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

Behavioral Neuroscience

Volumn 121, Issue 6, 2007, Pages 1293-1305

  Youngentob, Steven L ^a   Kent, Paul F ^a   Sheehe, Paul R ^a   Molina, Juan C ^a   Spear, Norman E ^a,b   Youngentob, Lisa M ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b BINGHAMTON UNIVERSITY   (United States)

Author keywords

ethanol odor preference; fetal ethanol exposure; olfactory plasticity; optical recordings; whole body plethysmography

Indexed keywords

ALCOHOL;

ALCOHOL ABUSE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FETUS; MALE; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; ODOR; OLFACTORY EPITHELIUM; OLFACTORY SYSTEM; PERINATAL PERIOD; PRENATAL EXPOSURE; RAT; SMELLING;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM DEPRESSANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FEMALE; MALE; NEURONAL PLASTICITY; ODORS; OLFACTORY PATHWAYS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, LONG-EVANS; REFLEX;

EID: 38149109112     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.121.6.1293     Document Type: Article

References (101)

1. Abate P., Pepino M.Y., Dominguez H.D., Spear N.E., and Molina J.C. Fetal associative learning mediated through maternal alcohol intoxication. Alcoholism: Clinical and Experimental Research 24 (2000) 39-47
2. Abate P., Spear N.E., and Molina J.C. Fetal and infantile alcohol-mediated associative learning in the rat. Alcoholism: Clinical and Experimental Research 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. Journal of Studies on Alcohol 40 (1979) 547-553
4. Alati R., Al Mamum 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. Archive of General Psychiatry 63 (2006) 1009-1016
5. Baer J.S., Bar 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. Journal of Studies on Alcohol 59 (1998) 533-543
6. Barron S., and Riley E.P. The effects of prenatal alcohol exposure on behavioral and neuroanatomical components of olfaction. Neurotoxicology and Teratology 14 (1992) 291-297
7. Bond N.W., and DiGiusto E.L. Effects of prenatal alcohol consumption on open-field behaviour and alcohol preference in rats. Psychopharmacology (Berlin) 46 (1976) 163-165
8. Chotro M.G., and Arias C. Prenatal exposure to ethanol increases ethanol consumption: A conditioned response?. Alcohol 30 (2003) 19-28
9. Chotro M.G., Cordoba N.E., and Molina J.C. Acute prenatal experience with alcohol in the amniotic fluid: Interactions with aversive and appetitive alcohol orosensory learning in the rat pup. Developmental Psychobiology 24 (1991) 431-451
10. 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
11. 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. Developmental Psychobiology 23 (1990) 535-547
12. Chotro M.G., and Molina J.C. Bradycardiac responses elicited by alcohol odor in rat neonates: Influence of in utero experience with ethanol. Psychopharmacology (Berlin) 106 (1992) 491-496
13. Chotro M.G., and Spear N.E. Repeated exposure to moderate doses of alcohol in the rat fetus: Evidence of sensitization to toxic and chemosensory aspects of alcohol. Alcoholism: Clinical and Experimental Research 21 (1997) 360-367
14. Coopersmith R., and Leon M. Enhanced neural response to familiar olfactory cues. Science 225 (1984, August 24) 849-851
15. Coopersmith R., and Leon M. Enhanced neural response by adult rats to odors experienced early in life. Brain Research 371 (1986) 400-403
16. Cunningham C.L. Drug conditioning and seeking behavior. In: O'Donohue W. (Ed). Learning and behavior therapy (1998), Allyn & Bacon, Boston 518-540
17. Cunningham C.L., Clemans J.M., and Fidler T.L. Injection timing determines whether intragastric ethanol produces conditioned place preference or aversion in mice. Pharmacology Biochemistry and Behavior 72 (2002) 659-668
18. 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. Behavioral and Neural Biology 60 (1993) 129-138
19. Dominguez H.D., Lopez M.F., and Molina J.C. Neonatal responsiveness to alcohol odor and infant alcohol intake as a function of alcohol experience during late gestation. Alcohol 16 (1998) 109-117
20. Driscoll C.D., Streissguth A.P., and Riley E.P. Prenatal alcohol exposure: Comparability of effects in human and animal models. Neurotoxicology and Teratology 12 (1990) 231-237
21. Farbman A.I. Developmental neurobiology of the olfactory system. In: Getchell T.V., Doty R., Bartoshuk L., and Snow J. (Eds). Smell and taste in health and disease (1991), Raven Press, New York 19-33
22. Gervais R., Holley A., and Keverne B. The importance of central noradrenergic influences on the olfactory bulb in the processing of learned olfactory cues. Chemical Senses 13 (1988) 1-12
23. Gervais R., and Pager J. Olfactory bulb excitability selectively modified in behaving rats after local 6-hydroxydopamine treatment. Behavioral Brain Research 9 (1983) 165-179
24. 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
25. Ghosh A., Carnahan J., and Greenberg M.E. Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263 (1994, March 18) 1618-1623
26. Gottlieb G. Ontogenesis of sensory function in birds and mammals. In: Tobach E., Aronson L.R., and Shaw E. (Eds). The biopsychology of development (1971), Academic Press, New York 67-128
27. Holson R.R., and Pearce B. Principles and pitfalls in the analysis of prenatal treatment effects in multiparious species. Neurotoxicology and Teratology 14 (1992) 221-228
28. Hudson R. Olfactory imprinting. Current Opinion in Neurobiology 7 (1993) 548-552
29. Hudson R. From molecule to mind: The role of experience in shaping olfactory function. Journal of Comparative Physiology 185 (1999) 297-304
30. Hudson R., and Distel H. Induced peripheral sensitivity in the developing vertebrate olfactory system. In: Murphy C. (Ed). Annals of the New York Academy of Sciences: Vol. 855. Olfaction and Taste XII-An international symposium (1998), New York Academy of Sciences, New York 109-115
31. Iwema C.L., Fang H., Kurtz D.B., Youngentob S.L., and Schwob J.E. Odorant receptor expression patterns are restored in lesion-recovered rat olfactory epithelium. Journal of Neuroscience 24 (2004) 356-369
32. Johnson B.A., Woo C.C., Duong H., Nguyen V., and Leon M. A learned odor evokes an enhanced Fos-like glomerular response in the olfactory bulb of young rats. Brain Research 699 (1995) 192-200
33. Katz L.C., and Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 274 (1996, November 15) 1133-1138
34. Kauer J.S., and Moulton D.G. Response of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander. Journal of Physiology 243 (1974) 717-737
35. Kent P.F., and Mozell M.M. The recording of odorant-induced mucosal activity patterns with a voltage-sensitive dye. Journal of Neurophysiology 68 (1992) 1804-1819
36. Kent P.F., Mozell M.M., Youngentob S.L., and Yurco P. Mucosal activity patterns as a basis for olfactory discrimination: Comparing behavior and optical recordings. Brain Research 981 (2003) 1-11
37. Kent P.F., Youngentob S.L., and Sheehe P.R. Odorant-specific spatial patterns in mucosal activity predict perceptual differences among odorants. Journal of Neurophysiology 74 (1995) 1777-1781
38. Laing D.G., and Panhuber H. Neural and behavioral changes in rats following continuous exposure to an odor. Journal of Comparative Physiology 124 (1978) 259-265
39. Laing D.G., and Panhuber H. Olfactory sensitivity of rats reared in an odorous or deodorized environment. Physiology & Behavior 25 (1980) 555-558
40. LeVay S., Wiesel T.N., and Hubel D.H. The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191 (1980) 1-51
41. Loo A.T., Youngentob S.L., Kent P.F., and Schwob J.E. The aging olfactory epithelium: Neurogenesis, response to damage and odorant-induced activity. International Journal of Developmental Neuroscience 14 (1996) 881-900
42. MacKay-Sim A., and Kesteven S. Topographic patterns of responsiveness to odorants in the rat olfactory epithelium. Journal of Neurophysiology 71 (1994) 150-160
43. MacKay-Sim A., and Shaman P. Topographic coding of odorant quality is maintained at different concentrations in the salamander olfactory epithelium. Brain Research 297 (1984) 207-217
44. McCollum J.F., Woo C.C., and Leon M. Granule and mitral cell densities are unchanged following early olfactory preference training. Developmental Brain Research 99 (1997) 118-120
45. 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 Science 34 (1984) 585-589
46. 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
47. Miller M.W. Development of the central nervous system: Effects of alcohol and opiates (1992), Wiley-Liss, New York
48. Molina J.C., Chotro M.G., and Dominguez H.D. Fetal alcohol learning resulting from alcohol contamination of the prenatal environment. In: Lecanuet J.P., Fifer W.P., Krasnegor N.A., and Smotherman W.P. (Eds). Fetal development: A psychological perspective (1995), Erlbaum, Hillsdale, NJ 419-438
49. Molina J.C., Ponce L.F., Truxell E., and Spear N.E. Infantile sensitivity to ethanol's motivational effects: Ethanol reinforcement during the third postnatal week. Alcoholism: Clinical and Experimental Research 30 (2006) 1509-1519
50. Molina J.C., Spear N.E., Spear L.P., Mennella J.A., and Lewis M.J. Alcohol and development: Beyond fetal alcohol syndrome. Developmental Psychobiology 49 (2007) 227-242
51. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., et al. Visualizing an olfactory sensory map. Cell 87 (1996) 675-686
52. Morrison D.F. Multivariate statistical methods (1967), McGraw-Hill, New York
53. Mozell M.M., Sheehe P.R., Swieck S.W., Kurtz D.B., and Hornung D.E. A parametric study of the stimulation variables affecting the magnitude of the olfactory nerve response. Journal of General Physiology 83 (1984) 233-267
54. Pedersen P.E., and Blass E.M. Prenatal and postnatal determinants of the 1st suckling episode in albino rats. Developmental Psychobiology 15 (1982) 349-355
55. Phillips D.S., and Stainbrook G.L. Effects of early alcohol exposure upon adult learning abilities and taste preferences. Physiological Psychology 4 (1976) 473-475
56. Randall C.L., Hughs S.S., Williams C.K., and Anton R.F. Effect of prenatal alcohol on consumption of alcohol and alcohol-induced sleep time in mice. Pharmacology Biochemistry and Behavior 18 (1983) 325-329
57. Reyes E., Garcia K.D., and Jones B.C. Effects of the maternal consumption of alcohol on alcohol selection in rats. Alcohol 2 (1985) 323-326
58. Rochefort C., Gheusi G., Vincent J.D., and Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. Journal of Neuroscience 22 (2002) 2679-2689
59. Salcedo E., Zhang C., Kronberg E., and Restrepo D. Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb. Chemical Senses 30 (2005) 615-626
60. Schaal B., Marlier L., and Soussignan R. Human fetuses learn odors from their pregnant mother's diet. Chemical Senses 25 (2000) 729-737
61. Schaal B., and Orgeur P. Olfaction in utero: Can the rodent model be generalized?. Quarterly Journal of Experimental Psychology: Journal of Comparative and Physiological Psychology 44 B (1992) 245-278
62. Semke E., Distel H., and Hudson R. Specific enhancement of olfactory receptor sensitivity associated with fetal learning of food odors in the rabbit. Naturwissenschaften 82 (1995) 148-149
63. Shepherd G.M. Computational structure of the olfactory system. In: Davis J.L., and Eichenbaum H. (Eds). Olfaction: A model system for computational neuroscience (1991), MIT Press, Cambridge, MA 3-42
64. Smotherman W.P. In utero chemosensory experience alters taste preferences and corticosterone responsiveness. Behavioral and Neural Biology 36 (1982) 61-68
65. Smotherman W.P. Odor aversion learning by the rat fetus. Physiology & Behavior 29 (1982) 769-771
66. Smotherman W.P., and Robinson S.R. The rat fetus in its environment: Behavioral adjustments to novel, familiar, aversive, and conditioned stimuli presented in utero. Behavioral Neuroscience 99 (1985) 521-530
67. Smotherman W.P., and Robinson S.R. Psychobiology of fetal experience in the rat. In: Krasnegor N.A., Blass E.M., Hofer M.A., and Smotherman W.P. (Eds). Perinatal development: A psychobiological perspective (1987), Academic Press, Orlando, FL 39-60
68. Smotherman W.P., and Robinson S.R. Behavior of rat fetuses following chemical or tactile stimulation. Behavioral Neuroscience 102 (1988) 24-34
69. Smotherman W.P., and Robinson S.R. Rat fetuses respond to chemical stimuli in gas phase. Physiology & Behavior 47 (1990) 863-868
70. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neuroscience & Biobehavioral Reviews 24 (2000) 417-463
71. Spear L.P., and Brake S.C. Periadolescence: Age-dependent behavior and psychopharmacological responsivity in rats. Developmental Psychobiology 16 (1983) 83-109
72. Spear N.E., and Molina J.C. Fetal or infantile exposure to ethanol promotes ethanol ingestion in adolescence and adulthood: A theoretical review. Alcoholism: Clinical and Experimental Research 29 (2005) 909-929
73. Stickrod G., Kimble D.P., and Smotherman W.P. In utero taste/odor aversion conditioning in the rat. Physiology & Behavior 28 (1982) 5-7
74. Streissguth, A. (1998, June). 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.
75. Sulik K.K., and Johnston M.C. Sequence of developmental alterations following acute ethanol exposure in mice: Craniofacial features of the fetal alcohol syndrome. American Journal of Anatomy 166 (1983) 257-259
76. Sullivan R.M., and Leon M. Early olfactory learning induces an enhanced olfactory bulb response in young rats. Brain Research 392 (1986) 278-282
77. Sullivan R.M., McGaugh J.L., and Leon M. Norepinephrine-induced plasticity and one-trial olfactory learning in neonatal rats. Developmental Brain Research 60 (1991) 219-228
78. Sullivan R.M., Wilson D.A., and Leon M. Norepinephrine and learning-induced plasticity in infant rat olfactory system. Journal of Neuroscience 9 (1989) 3998-4006
79. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., and Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell 79 (1994) 981-991
80. Vavrousek-Jakuba E.M., Baker R.A., and Shoemaker W.J. Effect of ethanol on maternal and offspring characteristics: Comparison of the formulations fed during gestation. Alcoholism: Clinical and Experimental Research 15 (1991) 129-135
81. Wilson D.A., Guthrie K.M., and Leon M. Modification of olfactory bulb synaptic inhibition by early unilateral olfactory deprivation. Neuroscience Letters 116 (1990) 250-256
82. Wilson D.A., and Leon M. Noradrenergic modulation of olfactory bulb excitability in the postnatal rat. Brain Research 470 (1988) 69-75
83. Wilson D.A., and Leon M. Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. Journal of Neurophysiology 59 (1988) 1770-1782
84. Wilson D.A., and Sullivan R.M. Neurobiology of associative learning in the neonate: Early olfactory learning. Behavioral and Neural Biology 61 (1994) 1-18
85. Woo C.C., Coopersmith R., and Leon M. Localized changes in olfactory bulb morphology associated with early olfactory learning. Journal of Comparative Neurology 263 (1987) 113-125
86. Woo C.C., Oshita M.H., and Leon M. A learned odor decreases the number of Fos-immunopositive granule cells in the olfactory bulb of young rats. Brain Research 716 (1996) 149-156
87. Yates W.R., Cadoret R.J., Troughton E.P., Steward M., and Giunta T.A. Effect of fetal alcohol exposure on adult symptoms of nicotine, alcohol and drug dependence. Alcoholism: Clinical and Experimental Research 22 (1998) 914-920
88. Youngentob S.L. Developing a strategy for the rapid identification of genetically altered mice: An olfactory system perspective. Lab Animal 30 (2001) 32-37
89. Youngentob S.L. A method for the rapid automated assessment of olfactory function. Chemical Senses 30 (2005) 219-229
90. Youngentob S.L., Johnson B.A., Leon M., Sheehe P.R., and Kent P.F. Predicting odorant quality perception from multidimensional scaling of olfactory bulb glomerular activity patterns. Behavioral Neuroscience 120 (2006) 1337-1345
91. Youngentob S.L., and Kent P.F. Enhancement of odorant-induced mucosal activity patterns in rats trained on an odorant identification task. Brain Research 670 (1995) 82-88
92. Youngentob S.L., Kent P.F., and Margolis F.L. OMP gene deletion results in an alteration in odorant-induced mucosal activity patterns. Journal of Neurophysiology 90 (2003) 3864-3873
93. Youngentob S.L., Kent P.F., Mooney S.M., Spear N.E., and Molina J.C. In utero ethanol experience and olfactory plasticity. Alcoholism: Clinical and Experimental Research 28 (2004) 94A
94. Youngentob S.L., Kent P.F., Sheehe P.R., Schwob J.E., and Tzoumaka E. Mucosal inherent activity patterns in the rat: Evidence from voltage-sensitive dyes. Journal of Neurophysiology 73 (1995) 387-398
95. Youngentob S.L., and Margolis F.L. OMP gene deletion causes an elevation in behavioral threshold sensitivity. NeuroReport 10 (1999) 15-19
96. Youngentob S.L., Margolis F.L., and Youngentob L.M. OMP gene deletion results in an alteration in odorant quality perception. Behavioral Neuroscience 115 (2001) 626-631
97. Youngentob S.L., Markert L.M., Mozell M.M., and Hornung D.E. A method for establishing a five odorant identification confusion matrix task in rats. Physiology & Behavior 47 (1990) 1053-1059
98. Youngentob, S. L., Molina, J. C., Spear, N. E., & Youngentob, L. M. (in press). The effect of gestational ethanol exposure on voluntary ethanol intake in early postnatal and adult rats. Behavioral Neuroscience
99. 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. Physiology & Behavior 41 (1987) 59-69
100. Youngentob S.L., Schwob J.E., Sheehe P.R., and Youngentob L.M. Odorant threshold following methyl bromide-induced lesions of the olfactory epithelium. Physiology & Behavior 62 (1997) 1241-1252
101. Zhao H., and Reed R.R. X inactivation of the OCNC1 channel gene reveals a role for activity-dependent competition in the olfactory system. Cell 104 (2001) 651-660