Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Behavioral and Brain Functions
Published in: Behavioral and Brain Functions 1/2009

Open Access 01-12-2009 | Research

The consequence of fetal ethanol exposure and adolescent odor re-exposure on the response to ethanol odor in adolescent and adult rats

Authors: Amber M Eade, Paul R Sheehe, Juan C Molina, Norman E Spear, Lisa M Youngentob, Steven L Youngentob

Published in: Behavioral and Brain Functions | Issue 1/2009

Login to get access

Abstract

Background

An epidemiologic predictive relationship exists between fetal ethanol exposure and the likelihood for adolescent use. Further, an inverse relationship exists between the age of first experience and the probability of adult abuse. Whether and how the combined effects of prenatal and adolescent ethanol experiences contribute to this progressive pattern remains unknown. Fetal ethanol exposure directly changes the odor attributes of ethanol important for both ethanol odor preference behavior and ethanol flavor perception. These effects persist only to adolescence. Here we tested whether adolescent ethanol odor re-exposure: (Experiment 1) augments the fetal effect on the adolescent behavioral response to ethanol odor; and/or (Experiment 2) perpetuates previously observed adolescent behavioral and neurophysiological responses into adulthood.

Methods

Pregnant rats received either an ethanol or control liquid diet. Progeny (observers) experienced ethanol odor in adolescence via social interaction with a peer (demonstrators) that received an intragastric infusion of either 1.5 g/kg ethanol or water. Social interactions were scored for the frequency that observers followed their demonstrator. Whole-body plethysmography evaluated the unconditioned behavioral response of observers to ethanol odor in adolescence (P37) or adulthood (P90). The olfactory epithelium of adults was also examined for its neural response to five odorants, including ethanol.

Results

Experiment 1: Relative to fetal or adolescent exposure alone, adolescent re-exposure enhanced the behavioral response to ethanol odor in P37 animals. Compared to animals with no ethanol experience, rats receiving a single experience (fetal or adolescent) show an enhanced, yet equivalent, ethanol odor response. Fetal ethanol experience also increased olfactory-guided following of an intoxicated peer. Experiment 2: Combined exposure yielded persistence of the behavioral effects only in adult females. We found no evidence for persistence of neurophysiological effects in either sex.

Conclusion

Fetal ethanol exposure influences adolescent re-exposure, in part, by promoting interactions with intoxicated peers. Re-exposure subsequently enhances ethanol odor responsivity during a key developmental transition point for emergent abuse patterns. While persistence of behavioral effects occurred in females, the level of re-exposure necessary to uniformly yield persistence in both sexes remains unknown. Nonetheless, these results highlight an important relationship between fetal and adolescent experiences that appears essential to the progressive pattern of developing ethanol abuse.
Appendix
Available only for authorised users
Literature
1.
Alati R, Al Mamum A, Williams GM, O'Callagham M, Najman JM, Bor W: In utero alcohol exposure and prediction of alcohol disorders in early adulthood: A birth cohort study. Arch Gen Psychiatry. 2006, 63: 1009-1016. 10.1001/archpsyc.63.9.1009.CrossRefPubMed
2.
Baer JS, Barr HM, Bookstein FL, Sampson PD, Streissguth AP: Prenatal alcohol exposure and family history of alcoholism in the etiology of adolescent alcohol problems. J Stud Alcohol. 1998, 59: 533-543.CrossRefPubMed
3.
Baer JS, Sampson PD, Barr HM, Connor PD, Streissguth AP: A 21-year longitudinal analysis of the effects of prenatal alcohol exposure on young adult drinking. Arch Gen Psychiatry. 2003, 60: 377-385. 10.1001/archpsyc.60.4.377.CrossRefPubMed
4.
Streissguth A: 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;. 1998, June
5.
Yates WR, Cadoret RJ, Troughton EP, Stewart M, Giunta TS: Effect of fetal alcohol exposure on adult symptoms of nicotine, alcohol, and drug dependence. Alcohol Clin Exp Res. 1998, 22: 914-920.CrossRefPubMed
6.
Hudson R: From molecule to mind: The role of experience in shaping olfactory function. J Comp Physiol A. 1999, 185: 297-304. 10.1007/s003590050390.CrossRefPubMed
7.
Faas AE, Sponton ED, Moya PR, Molina JC: Differential responsiveness to alcohol odor in human neonates: Effects of maternal consumption during gestation. Alcohol. 2000, 22: 7-17. 10.1016/S0741-8329(00)00103-8.CrossRefPubMed
8.
Schaal B, Marlier L, Soussignan R: Human foetuses learn odours from their pregnant mother's diet. Chem Senses. 2000, 25: 729-737. 10.1093/chemse/25.6.729.CrossRefPubMed
9.
Schaal B, Orgeur P: Olfaction in utero: Can the rodent model be generalized?. Q J Exp Psychol B. 1992, 44: 245-278.PubMed
10.
11.
Arias C, Chotro MG: Interactions between prenatal ethanol exposure and postnatal learning about ethanol in rat pups. Alcohol. 2006, 40: 51-59. 10.1016/j.alcohol.2006.10.002.CrossRefPubMed
12.
Bond NW, DiGiusto EL: Effects of prenatal alcohol consumption on open-field behaviour and alcohol preference in rats. Psychopharmacologia. 1976, 46: 163-165. 10.1007/BF00421386.CrossRefPubMed
13.
Chotro MG, Kraebel KS, McKinzie DL, Molina JC, Spear N: Prenatal and postnatal ethanol exposure influences preweanling rats' behavioral and autonomic responding to ethanol odor. Alcohol. 1996, 13: 377-385. 10.1016/0741-8329(96)00027-4.CrossRefPubMed
14.
Chotro MG, Molina JC: Acute ethanol contamination of the amniotic fluid during gestational day 21: Postnatal changes in alcohol responsiveness in rats. Dev Psychobiol. 1990, 23: 535-547. 10.1002/dev.420230608.CrossRefPubMed
15.
Chotro MG, Molina JC: Bradycardiac responses elicited by alcohol odor in rat neonates: Influence of in utero experience with ethanol. Psychopharmacology. 1992, 106: 491-496. 10.1007/BF02244820.CrossRefPubMed
16.
Dominguez HD, Lopez MF, Chotro MG, Molina JC: Perinatal responsiveness to alcohol's chemosensory cues as a function of prenatal alcohol administration during gestational days 17–20 in the rat. Neurobiol Learn Mem. 1996, 65: 103-112. 10.1006/nlme.1996.0012.CrossRefPubMed
17.
Dominguez HD, Lopez MF, Molina JC: Neonatal responsiveness to alcohol odor and infant alcohol intake as a function of alcohol experience during late gestation. Alcohol. 1998, 16: 109-117. 10.1016/S0741-8329(97)00169-9.CrossRefPubMed
18.
Molina JC, Chotro MG, Dominguez HD: Fetal alcohol learning resulting from alcohol contamination of the prenatal environment. Fetal Development: A Psychobiological Perspective. Edited by: Lecanuet JP, Fifer WP, Krasnegor NA, Smotherman WP. 1995, Hillsdale, NJ: Lawrence Erlbaum, 419-438.
19.
Youngentob SL, Kent PF, Sheehe PR, Molina JC, Spear NE, Youngentob LM: 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 Neurosc. 2007, 121: 1293-1305. 10.1037/0735-7044.121.6.1293.CrossRef
20.
Youngentob SL, Molina JC, Spear NE, Youngentob LM: The effect of gestational ethanol exposure on voluntary intake in early postnatal and adult rats. Behav Neurosci. 2007, 121: 1306-1315. 10.1037/0735-7044.121.6.1306.PubMedCentralCrossRefPubMed
21.
Youngentob SL, Eade AM, Kent PF, Youngentob LM: Fetal ethanol experience and olfactory plasticity: Its contribution to adolescent alcohol abuse [Abstract]. Chem Senses. 2008,
22.
Chotro MG, Arias C, Laviola G: Increased ethanol intake after prenatal ethanol exposure: studies with animals. Neurosci Biobehav Rev. 2007, 31: 181-191. 10.1016/j.neubiorev.2006.06.021.CrossRefPubMed
23.
Molina JC, Spear NE, Spear LP, Mennella JA, Lewis MJ: The International Society for Developmental Psychobiology 39th Annual Meeting Symposium: Alcohol and development: Beyond fetal alcohol syndrome. Dev Psychobiol. 2007, 49: 227-242. 10.1002/dev.20224.PubMedCentralCrossRefPubMed
24.
Spear NE, Molina JC: Fetal or infantile exposure to ethanol promotes ethanol ingestion in adolescence and adulthood: A theoretical review. Alcohol Clin Exp Res. 2005, 29: 909-929. 10.1097/01.ALC.0000171046.78556.66.CrossRefPubMed
25.
Driscoll CD, Streissguth AP, Riley EP: Prenatal alcohol exposure: Comparability of effects in human and animal models. Neurotoxicol Teratol. 1990, 12: 231-237. 10.1016/0892-0362(90)90094-S.CrossRefPubMed
26.
Vavrousek-Jakuba EM, Baker RA, Shoemaker WJ: Effect of ethanol on maternal and offspring characteristics: Comparison of the formulations fed during gestation. Alcohol Clin Exp Res. 1991, 15: 129-135. 10.1111/j.1530-0277.1991.tb00530.x.CrossRefPubMed
27.
Miller MW: Development of the Central Nervous System: Effects of Alcohol and Opiates. 1992, New York: Wiley-Liss
28.
Gesteland RC, Yancey RA, Farbman AI: Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience. 1982, 7: 3127-3136. 10.1016/0306-4522(82)90235-4.CrossRefPubMed
29.
Farbman AI: Developmental neurobiology of the olfactory system. Smell and Taste in Health and Disease. Edited by: Getchell TV, Doty R, Bartoshuk L, Snow J. 1991, New York: Raven Press, 19-33.
30.
Galef BG: Development of flavor preferences in man and animals: The role of social and nonsocial factors. Development of Perception. Psychobiological Perspectives. Edited by: Aslin RN, Alberts JR, Petersen MR. 1981, New York: Academic, 4: 411-431.CrossRef
31.
Galef BG, Stein M: Demonstrator influence on observer diet preference: Analysis of critical social interactions and olfactory signals. Anim Learn Behav. 1985, 13: 31-38.CrossRef
32.
Galef BG, Wigmore SW: Transfer of information concerning distant foods: A laboratory investigation of the 'information-centre' hypothesis. Anim Behav. 1983, 31: 748-758. 10.1016/S0003-3472(83)80232-2.CrossRef
33.
Fernandez-Vidal JM, Molina JC: Socially mediated alcohol preferences in adolescent rats following interactions with an intoxicated peer. Pharmacol Biochem Behav. 2004, 79: 229-241. 10.1016/j.pbb.2004.07.010.CrossRefPubMed
34.
Hunt PS, Holloway JL, Scordalakes EM: Social interaction with an intoxicated sibling can result in increased intake of ethanol by periadolescent rats. Dev Psychobiol. 2001, 38: 101-109. 10.1002/1098-2302(200103)38:2<101::AID-DEV1002>3.0.CO;2-4.CrossRefPubMed
35.
Varlinskaya EI, Spear LP, Spear NE: Acute effects of ethanol on behavior of adolescent rats: role of social context. Alcohol Clin Exp Res. 2001, 25: 377-385. 10.1111/j.1530-0277.2001.tb02224.x.CrossRefPubMed
36.
Vanderschuren LJMJ, Niesink RJM, VanRee JM: The neurobiology of social play behavior in rats. Neurosci Biobehav Rev. 1997, 21: 309-326. 10.1016/S0149-7634(96)00020-6.CrossRefPubMed
37.
38.
Youngentob SL, Mozell MM, Sheehe PR, Hornung DE: A quantitative analysis of sniffing strategies in rats performing odor detection tasks. Physiol Behav. 1987, 41: 59-69. 10.1016/0031-9384(87)90131-4.CrossRefPubMed
39.
Mozell MM, Sheehe PR, Swieck SW, Kurtz DB, Hornung DE: A parametric study of the stimulation variables affecting the magnitude of the olfactory nerve response. J Gen Physiol. 1984, 83: 233-267. 10.1085/jgp.83.2.233.CrossRefPubMed
40.
Youngentob SL, Kent PF, Sheehe PR, Schwob JE, Tzoumaka E: Mucosal inherent activity patterns in the rat: Evidence from voltage-sensitive dyes. J Neurophysiol. 1995, 73: 387-398.PubMed
41.
Youngentob SL, Kent PF, Margolis FL: OMP deletion results in an alteration in odorant-induced mucosal activity patterns. J Neurophysiol. 2003, 90: 3864-3873. 10.1152/jn.00806.2002.CrossRefPubMed
42.
Wang HW, Wysocki CJ, Gold GH: Induction of olfactory receptor sensitivity in mice. Science. 1993, 260: 998-1000. 10.1126/science.8493539.CrossRefPubMed
43.
Wysocki CJ, Dorries KM, Beauchmp GK: Ability to perceive androstenone can be acquired by ostensibly anosmic people. Proc Natl Acad Sci USA. 1989, 86: 7976-7978. 10.1073/pnas.86.20.7976.PubMedCentralCrossRefPubMed
44.
Youngentob SL, Kent PF: Enhancement of odorant-induced mucosal activity patterns in rats trained on an odorant identification task. Brain Res. 1995, 670: 82-88. 10.1016/0006-8993(94)01275-M.CrossRefPubMed
45.
Spear LP: The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev. 2000, 24: 417-463. 10.1016/S0149-7634(00)00014-2.CrossRefPubMed
46.
Chotro MG, Arias C: Prenatal exposure to ethanol increases ethanol consumption: A conditioned response?. Alcohol. 2003, 30: 19-28. 10.1016/S0741-8329(03)00037-5.CrossRefPubMed
47.
Randall CL, Hughes SS, Williams CK, Anton RF: Effect of prenatal alcohol exposure on consumption of alcohol and alcohol-induced sleep time in mice. Pharmacol Biochem Behav. 1983, 18: 325-329. 10.1016/0091-3057(83)90194-6.CrossRefPubMed
48.
Hunt PS, Hallmark RA: Increases in ethanol ingestion by young rats following interaction with intoxicated siblings: A review. Integr Physiol Behav Sci. 2001, 36: 239-248. 10.1007/BF02734096.CrossRefPubMed
49.
Hunt PS, Lant GM, Carroll CA: Enhanced intake of ethanol in preweanling rats following interactions with intoxicated siblings. Dev Psychobiol. 2000, 37: 90-99. 10.1002/1098-2302(200009)37:2<90::AID-DEV4>3.0.CO;2-D.CrossRefPubMed
50.
Galef BG, Kennett DJ, Stein M: Demonstrator influence on observer diet preference: Effects of simple exposure and the presence of a demonstrator. Anim Learn Behav. 1985, 13: 25-30.CrossRef
51.
Maldonado AM, Finkbeiner LM, Kirstein CL: Voluntary ethanol intake is differentially affected depending on familiarity in the social interaction in adolescent male and female rats [Abstract]. Alcohol Clin Exp Res. 2008, 32: 167A-10.1111/j.1530-0277.2008.00733.x.CrossRef
52.
Choleris E, Valseccchi P, Wang Y, Ferrari P, Kavaliers M, Mainardi M: Social learning of a food preference in male and female Mongolian Gerbils is facilitated by the anxiolytic, Chlordiazepoxide. Pharmacol Biochem Behav. 1998, 60: 575-584. 10.1016/S0091-3057(98)00005-7.CrossRefPubMed
53.
Pellis SM, Field EF, Smith LK, Pellis VC: Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci Biobehav Rev. 1997, 21: 105-120. 10.1016/0149-7634(95)00060-7.CrossRefPubMed
54.
Gheusi G, Lledo PM: Control of early events in olfactory processing by adult neurogenesis. Chem Senses. 2007, 32: 397-409. 10.1093/chemse/bjm012.CrossRefPubMed
55.
Mair RG, Gellman RL, Gesteland RC: Postnatal proliferation and maturation of olfactory bulb neurons in the rat. Neuroscience. 1982, 7: 3105-3116. 10.1016/0306-4522(82)90233-0.CrossRefPubMed
56.
Weiler E, Farbman AI: Proliferation in the rat olfactory epithelium: Age-dependent changes. J Neurosci. 1997, 17: 3610-3622.PubMed
57.
Graziadei PPC, Monti Graziadei GA: Neurogenesis and neuron regeneration in the olfactory system of mammals. I. Morphological aspects of differentiation and structural organization of the olfactory sensory neuron. J Neurocytol. 1979, 8: 1-18. 10.1007/BF01206454.CrossRefPubMed
58.
Graziadei PPC, Monti Graziadei GA: Neurogenesis and neuron regeneration in the olfactory system of mammals. III. Deafferentation and reinnervation of the olfactory bulb following section of the fila olfactoria. J Neurocytol. 1980, 9: 145-162. 10.1007/BF01205155.CrossRefPubMed
59.
Honey PL, Galef BG: Ethanol consumption by rat dams during gestation, lactation and weaning increases ethanol consumption by their adolescent young. Dev Psychobiol. 2003, 42: 252-260. 10.1002/dev.10098.CrossRefPubMed
60.
Cao L, Dhilla A, Mukai J, Blazeski R, Lodovichi C, Mason CA, Gogos JA: Genetic modulation of BDNF signaling affects the outcome of axonal competition in vivo. Curr Biol. 2007, 17: 911-921. 10.1016/j.cub.2007.04.040.PubMedCentralCrossRefPubMed
61.
Lledo PM, Gheusi G: Olfactory processing in a changing brain. Neuroreport. 2003, 14: 1655-1663. 10.1097/00001756-200309150-00001.CrossRefPubMed
62.
Yu CR, Power J, Barnea G, O'Donnell S, Osborne J, Axel R, Gogos JA: Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron. 2004, 42: 553-566. 10.1016/S0896-6273(04)00224-7.CrossRefPubMed
63.
Purves D: Body and Brain. A Trophic Theory of Neural Connections. 1988, Cambridge, MA: Harvard University Press
64.
Funakoshi H, Belluardo N, Arenas E, Yamamoto Y, Casabona A, Persson H, Ibanez CF: Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science. 1995, 268: 1495-1499. 10.1126/science.7770776.CrossRefPubMed
65.
Belluardo N, Westreblad H, Mudo G, Casabona A, Bruton J, Caniglia G, Pastoris O, Grassi F, Ibanez CF: Neuromuscular junction disassembly and muscle fatigue in mice lacking neurotrophin-4. Mol Cell Neurosci. 2001, 18: 56-67. 10.1006/mcne.2001.1001.CrossRefPubMed
66.
McLaughlin T, Hindges R, Yates PA, O'Leary DD: Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsl-ventral retinotopic mapping. Development. 2003, 130: 2407-2418. 10.1242/dev.00467.CrossRefPubMed
67.
McLaughlin T, Torborg CL, Feller MB, O'Leary DD: Retinotopic map refinement requires spontaneous retinal waves during brief critical period of development. Neuron. 2003, 40: 1147-1160. 10.1016/S0896-6273(03)00790-6.CrossRefPubMed
Metadata
Title
The consequence of fetal ethanol exposure and adolescent odor re-exposure on the response to ethanol odor in adolescent and adult rats
Authors
Amber M Eade
Paul R Sheehe
Juan C Molina
Norman E Spear
Lisa M Youngentob
Steven L Youngentob
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2009
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/1744-9081-5-3

Other articles of this Issue 1/2009

Behavioral and Brain Functions 1/2009 Go to the issue

Research

Motor function may differentiate attention deficit hyperactivity disorder from early onset bipolar disorder

Research

Developmental dyscalculia: compensatory mechanisms in left intraparietal regions in response to nonsymbolic magnitudes

Research

Effects of methylphenidate on motor system excitability in a response inhibition task

Research

Attention Deficit Hyperactivity Disorder comorbid oppositional defiant disorder and its predominately inattentive type: evidence for an association with COMT but not MAOA in a Chinese sample

Research

Effect of lisdexamfetamine dimesylate on sleep in adults with attention-deficit/hyperactivity disorder

Research

Hyperresponsiveness to social rewards in children and adolescents with attention-deficit/hyperactivity disorder (ADHD)