Variants of contextual fear conditioning are differentially impaired in the juvenile rat by binge ethanol exposure on postnatal days 4-9

Behavioural Brain Research

Volumn 212, Issue 2, 2010, Pages 133-142

  Murawski, Nathen J ^a   Stanton, Mark E ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Amygdala; Cognitive development; Fear conditioning; Fetal alcohol spectrum disorder; Hippocampus

Indexed keywords

ALCOHOL; CENTRAL DEPRESSANT AGENT;

AMYGDALOID NUCLEUS; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BODY WEIGHT; BRAIN FUNCTION; CONDITIONING; CONTEXTUAL FEAR CONDITIONING; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FACILITATION; FEMALE; FREEZING; HIPPOCAMPUS; MALE; NONHUMAN; PERFORMANCE; PERINATAL PERIOD; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; ASSOCIATION; AUDITORY STIMULATION; CATALEPSY; CONDITIONED REFLEX; DRUG EFFECTS; ELECTRIC SHOCK; FEAR; HEARING; LONG EVANS RAT; NEUROPSYCHOLOGICAL TEST; NEWBORN; RANDOMIZATION; TIME;

ACOUSTIC STIMULATION; ANIMALS; ANIMALS, NEWBORN; AUDITORY PERCEPTION; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CONDITIONING, CLASSICAL; CUES; ELECTROSHOCK; ETHANOL; FEAR; FEMALE; FREEZING REACTION, CATALEPTIC; MALE; NEUROPSYCHOLOGICAL TESTS; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; TIME FACTORS;

EID: 77953029026     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.04.003     Document Type: Article

References (83)

1. Abel E.L., Sokol R.J. Fetal alcohol syndrome is now leading cause of mental retardation. Lancet 1986, 2:1222.
2. Allan A.M., Chynoweth J., Tyler L.A., Caldwell K.K. A mouse model of prenatal ethanol exposure using a voluntary drinking paradigm. Alcohol-Clin Exp Res 2003, 27:2009-2016.
3. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 2001, 11:8-17.
4. Barrientos R.M., O'Reilly R.C., Rudy J.W. Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav Brain Res 2002, 134:299-306.
5. Biedenkapp J.C., Rudy J.W. Hippocampal and extrahippocampal systems compete for control of contextual fear: Role of ventral subiculum and amygdala. Learn Memory 2009, 16:38-45.
6. Bloomer W.A., VanDongen H.M., VanDongen A.M. Arc/Arg3.1 translation is controlled by convergent N-methyl-D-aspartate and Gs-coupled receptor signaling pathways. J Biol Chem 2008, 283:582-592.
7. Bonthius D.J., Pantazis N.J., Karacay B., Bonthius N.E., Taggard Da, Lothman E.W. Alcohol exposure during the brain growth spurt promotes hippocampal seizures, rapid kindling, and spreading depression. Alcohol Clin Exp Res 2001, 25:734-745.
8. Bonthius D.J., West J.R. Alcohol-induced neuronal loss in developing rats: increased brain damage with binge exposure. Alcohol Clin Exp Res 1990, 14:107-118.
9. Bonthius D.J., West J.R. Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology 1991, 44:147-163.
10. Brown K.L., Burman M.A., Duong H.B., Stanton M.E. Neonatal binge alcohol exposure produces dose-dependent deficits in interstimulus interval discrimination eyeblink conditioning in juvenile rats. Brain Res 2009, 1248:162-175.
11. Brown K.L., Calizo L.H., Goodlett C.R., Stanton M.E. Neonatal alcohol exposure impairs acquisition of eyeblink conditioned responses during discrimination learning and reversal in weanling rats. Dev Psychobiol 2007, 49:243-257.
12. Brown K.L., Calizo L.H., Stanton M.E. Dose-dependent deficits in dual interstimulus interval classical eyeblink conditioning tasks following neonatal binge alcohol exposure in rats. Alcohol Clin Exp Res 2008, 32:277-293.
13. Burman M.A., Murawski N.J., Schiffino F.L., Rosen J.B., Stanton M.E. Factors governing single-trial contextual fear conditioning in the weanling rat. Behav. Neurosci. 2009, 123:1148-1152.
14. Burman M.A., Starr M.J., Gewirtz J.C. Dissociable effects of hippocampus lesions on expression of fear and trace fear conditioning memories in rats. Hippocampus 2006, 16:103-113.
15. Cho Y.H., Friedman E., Silva A.J. Ibotenate lesions of the hippocampus impair spatial learning but not contextual fear conditioning in mice. Behav Brain Res 1999, 98:77-87.
16. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev 2001, 36:60-90.
17. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979, 3:79-83.
18. Fanselow M.S. Factors governing one-trial contextual conditioning. Anim Learn Behav 1990, 18:264-270.
19. Fitzgerald P. FAS persists despite broad public awareness. Mich Med 1988, 87. 262-264, 268.
20. Frankland P.W., Cestari V., Filipkowski R.K., McDonald R.J., Silva A.J. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 1998, 112:863-874.
21. Girard T.A., Xing H.C., Ward G.R., Wainwright P.E. Early postnatal ethanol exposure has long-term effects on the performance of male rats in a delayed matching-to-place task in the Morris water maze. Alcohol Clin Exp Res 2000, 24:300-306.
22. Gold A.E., Kesner R.P. The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 2005, 15:808-814.
23. Goodlett C.R., Johnson T.B. Neonatal binge ethanol exposure using intubation: timing and dose effects on place learning. Neurotoxicol Teratol 1997, 19:435-446.
24. Goodlett C.R., Peterson S.D. Sex differences in vulnerability to developmental spatial learning deficits induced by limited binge alcohol exposure in neonatal rats. Neurobiol Learn Mem 1995, 64:265-275.
25. Green J.T. The effects of ethanol on the developing cerebellum and eyeblink classical conditioning. Cerebellum 2004, 3:178-187.
26. Guzowski J.F., McNaughton B.L., Barnes C.A., Worley P.F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 1999, 2:1120-1124.
27. Hamre K.M., West J.R. The effects of the timing of ethanol exposure during the brain growth spurt on the number of cerebellar Purkinje and granule cell nuclear profiles. Alcohol Clin Exp Res 1993, 17:610-622.
28. Huff N.C., Frank M., Wright-Hardesty K., Sprunger D., Matus-Amat P., Higgins E., et al. Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. J Neurosci 2006, 26:1616-1623.
29. Hunsaker M.R., Kesner R.P. Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol Learn Mem 2008, 89:61-69.
30. Inoue K., Fukazawa Y., Ogura A., Inokuchi K. Two-dimensional neural activity mapping of the entire population of hippocampal CA1 pyramidal cells responding to fear conditioning. Neurosci Res 2005, 51:417-425.
31. Johnson T.B., Goodlett C.R. Selective and enduring deficits in spatial learning after limited neonatal binge alcohol exposure in male rats. Alcohol Clin Exp Res 2002, 26:83-93.
32. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
33. Kim J.J., Rison R.A., Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 1993, 107:1093-1098.
34. Klintsova A.Y., Helfer J.L., Calizo L.H., Dong W.K., Goodlett C.R., Greenough W.T. Persistent impairment of hippocampal neurogenesis in young adult rats following early postnatal alcohol exposure. Alcohol Clin Exp Res 2007, 31:2073-2082.
35. Krahl S.E., Berman R.F., Hannigan J.H. Electrophysiology of hippocampal CA1 neurons after prenatal ethanol exposure. Alcohol 1999, 17:125-131.
36. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184.
37. Lehmann H., Lacanilao S., Sutherland R.J. Complete or partial hippocampal damage produces equivalent retrograde amnesia for remote contextual fear memories. Eur J Neurosci 2007, 25:1278-1286.
38. 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. Neurotoxicol Teratol 2003, 25:447-458.
39. Maier SE, Chen WJ, West JR, eds. The effects of timing and duration of alcohol exposure on development of the fetal brain. Fetal Alcohol Syndrome: From Mechanisms to Prevention, ed. E.L. Abel. 1996, CRC Press: Boca Raton. 27-50.
40. Maier S.E., West J.R. Drinking patterns and alcohol-related birth defects. Alcohol Res Health 2001, 25:168-174.
41. Manning M.A., Eugene Hoyme H. Fetal alcohol spectrum disorders: a practical clinical approach to diagnosis. Neurosci Biobehav Rev 2007, 31:230-238.
42. Maren S., Aharonov G., Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav Brain Res 1997, 88:261-274.
43. Marino M.D., Aksenov M.Y., Kelly S.J. Vitamin E protects against alcohol-induced cell loss and oxidative stress in the neonatal rat hippocampus. Int J Dev Neurosci 2004, 22:363-377.
44. Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 1971, 262:23-81.
45. Mattson S.N., Riley E.P. A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 1998, 22:279-294.
46. Mattson S.N., Schoenfeld A.M., Riley E.P. Teratogenic effects of alcohol on brain and behavior. Alcohol Res Health 2001, 25:185-191.
47. Matus-Amat P., Higgins E.A., Barrientos R.M., Rudy J.W. The role of the dorsal hippocampus in the acquisition and retrieval of context memory representations. J Neurosci 2004, 24:2431-2439.
48. Matus-Amat P., Higgins E.A., Sprunger D., Wright-Hardesty K., Rudy J.W. The role of dorsal hippocampus and basolateral amygdala NMDA receptors in the acquisition and retrieval of context and contextual fear memories. Behav Neurosci 2007, 121:721-731.
49. May P.A., Gossage J.P. Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res Health 2001, 25:159-167.
50. McHugh T.J., Tonegawa S. CA3 NMDA receptors are required for the rapid formation of a salient contextual representation. Hippocampus 2009, 335-339.
51. Miki T., Harris S.J., Wilce P.A., Takeuchi Y., Bedi K.S. Effects of age and alcohol exposure during early life on pyramidal cell numbers in the CA1-CA3 region of the rat hippocampus. Hippocampus 2004, 14:124-134.
52. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
53. Murawski NJ, Stanton ME, Variants of contextual fear conditioning are differentially impaired in the juvenile rat by binge ethanol exposure on postnatal days 4-9. in Fetal Alcohol Spectrum Disorder Study Group. 2009. San Diego, CA.
54. O'Leary-Moore S.K., McMechan A.P., Mathison S.N., Berman R.F., Hannigan J.H. Reversal learning after prenatal or early postnatal alcohol exposure in juvenile and adult rats. Alcohol 2006, 38:99-110.
55. Pauli J., Wilce P., Bedi K.S. Spatial learning ability of rats following acute exposure to alcohol during early postnatal life. Physiol Behav 1995, 58:1013-1020.
56. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992, 106:274-285.
57. Pitkanen A., Kelly J.L., Amaral D.G. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the entorhinal cortex in the macaque monkey. Hippocampus 2002, 12:186-205.
58. Redila V.A., Olson A.K., Swann S.E., Mohades G., Webber A.J., Weinberg J., et al. Hippocampal cell proliferation is reduced following prenatal ethanol exposure but can be rescued with voluntary exercise. Hippocampus 2006, 16:305-311.
59. Richmond M.A., Yee B.K., Pouzet B., Veenman L., Rawlins J.N., Feldon J., et al. Dissociating context and space within the hippocampus: effects of complete, dorsal, and ventral excitotoxic hippocampal lesions on conditioned freezing and spatial learning. Behav Neurosci 1999, 113:1189-1203.
60. Riikonen R., Salonen I., Partanen K., Verho S. Brain perfusion SPECT and MRI in foetal alcohol syndrome. Dev Med Child Neurol 1999, 41:652-659.
61. Riley E.P., McGee C.L. Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp Biol Med (Maywood) 2005, 230:357-365.
62. Rudy J.W. Context representations, context functions, and the parahippocampal-hippocampal system. Learn Mem 2009, 16:573-585.
63. Rudy J.W., Barrientos R.M., O'Reilly R.C. Hippocampal formation supports conditioning to memory of a context. Behav Neurosci 2002, 116:530-538.
64. Rudy J.W., Huff N.C., Matus-Amat P. Understanding contextual fear conditioning: insights from a two-process model. Neurosci Biobehav Rev 2004, 28:675-685.
65. Rudy J.W., Matus-Amat P. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: implications for a unitary function of the hippocampus. Behav Neurosci 2005, 119:154-163.
66. Rudy J.W., O'Reilly R.C. Conjunctive representations, the hippocampus, and contextual fear conditioning. Cogn Affect Behav Neurosci 2001, 1:66-82.
67. Sacchetti B., Baldi E., Lorenzini C.A., Bucherelli C. Cerebellar role in fear conditioning consolidation. Proc Natl Acad Sci U S A 2002, 99:8406-8411.
68. Schiffino FL, Murawski NJ, Rosen JB, Stanton ME, Ontogeny of the context preexposure facilitation effect: role of hippocampal NMDA receptors, (in preparation).
69. Sokol R.J., Delaney-Black V., Nordstrom B. Fetal alcohol spectrum disorder. Jama 2003, 290:2996-2999.
70. Spadoni A.D., McGee C.L., Fryer S.L., Riley E.P. Neuroimaging and fetal alcohol spectrum disorders. Neurosci Biobehav Rev 2007, 31:239-245.
71. Sulik K.K. Genesis of alcohol-induced craniofacial dysmorphism. Exp Biol Med (Maywood) 2005, 230:366-375.
72. Sulik K.K., Johnston M.C., Webb M.A. Fetal alcohol syndrome: embryogenesis in a mouse model. Science 1981, 214:936-938.
73. 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.
74. Sutherland R.J., O'Brien J., Lehmann H. Absence of systems consolidation of fear memories after dorsal, ventral, or complete hippocampal damage. Hippocampus 2008, 18:0-8.
75. Thomas J.D., Sather T.M., Whinery L.A. Voluntary exercise influences behavioral development in rats exposed to alcohol during the neonatal brain growth spurt. Behav Neurosci 2008, 122:1264-1273.
76. Thomas J.D., Wasserman E.A., West J.R., Goodlett C.R. Behavioral deficits induced by binge-like exposure to alcohol in neonatal rats: importance of developmental timing and number of episodes. Dev Psychobiol 1996, 29:433-452.
77. Tran T.D., Kelly S.J. Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicol Teratol 2003, 25:519-528.
78. Wagner A.F., Hunt P.S. Impaired trace fear conditioning following neonatal ethanol: reversal by choline. Behav Neurosci 2006, 120:482-487.
79. Weeber E.J., Savage D.D., Sutherland R.J., Caldwell K.K. Fear conditioning induced alterations of phospholipase C-beta1a protein level and enzyme activity in rat hippocampal formation and medial frontal cortex. Neurobiol Learn Mem 2001, 76:151-182.
80. Whitcher L.T., Klintsova A.Y. Postnatal binge-like alcohol exposure reduces spine density without affecting dendritic morphology in rat mPFC. Synapse 2008, 566-573.
81. Willoughby K.A., Sheard E.D., Nash K., Rovet J. Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. J Int Neuropsych Soc 2008, 14:1022-1033.
82. Wiltgen B.J., Sanders M.J., Anagnostaras S.G., Sage J.R., Fanselow M.S. Context fear learning in the absence of the hippocampus. J Neurosci 2006, 26:5484-5491.
83. Woodruff-Pak D.S., Green J.T., Levin S.I., Meisler M.H. Inactivation of sodium channel Scn8A (Na-sub(v)1.6) in Purkinje neurons impairs learning in Morris water maze and delay but not trace eyeblink classical conditioning. Behav Neurosci 2006, 120:229-240.