Gestational ethanol exposure alters the behavioral response to ethanol odor and the expression of neurotransmission genes in the olfactory bulb of adolescent rats

Brain Research

Volumn 1252, Issue , 2009, Pages 105-116

  Middleton, Frank A ^a,b   Carrierfenster, Kellyn ^a,b   Mooney, Sandra M ^a,b   Youngentob, Steven L ^a,b  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Fetal ethanol exposure; Gene expression; Odor preference; Olfactory bulb

Indexed keywords

ALCOHOL;

ADOLESCENCE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FATE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GESTATION PERIOD; INFANCY; MALE; MATERNAL NUTRITION; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER; NERVE FIBER GROWTH; NEUROTRANSMISSION; NONHUMAN; ODOR; OLFACTORY BULB; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; SNIFFING; SYNAPTIC TRANSMISSION;

ALCOHOL DRINKING; ANIMALS; BEHAVIOR, ANIMAL; ETHANOL; FEMALE; FETUS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; MALE; MICROARRAY ANALYSIS; MOTHERS; ODORS; OLFACTORY BULB; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, LONG-EVANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SMELL; SYNAPTIC TRANSMISSION;

ANIMALIA; RATTUS; RODENTIA;

EID: 58549105690     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.11.023     Document Type: Article

References (81)

1. Abate P., Pepino M.Y., Dominguez H.D., Spear N.E., and Molina J.C. Fetal associative learning mediated through maternal alcohol intoxication. Alcohol: Clin. Exp. Res. 24 (2000) 39-47
2. Abate P., Spear N.E., and Molina J.C. Fetal and infantile alcohol-mediated associative learning in the rat. Alcohol: Clin. Exp. Res. 25 (2001) 989-998
3. Abel E.L., and York J.L. Absence of effect of prenatal ethanol on adult emotionality and ethanol consumption in rats. J. Stud. Alcohol 40 (1979) 547-553
4. Alati R., AlMamum A., Williams G.M., O, Callagham M., Najman J.M., and Bor W. In utero alcohol exposure and prediction of alcohol disorders in early adulthood: a birth cohort study. Arch. Gen. Psych. 63 (2006) 1009-1016
5. Arias C., and Chotro M.G. Increased preference for ethanol in the infant rat after prenatal ethanol exposure, expressed on intake and taste reactivity tests. Alcoholism: Clin. Exp. Res. 29 (2005) 337-346
6. Baer J.S., Sampson P.D., Barr H.M., Conner P.D., and Streissguth A.P. A 21-year longitudinal analysis of the effects of prenatal alcohol exposure on young adult drinking. Arch. Gen. Psych. 60 (2003) 377-386
7. Baer J.S., Barr H.M., Bookstein F.L., Sampson P.D., and Streissguth A.P. Prenatal alcohol exposure and family history of alcoholism in the etiology of adolescent alcohol problems. J. Stud. Alcohol 59 (1998) 533-543
8. Barron S., and Riley E.P. The effects of prenatal alcohol exposure on behavioral and neuroanatomical components of olfaction. Neurotoxicol. Teratol. 14 (1992) 291-297
9. Bond N.W., and Di Giusto E.L. Effects of prenatal alcohol consumption on open-field behaviour and alcohol preference in rats. Psychopharmacology 46 (1976) 163-165
10. Bonthius D.J., and West J.R. Acute and long-term neuronal deficits in the rat olfactory bulb following alcohol exposure during the brain growth spurt. Neurotoxicol. Teratol. 13 (1991) 611-619
11. Bonthius D.J., Bonthius N.E., Napper R.M., and West J.R. Early postnatal alcohol exposure acutely and permanently reduces the number of granule cells and mitral cells in the rat olfactory bulb: a stereological study. J. Comp. Neurol. 324 (1992) 557-566
12. Brennan P.A., and Keverne E.B. Neural mechanisms of mammalian olfactory learning. Prog. Neurobiol. 51 (1997) 457-481
13. Chotro M.G., and Arias C. Prenatal exposure to ethanol increases ethanol consumption: a conditioned response?. Alcohol 30 (2003) 19-28
14. Chotro M.G., and Molina J.C. Acute ethanol contamination of the amniotic fluid during gestational day 21: postnatal changes in alcohol responsiveness in rats. Dev. Psychobiol. 23 (1990) 535-547
15. Chotro M.G., and Molina J.C. Bradycardiac responses elicited by alcohol odor in rat neonates: Influence of in utero experience with ethanol. Psychopharmacology (Berl) 106 (1992) 491-496
16. Chotro M.G., Kraebel K.S., McKinzie D.L., Molina J.C., and Spear N. Prenatal and postnatal ethanol exposure influences preweanling rats' behavioral and autonomic responding to ethanol odor. Alcohol 13 (1996) 377-385
17. Chotro M.G., Arias C., and Laviola G. Increased ethanol intake after prenatal ethanol exposure: studies with animals. Neurosci. Biobehav. Rev. 31 (2007) 181-191
18. Coopersmith R., and Leon M. Enhanced neural response to familiar olfactory cues. Science 225 (1984) 849-851
19. Coopersmith R., and Leon M. Enhanced neural response by adult rats to odors experienced early in life. Brain Res. 371 (1986) 400-403
20. Coopersmith R., Henderson S.R., and Leon M. Odor specificity of the enhanced neural response following early odor experience in rats. Brain Res. 392 (1986) 191-197
21. Cowell R.M., Blake K.R., and Russell J.W. Localization of the transcriptional coactivator PGC-1alpha to GABAergic neurons during maturation of the rat brain. J. Comp. Neurol. 502 (2007) 1-18
22. Dominguez H.D., Chotro M.G., and Molina J.C. Alcohol in the amniotic fluid prior to cesarean delivery: effects of subsequent exposure to the drug's odor upon alcohol responsiveness. Behav. Neural Biol. 60 (1993) 129-138
23. Driscoll C.D., Streissguth A.P., and Riley E.P. Prenatal alcohol exposure: comparability of effects in humans and animal models. Neurotoxicol. Teratol. 12 (1990) 231-237
24. Ennis M., Zimmer L.A., and Shipley M.T. Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. Neuroreport 7 (1996) 989-992
25. Ennis M., Zhou F.M., Ciombor K.J., Aroniadou-Anderjaska V., Hayar A., Borrelli E., Zimmer L.A., Margolis F., and Shipley M.T. Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. J. Neurophysiol. 86 (2001) 2173-2182
26. Faas A.E., Sponton E.D., Moya P.R., and Molina J.C. Differential responsiveness to alcohol odor in human neonates: effects of maternal consumption during gestation. Alcohol 22 (2000) 7-17
27. Farbman A.I. Developmental neurobiology of the olfactory system. In: Getchell T.V. (Ed). Smell and Taste in Health and Disease (1991), Raven Press, New York 19-33
28. Fernandez-Vidal J.M., and Molina J.C. Socially mediated alcohol preferences in adolescent rats following interactions with an intoxicated peer. Pharmacol. Biochem. Behav. 79 (2004) 229-241
29. Gervais R., and Pager J. Olfactory bulb excitability selectively modified in behaving rats after local 6-hydroxydopamine treatment. Behav. Brain Res. 9 (1983) 165-179
30. Gervais R., Holley A., and Keverne B. The importance of central noradrenergic influences on the olfactory bulb in the processing of learned olfactory cues. Chem. Senses 13 (1988) 1-12
31. Gesteland R.C., Yancey R.A., and Farbman A.I. Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience 7 (1982) 3127-3136
32. Handschin C., and Spiegelman B.M. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocrine Rev. 27 (2006) 728-735
33. Hayar A., Heyward P.M., Heinbockel T., Shipley M.T., and Ennis M. Direct excitation of mitral cells via activation of alpha1-noradrenergic receptors in rat olfactory bulb slices. J. Neurophysiol. 86 (2001) 2173-2182
34. Hinds J.W., and McNelly N.A. Aging of the rat olfactory bulb: growth and atrophy of constituent layers and changes in size and number of mitral cells. J. Comp. Neurol. 171 (1977) 345-368
35. Hinds J.W., and McNelly N.A. Aging in the rat olfactory system: correlation of changes in the olfactory epithelium and olfactory bulb. J. Comp. Neurol. 203 (1981) 441-453
36. Hudson R. From molecule to mind: the role of experience in shaping olfactory function. J. Comp. Physiol. A. 185 (1999) 297-304
37. Ikonomidou C., Bittigau P., Ishimaru M.J., Wozniak D.F., Koch C., Genz K., Price M.T., Stefovska V., Hörster F., Tenkova T., Dikranian K., and Olney J.W. Ethanol-Induced Apoptotic Neurodegeneration and Fetal Alcohol Syndrome. Science 287 (2000) 1056-1060
38. Isaacson J.S., and Strowbridge B.W. Olfactory reciprocal synapses: Dendritic signaling in the CNS. Neuron 20 (1998) 749-761
39. Kosaka T., Hataguchi Y., Hama K., Nagatsu I., and Wu J.Y. Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine. Brain Res. 343 (1985) 166-171
40. Kosaka T., Kosaka K., Heizmann C.W., Nagatsu I., Wu J.Y., Yanaihara N., and Hama K. An aspect of organization of the GABAergic system in the rat main olfactory bulb: laminar distribution of immunohistochemsitry defined subpopulations of GABAergic neurons. Brain Res. 411 (1987) 373-378
41. Laing D.G., and Panhuber H. Olfactory sensitivity of rats reared in an odorous or deodorized environment. Physiol. Behav. 25 (1980) 555-558
42. Laing D.G., Panhuber H., Pittman E.A., Willcox M.E., and Eagleson G.K. Prolonged exposure to an odor or deodorized air alters the size of mitral cells in the olfactory bulb. Brain Res. 336 (1985) 81-87
43. Leshchyns ka I., Sytnyk V., Morrow J.S., and Schachner M. Neural cell adhesion molecule (NCAM) association with PKCbeta2 via betaI spectrin is implicated in NCAM-mediated neurite outgrowth. J. Cell Biol. 161 (2003) 625-639
44. McGivern R.F., Clancy A.N., Mousa S., Couri D., and Noble E.P. Prenatal alcohol exposure alters enkephalin levels, without affecting ethanol preference. Life Sci. 34 (1984) 585-589
45. McLean J.H., and Harley C.W. Olfactory learning in the rat pup: a model that may permit visualization of a mammalian memory trace. Neuroreport 15 (2004) 1691-1697
46. McLean J.H., Harley C.W., Darby-King A., and Yuan Q. pCREB in the neonate rat olfactory bulb is selectively and transiently increased by odor preference-conditioned training. Learn Mem. 6 (1999) 608-618
47. Mennella J.A. The transfer of alcohol to human milk: sensory implications and effects on mother-infant interaction. In: Hannigan J.H., Spear L.P., Spear N.E., and Goodlett C.R. (Eds). Alcohol: Effects in Brain and Development (1999), Erlbaum, Mahwah, NJ 177-198
48. Mennella J.A. Regulation of milk intake after exposure to alcohol in mothers' milk. Alcoholism: Clin. Exp. Res. 25 (2001) 590-593
49. Mennella J.A., and Beauchamp G.K. Infants' exploration of scented toys: effects of prior experiences. Chem. Senses 23 (1998) 11-17
50. Miller M.W. Circadian rhythm of cell proliferation in the telencephalic ventricular zone: effect of in utero exposure to ethanol. Brain Res. 595 (1992) 17-24
51. Molina J.C., Chotro M.G., and Dominguez H.D. Fetal alcohol learning resulting from alcohol contamination of the prenatal environment. In: Lecanuet J., Fifer W.P., Krasnegor N.A., and Smotherman W.P. (Eds). Fetal Development: A Psychobiological Perspective (1995), Erlbaum, Hillsdale, NJ 419-438
52. Molina J.C., Dominguez H.D., Lopez M.F., Pepino M.Y., and Faas A.E. The role of fetal and infantile experience with alcohol in later recognition and acceptance patterns of the drug. In: Hannigan J.H., Spear L.P., Spear N.E., and Goodlett C.R. (Eds). Alcohol: Effects on Brain and Development (1999), Erlbaum, Mahwah, NJ 199-228
53. Molina J.C., Spear N.E., Spear L.P., Mennella J.A., and Lewis M.J. Alcohol and development: beyond fetal alcohol syndrome. Dev. Psychobiol. 49 (2007) 227-242
54. Nicoll R.A. Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res. 35 (1971) 137-149
55. Nyquist-Battie C., and Gochee A. Alterations in the development of the mouse after ethanol exposure. Int. J. Dev. Neurosci. 3 (1985) 211-222
56. Olney J.W., Wozniak D.F., Jevtovic-Todorovic V., Farber N.B., Bittigau P., and Ikonomidou C. Glutamate and GABA receptor dysfunction in the fetal alcohol syndrome. Neurotoxicol. Res. 4 (2002) 315-325
57. Panhuber H., and Laing D.G. The size of mitral cells is altered when rats are exposed to an odor from their day of birth. Brain Res. 431 (1987) 133-140
58. Panhuber H., Mackay-Sim A., and Laing D.G. Prolonged odor exposure causes severe cell shrinkage in the adult rat olfactory bulb. Brain Res. 428 (1987) 307-311
59. Phillips D., and Stainbrook G. Effects of early alcohol exposure upon adult learning abilities and taste preferences. Physiol. Psychol. 4 (1976) 473-475
60. Rehn B., Panhuber H., Laing D.G., and Breipohl W. Spine density on olfactory granule cell dendrites is reduced in rats reared in a restricted olfactory environment. Brain Res. 468 (1988) 143-147
61. Riback C.E., Vaughn J.E., Saito K., Barber R., and Roberts E. Glutamate decarboxylase localization in neurons of the olfactory bulb. Brain Res. 126 (1977) 1-18
62. Schevzov G., Gunning P., Jeffrey P.L., Temm-Grove C., Helfman D.M., Lin J.J., and Weinberger R.P. Tropomyosin localization reveals distinct populations of microfilaments in neurites and growth cones. Mol. Cell. Neurosci. 8 (1997) 439-454
63. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24 (2000) 417-463
64. Spear N.E., and Molina J.C. Consequences of early exposure to alcohol: how animal studies reveal later patterns of use and abuse in humans. In: Carroll M., and Overmier B. (Eds). Animal Research and Human Health (2001), APA, Washington DC 85-99
65. Spear N.E., and Molina J.C. Fetal or infantile exposure to ethanol promotes ethanol ingestion in adolescence and adulthood. Alcoholism: Clin. Exp. Res. 29 (2005) 909-929
66. Streissguth, A., 1998. Teratogenic and genetic influences on adolescent and adult alcohol use and abuse. Symposium presented at the annual meeting of the Research Society on Alcoholism, Hilton Head, SC.
67. Sulik K.K., and Johnston M.C. Sequence of developmental alterations following acute ethanol exposure in mice: craniofacial features of the fetal alcohol syndrome. Am. J. Anat. 166 (1983) 257-269
68. Sullivan R.M., Wilson D.A., and Leon M. Norepinephrine and learning-induced plasticity in infant rat olfactory system. J. Neurosci. 9 (1989) 3998-4006
69. Tabuchi K., Biederer T., Butz S., and Sudhof T. CASK participates in alternative tripartite complexes in which mint 1 competes for binding with caskin 1, a novel CASK-binding protein. J. Neurosci. 22 (2002) 4264-4273
70. Vavrousek-Jakuba E.M., Baker R.A., and Shoemaker W.J. Effect of ethanol on maternal and offspring characteristics: comparison of three liquid diet formulations fed during gestation.[erratum appears in Alcoholism: Clin. Exp. Res. 1992,16, 479]. Alcoholism: Clin. Exp. Res. 15 (1991) 129-135
71. Wilson D.A., and Leon M. Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. J. Neurophysiol. 59 (1988) 1770-1782
72. Wilson D.A., and Leon M. Noradrenergic modulation of olfactory bulb exicitability in the postnatal rat. Dev. Brain Res. 42 (1988) 69-75
73. Wilson D.A., and Sullivan R.M. Neurobiology of associative learning in the neonate: early olfactory learning. Behav. Neural. Biol. 61 (1994) 1-18
74. Yates W.R., Cadoret R.J., Troughton E.P., Stewart M., and Giunta T.S. Effect of fetal alcohol exposure on adult symptoms of nicotine, alcohol, and drug dependence. Alcoholism: Clin. Exp. Res. 22 (1998) 914-920
75. Young W.S., and Kuhar M.J. Noradrenergic alpha 1 and alpha 2 receptors: light microscopic autoradiographic localization. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 1696-1700
76. Youngentob S.L. A method for the rapid automated assessment of olfactory function. Chem. Senses 30 (2005) 219-229
77. Youngentob S.L., Mozell M.M., Sheehe P.R., and Hornung D.E. A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol. Behav. 41 (1987) 59-69
78. Youngentob S.L., Kent P.F., Sheehe P.R., Molina J.C., Spear N.E., and Youngentob L.M. Experience-induced fetal plasticity: the effect of gestational ethanol exposure on the behavioral and neurophysiologic olfactory response to ethanol odor in early postnatal and adult rats. Behav. Neurosci. 121 (2007) 1293-1305
79. Youngentob S.L., Molina J.C., Kent P.F., Spear N.E., and Youngentob L.M. The effect of gestational ethanol exposure on voluntary ethanol intake in early postnatal and adult rats. Behav. Neurosci. 121 (2007) 1306-1315
80. Yuan Q., Harley C.W., McLean J.H., and Knopfel T. Optical imaging of odor preference memory in the rat olfactory bulb. J. Neurophysiol. 87 (2002) 3156-3159
81. Yuan Q., Harley C.W., and McLean J.H. Mitral cell beta1 and 5-HT2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. Learn. Mem. 10 (2003) 5-15