrossRef Medline
19. Gallopin T, Luppi PH, Rambert FA, Frydman A, Fort P (2004) Effect of the wake-promoting agent modafinil on sleep-promoting neurons from the ventrolateral preoptic nucleus: an in vitro pharmacologic study. Sleep 27:19-25. Medline
20. Gallopin T, Luppi PH, Cauli B, Urade Y, Rossier J, Hayaishi O, Lambolez B, Fort P (2005) The endogenous somnogen adenosine excites a subset of sleep-promoting neurons via A2A receptors in the ventrolateral preoptic nucleus. Neuroscience 134:1377-1390. CrossRef Medline
21. Gilsbach R, Röser C, Beetz N, Brede M, Hadamek K, Haubold M, Leemhuis J, Philipp M, Schneider J, Urbanski M, Szabo B, Weinshenker D, Hein L (2009) Genetic dissection of_2-adrenoceptor functions in adrenergic versus nonadrenergic cells. Mol Pharmacol 75:1160-1170. CrossRef Medline
22. Han B, McCarren HS, O’Neill D, Kelz MB (2014) Distinctive recruitment of endogenous sleep-promoting neurons by volatile anesthetics and a nonimmobilizer. Anesthesiology 121:999-1009. CrossRef Medline
23. Hsieh KC, Gvilia I, Kumar S, Uschakov A, McGinty D, Alam MN, Szymusiak R (2011) c-Fos expression in neurons projecting from the preoptic and lateral hypothalamic areas to the ventrolateral periaqueductal gray in relation to sleep states. Neuroscience 188:55-67. CrossRef Medline
24. Hu FY, Hanna GM, Han W, Mardini F, Thomas SA, Wyner AJ, Kelz MB (2012) Hypnotic hypersensitivity to volatile anesthetics and dexmedetomidine in dopamine β-hydroxylase knockout mice. Anesthesiology 117: 1006-1017. CrossRef Medline
25. Jahn-Eimermacher A, Lasarzik I, Raber J (2011) Statistical analysis of latency outcomes in behavioral experiments. Behav Brain Res 221:271-275. CrossRef Medline
26. Jha SK, Mallick BN (2009) Presence of α-1 norepinephrinergic and GABA-A receptors on medial preoptic hypothalamus thermosensitive neurons and their role in integrating brainstem ascending reticular activating system inputs in thermoregulation in rats. Neuroscience 158:833-844. CrossRef Medline
27. 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. CrossRef Medline
28. Kolaj M, Renaud LP (2001) Norepinephrine acts via 2 adrenergic receptors to suppress N-type calcium channels in dissociated rat median preoptic nucleus neurons. Neuropharmacology 41:472-479. CrossRef Medline
29. Kolaj M, Renaud LP (2007) Presynaptic {alpha}-adrenoceptors in median preoptic nucleus modulate inhibitory neurotransmission from subfornical organ and organum vasculosum lamina terminalis. Am J Physiol Regul Integr Comp Physiol 292:R1907-R1915. CrossRef Medline
30. Kottler B, Bao H, Zalucki O, Imlach W, Troup M, van Alphen B, Paulk A, Zhang B, van Swinderen B (2013) A sleep/wake circuit controls isoflurane sensitivity in Drosophila. Curr Biol 23:594-598. CrossRef Medline
31. Kumar VM, Vetrivelan R, Mallick HN (2006) Alpha-1 adrenergic receptors in the medial preoptic area are involved in the induction of sleep. Neurochem Res 31:1095-1102. CrossRef Medline
32. Kumar VM, Vetrivelan R, Mallick HN (2007) Noradrenergic afferents and receptors in the medial preoptic area: neuroanatomical and neurochemical links between the regulation of sleep and body temperature. Neurochem Int 50:783-790. CrossRef Medline
33. Kushikata T, Yoshida H, Kudo M, Kudo T, Kudo T, Hirota K (2011) Role of coerulean noradrenergic neurones in general anaesthesia in rats. Br J Anaesth 107:924-929. CrossRef Medline
34. Lakhlani PP, MacMillan LB, Guo TZ, McCool BA, Lovinger DM, Maze M, Limbird LE (1997) Substitution of a mutant α2a-adrenergic receptor via “hit and run” gene targeting reveals the role of this subtype in sedative, analgesic, and anesthetic-sparing responses in vivo. Proc Natl Acad Sci U S A 94:9950-9955. CrossRef Medline
35. Lazarenko RM, Fortuna MG, Shi Y, Mulkey DK, Takakura AC, Moreira TS, Guyenet PG, Bayliss DA (2010) Anesthetic activation of central respiratory chemoreceptor neurons involves inhibition of a THIK-1-like background K current. J Neurosci 30:9324-9334. CrossRef Medline
36. Li KY, Guan YZ, Krnjevic´ K, Ye JH (2009) Propofol facilitates glutamatergic transmission to neurons of the ventrolateral preoptic nucleus. Anesthesiology 111:1271-1278. CrossRef Medline
37. Liu YW, Li J, Ye JH (2010) Histamine regulates activities of neurons in the ventrolateral preoptic nucleus. J Physiol 588:4103-4116. CrossRef Medline
38. 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. CrossRef Medline
39. Lydic R, Baghdoyan HA (2005) Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103:1268-1295. CrossRef Medline
40. Ma J, Leung LS (2006) Limbic system participates in mediating the effects of general anesthetics. Neuropsychopharmacology 31:1177-1192. Medline
41. Mason ST, King RAJ, Banks P, Angel A (1983) Brain noradrenaline and anaesthesia: behavioural and electrophysiological evidence. Neuroscience 10:177-185. CrossRef Medline
42. Matsuo S, Jang IS, Nabekura J, Akaike N (2003) alpha 2-Adrenoceptormediated presynaptic modulation of GABAergic transmission in mechanically dissociated rat ventrolateral preoptic neurons. J Neurophysiol 89:1640-1648. Medline
43. McCarren HS, Moore JT, Kelz MB (2013) Assessing changes in volatile general anesthetic sensitivity of mice after local or systemic pharmacological intervention. J Vis Exp (80):e51079. CrossRef
44. Modirrousta M, Mainville L, Jones BE (2004) Gabaergic neurons with [alpha]2-adrenergic receptors in basal forebrain and preoptic area express c-Fos during sleep. Neuroscience 129:803-810. CrossRef Medline
45. Moore JT, Chen J, Han B, Meng QC, Veasey SC, Beck SG, Kelz MB (2012) Direct activation of sleep-promoting VLPO neurons by volatile anesthetics contributes to anesthetic hypnosis. Curr Biol 22:2008-2016. CrossRef Medline
46. Morairty S, Rainnie D, McCarley R, Greene R (2004) Disinhibition of ventrolateral preoptic area sleep-active neurons by adenosine: a new mechanism for sleep promotion. Neuroscience 123:451-457. CrossRef Medline
47. Morrison PF, Chen MY, Chadwick RS, Lonser RR, Oldfield EH (1999) Focal delivery during direct infusion to brain: role of flow rate, catheter diameter, and tissue mechanics. Am J Physiol Regul Integr Comp Physiol 277:R1218-R1229.
48. Nelson LE, Guo TZ, Lu J, Saper CB, Franks NP, Maze M (2002) The sedative component of anesthesia is mediated by GABAA receptors in an endogenous sleep pathway. Nat Neurosci 5:979-984. CrossRef Medline
49. 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. CrossRef Medline
50. Nicholson C (1985) Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 333: 325-329. CrossRef Medline
51. Orth M, Bravo E, Barter L, Carstens E, Antognini JF (2006) The differential effects of halothane and isoflurane on electroencephalographic responses to electrical microstimulation of the reticular formation. Anesth Analg 102:1709-1714. CrossRef Medline
52. Osaka T, Matsumura H (1995) Noradrenaline inhibits preoptic sleep-active neurons through [alpha]2-receptors in the rat. Neurosci Res 21:323-330. CrossRef Medline
53. Pillay S, Vizuete JA, McCallum JB, Hudetz AG (2011) Norepinephrine infusion into nucleus basalis elicits micro-arousal in desfluraneanesthetized rats. Anesthesiology 115:733-742. CrossRef Medline
54. Preibisch S, Saalfeld S, Tomancak P (2009) Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinforma 25:1463-1465. CrossRef Medline
55. Rojas MJ, Navas JA, Rector DM (2006) Evoked response potential markers for anesthetic and behavioral states. Am J Physiol Regul Integr Comp Physiol 291:R189-R196. CrossRef Medline
56. Roy NC, Bessaih T, Contreras D (2011) Comprehensive mapping of whisker-evoked responses reveals broad, sharply tuned thalamocortical input to layer 4 of barrel cortex. J Neurophysiol 105:2421-2437. CrossRef Medline
57. Saint-Mleux B, Eggermann E, Bisetti A, Bayer L, Machard D, Jones BE, Mühlethaler M, Serafin M (2004) Nicotinic enhancement of the noradrenergic inhibition of sleep-promoting neurons in the ventrolateral preoptic area. J Neurosci 24:63-67. CrossRef Medline
58. Shames JL, Ring H (2008) Transient reversal of anoxic brain injury-related minimally conscious state after zolpidem administration: a case report. Arch Phys Med Rehabil 89:386-388. CrossRef Medline
59. Sherin JE, Shiromani PJ, McCarley RW, Saper CB (1996) Activation of ventrolateral preoptic neurons during sleep. Science 271:216-219. CrossRef Medline
60. Sherin JE, Elmquist JK, Torrealba F, Saper CB (1998) Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18: 4705-4721. Medline
61. Solt K, Cotten JF, Cimenser A, Wong KFK, Chemali JJ, Brown EN (2011) Methylphenidate actively induces emergence from general anesthesia. Anesthesiology 115:791-803. CrossRef Medline
62. Sukhotinsky I, Zalkind V, Lu J, Hopkins DA, Saper CB, Devor M (2007) Neural pathways associated with loss of consciousness caused by intracerebral microinjection of GABAA-active anesthetics. Eur J Neurosci 25: 1417-1436. CrossRef Medline
63. Taylor NE, Chemali JJ, Brown EN, Solt K (2013) Activation of D1 dopamine receptors induces emergence from isoflurane general anesthesia. Anesthesiology 118:30-39. CrossRef Medline
64. Van Dort CJ, Baghdoyan HA, Lydic R (2009) Adenosine A1 and A2A receptors in mouse prefrontal cortex modulate acetylcholine release and behavioral arousal. J Neurosci 29:871-881. CrossRef Medline
65. van Swinderen B, Kottler B (2014) Explaining general anesthesia: a two-step hypothesis linking sleep circuits and the synaptic release machinery. BioEssays 36:372-381. CrossRef Medline
66. Vanderwolf CH (1992) The electrocorticogram in relation to physiology and behavior: a new analysis. Electroencephalogr Clin Neurophysiol 82: 165-175. CrossRef Medline
67. Vazey EM, Aston-Jones G (2014) Designer receptor manipulations reveal a role of the locus coeruleus noradrenergic system in isoflurane general anesthesia. Proc Natl Acad Sci U S A 111:3859-3864. CrossRef Medline
68. Virtanen R, Savola JM, Saano V, Nyman L (1988) Characterization of the selectivity, specificity and potency of medetomidine as an α2-adrenoceptor agonist. Eur J Pharmacol 150:9-14. CrossRef Medline
69. Wei H, Kang B, Wei W, Liang G, Meng QC, Li Y, Eckenhoff RG (2005) Isoflurane and sevoflurane affect cell survival and BCL-2/BAX ratio differently. Brain Res 1037:139-147. CrossRef Medline
70. Whyte J, Myers R (2009) Incidence of clinically significant responses to zolpidem among patients with disorders of consciousness: a preliminary placebo controlled trial. Am J Phys Med Rehabil 88:410-418. CrossRef Medline
71. Williams ST, Conte MM, Goldfine AM, Noirhomme Q, Gosseries O, Thonnard M, Beattie B, Hersh J, Katz DI, Victor JD, Laureys S, Schiff ND (2013) Common resting brain dynamics indicate a possible mechanism underlying zolpidem response in severe brain injury. eLife 2:e01157. CrossRef Medline