Neocortical plasticity deficits in fetal alcohol spectrum disorders: Lessons from barrel and visual cortex

Journal of Neuroscience Research

Volumn 86, Issue 2, 2008, Pages 256-263

  Medina, Alexandre E ^a,b   Krahe, Thomas E ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

CREB; Enriched environment; Fetal alcohol syndrome; Phosphodiesterase; Vinpocetine

Indexed keywords

ANTIOXIDANT; CHOLINE; PHOSPHODIESTERASE INHIBITOR; ROLIPRAM; VINPOCETINE;

BRAIN CORTEX; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; EXPOSURE; FETAL ALCOHOL SYNDROME; HUMAN; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; SOMATOSENSORY CORTEX; VISUAL CORTEX;

ALCOHOLIC BEVERAGES; ANIMALS; FEMALE; FETAL ALCOHOL SYNDROME; FETUS; HUMANS; NEURONAL PLASTICITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; VIBRISSAE; VISUAL CORTEX;

EID: 38849157893     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21447     Document Type: Short Survey

References (134)

1. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E. 1998. Rolipram, a type IV-specific phophodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci U S A 95:15020-15025.
2. Baydala L, Sherman J, Rasmussen C, Wikman E, Janzen H. 2006. ADHD characteristics in Canadian Aboriginal children. J Atten Disord 9:642-647.
3. Bear MF, Kleinschmidt A, Gu QA, Singer W. 1990. Disruption of experience-dependent synaptic modifications in striate cortex by infusion of an NMDA receptor antagonist. J Neurosci 10:909-925.
4. Beaver CJ, Ji Q, Fischer QS, Daw NW. 2001. Cyclic AMP-dependent protein kinase mediates ocular dominance shifts in cat visual cortex. Nat Neurosci 4:159-163.
5. Beavo JA. 1995. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 75:725-748.
6. Berardi N, Pizzorusso T, Ratto GM, Maffei L. 2003. Molecular basis of plasticity in the visual cortex. Trends Neurosci 26:369-378.
7. Berman RF, Hannigan JH, Sperry MA, Zajac CS. 1996. Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 13:209-216.
8. Bhatara V, Loudenberg R, Ellis R. 2006. Association of attention deficit hyperactivity disorder and gestational alcohol exposure: an exploratory study. J Atten Disord 9:515-522.
9. 2+ and stimulus duration dependent switch for hippocampal gene expression. Cell 87:1203-1214.
10. Bonhoeffer T, Grinvald A. 1991. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353:429-431.
11. Bourne HR, Nicoll R. 1993. Molecular machines integrate coincident synaptic signals. Cell 72:65-75.
12. Cancedda L, Putignano E, Impey S, Maffei L, Ratto GM, Pizzorusso T. 2003. Patterned vision causes CRE-mediated gene expression in the visual cortex through PKA and ERK. J Neurosci 23:7012-7020.
13. Cancedda L, Putignano E, Sale A, Viegi A, Berardi N, Maffei L. 2004. Acceleration of visual system development by environmental enrichment. J Neurosci 24:4840-4848.
14. Chapman B, Stryker MP, Bonhoeffer T. 1996. Development of orientation preference maps in ferret primary visual cortex. J Neurosci 16:6443-6453.
15. Chen SY, Dehart DB, Sulik KK. 2007. Protection from ethanol-induced limb malformations by the superoxide dismutase/catalase mimetic, EUK-134. FASEB J 18:1234-1236.
16. Clements KM, Girard TA, Ellard CG, Wainwright PE. 2005. Short-term memory impairment and reduced hippocampal c-Fos expression in an animal model of fetal alcohol syndrome. Alcohol Clin Exp Res 29:1049-1059.
17. Constantine-Paton M, Cline HT, Debski E. 1990. Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci 13:129-154.
18. Coppola DM, White LE. 2004. Visual experience promotes the isotropic representation of orientation preference. Vis Neurosci 21:39-51.
19. Coppola DM, Purves HR, McCoy AN, Purves D. 1998. The distribution of oriented contours in the real world. Proc Natl Acad Sci U S A 95:4002-4006.
20. Costa ET, Savage DD, Valenzuela CF. 2000. A review of the effects of prenatal or early postnatal ethanol exposure on brain ligand-gated ion channels. Alcohol Clin Exp Res 24:706-715.
21. Curtis J, Finkbeiner S. 1999. Sending signals from the synapse to the nucleus: possible roles for CaMK, Ras/ERK, and SAPK pathways in the regulation of synaptic plasticity and neuronal growth. J Neurosci Res 58:88-95.
22. Deisseroth K, Bito H, Tsien RW. 1996. Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16:89-101.
23. DeNoble VJ. 1987. Vinpocetine enhances retrieval of a step-through passive avoidance response in rats. Pharmacol Biochem Behav 26:183-186.
24. Di Cristo G, Berardi N, Cancedda L, Pizzorusso T, Putignano E, Ratto GM, Maffei L. 2001. Requirement of ERK activation for visual cortical plasticity. Science 292:2337-2340.
25. Epelbaum M, Milleret C, Buisseret P, Dufier JL. 1993. The sensitive period for strabismic amblyopia in humans. Ophtalmology 100:323-327.
26. A circuits for visual cortical plasticity. Science 303:1681-1683.
27. Fox K. 2002. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111:799-814.
28. A receptor binding in the barrel cortex of developing and adult rats. J Comp Neurol 395:209-216.
29. Galindo R, Zamudio PA, Valenzuela CF. 2005. Alcohol is a potent stimulant of immature neuronal networks: implications for fetal alcohol spectrum disorder. J Neurochem 94:1500-1511.
30. Glazewski S, Fox K. 1996. The time-course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J Neurophysiol 75:1714-1729.
31. Glazewski S, Barth AL, Wallace H, McKenna M, Silva A, Fox K. 1999. Impaired experience-dependent plasticity in barrel cortex of mice lacking the alpha and delta isoforms of CREB. Cerebral Cortex 9:249-256.
32. Gong B, Vitolo OV, Trinchese F, Liu S, Shelanski M, Arancio O. 2004. Persistent improvement in synaptic and cognitive functions in an Alzheimer mouse model after rolipram treatment. J Clin Invest 114:1624-1634.
33. Grinvald A, Lieke E, Frostiq RD, Gilbert CD, Wiesel TN. 1986. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324:361-364.
34. Hannigan JH, Berman RF, Zajac CS. 1993. Environmental enrichment and the behavioral effects of prenatal exposure to alcohol in rats. Neurotoxicol Teratol 15:261-266.
35. Harris SR, MacKay LL, Osborn JA. 1995. Autistic behaviors in offspring of mothers abusing alcohol and other drugs: a series of case reports. Alcohol Clin Exp Res 19:660-665.
36. Heaton MB, Mitchell JJ, Paiva M. 2000. Amelioration of ethanol-induced neurotoxicity in the neonatal rat central nervous system by antioxidant therapy. Alcohol Clin Exp Res 24:512-518.
37. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF. 1998. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504-1508.
38. Hevroni D, Rattner A, Bundman M, Lederfein D, Gabarah A, Mangelus M, Silverman MA, Kedar H, Naor C, Kornuc M, Hanoch T, Seger R, Theill LE, Nedivi E, Richter-Levin G, Citri Y. 1998. Hippocampal plasticity involves extensive gene induction and multiple cellular mechanisms. J Mol Neurosci 10:75-98.
39. Hindmarch I, Fuchs HH, Erzigkeit H. 1991. Efficacy and tolerance of vinpocetine in ambulant patients suffering from mild to moderate organic psychosyndromes. Int Clin Psychopharmacol 6:31-43.
40. Horton JC, Adams DL. 2005. The cortical column: a structure without a function. Philos Trans R Soc Lond B Biol Sci 360:837-862.
41. A receptors on medial septum/diagonal band (MS/DB) neurons after postnatal ethanol exposure. Brain Res 810:100-113.
42. A receptor currents in Purkinje neurons. Brain Res 832:124-135.
43. Hubel DH, Wiesel TN. 1959. Receptive fields of single neurones in the cat's striate cortex. J Physiol 148:574-591.
44. Hubel DH, Wiesel TN. 1962. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106-154.
45. Hubel DH, Wiesel TN. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206:419-436.
46. Hubel DH, Wiesel TN, LeVay S. 1977. Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278:377-409.
47. Hughes PD, Kim YN, Randall PK, Leslie SW. 1998. Effect of prenatal ethanol exposure on the developmental profile of the NMDA receptor subunits in rat forebrain and hippocampus. Alcohol Clin Exp Res 22:1255-1261.
48. Ieraci A, Herrera DG. 2006. Nicotinamide protects against ethanol-induced apoptotic neurodegeneration in the developing mouse brain. PLoS Med 3:0547-0557.
49. Issa NP, Trachtenberg JT, Chapman B, Zahs KR, Stryker MP. 1999. The critical period for ocular dominance plasticity in the ferret's visual cortex. J Neurosci 19:6965-6978.
50. Jones JP, Meck W, Williams CL, Wilson MA, Swartzwelder HS. 1999. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Brin Res Dev Brain Res 118:159-167.
51. Kakkar R, Raju RVS, Sharma RK. 1999. Calmodulin-dependent cyclic nucleotide phosphodiesterase (PDE1). Cell Mol Life Sci 55:1164-1186.
52. Karacay B, Li G, Pantazis NJ, Bonthius DJ. 2007. Stimulation of the cAMP pathway protects cultured cerebellar granule neurons against alcohol-induced cell death by activating the neuronal nitric oxide synthase (nNOS) gene. Brain Res [E-pub ahead of print].
53. Katz LC, Shatz CJ. 1996. Synaptic activity and the constuction of cortical circuits. Science 274:1133-1138.
54. Kelly SJ, Black AC Jr, West JR. 1989. Changes in muscarinic cholinergic receptors in the hippocampus of rats exposed to ethyl alcoholduring the brain growth spurt. J Pharmacol Exp Them 249:798-804.
55. Klintsova AY, Cowell RM, Swain RA, Napper RMA, Goodlett CR, Greenough WT. 1998. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats. I. Behavioral results. Brain Res 800:48-61.
56. Lendvai B, Zelles T, Rozsa B, Vizi ES. 2003. A vinca alkaloid enhances morphological dynamics of dendritic spines of neocortical layer 2/3 pyramidal cells. Brain Res Bull 59:257-260.
57. Li C, Niu W, Jiang CH, Hu Y. 2007. Effects of enriched environment on gene expression and signal pathways in cortex of hippocampal CA1 specific NMDAR1 knockout mice. Brain Res Bull 71:568-577.
58. Li Q, Guo-Ross S, Lewis DV, Turner D, White AM, Wilson WA, Swartzwelder HS. 2004. Dietary prenatal choline supplementation alters postnatal hippocampal structure and function. J Neurophysiol 91:1545-1555.
59. Lovinger DM, White G, Weight FF. 1989. Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 243:1721-1724.
60. Lynch G. 2002. Memory enhancement: the search for mechanism-based drugs. Nat Neurosci 5:1035-1038.
61. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL. 1986. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321:519-522.
62. Maffei L, Berardi N, Domenici L, Parisi V, Pizzorusso T. 1992. Nerve growth factor (NGF) prevents the shift in ocular dominance plasticity in ocular dominance distribuiton of visual cortical neurons in monocularly deprived rats. J Neurosci 12:4651-4662.
63. Malenka RC, Kauer JA, Perkel DJ, Nicoll RA. 1989. The impact of postsynaptic calcium on synaptic transmission - its role in long-term potentiation. Trends Neurosci 12:444-450.
64. Malisza KL, Allman AA, Shiloff D, Jakobson L, Longstaffe S, Chudley AE. 2005. Evaluation of spatial working memory function in children and adults with fetal alcohol spectrum disorders: a functional magnetic resonance imaging study. Pediatr Res 58:1150-1157.
65. Mameli M, Zamudio PA, Carta M, Valenzuela CF. 2005. Developmentally regulated actions of alcohol on hippocampal glutamatergic transmission. J Neurosci 25:8027-8036.
66. Marino MD, Aksenov MY, Kelly SJ. 2004. Vitamin E protects against alcohol-induced cell loss and oxidative stress in the neonatal rat hippocampus. Int J Dev Neurosci 22:363-377.
67. Mattson SN, Riley EP. 1998. A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 22:279-294.
68. Mattson SN, Gramling L, Delis DC, Jones KL, Riley EP. 1996. Global-local processing in children prenatally exposed to alcohol. Child Neuropsychol 2:165-175.
69. Mattson SN, Schoenfeld AM, Riley EP. 2001. Teratogenic effects of alcohol on brain and behavior. Alcohol Res Health 25:185-191.
70. May PA, Gossage JP. 2001. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res Health 25:159-167.
71. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
72. McCasland JS, Bernardo KL, Probst KL, Woolsey TA. 1992. Cortical local circuit axons do not mature after early deafferentation. Proc Natl Acad Sci U S A 89:1832-1836.
73. Meck WH, Smith RA, Williams CL. 1989. Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both. Behav Neurosci 103:1234-1241.
74. Medina AE, Ramoa AS. 2005. Early alcohol exposure impairs ocular dominance plasticity throughout the critical period. Brain Res Dev Brain Res 157:107-111.
75. Medina AE, Liao DS, Mower AF, Ramoa AS. 2001. Do NMDA receptor kinetics regulate the end of critical periods of plasticity? Neuron 32:553-555.
76. Medina AE, Krahe TE, Coppola DM, Ramoa AS. 2003. Neonatal alcohol exposure induces long-lasting impairment of visual cortical plasticity in ferrets. J Neurosci 23:10002-10012.
77. Medina AE, Krahe TE, Ramoa AS. 2005. Early alcohol exposure induces persistent alteration of cortical columnar organization and reduced orientation selectivity in the visual cortex. J Neurophysiol 93:1317-1325.
78. Medina AE, Krahe TE, Ramoa AS. 2006. Restoration of neuronal plasticity by a phosphodiesterase type 1 inhibitor in a model of fetal alcohol exposure. J Neurosci 26:1057-1060.
79. Mellott TJ, Williams CL, Meck WH, Blusztajn JK. 2004. Prenatal choline supplementation advances hippocampal development and enhances MAPK and CREB activation. FASEB J 18:545-547.
80. Miller MW. 2006. Effect of prenatal exposure to ethanol on glutamate and GABA immunoreactivity in macaque somatosensory and motor cortices: critical timing of exposure. Neuroscience 138:97-107.
81. Mitchell DE, Freeman RD, Millodot M, Haegerstrom G. 1973. Meridional amblyopia: evidence for modification of the human visual system by early visual experience. Vis Res 13:535-558.
82. Molnar P, Gaal L. 1992. Effect of different subtypes of cognition enhancers on long-term potentiation in the rat dentate gyrus in vivo. Eur J Pharmacol 215:17-22.
83. Molnar P, Gaal L, Horvath C. 1994. The impairment of long-term potentiation in rats with medial septal lesion and its restoration by cognition enhancers. Neurobiology 2:255-266.
84. 2+ response element-binding protein function is essential for ocular dominance plasticity. J Neurosci 22:2237-2245.
85. Nagahara AH, Handa RJ. 1995. Fetal alcohol exposure alters the induction of immediate early gene mRNA in the rat prefrontal cortex after an alternation task. Alcohol Clin Exp Res 19:1389-1397.
86. Nanson JL. 1992. Autism in fetal alcohol syndrome: a report of six cases. Alcohol Clin. Exp. Res. 16:558-565.
87. Nedivi E, Hevroni D, Naot D, Israeli D, Citri Y. 1993. Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363:718-722.
88. Nithianantharajah J, Hannan AJ. 2006. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 7:697-709.
89. Nixon K, Hughes PD, Amsel A, Leslie SW. 2002. NMDA receptor subunit expression following early postnatal exposure to ethanol. Brain Res Dev Brain Res 139:295-299.
90. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. 1984. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465.
91. Olson HC, Feldman JJ, Streissguth AP, Sampson PD, Bookstein FL. 1998. Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcohol Clin Exp Res 22:1998-2012.
92. O'Malley KD, Nanson J. 2002. Clinical implications of a link between fetal alcohol spectrum disorder and attention-deficit hyperactivity disorder. Can J Psychiatry 47:349-354.
93. Otmakhov N, Khibnick L, Otmakhova N, Carpenter S, Riahi S, Asrican B, Lisman J. 2004. Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91:1955-1962.
94. Pandey SC, Roy A, Mitral N. 2001. Effects of chronic ethanol intake and its withdrawal on the expression and phosphorylation of the CREB gene transcription factor in rat cortex. J Pharmacol Exp Ther 296:857-868.
95. Pham TA, Impey S, Storm DR, Stryker MP. 1999a. CRE-mediated gene transcription in neocortical neuronal plasticity during the developmental critical period. Neuron 22:63-72.
96. Pham TM, Ickes B, Albeck D, Soderstrom S, Granholm AC, Mohammed AH. 1999b. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience 94:279-286.
97. Pick GG, Cooperman M, Trombka D, Rogel-Fuchs Y, Yanai J. 1993. Hippocampal cholinergic alterations and related behavioral deficits after early exposure to ethanol. Int J Dev Neurosci 11:379-385.
98. Pinaud R, Penner MR, Robertson HA, Currie RW. 2001. Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Res Mol Brain Res 91:50-56.
99. Platenik J, Kuramoto N, Yoneda Y. 2000. Molecular mechanisms associated with long-term consolidation of the NMDA signals. Life Sci 67:335-364.
100. Prakash N, Cohen-Cory S, Frostig RD. 1996. Rapid and opposite effects of BDNF and NGF on the functional organization of the adult cortex in vivo. Nature 381:702-706.
101. Puurunen K, Koistinaho J, Sirvio J, Jolkkonen J, Silvenius J. 2001. Enriched-environment housing increases neuronal Fos-staining in the dentate gyrus after a water maze spatial learning task. Neuropharmacology 40:440-447.
102. Pyapali G, Turner D, Williams C, Meck W, Swartzwelder HS. 1998. Prenatal choline supplementation decreases the threshold for inducing of long-term potentiation in young adult rats. J Neurophysiol 79:1790-1796.
103. Ramoa AS, Mower AF, Liao DS, Jafri SI. 2001. Suppression of cortical NMDA receptor function prevents development of orientation selectivity in the primary visual cortex. J Neurosci 21:4299-4309.
104. Rampon C, Jiang CH, Dong H, Tang YP, Lockhart DJ, Schultz PG, Tsien JZ, Hu Y. 2000. Effects of environmental enrichment on gene expression in the brain. Proc Natl Acad Sci U S A 97:12880-12884.
105. Rasmussen C. 2005. Executive functioning and working memory in fetal alcohol spectrum disorder. Alcohol Clin Exp Res 29:1359-1367.
106. Rema V, Ebner FF. 1999. Effect of enriched environment rearing on impairments in cortical excitability and plasticity after prenatal alcohol exposure. J Neurosci 19:10993-11006.
107. Rema V, Armstrong-James M, Ebner FF. 1998. Experience-dependent plasticity of adult rat S1 cortex requires local NMDA receptor activation. J Neurosci 18:10196-10206.
108. Richardson DP, Byrnes ML, Brien JF, Reynolds JN, Dringenberg HC. 2002. Impaired acquisition in the water maze and hippocampal long-term potentiation after chronic prenatal ethanol exposure in the guinea-pig. Eur J Neurosci 16:1593-1598.
109. Roberts EB, Meredith AM, Ramoa AS. 1998. Suppression of NMDA receptor function using antisense DNA blocks ocular dominance plasticity while preserving visual responses. J Neurophysiol 80:1021-1032.
110. Rose GM, Hopper A, De Vivo M, Tehim A. 2005. Phosphodiesterase inhibitors for cognitive enhancement. Curr Pharm Des 11:3329-3334.
111. Rozas C, Frank H, Heynen AJ, Morales B, Bear MF, Kirkwood A. 2001. Developmental inhibitory gate controls the relay of activity to the superficial layers of the visual cortex. J Neurosci 21:6791-6801.
112. Sampson PD, Streissguth AP, Bookstein FL, Little RE, Clarren SK, Dehaene P, Hanson JW, Graham JM Jr. 1997. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56:317-326.
113. Savage DD, Queen SA, Sanchez CF, Paxton LL, Mahoney JC, Goodlett CR, West JR. 1992. Prenatal ethanol exposure during the last third of gestation in rat reduces hippocampal NMDA agonist binding site density in 45-day-old offspring. Alcohol 9:37-41.
114. Schambra UB, Lauder JM, Petrusz P, Sulik KK. 1990. Development of neurotransmitter systems in the mouse embryo following acute ethanol exposure: A hostological and immunocytochemical study. Int J Dev Neurosci 8:507-522.
115. Schonfeld AM, Mattson SN, Lang AR, Delis DC, Riley EP. 2001. Verbal and nonverbal fluency in children with heavy prenatal alcohol exposure. J Stud Alcohol 62:239-246.
116. Stanton ME, Goodlett CR. 1998. Neonatal ethanol exposure impairs eye-blink conditioning in weanling rats. Alcohol Clin Exp Res 22:270-275.
117. Stromland K, Pinazo-Duran M. 2002. Ophthalmic involvement in the fetal alcohol syndrome: clinical and animal model studies. Alcohol Alcoholism 37:2-8.
118. Taha S, Hanover JL, Silva AJ, Stryker MP. 2002. Autophosphorylation of αCaMKII is required for ocular dominance plasticity. Neuron 36:483-491.
119. Thomas JD, La Fiette H, Qumn VRE, Riley EP. 2000. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol Teratol 22:703-711.
120. Thomas JD, Garrison M, O'Neill TM. 2004. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 26:35-45.
121. Thomas JD, Biane JS, O'Bryan KA, O'Neill TM, Dominguez HD. 2007. Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav Neurosci 121:120-130.
122. Torasdotter M, Metsis M, Henriksson BG, Winblad B, Mohammed AH. 1998. Enviromnental enrichment results in higher levels of nerve growth factor mRNA in the rat visual cortex and hippocampus. Behav Brain Res 93:83-90.
123. Toscano CD, McGlothan JL, Guilarte TR. 2006. Experience-dependent regulation of zif268 gene expression and spatial learning. Exp Neurol 200:209-215.
124. Toso L, Poqqi SH, Abebe D, Roberson R, Dunlap V, Park J, Spong CY. 2005. N-methyl-D-aspartate subunit expression during mouse development altered by in utero alcohol exposure. Am J Obstet Gynecol 193:1534-1539.
125. Uecker A, Nadel L. 1996. Spatial locations gone awry: object and spatial memory deficits in children with fetal alcohol syndrome. Neuropsychologia 34:209-223.
126. Van der Loos H, Woolsey TA. 1973. Somatosensory cortex: structural alterations following early injury to sensory organs. p 395-398.
127. Waltereit R, Weller M. 2003. Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol Neurobiol 27:99-106.
128. Weliky M, Katz LC. 1997. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386:680-685.
129. Williams BM, Luo Y, Ward C, Redd KK, Gibson R, Kuczaj SA, McCoy JG. 2001. Environmental enrichment: effects on spatial memory and hippocampal CREB immunoreactivity. Physiol Behav 73:649-658.
130. Woolsey TA. 1967. Somatosensory, auditory and visual cortical areas of the mouse. Johns Hopkins Med J 121:91-112.
131. Woolsey TA, Van der Loos H. 1970. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242.
132. Yang X, Horn K, Baraban JM, Wand GS. 1988. Chronic ethanol adminstration decreases phosphorylation of cyclic AMP response element-binding protein in granule cells of rat cerebellum. J Neurochem 70:224-232.
133. Yang X, Horn K, Wand GS. 1998. Chronic ethanol exposure impairs phosphorylation of CREB and CRE-binding activity in rat striatum. Alcohol Clin Exp Res 22:382-390.
134. Zhu SW, Pham TM, Aberg E, Brene S, Winblad B, Mohammed AH, Baumans V. 2006. Neurotrophin levels and behaviour in BALB/c mice: impact of intermittent exposure to individual housing and wheel running. Behav Brain Res 167:1-8.