A conserved behavioral state barrier impedes transitions between anesthetic-induced unconsciousness and wakefulness: Evidence for neural inertia

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Friedman, Eliot B ^a,c   Sun, Yi ^a   Moore, Jason T ^a,c   Hung, Hsiao Tung ^a,c   Meng, Qing Cheng ^a   Perera, Priyan ^a   Joiner, William J ^b,d   Thomas, Steven A ^a   Eckenhoff, Roderic G ^a   Sehgal, Amita ^b,c   Kelz, Max B ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; ANESTHETIC AGENT;

ANESTHESIA INDUCTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE MUTATION; GENETIC MANIPULATION; HYSTERESIS; INDUCED RESISTANCE; MALE; MOUSE; NERVE CELL NETWORK; NONHUMAN; QUANTITATIVE ANALYSIS; SLEEP WAKING CYCLE; UNCONSCIOUSNESS; WAKEFULNESS; WILD TYPE; ANIMAL; BRAIN; C57BL MOUSE; CENTRAL NERVOUS SYSTEM; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; PHYSIOLOGY;

HEXAPODA; MAMMALIA; MUS;

ANESTHETICS; ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM; DROSOPHILA; MALE; MICE; MICE, INBRED C57BL; UNCONSCIOUSNESS; WAKEFULNESS;

EID: 77955613374     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011903     Document Type: Article

References (53)

1. Fort P, Bassetti CL, Luppi PH (2009) Alternating vigilance states: New insights regarding neuronal networks and mechanisms. Eur J Neurosci 29: 1741-1753.
2. Saper CB, Chou TC, Scammell TE (2001) The sleep switch: Hypothalamic control of sleep and wakefulness. Trends Neurosci 24: 726-731.
3. Chatterjee A, Kaznessis YN, Hu WS (2008) Tweaking biological switches through a better understanding of bistability behavior. Curr Opin Biotechnol 19: 475-481.
4. Jonson B, Svantesson C (1999) Elastic pressure-volume curves: What information do they convey? Thorax 54: 82-87.
5. Sethna JP, Dahmen K, Kartha S, Krumhansl JA, Roberts BW, et al. (1993) Hysteresis and hierarchies: Dynamics of disorder-driven first-order phase transformations. Phys Rev Lett 70: 3347-3350.
6. Shadwick RE (1990) Elastic energy storage in tendons: Mechanical differences related to function and age. J Appl Physiol 68: 1033-1040.
7. Steyn-Ross ML, Steyn-Ross DA, Sleigh JW (2004) Modelling general anaesthesia as a first-order phase transition in the cortex. Prog Biophys Mol Biol 85: 369-385.
8. Rudolph U, Antkowiak B (2004) Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 5: 709-720.
9. Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322: 876-880.
10. Franks NP (2008) General anaesthesia: From molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9: 370-386.
11. Lydic R, Baghdoyan HA (2005) Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103: 1268-1295.
12. Bruhn J, Ropcke H, Rehberg B, Bouillon T, Hoeft A (2000) Electroencephalogram approximate entropy correctly classifies the occurrence of burst suppression pattern as increasing anesthetic drug effect. Anesthesiology 93: 981-985.
13. Kreuer S, Wilhelm W, Grundmann U, Larsen R, Bruhn J (2004) Narcotrend index versus bispectral index as electroencephalogram measures of anesthetic drug effect during propofol anesthesia. Anesth Analg 98: 692-697.
14. McKay ID, Voss LJ, Sleigh JW, Barnard JP, Johannsen EK (2006) Pharmacokinetic-pharmacodynamic modeling the hypnotic effect ofsevoflurane using the spectral entropy of the electroencephalogram. Anesth Analg 102: 91-97.
15. Laureys S (2005) The neural correlate of (un)awareness: Lessons from the vegetative state. Trends Cogn Sci 9: 556-559.
16. Allada R, Nash HA (1993) Drosophila melanogaster as a model for study of general anesthesia: The quantitative response to clinical anesthetics and alkanes. Anesth Analg 77: 19-26.
17. Gamo S (2002) Studies on target genes of general anesthetics. Curr Drug Targets 3: 31-41.
18. van Swinderen B (2006) A succession ofanesthetic endpoints in the Drosophila brain. JNeurobiol 66: 1195-1211.
19. van Swinderen B, Andretic R (2003) Arousal in Drosophila. Behav Processes 64: 133-144.
20. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287: 1834-1837.
21. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA, et al. (2000) Rest in Drosophila is a sleep-like state. Neuron 25: 129-138.
22. Campbell JL, Nash HA (2001) Volatile general anesthetics reveal a neurobiological role for the white and brown genes of Drosophila melanogaster. J Neurobiol 49: 339-349.
23. Miller RD, Way WL, Eger EI, 2nd (1968) The effects of alpha-methyldopa, reserpine, guanethidine, and iproniazid on minimum alveolar anesthetic requirement (MAC). Anesthesiology 29: 1153-1158.
24. Mueller RA, Smith RD, Spruill WA, Breese GR (1975) Central monaminergic neuronal effects on minimum alveolar concentrations (MAC) of halothane and cyclopropane in rats. Anesthesiology 42: 143-152.
25. Roizen MF, White PF, Eger EI, 2nd, Brownstein M (1978) Effects ofablation of serotonin or norepinephrine brain-stem areas on halothane and cyclopropane MACs in rats. Anesthesiology 49: 252-255.
26. Thomas SA, Marck BT, Palmiter RD, Matsumoto AM (1998) Restoration of norepinephrine and reversal of phenotypes in mice lacking dopamine beta-hydroxylase. J Neurochem 70: 2468-2476.
27. Tinklenberg JA, Segal IS, Guo TZ, Maze M (1991) Analysis of anesthetic action on the potassium channels of the Shaker mutant of Drosophila. Ann N Y Acad Sci 625: 532-539.
28. Weber B, Schaper C, Bushey D, Rohlfs M, Steinfath M, et al. (2009) Increased Volatile Anesthetic Requirement in Short-sleeping Drosophila Mutants. Anesthesiology 110: 313-316.
29. Walcourt A, Scott RL, Nash HA (2001) Blockage of one class of potassium channel alters the effectiveness of halothane in a brain circuit of Drosophila. Anesth Analg 92: 535-541.
30. Steyn-Ross DA, Steyn-Ross ML, Wilcocks LC, Sleigh JW (2001) Toward a theory ofthe general-anesthetic-induced phase transition ofthe cerebral cortex. II. Numerical simulations, spectral entropy, and correlation times. Phys Rev E Stat Nonlin Soft Matter Phys 64: 011918.
31. Campbell JL, Gu Q, Guo D, Nash HA (2009) Genetic Effects in Drosophila on the Potency of Diverse General Anesthetics: A Distinctive Pattern of Altered Sensitivity. J Neurogenet: 1-10.
32. Correa AM (1998) Gating kinetics of Shaker K+ channels are differentially modified by general anesthetics. Am J Physiol 275: C1009-1021.
33. Eckenhoff MF, Eckenhoff RG (1998) Quantitative autoradiography ofhalothane binding in rat brain. J Pharmacol Exp Ther 285: 371-376.
34. Gompf HS, Chen J, Sun Y, Yanagisawa M, Aston-Jones G, et al. (2009) Halothane-induced Hypnosis is not Accompanied by Inactivation of Orexinergic Output in Rodents. Anesthesiology 111: 1001-1009.
35. Keifer JC, Baghdoyan HA, Lydic R (1996) Pontine cholinergic mechanisms modulate the cortical electroencephalographic spindles of halothane anesthesia. Anesthesiology 84: 945-954.
36. Tassi P, Muzet A (2000) Sleep inertia. Sleep Med Rev 4: 341-353.
37. Uv A, Cantera R, Samakovlis C (2003) Drosophila tracheal morphogenesis: Intricate cellular solutions to basic plumbing problems. Trends Cell Biol 13: 301-309.
38. Lighton JR (2005) Respiratory physiology: Strange cycles and the fruit-fly's tongue. Curr Biol 15: R965-R966.
39. McCormick DA, Pape HC, Williamson A (1991) Actions of norepinephrine in the cerebral cortex and thalamus: Implications for function of the central noradrenergic system. Prog Brain Res 88: 293-305.
40. Gallopin T, Fort P, Eggermann E, Cauli B, Luppi PH, et al. (2000) Identification of sleep-promoting neurons in vitro. Nature 404: 992-995.
41. Berridge CW, Foote SL (1996) Enhancement ofbehavioral and electroenceph-alographic indices of waking following stimulation of noradrenergic beta-receptors within the medial septal region ofthe basal forebrain. J Neurosci 16: 6999-7009.
42. Berridge CW, O'Neill J (2001) Differential sensitivity to the wake-promoting actions of norepinephrine within the medial preoptic area and the substantia innominata. Behav Neurosci 115: 165-174.
43. 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.
44. Mesa A, Diaz AP, Frosth M (2000) Narcolepsy and anesthesia. Anesthesiology 92: 1194-1196.
45. Burrow B, Burkle C, Warner DO, Chini EN (2005) Postoperative outcome of patients with narcolepsy. A retrospective analysis. J Clin Anesth 17: 21-25.
46. Ohno K, Sakurai T (2008) Orexin neuronal circuitry: Role in the regulation of sleep and wakefulness. Front Neuroendocrinol 29: 70-87.
47. Siegel JM (1999) Narcolepsy: A key role for hypocretins (orexins). Cell 98: 409-412.
48. Kelz MB, Sun Y, Chen J, Cheng Meng Q, Moore JT, et al. (2008) An essential role for orexins in emergence from general anesthesia. Proc Natl Acad Sci USA 105: 1309-1314.
49. Ouyang M, Hellman K, Abel T, Thomas SA (2004) Adrenergic signaling plays a critical role in the maintenance of waking and in the regulation of REM sleep. J Neurophysiol 92: 2071-2082.
50. Cirelli C, Bushey D, Hill S, Huber R, Kreber R, et al. (2005) Reduced sleep in Drosophila Shaker mutants. Nature 434: 1087-1092.
51. Sun Y, Chen J, Pruckmayr G, Baumgardner JE, Eckmann DM, et al. (2006) High throughput modular chambers for rapid evaluation of anesthetic sensitivity. BMC Anesthesiology 6: 13.
52. Thomas SA, Matsumoto AM, Palmiter RD (1995) Noradrenaline is essential for mouse fetal development. Nature 374: 643-646.
53. Joiner WJ, Crocker A, White BH, Sehgal A (2006) Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441: 757-760.