Inhibition of cortical activity and apoptosis caused by ethanol in neonatal rats in vivo

Cerebral Cortex

Volumn 27, Issue 2, 2017, Pages 1068-1082

  Lebedeva, Julia ^a,b,c   Zakharov, Andrei ^a,d   Ogievetsky, Elena ^b,c   Minlebaeva, Alina ^b,c   Kurbanov, Rustem ^a   Gerasimova, Elena ^a   Sitdikova, Guzel ^a   Khazipov, Roustem ^a,b,c  

^a KAZAN FEDERAL UNIVERSITY   (Russian Federation)

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

^c AIX MARSEILLE UNIVERSITY   (France)

^d KAZAN STATE MEDICAL UNIVERSITY   (Russian Federation)

Author keywords

Apoptosis; Electroencephalogram; Ethanol; Fetal alcohol syndrome; Neonate; Neuronal network; Rat; Sensory evoked potentials

Indexed keywords

ALCOHOL; CENTRAL DEPRESSANT AGENT;

AGING; ANIMAL; APOPTOSIS; BLOOD; BRAIN CORTEX; DELTA RHYTHM; DOSE RESPONSE; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; FEMALE; GAMMA RHYTHM; GROWTH, DEVELOPMENT AND AGING; MALE; NERVE CELL; NEWBORN; RAT; SOMATOSENSORY CORTEX; WISTAR RAT;

AGING; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CEREBRAL CORTEX; DELTA RHYTHM; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGICAL PHENOMENA; ETHANOL; FEMALE; GAMMA RHYTHM; MALE; NEURONS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX;

EID: 85029160109     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv293     Document Type: Article

References (71)

1. An S, Yang JW, Sun H, Kilb W, Luhmann HJ. 2012. Long-term potentiation in the neonatal rat barrel cortex in vivo. J Neurosci. 32:9511-9516.
2. Andre M, Lamblin MD, d'Allest AM, Curzi-Dascalova L, Moussalli- Salefranque F, The SN, Vecchierini-Blineau MF, Wallois F, Walls-Esquivel E, Plouin P. 2010. Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol Clin. 40:59-124.
3. Ben Ari Y. 2001. Developing networks play a similar melody. Trends Neurosci. 24:353-360.
4. Ben Ari Y, Gaiarsa JL, Tyzio R, Khazipov R. 2007. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev. 87:1215-1284.
5. Benders MJ, Palmu K, Menache C, Borradori-Tolsa C, Lazeyras F, Sizonenko S, Dubois J, Vanhatalo S, Huppi PS. 2015. Early brain activity relates to subsequent brain growth in premature infants. Cereb Cortex. 25:3014-3024.
6. BittigauP, SifringerM, GenzK, ReithE, Pospischil D, Govindarajalu S, DzietkoM, Pesditschek S, Mai I, Dikranian K, et al. 2002. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc Natl Acad Sci. 99:15089-15094.
7. Blankenship AG, Feller MB. 2010. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci. 11:18-29.
8. Burd L, Blair J, Dropps K. 2012. Prenatal alcohol exposure, blood alcohol concentrations and alcohol elimination rates for the mother, fetus and newborn. J Perinatol. 32:652-659.
9. Carmignoto G, Vicini S. 1992. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science. 258:1007-1011.
10. Chipaux M, Colonnese MT, Mauguen A, Fellous L, Mokhtari M, Lezcano O, Milh M, Dulac O, Chiron C, Khazipov R, et al. 2013. Auditory stimuli mimicking ambient sounds drive temporal "delta-brushes" in premature infants. PLoS One. 8: e79028.
11. Colonnese M, Khazipov R. 2012. Spontaneous activity in developing sensory circuits: implications for resting state fMRI. Neuroimage. 62:2212-2221.
12. Colonnese MT, Kaminska A, Minlebaev M, Milh M, Bloem B, Lescure S, Moriette G, Chiron C, Ben-Ari Y, Khazipov R. 2010.
13. A conserved switch in sensory processing prepares developing neocortex for vision. Neuron. 67:480-498.
14. Colonnese MT, Khazipov R. 2010. "Slow activity transients" in infant rat visual cortex: a spreading synchronous oscillation patterned by retinal waves. J Neurosci. 30:4325-4337.
15. Cornford EM, Braun LD, Oldendorf WH, Hill MA. 1982. Comparison of Lipid-Mediated Blood-Brain-Barrier Penetrability in Neonates and Adults. Am J Physiol. 243:C161-C168.
16. Creeley CE, Dikranian KT, Johnson SA, Farber NB, Olney JW. 2013. Alcohol-induced apoptosis of oligodendrocytes in the fetal macaque brain. Acta Neuropathol Commun. 1:23.
17. Creeley CE, Olney JW. 2013. Drug-induced apoptosis: mechanism by which alcohol and many other drugs can disrupt brain development. Brain Sci. 3:1153-1181.
18. Dildymayfield JE, Harris RA. 1995. Ethanol inhibits kainate responses of glutamate receptors expressed in Xenopus oocytes- role of calcium and protein-kinase-C. J Neurosci. 15:3162-3171.
19. Erzurumlu RS, Gaspar P. 2012. Development and critical period plasticity of the barrel cortex. Eur J Neurosci. 35:1540-1553.
20. Farber NB, Creeley CE, Olney JW. 2010. Alcohol-induced neuroapoptosis in the fetal macaque brain. Neurobiol Dis. 40: 200-206.
21. Galindo R, Zamudio PA, Valenzuela CF. 2005. Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J Neurochem. 94:1500-1511.
22. Gerasimova EV, Zakharov AV, Lebedeva YA, Inacio AR, Minlebaev MG, Sitdikova GF, Khazipov RN. 2014. Gamma oscillations in the somatosensory cortex of newborn rats. Bull Exp Biol Med. 156:295-298.
23. Glykys J, Peng ZC, Chandra D, Homanics GE, Houser CR, Mody I. 2007. A new naturally occurring GABA(A) receptor subunit partnership with high sensitivity to ethanol. Nat Neurosci. 10:40-48.
24. Golshani P, Goncalves JT, Khoshkhoo S, Mostany R, Smirnakis S, Portera-Cailliau C. 2009. Internally mediated developmental desynchronization of neocortical network activity. J Neurosci. 29:10890-10899.
25. Hagenston AM, Bading H. 2011. Calcium signaling in synapse-tonucleus communication. Cold Spring Harb Perspect Biol. 3:1-31.
26. Hanganu IL, Ben Ari Y, Khazipov R. 2006. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci. 26:6728-6736.
27. Hanganu IL, Staiger JF, Ben Ari Y, Khazipov R. 2007. Cholinergic modulation of spindle bursts in the neonatal rat visual cortex in vivo. J Neurosci. 27:5694-5705.
28. Heck N, Golbs A, Riedemann T, Sun JJ, Lessmann V, Luhmann HJ. 2008. Activity-dependent regulation of neuronal apoptosis in neonatal mouse cerebral cortex. Cereb Cortex. 18:1335-1349.
29. Ikonomidou C, Bittigau P, Ishimaru MJ, Wozniak DF, Koch C, Genz K, Price MT, Stefovska V, Horster F, Tenkova T, et al. 2000. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 287:1056-1060.
30. Ikonomidou C, Bosch F, Miksa M, Bittigau P, Vockler J, Dikranian K, Tenkova TI, Stefovska V, Turski L, Olney JW. 1999. Blockade ofNMDAreceptors and apoptotic neurodegeneration in the developing brain. Science. 283:70-74.
31. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, Olney JW, Wozniak DF. 2003.
32. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci. 23:876-882.
33. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science. 274:1133-1138.
34. Khalilov I, Minlebaev M, Mukhtarov M, Khazipov R. 2015. Dynamic changes from depolarizing to hyperpolarizing gabaergic actions during giant depolarizing potentials in the neonatal rat hippocampus. J Neurosci. 35:12635-12642.
35. Khazipov R, Luhmann HJ. 2006. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 29:414-418.
36. Khazipov R, Minlebaev M, Valeeva G. 2013. Early gamma oscillations. Neuroscience. 250:240-252.
37. Khazipov R, Ragozzino D, Bregestovski P. 1995. Kinetics and Mg2+ block ofN-methyl-D-aspartate receptor channels during postnatal development of hippocampal CA3 pyramidal neurons. Neuroscience. 69:1057-1065.
38. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben Ari Y, Buzsaki G. 2004. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature. 432:758-761.
39. Kidd FL, Isaac JT. 1999. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature. 400:569-573.
40. Kirmse K, Kummer M, Kovalchuk Y, Witte OW, Garaschuk O, Holthoff K. 2015. GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo. Nat Commun. 6:7750.
41. Laurie DJ, Wisden W, Seeburg PH. 1992. The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci. 12: 4151-4172.
42. Leveille F, Papadia S, Fricker M, Bell KF, Soriano FX, Martel MA, Puddifoot C, Habel M, Wyllie DJ, Ikonomidou C, et al. 2010. Suppression of the intrinsic apoptosis pathway by synaptic activity. J Neurosci. 30:2623-2635.
43. Lovinger DM, White G, Weight FF. 1989. Ethanol Inhibits NMDAactivated ion current in hippocampal-neurons. Science. 243:1721-1724.
44. Masood K, Wu CP, Brauneis U, Weight FF. 1994. Differential ethanol sensitivity of recombinant N-methyl-D-aspartate receptor subunits. Mol Pharmacol. 45:324-329.
45. Mennerick S, Zorumski CF. 2000. Neural activity and survival in the developing nervous system. Mol Neurobiol. 22:41-54.
46. Milh M, Kaminska A, Huon C, Lapillonne A, Ben Ari Y, Khazipov R. 2007. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex. 17:1582-1594.
47. Minlebaev M, Ben-Ari Y, Khazipov R. 2007. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol. 97:692-700.
48. Minlebaev M, Ben Ari Y, Khazipov R. 2009. NMDA receptors pattern early activity in the developing barrel cortex In vivo. Cereb Cortex. 19:688-696.
49. Minlebaev M, Colonnese M, Tsintsadze T, Sirota A, Khazipov R. 2011. Early gamma oscillations synchronize developing thalamus and cortex. Science. 334:226-229.
50. Minlebaev M, Khazipov R. 2011. Antiepileptic effects of endogenous beta-hydroxybutyrate in suckling infant rats. Epilepsy Res. 95:100-109.
51. Mitrukhina O, Suchkov D, Khazipov R, Minlebaev M. 2015. Imprecise whisker map in the neonatal rat barrel cortex. Cereb Cortex. 25:3458-3467.
52. Mody I, Glykys J, Wei WZ. 2007. A new meaning for "Gin & Tonic": tonic inhibition as the target for ethanol action in the brain. Alcohol. 41:145-153.
53. Mohns EJ, Blumberg MS. 2010. Neocortical activation of the hippocampus during sleep in infant rats. J Neurosci. 30: 3438-3449.
54. Monyer H, BurnashevN, Laurie DJ, SakmannB, Seeburg PH. 1994.Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron. 12:529-540.
55. Nimmervoll B, White R, Yang JW, An SM, Henn C, Sun JJ, Luhmann HJ. 2013. LPS-induced microglial secretion of TNF alpha increases activity-dependent neuronal apoptosis in the neonatal cerebral cortex. Cereb Cortex. 23:1742-1755.
56. Olney JW. 2014. Focus on apoptosis to decipher how alcohol and many other drugs disrupt brain development. Front Pediatr. 2:81.
57. Olney JW, Tenkova T, Dikranian K, Muglia LJ, Jermakowicz WJ, D'Sa C, Roth KA. 2002. Ethanol-induced caspase-3 activation in the in vivo developingmouse brain. Neurobiol Dis. 9:205-219.
58. Olney JW, Wozniak DF, Farber NB, Jevtovic-Todorovic V, Bittigau P, Ikonomidou C. 2002. The enigma of fetal alcohol neurotoxicity. Ann Med. 34:109-119.
59. Rheims S, Minlebaev M, Ivanov A, Represa A, Khazipov R, Holmes GL, Ben Ari Y, Zilberter Y. 2008. Excitatory GABA in rodent developing neocortex in vitro. J Neurophysiol. 100:609-619.
60. Sitdikova G, Zakharov A, Janackova S, Gerasimova E, Lebedeva J, Inacio AR, Zaynutdinova D, Minlebaev M, Holmes GL, Khazipov R. 2014. Isoflurane suppresses early cortical activity. Ann Clin Transl Neurol. 1:15-26.
61. Stjerna S, Voipio J, Metsaranta M, Kaila K, Vanhatalo S. 2012. Preterm EEG: a multimodal neurophysiological protocol. J Vis Exp. 60:3774.
62. Tiriac A, Uitermarkt BD, Fanning AS, Sokoloff G, Blumberg MS. 2012. Rapid whisker movements in sleeping newborn rats. Curr Biol. 22:2075-2080.
63. Viamontes J, PiotrowskiKW, Powell BJ, GoodwinDW. 1972. Alcohol in breath, blood, and cerebrospinal fluid. JAMA. 220:865-866.
64. Willingham MC. 1999. Cytochemical methods for the detection of apoptosis. J Histochem Cytochem. 47:1101-1110.
65. Wright JM, Peoples RW, Weight FF. 1996. Single-channel and whole-cell analysis of ethanol inhibition of NMDA-activated currents in cultured mouse cortical and hippocampal neurons. Brain Res. 738:249-256.
66. Wright RA, Schoepp DD. 1996. Differentiation of group 2 and group 3 metabotropic glutamate receptor cAMP responses in the rat hippocampus. Eur J Pharmacol. 297: 275-282.
67. Yang JW, An S, Sun JJ, Reyes-Puerta V, Kindler J, Berger T, KilbW, Luhmann HJ. 2013. Thalamic network oscillations synchronize ontogenetic columns in the newborn rat barrel cortex. Cereb Cortex. 23:1299-1316.
68. Yang JW, Hanganu-Opatz IL, Sun JJ, Luhmann HJ. 2009. Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J Neurosci. 29: 9011-9025.
69. Young C, Jevtovic-Todorovic V, Qin YQ, Tenkova T, Wang HH, Labruyere J, Olney JW. 2005. Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br J Pharmacol. 146:189-197.
70. Young CL, Straiko MMW, Johnson SA, Creeley C, Olney JW. 2008. Ethanol causes and lithium prevents neuroapoptosis and suppression of pERK in the infant mouse brain. Neurobiol Dis. 31:355-360.
71. Zhong J, Yang XL, Yao WG, Lee WH. 2006. Lithium protects ethanol-induced neuronal apoptosis. Biochem Biophys Res Commun. 350:905-910.