Isoflurane suppresses early cortical activity

Annals of Clinical and Translational Neurology

Volumn 1, Issue 1, 2014, Pages 15-26

  Sitdikova, Guzel ^a,b,c   Zakharov, Andrei ^c   Janackova, Sona ^a,b   Gerasimova, Elena ^c   Lebedeva, Julia ^c   Inacio, Ana R ^b,c   Zaynutdinova, Dilyara ^b,c   Minlebaev, Marat ^a,b,c   Holmes, Gregory L ^d   Khazipov, Roustem ^a,b,c  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOFLURANE;

ADOLESCENT; ADRENAL CORTEX; ADULT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EVOKED SOMATOSENSORY RESPONSE; FEMALE; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX;

EID: 84901609972     PISSN: None     EISSN: 23289503     Source Type: Journal    
DOI: 10.1002/acn3.16     Document Type: Article

References (71)

1. Kroeger D, Amzica F. Hypersensitivity of the anesthesia-induced comatose brain. J Neurosci 2007;27:10597-10607.
2. Ferron JF, Kroeger D, Chever O, et al. Cortical inhibition during burst suppression induced with isoflurane anesthesia. J Neurosci 2009;29:9850-9860.
3. Swank RL, Watson CW. Effects of barbiturates and ether on spontaneous electrical activity of dog brain. J Neurophysiol 1949;12:137-160.
4. Patel P, Sun L. Update on neonatal anesthetic neurotoxicity: insight into molecular mechanisms and relevance to humans. Anesthesiology 2009;110:703-708.
5. Jevtovic-Todorovic V. Developmental synaptogenesis and general anesthesia: a kiss of death? Curr Pharm Des 2012;18:6225-6231.
6. Flick RP, Katusic SK, Colligan RC, et al. Cognitive and behavioral outcomes after early exposure to anesthesia and surgery. Pediatrics 2011;128:e1053-e1061.
7. Orliaguet G, Vivien B, Langeron O, et al. Minimum alveolar concentration of volatile anesthetics in rats during postnatal maturation. Anesthesiology 2001;95:734-739.
8. Jevtovic-Todorovic V, Hartman RE, Izumi Y, et al. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits J Neurosci 2003;23:876-882.
9. Wise-Faberowski L, Zhang H, Ing R, et al. Isoflurane-induced neuronal degeneration: an evaluation in organotypic hippocampal slice cultures. Anesth Analg 2005;101:651-657.
10. Ikonomidou C, Bittigau P, Ishimaru MJ, et al. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000;287:1056-1060.
11. Leveille F, Papadia S, Fricker M, et al. Suppression of the intrinsic apoptosis pathway by synaptic activity. J Neurosci 2010;30:2623-2635.
12. Istaphanous GK, Ward CG, Nan X, et al. Characterization and quantification of isoflurane-induced developmental apoptotic cell death in mouse cerebral cortex. Anesth Analg 2013;116:845-854.
13. Stratmann G, May LD, Sall JW, et al. Effect of hypercarbia and isoflurane on brain cell death and neurocognitive dysfunction in 7-day-old rats. Anesthesiology 2009;110:849-861.
14. Olney JW, Young C, Wozniak DF, et al. Anesthesia-induced developmental neuroapoptosis. Does it happen in humans? Anesthesiology 2004;101:273-275.
15. Mennerick S, Zorumski CF. Neural activity and survival in the developing nervous system. Mol Neurobiol 2000;22:41-54.
16. Colonnese M, Khazipov R. Spontaneous activity in developing sensory circuits: implications for resting state fMRI. Neuroimage 2012;62:2212-2221.
17. Khazipov R, Luhmann HJ. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 2006;29:414-418.
18. Blankenship AG, Feller MB. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 2010;11:18-29.
19. Clancy B, Darlington RB, Finlay BL. Translating developmental time across mammalian species. Neuroscience 2001;105:7-17.
20. Colonnese MT, Kaminska A, Minlebaev M, et al. A conserved switch in sensory processing prepares developing neocortex for vision. Neuron 2010;67:480-498.
21. Avishai-Eliner S, Brunson KL, Sandman CA, et al. Stressed-out, or in (utero)? Trends Neurosci 2002;25:518-524.
22. Khazipov R, Sirota A, Leinekugel X, et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 2004;432:758-761.
23. Minlebaev M, Colonnese M, Tsintsadze T, et al. Early gamma oscillations synchronize developing thalamus and cortex. Science 2011;334:226-229.
24. Yang JW, Hanganu-Opatz IL, Sun JJ, et al. Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J Neurosci 2009;29:9011-9025.
25. Yang JW, An S, Sun JJ, et al. Thalamic network oscillations synchronize ontogenetic columns in the newborn rat barrel cortex. Cereb Cortex 2013;23:1299-1316.
26. Hanganu IL, Ben Ari Y, Khazipov R. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci 2006;26:6728-6736.
27. Colonnese MT, Khazipov R. "Slow activity transients" in infant rat visual cortex: a spreading synchronous oscillation patterned by retinal waves. J Neurosci 2010;30:4325-4337.
28. Hrbek A, Karlberg P, Olsson T. Development of visual and somatosensory evoked responses in pre-term newborn infants. Electroencephalogr Clin Neurophysiol 1973;34:225-232.
29. Milh M, Kaminska A, Huon C, et al. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex 2007;17:1582-1594.
30. Stockard-Pope, JE, Werner, SS, Bickford RG . Atlas of neonatal electroencelography. 2nd ed. New York: Raven Press, 1992.
31. Lamblin MD, Andre M, Challamel MJ, et al. [Electroencephalography of the premature and term newborn. Maturational aspects and glossary]. Neurophysiol Clin 1999;29:123-219.
32. Anderson CM, Torres F, Faoro A. The EEG of the early premature. Electroencephalogr Clin Neurophysiol 1985;60:95-105.
33. Scher MS. Electroencephalography of the newborn: normal features. In: Holmes GL, Moshe S, Jones RH, eds. Clinical neurophysiology of infancy, childhood and adolescence. Philadelphia, USA: Elsevier, 2006; 46-69.
34. Andre M, Lamblin MD, d'Allest AM, et al. Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol Clin 2010;40:59-124.
35. Stjerna S, Voipio J, Metsaranta M, et al. Preterm EEG: a multimodal neurophysiological protocol. J Vis Exp 2012;60. pii: 3774.
36. Minlebaev, M, Ben Ari, Y, Khazipov R. NMDA receptors pattern early activity in the developing barrel cortex in vivo. Cereb Cortex 2009;19:688-696
37. Catsicas M, Pequignot Y, Clarke PG. Rapid onset of neuronal death induced by blockade of either axoplasmic transport or action potentials in afferent fibers during brain development. J Neurosci 1992;12:4642-4650.
38. Linden R. The survival of developing neurons: a review of afferent control. Neuroscience 1994;58:671-682.
39. Heck N, Golbs A, Riedemann T, et al. Activity-dependent regulation of neuronal apoptosis in neonatal mouse cerebral cortex. Cereb Cortex 2008;18:1335-1349.
40. Rochefort NL, Garaschuk O, Milos RI, et al. Sparsification of neuronal activity in the visual cortex at eye-opening. Proc Natl Acad Sci USA 2009;106:15049-15054.
41. Golshani P, Goncalves JT, Khoshkhoo S, et al. Internally mediated developmental desynchronization of neocortical network activity. J Neurosci 2009;29:10890-10899.
42. Siegel F, Heimel JA, Peters J, et al. Peripheral and central inputs shape network dynamics in the developing visual cortex in vivo. Curr Biol 2012;22:253-258.
43. Mitra PP, Pesaran B. Analysis of dynamic brain imaging data. Biophys J 1999;76:691-708.
44. Torrence C, Compo GP. A practical guide to wavelet analysis. Bull Am Meteorol Soc 1998;79:61-78.
45. Nicholson C, Freeman JA. Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J Neurophysiol 1975;38:356-368.
46. Minlebaev M, Ben-Ari Y, Khazipov R. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol 2007;97:692-700.
47. Minlebaev, M, Khazipov, R. Antiepileptic effects of endogenous beta-hydroxybutyrate in suckling infant rats. Epilepsy Res 2011;95:100-109.
48. Sakata S, Harris KD. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 2009;64:404-418.
49. Tiriac A, Uitermarkt BD, Fanning AS, et al. Rapid whisker movements in sleeping newborn rats. Curr Biol 2012;22:2075-2080.
50. Shelton KL, Nicholson KL. GABA(A) positive modulator and NMDA antagonist-like discriminative stimulus effects of isoflurane vapor in mice. Psychopharmacology 2010;212:559-569.
51. Brosnan RJ. GABA(A) receptor antagonism increases NMDA receptor inhibition by isoflurane at a minimum alveolar concentration. Vet Anaesth Analg 2011;38:231-239.
52. Dong Y, Wu X, Zhang G, et al. Isoflurane facilitates synaptic NMDA receptor endocytosis in mice primary neurons. Curr Mol Med 2013;13:488-498.
53. Harrison NL, Kugler JL, Jones MV, et al. Positive modulation of human gamma-aminobutyric acid type A and glycine receptors by the inhalation anesthetic isoflurane. Mol Pharmacol 1993;44:628-632.
54. Banks MI, Pearce RA. Dual actions of volatile anesthetics on GABA(A) IPSCs: dissociation of blocking and prolonging effects. Anesthesiology 1999;90:120-134.
55. Wu XS, Sun JY, Evers AS, et al. Isoflurane inhibits transmitter release and the presynaptic action potential. Anesthesiology 2004;100:663-670.
56. Franks NP, Lieb WR. Volatile general anesthestics activate a novel neuronal K+ current. Nature 1988;333:662-664.
57. Patel AJ, Honore E, Lesage F, et al. Inhalational anesthetics activate two-pore-domain background K+ channels. Nat Neurosci 1999;2:422-426.
58. Constantinople CM, Bruno RM. Effects and mechanisms of wakefulness on local cortical networks. Neuron 2011;69:1061-1068.
59. Takenoshita M, Takahashi T. Mechanisms of halothane action on synaptic transmission in motoneurons of the newborn rat spinal cord in vitro. Brain Res 1987;402:303-310.
60. Sirois JE, Pancrazio JJ, Lynch C III, et al. Multiple ionic mechanisms mediate inhibition of rat motoneurones by inhalation anaesthetics. J Physiol 1998;512:851-862.
61. Hanganu IL, Staiger JF, Ben Ari Y, et al. Cholinergic modulation of spindle bursts in the neonatal rat visual cortex in vivo. J Neurosci 2007;27:5694-5705.
62. Stroh A, Adelsberger H, Groh A, et al. Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron 2013;77:1136-1150.
63. Hudetz AG, Imas OA. Burst activation of the cerebral cortex by flash stimuli during isoflurane anesthesia in rats. Anesthesiology 2007;107:983-991.
64. Hartikainen K, Rorarius M, Makela K, et al. Propofol and isoflurane induced EEG burst suppression patterns in rabbits. Acta Anaesthesiol Scand 1995;39:814-818.
65. Hartikainen K, Rorarius M, Makela K, et al. Visually evoked bursts during isoflurane anesthesia. Br J Anaesth 1995;74:681-685.
66. Timofeev I, Steriade M. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J Neurophysiol 1996;76:4152-4168.
67. Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 2000;3:1027-1034.
68. Seelke AM, Blumberg MS. The microstructure of active and quiet sleep as cortical delta activity emerges in infant rats. Sleep 2008;31:691-699.
69. Rheims S, Minlebaev M, Ivanov A, et al. Excitatory GABA in rodent developing neocortex in vitro. J Neurophysiol 2008;100:609-619.
70. Ikonomidou C, Bosch F, Miksa M, et al. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999;283:70-74.
71. Olney JW, Young C, Wozniak DF, et al. Do pediatric drugs cause developing neurons to commit suicide? Trends Pharmacol Sci 2004;25:135-139.