Distinct neurobehavioral dysfunction based on the timing of developmental binge-like alcohol exposure

Neuroscience

Volumn 280, Issue , 2014, Pages 204-219

  Sadrian, B ^a,b   Lopez Guzman, M ^b   Wilson, D A ^a,b   Saito, M ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

Author keywords

FASD; Hippocampus; Neural circuit development; Parvalbumin; Piriform

Indexed keywords

ALCOHOL; PARVALBUMIN; CENTRAL DEPRESSANT AGENT;

ADULT; ALCOHOL CONSUMPTION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINGE DRINKING; BRAIN REGION; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; FEMALE; FETAL ALCOHOL SYNDROME; HIPPOCAMPUS; IN VIVO STUDY; INTERNEURON; LONG TERM MEMORY; MALE; MOUSE; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SPATIAL MEMORY; ANIMAL; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; MEMORY DISORDER; NERVE TRACT; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SMELLING;

ANIMALS; ANIMALS, NEWBORN; BINGE DRINKING; BRAIN; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DISEASE MODELS, ANIMAL; ETHANOL; FEMALE; INTERNEURONS; MALE; MEMORY DISORDERS; MICE, INBRED C57BL; NEURAL PATHWAYS; NEUROGENESIS; OLFACTORY PERCEPTION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SPATIAL MEMORY;

EID: 84929381980     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.09.008     Document Type: Article

References (100)

1. Abel E.L. Fetal alcohol syndrome: the 'American Paradox'. Alcohol Alcohol 1998, 33:195-201.
2. Alonso M., Lepousez G., Sebastien W., Bardy C., Gabellec M.M., Torquet N., Lledo P.M. Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 2012, 15:897-904.
3. Balaszczuk V., Bender C., Pereno G.L., Beltramino C.A. Alcohol-induced neuronal death in central extended amygdala and pyriform cortex during the postnatal period of the rat. Int J Dev Neurosci 2011, 29:733-742.
4. Bekkers J.M., Suzuki N. Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci 2013, 36:429-438.
5. Belnoue L., Grosjean N., Ladeveze E., Abrous D.N., Koehl M. Prenatal stress inhibits hippocampal neurogenesis but spares olfactory bulb neurogenesis. PLoS One 2013, 8:e72972.
6. Best A.R., Wilson D.A. Coordinate synaptic mechanisms contributing to olfactory cortical adaptation. J Neurosci 2004, 24:652-660.
7. Bevelier D., Levi D., Li R.W., Dan Y., Hensch T.K. Removing brakes on adult plasticity: from the molecular level to behavioral interventions. J Neurosci 2010, 45:14964-14971.
8. Bonthius D.J., West J.R. Acute and long-term neuronal deficits in the rat olfactory bulb following alcohol exposure during the brain growth spurt. Neurotoxicol Teratol 1991, 13:611-619.
9. Brown J., Cooper-Kuhn C.M., Kempermann G., Van Praag H., Winkler J., Gage F.H., Kuhn H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 2003, 17:2042-2046.
10. Brunjes P.C. Unilateral naris closure and olfactory system development. Brain Res Brain Res Rev 1994, 19:146-160.
11. Burd L., Blair J., Dropps K. Prenatal alcohol exposure, blood alcohol concentrations and alcohol elimination rates for the mother, fetus and newborn. J Perinatol 2012, 32:652-659.
12. Buzsaki G., Draguhn A. Neuronal oscillations in cortical networks. Science 2004, 304:1926-1929.
13. Buzsaki G., Kaila K., Raichle M. Inhibition and brain work. Neuron 2007, 56:771-783.
14. Cardin J.A., Carlen M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
15. Chakraborty G., Saito M., Mao R.F., Wang R., Vadasz C. Lithium blocks ethanol-induced modulation of protein kinases in the developing brain. Biochem Biophys Res Commun 2008, 367:597-602.
16. Clancy B., Finlay B.L., Darlington R.B., Anand K.J. Extrapolating brain development from experimental species to humans. Neurotoxicology 2007, 28:931-937.
17. Coleman L.G., Oguz I., Lee J., Styner M., Crews F.T. Postnatal day 7 ethanol treatment causes persistent reductions in adult mouse brain volume and cortical neurons with sex specific effects on neurogenesis. Alcohol 2012, 46:603-612.
18. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
19. Cudd T.A. Animal model systems for the study of alcohol teratology. Exp Biol Med (Maywood) 2005, 230:389-393.
20. De Giorgio A., Comparini S.E., Intra F.S., Granato A. Long-term alterations of striatal parvalbumin interneurons in a rat model of early exposure to alcohol. J Neurodev Disord 2012, 4:18.
21. Deng W., Aimone J.B., Gage F.H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat Rev Neurosci 2010, 11:339-350.
22. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979, 3:79-83.
23. Dunty W.C., Chen S.Y., Zucker R.M., Dehart D.B., Sulik K.K. Selective vulnerability of embryonic cell populations to ethanol-induced apoptosis: implications for alcohol-related birth defects and neurodevelopmental disorder. Alcohol Clin Exp Res 2001, 25:1523-1535.
24. Ehlers C.L., Oguz I., Budin F., Wills D.N., Crews F.T. Peri-adolescent ethanol vapor exposure produces reductions in hippocampal volume that are correlated with deficits in prepulse inhibition of the startle. Alcohol Clin Exp Res 2013, 37:1466-1475.
25. Franks K.M., Isaacson J.S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 2006, 49:357-363.
26. Freeman J.H., Barone S., Stanton M.E. Cognitive and neuroanatomical effects of triethyltin in developing rats: role of age of exposure. Brain Res 1994, 634:85-95.
27. Galindo R., Zamudio P.A., Valenzuela C.F. Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J Neurochem 2005, 94:1500-1511.
28. Gohlke J.M., Griffith W.C., Faustman E.M. A systems-based computational model for dose-response comparisons of two mode of action hypotheses for ethanol-induced neurodevelopmental toxicity. Toxicol Sci 2005, 86:470-484.
29. Gould E., Beylin A., Tanapat P., Reeves A., Shors T.J. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999, 2:260-265.
30. Greicius M. Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol 2008, 21:424-430.
31. Harris K.R., Bucens I.K. Prevalence of fetal alcohol syndrome in the Top End of the Northern Territory. J Paediatr Child Health 2003, 39:528-533.
32. Hensch T.K. Critical period mechanisms in developing visual cortex. Curr Top Dev Biol 2005, 69:215-237.
33. Hoekzema E., Carmona S., Ramos-Quiroga J.A., Richarte Fernandez V., Bosch R., Soliva J.C., Rovira M., Bulbena A., Tobena A., Casas M., Vilarroya O. An independent components and functional connectivity analysis of resting state fMRI data points to neural network dysregulation in adult ADHD. Hum Brain Mapp 2013.
34. Ikonomidou C., Bittigau P., Ishimaru M.J., Wozniak D.F., Koch C., Genz K., Price M.T., Stefovska V., Horster F., Tenkova T., Dikranian K., Olney J.W. Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science 2000, 287:1056-1060.
35. Isayama R.N., Leite P.E., Lima J.P., Uziel D., Yamasaki E.N. Impact of ethanol on the developing GABAergic system. Anat Rec (Hoboken) 2009, 292:1922-1939.
36. Izumi Y., Kitabayashi R., Funatsu M., Izumi M., Yuede C., Hartman R.E., Wozniak D.F., Zorumski C.F. A single day of ethanol exposure during development has persistent effects on bi-directional plasticity, N-methyl-D-aspartate receptor function and ethanol sensitivity. Neuroscience 2005, 136:269-279.
37. Ketchum K.L., Haberly L.B. Membrane currents evoked by afferent fiber stimulation in rat piriform cortex. I. Current source-density analysis. J Neurophysiol 1993, 69:248-260.
38. Klintsova A.Y., Helfer J.L., Calizo L.H., Dong W.K., Goodlett C.R., Greenough W.T. Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol Clin Exp Res 2007, 31:2073-2082.
39. Komitova M., Xenos D., Salmaso N., May Tran K., Brand T., Schwartz M.L., Ment L., Vaccarino F.M. Hypoxia-induced developmental delays of inhibitory interneurons are reversed by environmental enrichment in the postnatal mouse forebrain. J Neurosci 2013, 33:13375-13387.
40. Leasure J.L., Nixon K. Exercise neuroprotection in a rat model of binge alcohol consumption. Alcohol Clin Exp Res 2010, 34:404-414.
41. Leuner B., Gould E., Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 2006, 16:216-224.
42. Lledo P.M., Alonso M., Grubb M.S. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 2006, 7:179-193.
43. Lledo P.M., Saghatelyan A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci 2005, 28:248-254.
44. Lowry C.A., Kay L.M. Chemical factors determine olfactory system beta oscillations in waking rats. J Neurophysiol 2007, 98:394-404.
45. Luine V.N., Jacome L.F., Maclusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 2003, 144:2836-2844.
46. Macbeth A.H., Gautreaux C., Luine V.N. Pregnant rats show enhanced spatial memory, decreased anxiety, and altered levels of monoaminergic neurotransmitters. Brain Res 2008, 1241:136-147.
47. Maier S.E., Chen W.J., Miller J.A., West J.R. Fetal alcohol exposure and temporal vulnerability regional differences in alcohol-induced microencephaly as a function of the timing of binge-like alcohol exposure during rat brain development. Alcohol Clin Exp Res 1997, 21:1418-1428.
48. Mandairon N., Jourdan F., Didier A. Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 2003, 119:507-516.
49. Martin C., Beshel J., Kay L.M. An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J Neurophysiol 2007, 98:2196-2205.
50. Martin C., Ravel N. Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks?. Front Behav Neurosci 2014, 8:218.
51. May P.A., Fiorentino D., Coriale G., Kalberg W.O., Hoyme H.E., Aragon A.S., Buckley D., Stellavato C., Gossage J.P., Robinson L.K., Jones K.L., Manning M., Ceccanti M. Prevalence of children with severe fetal alcohol spectrum disorders in communities near Rome, Italy: new estimated rates are higher than previous estimates. Int J Environ Res Public Health 2011, 8:2331-2351.
52. May P.A., Gossage J.P. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res Health 2001, 25:159-167.
53. May P.A., Gossage J.P. Maternal risk factors for fetal alcohol spectrum disorders: not as simple as it might seem. Alcohol Res Health 2011, 34:15-26.
54. Miller S.S., Spear N.E. Olfactory learning in the rat immediately after birth: unique salience of first odors. Dev Psychobiol 2009, 51:488-504.
55. Mitchell J.J., Paiva M., Heaton M.B. Effect of neonatal ethanol exposure on parvalbumin-expressing GABAergic neurons of the rat medial septum and cingulate cortex. Alcohol 2000, 21:49-57.
56. Moriceau S., Sullivan R.M. Unique neural circuitry for neonatal olfactory learning. J Neurosci 2004, 24:1182-1189.
57. Neville K.R., Haberly L.B. The synaptic organization of the brain 2004, Oxford University Press, Oxford; New York.
58. Nixon K., Hughes P.D., Amsel A., Leslie S.W. NMDA receptor subunit expression following early postnatal exposure to ethanol. Brain Res Dev Brain Res 2002, 139:295-299.
59. Nunes F., Ferreira-Rosa K., Pereira Mdos S., Kubrusly R.C., Manhaes A.C., Abreu-Villaca Y., Filgueiras C.C. Acute administration of vinpocetine, a phosphodiesterase type 1 inhibitor, ameliorates hyperactivity in a mice model of fetal alcohol spectrum disorder. Drug Alcohol Depend 2011, 119:81-87.
60. O'Leary C.M., Nassar N., Kurinczuk J.J., de Klerk N., Geelhoed E., Elliott E.J., Bower C. Prenatal alcohol exposure and risk of birth defects. Pediatrics 2010, 126:e843-e850.
61. Olney J.W., Tenkova T., Dikranian K., Qin Y.Q., Labruyere J., Ikonomidou C. Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Brain Res Dev Brain Res 2002, 133:115-126.
62. Oyedele O.O., Kramer B. Acute ethanol administration causes malformations but does not affect cranial morphometry in neonatal mice. Alcohol 2008, 42:21-27.
63. Parnell S.E., O'Leary-Moore S.K., Godin E.A., Dehart D.B., Johnson B.W., Allan Johnson G., Styner M.A., Sulik K.K. Magnetic resonance microscopy defines ethanol-induced brain abnormalities in prenatal mice: effects of acute insult on gestational day 8. Alcohol Clin Exp Res 2009, 33:1001-1011.
64. Patneau D.K., Stripling J.S. Functional correlates of selective long-term potentiation in the olfactory cortex and olfactory bulb. Brain Res 1992, 585:219-228.
65. Paxinos G., Franklin K. The mouse brain in stereotaxic coordinates 2008, Academic Press, New York.
66. Paxinos G., Halliday G., Watson C., Koutcherov Y., Wang H.Q. Atlas of the developing mouse brain at E17.5, P0 and P6 2007, Academic Press, Burlington, MA.
67. Raineki C., Holman P.J., Debiec J., Bugg M., Beasley A., Sullivan R.M. Functional emergence of the hippocampus in context fear learning in infant rats. Hippocampus 2010, 20:1037-1046.
68. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 2002, 22:2679-2689.
69. Rudy J.W. Ontogeny of context-specific latent inhibition of conditioned fear: implications for configural associations theory and hippocampal formation development. Dev Psychobiol 1994, 27:367-379.
70. Sadrian B., Subbanna S., Wilson D.A., Basavarajappa B.S., Saito M. Lithium prevents long-term neural and behavioral pathology induced by early alcohol exposure. Neuroscience 2012, 206:122-135.
71. Sadrian B., Wilson D., Saito M. Long-lasting neural circuit dysfunction following developmental ethanol exposure. Brain Sci 2013, 3:704-727.
72. Sahay A., Wilson D.A., Hen R. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 2011, 70:582-588.
73. Saito M., Chakraborty G., Mao R.F., Paik S.M., Vadasz C. Tau phosphorylation and cleavage in ethanol-induced neurodegeneration in the developing mouse brain. Neurochem Res 2010, 35:651-659.
74. Saito M., Mao R.F., Wang R., Vadasz C., Saito M. Effects of gangliosides on ethanol-induced neurodegeneration in the developing mouse brain. Alcohol Clin Exp Res 2007, 31:665-674.
75. Samuels B.A., Hen R. Neurogenesis and affective disorders. Eur J Neurosci 2011, 33:1152-1159.
76. Sanderson J.L., Donald Partridge L., Valenzuela C.F. Modulation of GABAergic and glutamatergic transmission by ethanol in the developing neocortex: an in vitro test of the excessive inhibition hypothesis of fetal alcohol spectrum disorder. Neuropharmacology 2009, 56:541-555.
77. Sari Y., Hammad L.A., Saleh M.M., Rebec G.V., Mechref Y. Alteration of selective neurotransmitters in fetal brains of prenatally alcohol-treated C57BL/6 mice: quantitative analysis using liquid chromatography/tandem mass spectrometry. Int J Dev Neurosci 2010, 28:263-269.
78. Sarma A.A., Richard M.B., Greer C.A. Developmental dynamics of piriform cortex. Cereb Cortex 2011, 21:1231-1245.
79. Seeley W.W., Crawford R.K., Zhou J., Miller B.L., Greicius M.D. Neurodegenerative diseases target large-scale human brain networks. Neuron 2009, 62:42-52.
80. Segal M., Greenberger V., Israeli M., Biegon A. A correlation between regional acetylcholinesterase activity in rat brain and performance in a spatial task. Behav Brain Res 1988, 30:215-219.
81. Selby L., Zhang C., Sun Q.Q. Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci Lett 2007, 412:227-232.
82. Seress L. Comparative anatomy of the hippocampal dentate gyrus in adult and developing rodents, non-human primates and humans. Prog Brain Res 2007, 163:23-41.
83. Shirasaka T., Hashimoto E., Ukai W., Yoshinaga T., Ishii T., Tateno M., Saito T. Stem cell therapy: social recognition recovery in a FASD model. Transl Psychiatry 2012, 2:e188.
84. Spear L.P., Swartzwelder H.S. Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neurosci Biobehav Rev 2014, 45C:1-8.
85. Suzuki N., Bekkers J.M. Microcircuits mediating feedforward and feedback synaptic inhibition in the piriform cortex. J Neurosci 2012, 32:919-931.
86. Tang J., Liao Y., Song M., Gao J.H., Zhou B., Tan C., Liu T., Tang Y., Chen J., Chen X. Aberrant default mode functional connectivity in early onset schizophrenia. PLoS One 2013, 8:e71061.
87. Tran T.D., Kelly S.J. Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicol Teratol 2003, 25:519-528.
88. Tukker J.J., Fuentealba P., Hartwich K., Somogyi P., Klausberger T. Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J Neurosci 2007, 27:8184-8189.
89. Turner D.A., Buhl E.H., Hailer N.P., Nitsch R. Morphological features of the entorhinal-hippocampal connection. Prog Neurobiol 1998, 55:537-562.
90. van Groen T., Wyss J.M. Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 1990, 302:515-528.
91. Viljoen D.L., Gossage J.P., Brooke L., Adnams C.M., Jones K.L., Robinson L.K., Hoyme H.E., Snell C., Khaole N.C., Kodituwakku P., Asante K.O., Findlay R., Quinton B., Marais A.S., Kalberg W.O., May P.A. Fetal alcohol syndrome epidemiology in a South African community: a second study of a very high prevalence area. J Stud Alcohol 2005, 66:593-604.
92. Volk D.W., Lewis D.A. Prenatal ontogeny as a susceptibility period for cortical GABA neuron disturbances in schizophrenia. Neuroscience 2013, 248C:154-164.
93. Wang H., Dubois D.W., Tobery A.N., Griffith W.H., Brandt P., Frye G.D. Long-lasting distortion of GABA signaling in MS/DB neurons after binge-like ethanol exposure during initial synaptogenesis. Brain Res 2013, 1520:36-50.
94. Webster W.S., Walsh D.A., McEwen S.E., Lipson A.H. Some teratogenic properties of ethanol and acetaldehyde in C57BL/6J mice: implications for the study of the fetal alcohol syndrome. Teratology 1983, 27:231-243.
95. Wesson D.W., Borkowski A.H., Landreth G.E., Nixon R.A., Levy E., Wilson D.A. Sensory network dysfunction, behavioral impairments, and their reversibility in an Alzheimer's beta-amyloidosis mouse model. J Neurosci 2011, 31:15962-15971.
96. Whitfield-Gabrieli S., Ford J.M. Default mode network activity and connectivity in psychopathology. Annu Rev Clin Psychol 2012, 8:49-76.
97. Wilson D.A., Peterson J., Basavaraj B.S., Saito M. Local and regional network function in behaviorally relevant cortical circuits of adult mice following postnatal alcohol exposure. Alcohol Clin Exp Res 2011, 35:1974-1984.
98. Workman A.D., Charvet C.J., Clancy B., Darlington R.B., Finlay B.L. Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci 2013, 33:7368-7383.
99. Wozniak D.F., Hartman R.E., Boyle M.P., Vogt S.K., Brooks A.R., Tenkova T., Young C., Olney J.W., Muglia L.J. Apoptotic neurodegeneration induced by ethanol in neonatal mice is associated with profound learning/memory deficits in juveniles followed by progressive functional recovery in adults. Neurobiol Dis 2004, 17:403-414.
100. Young C., Olney J.W. Neuroapoptosis in the infant mouse brain triggered by a transient small increase in blood alcohol concentration. Neurobiol Dis 2006, 22:548-554.