Effects of exposure to moderate levels of ethanol during prenatal brain development on dendritic length, branching, and spine density in the nucleus accumbens and dorsal striatum of adult rats

Alcohol

Volumn 46, Issue 6, 2012, Pages 577-584

  Rice, James P ^a   Suggs, Lisa E ^a   Lusk, Alexandra V ^a   Parker, Matthew O ^b   Candelaria Cook, Felicha T ^a   Akers, Katherine G ^a   Savage, Daniel D ^a,c   Hamilton, Derek A ^a,c  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Golgi Cox; Medium spiny neurons; Mesolimbic dopamine system; Prenatal alcohol

Indexed keywords

ALCOHOL; SACCHARIN;

ADULT ANIMAL; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; BRAIN WEIGHT; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITE; DENDRITIC BRANCHING; DENDRITIC LENGTH; DENDRITIC SPINE DENSITY; EXPOSURE; FEMALE; GESTATION PERIOD; MALE; MEDIUM SPINY NEURON; MORPHOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; PRENATAL DEVELOPMENT; PROGENY; RAT;

ANIMALS; BRAIN; CORPUS STRIATUM; DENDRITES; DENDRITIC SPINES; ETHANOL; FEMALE; MALE; NUCLEUS ACCUMBENS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

ANIMALIA; RATTUS;

EID: 84864525533     PISSN: 07418329     EISSN: 18736823     Source Type: Journal    
DOI: 10.1016/j.alcohol.2011.11.008     Document Type: Article

References (71)

1. Abel E.L. An update on incidence of FAS: FAS is not an equal opportunity birth defect. Neurotoxicology and Teratology 1995, 17:437-443.
2. Abel E.L., Berman R.F. Long-term behavioral effects of prenatal alcohol exposure in rats. Neurotoxicology and Teratology 1994, 16:467-470.
3. Allan A.M., Weeber E.J., Savage D.D., Caldwell K.K. Effects of prenatal ethanol exposure on phospholipase C-beta 1 and phospholipase A2 in hippocampus and medial frontal cortex of adult rat offspring. Alcoholism: Clinical & Experimental Research 1997, 21:1534-1541.
4. Allan A., Wu H., Paxton L., Savage D. Prenatal ethanol exposure alters the modulation of the gamma-aminobutyric acid(A) receptor-gated chloride ion channel in adult rat offspring. Journal of Pharmacology and Experimental Therapeutics 1998, 284:250-257.
5. Barbier E., Houchi H., Warnault V., Pierrefiche O., Daoust M., Naassila M. Effects of prenatal and postnatal maternal ethanol on offspring response to alcohol and psychostimulants in long evans rats. Neuroscience 2009, 161:427-440.
6. Barbier E., Pierrefiche O., Vaudry D., Vaudry H., Daoust M., Naassila M. Long-term alterations in vulnerability to addiction to drugs of abuse and in brain gene expression after early life ethanol exposure. Neuropharmacology 2008, 55:1199-1211.
7. Berman R.F., Hannigan J.H., Sperry M.A., Zajac C.S. Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 1996, 13:209-216.
8. Bernier B.E., Whitaker L.R., Morikawa H. Previous ethanol experience enhances synaptic plasticity of NMDA receptors in the ventral tegmental area. Journal of Neuroscience 2011, 31:5205-5212.
9. Besheer J., Grondin J.J., Cannady R., Sharko A.C., Faccidomo S., Hodge C.W. Metabotropic glutamate receptor 5 activity in the nucleus accumbens is required for the maintenance of ethanol self-administration in a rat genetic model of high alcohol intake. Biological Psychiatry 2010, 67:812-822.
10. Brown R.W., Gonzalez C.L.R., Whishaw I.Q., Kolb B. Nicotine improvement of Morris water task performance after fimbria-fornix lesion is blocked by mecamylamine. Behavioural Brain Research 2001, 119:185-192.
11. Centers for Disease Control and Prevention Report Frequent alcohol consumption among women of childbearing age-behavioral risk factor surveillance system. Journal of the American Medical Association 1994, 271:1820-1821.
12. Chaudhri N., Sahuque L.L., Schairer W.W., Janak P.H. Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking. Neuropsychopharmacology 2010, 35:783-791.
13. Clarren S.K., Smith D.W. The fetal alcohol syndrome. New England Journal of Medicine 1978, 298:1063-1067.
14. Coleman P.D., Riesen A.H. Evironmental effects on cortical dendritic fields. I. Rearing in the dark. Journal of Anatomy 1968, 102:363-374.
15. Conry J. Neuropsychological deficits in fetal alcohol syndrome and fetal alcohol effects. Alcoholism: Clinical & Experimental Research 1990, 14:650-655.
16. Cui Z.-J., Zhao K.-B., Zhao H.-J., Yu D.-M., Niu Y.-L., Zhang J.-S., et al. Prenatal alcohol exposure induces long-term changes in dendritic spines and synapses in the mouse visual cortex. Alcohol and Alcoholism 2010, 45:312-319.
17. Day N.L., Cottreau C.M., Richardson G.A. The epidemiology of alcohol, marijuana, and cocaine use among women of childbearing age and pregnant women. Clinical Obstetrics and Gynecology 1993, 36:232-245.
18. Engleman E.A., Ding Z.M., Oster S.M., Toalston J.E., Bell R.L., Murphy J.M., et al. Ethanol is self-administered into the nucleus accumbens shell, but not the core: evidence of genetic sensitivity. Alcoholism: Clinical & Experimental Research 2009, 33:2162-2171.
19. Everitt B.J., Belin D., Economidou D., Pelloux Y., Dalley J.W., Robbins T.W. Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 2008, 363:3125-3135.
20. Freund T.F., Powell J.F., Smith A.D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 1984, 13:1189-1215.
21. Galindo R., Frausto S., Wolff C., Caldwell K.K., Perrone-Bizzozero N.I., Savage D.D. Prenatal ethanol exposure reduces mGluR5 receptor number and function in the dentate gyrus of adult offspring. Alcoholism: Clinical & Experimental Research 2004, 28:1587-1597.
22. Gibb R., Kolb B. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. Journal of Neuroscience Methods 1998, 79:1-4.
23. Glaser E.M., Van der Loos H. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. Journal of Neuroscience Methods 1981, 4:117-125.
24. Goodlett C.R., Horn K.H. Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol Research & Health 2001, 25:175-184.
25. Goodlett C.R., Horn K.H., Zhou F.C. Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Experimental Biology and Medicine (Maywood, NJ) 2005, 230:394-406.
26. Hamilton D.A., Akers K.G., Rice J.P., Johnson T., Candelaria-Cook F.T., Maes L.I., et al. Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: relationship to structural plasticity and immediate early gene expression in frontal cortex. Behavioural Brain Research 2010, 207:290-304.
27. Hamilton D.A., Candelaria-Cook F.T., Akers K.G., Rice J.P., Maes L.I., Rosenberg M., et al. Patterns of social-experience-related c-fos and Arc expression in the frontal cortices of rats exposed to saccharin or moderate levels of ethanol during prenatal brain development. Behavioural Brain Research 2010, 214:66-74.
28. Hamilton D.A., Kolb B. Differential effects of nicotine and complex housing on subsequent experience-dependent structural plasticity in the nucleus accumbens. Behavioral Neuroscience 2005, 119:355-365.
29. Hannigan J.H. What research with animals is telling us about alcohol-related neurodevelopmental disorder. Pharmacology Biochemistry & Behavior 1996, 55:489-499.
30. Hannigan J.H., Pilati M.L. The effects of chronic postweaning amphetamine on rats exposed to alcohol in utero: weight gain and behavior. Neurotoxicology and Teratology 1991, 13:649-656.
31. Hernandez G., Hamdani S., Rajabi H., Conover K., Stewart J., Arvanitogiannis A., et al. Prolonged rewarding stimulation of the rat medial forebrain bundle: neurochemical and behavioral consequences. Behavioral Neuroscience 2006, 120:888-904.
32. Hoyme H., May P., Kalberg W., Kodituwakku P., Gossage J., Trujillo P., et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 Institute of Medicine criteria. Pediatrics 2005, 115:39-47.
33. Hutchison K.E., Ray L., Sandman E., Rutter M.C., Peters A., Davidson D., et al. The effect of olanzapine on craving and alcohol consumption. Neuropsychopharmacology 2006, 31:1310-1317.
34. Hyman S.E., Malenka R.C., Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annual Review of Neuroscience 2006, 29:565-598.
35. Izzo P.N., Bolam J.P. Cholinergic synaptic input to different parts of spiny striatonigral neurons in the rat. Journal of Comparative Neurology 1988, 269:219-234.
36. Jones K.L., Smith D.W. Recognition of the fetal alcohol syndrome in early infancy. Lancet 1973, 302:999-1001.
37. Jones K.L., Smith D.W. The fetal alcohol syndrome. Teratology 1975, 12:1-10.
38. Jones K.L., Smith D.W., Ulleland C.N., Streissguth P. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973, 1:1267-1271.
39. Kelly S.J., Day N., Streissguth A.P. Effects of prenatal alcohol exposure on social behavior in humans and other species. Neurotoxicology and Teratology 2000, 22:143-149.
40. Kelly S.J., Dillingham R.R. Sexually dimorphic effects of perinatal alcohol exposure on social interactions and amygdala DNA and DOPAC concentrations. Neurotoxicology and Teratology 1994, 16:377-384.
41. Kemp J.M., Powell T.P. The site of termination of afferent fibres in the caudate nucleus. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 1971, 262:413-427.
42. Kodituwakku P.W. Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: a review. Neuroscience & Biobehavioral Reviews 2007, 31:192-201.
43. Kolb B., Gorny G., Li Y., Samaha A.N., Robinson T.E. Amphetamine or cocaine limits the ability of later experience to promote structural plasticity in the neocortex and nucleus accumbens. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:10523-10528.
44. Krause M., German P.W., Taha S.A., Fields H.L. A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. Journal of Neuroscience 2010, 30:4746-4756.
45. Livy D.J., Miller E.K., Maier S.E., West J.R. Fetal alcohol exposure and temporal vulnerability: effects of binge-like alcohol exposure on the developing rat hippocampus. Neurotoxicology and Teratology 2003, 25:447-458.
46. Mooney S.M., Napper R.M. Early postnatal exposure to alcohol reduces the number of neurons in the occipital but not the parietal cortex of the rat. Alcoholism: Clinical & Experimental Research 2005, 29:683-691.
47. Mooney S.M., Varlinskaya E.I. Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure. Behavioural Brain Research 2011, 216:358-364.
48. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annual Review of Physiology 2002, 64:313-353.
49. Oleson E.B., Richardson J.M., Roberts D.C. A novel IV cocaine self-administration procedure in rats: differential effects of dopamine, serotonin, and GABA drug pre-treatments on cocaine consumption and maximal price paid. Psychopharmacology (Berl) 2011, 214:567-577.
50. Rewal M., Jurd R., Gill T.M., He D.Y., Ron D., Janak P.H. Alpha4-containing GABAA receptors in the nucleus accumbens mediate moderate intake of alcohol. Journal of Neuroscience 2009, 29:543-549.
51. Robinson T.E., Kolb B. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. European Journal of Neuroscience 1999, 11:1598-1604.
52. Savage D., Cruz L., Duran L., Paxton L. Prenatal ethanol exposure diminishes activity-dependent potentiation of amino acid neurotransmitter release in adult rat offspring. Alcoholism: Clinical & Experimental Research 1998, 22:1771-1777.
53. Savage D.D., Montano C.Y., Otero M.A., Paxton L.L. Prenatal ethanol exposure decreases hippocampal NMDA-sensitive [3H]-glutamate binding site density in 45-day-old rats. Alcohol 1991, 8:193-201.
54. Savage D.D., Rosenberg M.J., Wolff C.R., Akers K.G., El-Emawy A., Staples M.C., et al. Effects of a novel cognition-enhancing agent on fetal ethanol-induced learning deficits. Alcoholism: Clinical & Experimental Research 2010, 34:1793-1802.
55. Schoenbaum G., Roesch M.R., Stalnaker T.A. Orbitofrontal cortex, decision-making and drug addiction. Trends in Neurosciences 2006, 29:116-124.
56. Sholl D.A. The organization of the cerebral cortex 1981, Methuen, London.
57. Streissguth A.P., Aase J.M., Clarren S.K., Randels S.P., LaDue R.A., Smith D.F. Fetal alcohol syndrome in adolescents and adults. Journal of the American Medical Association 1991, 265:1961-1967.
58. Streissguth A.P., Barr H.M., Sampson P.D. Moderate prenatal alcohol exposure: effects on child IQ and learning problems at age 7 1/2 years. Alcoholism: Clinical & Experimental Research 1990, 14:662-669.
59. Sutherland R.J., McDonald R.J., Savage D.D. Prenatal exposure to moderate levels of ethanol can have long-lasting effects on hippocampal synaptic plasticity in adult offspring. Hippocampus 1997, 7:232-238.
60. Sutherland R.J., McDonald R.J., Savage D.D. Prenatal exposure to moderate levels of ethanol can have long-lasting effects on learning and memory in adult offspring. Psychobiology 2000, 28:532-539.
61. Thomas J.D., Abou E.J., Dominguez H.D. Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats. Neurotoxicology and Teratology 2009, 31:303-311.
62. Tuesta L., Fowler C.D., Kenny P.J. Recent advances in understanding nicotinic receptor signaling mechanisms that regulate drug self-administration behavior. Biochemical Pharmacology 2011.
63. Varaschin R.K., Rosenberg M.J., Akers K.G., Hamilton D.A., Savage D.D. Effects of the cognition-enhancing agent ABT-239 on fetal ethanol-induced deficits in dentate gyrus synaptic plasticity. Journal of Pharmacology and Experimental Therapeutics 2010, 334:191-198.
64. Vetter C.S., Doremus-Fitzwater T.L., Spear L.P. Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. Alcoholism: Clinical & Experimental Research 2007, 31:1159-1168.
65. Voorn P., Vanderschuren L.J., Groenewegen H.J., Robbins T.W., Pennartz C.M. Putting a spin on the dorsal-ventral divide of the striatum. Trends in Neurosciences 2004, 27:468-474.
66. Whitcher L.T., Klintsova A.Y. Postnatal binge-like alcohol exposure reduces spine density without affecting dendritic morphology in rat mPFC. Synapse 2008, 62:566-573.
67. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nature Reviews Neuroscience 2006, 7:464-476.
68. Yin H.H., Ostlund S.B., Balleine B.W. Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. European Journal of Neuroscience 2008, 28:1437-1448.
69. Yin H.H., Park B.S., Adermark L., Lovinger D.M. Ethanol reverses the direction of long-term synaptic plasticity in the dorsomedial striatum. European Journal of Neuroscience 2007, 25:3226-3232.
70. Zhou F.C., Anthony B., Dunn K.W., Lindquist W.B., Xu Z.C., Deng P. Chronic alcohol drinking alters neuronal dendritic spines in the brain reward center nucleus accumbens. Brain Research 2007, 1134:148-161.
71. Zhou F.C., Bledsoe S., Lumeng L., Li T.K. Immunostained serotonergic fibers are decreased in selected brain regions of alcohol-preferring rats. Alcohol 1991, 8:425-431.