Neonatal ethanol exposure results in dose-dependent impairments in the acquisition and timing of the conditioned eyeblink response and altered cerebellar interpositus nucleus and hippocampal CA1 unit activity in adult rats

Alcohol

Volumn 47, Issue 6, 2013, Pages 447-457

  Lindquist, Derick H ^a   Sokoloff, Greta ^b   Milner, Eric ^c   Steinmetz, Joseph E ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b University of Iowa   (United States)

^c WASHINGTON UNIVERSITY   (United States)

Author keywords

Cerebellum; Eyeblink conditioning; Fetal alcohol syndrome disorders; Hippocampus; Postnatal ethanol

Indexed keywords

ALCOHOL;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONED REFLEX; CONTROLLED STUDY; DOSE RESPONSE; EYELID REFLEX; FEMALE; HIPPOCAMPAL CA1 REGION; INTERPOSITUS NUCLEUS; LATENT PERIOD; LEARNING; MALE; NEWBORN; NONHUMAN; PERINATAL DRUG EXPOSURE; RAT; STIMULUS RESPONSE;

ANIMALIA; RATTUS;

EID: 84881544818     PISSN: 07418329     EISSN: 18736823     Source Type: Journal    
DOI: 10.1016/j.alcohol.2013.05.007     Document Type: Article

References (94)

1. Akase E., Alkon D.L., Disterhoft J.F. Hippocampal lesions impair memory of short-delay conditioned eye blink in rabbits. Behavioral Neuroscience 1989, 103:935-943.
2. Attwell P.J., Ivarsson M., Millar L., Yeo C.H. Cerebellar mechanisms in eyeblink conditioning. Annals of the New York Academy of Sciences 2002, 978:79-92.
3. Backman C., West J.R., Mahoney J.C., Palmer M.R. Electrophysiological characterization of cerebellar neurons from adult rats exposed to ethanol during development. Alcoholism, Clinical and Experimental Research 1998, 22:1137-1145.
4. Bauer-Moffett C., Altman J. The effect of ethanol chronically administered to preweanling rats on cerebellar development: a morphological study. Brain Research 1977, 119:249-268.
5. Bayer S.A., Altman J., Russo R.J., Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 1993, 14:83-144.
6. Belmeguenai A., Botta P., Weber J.T., Carta M., De Ruiter M., De Zeeuw C.I., et al. Alcohol impairs long-term depression at the cerebellar parallel fiber-Purkinje cell synapse. Journal of Neurophysiology 2008, 100:3167-3174.
7. Berger T.W., Laham R.I., Thompson R.F. Hippocampal unit-behavior correlations during classical conditioning. Brain Research 1980, 193:229-248.
8. Berger T.W., Thompson R.F. Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response. I. The hippocampus. Brain Research 1978, 145:323-346.
9. Berthier N.E., Moore J.W. Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Experimental Brain Research 1990, 83:44-54.
10. Bonthius D.J., West J.R. Permanent neuronal deficits in rats exposed to alcohol during the brain growth spurt. Teratology 1991, 44:147-163.
11. 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 Research 2009, 1248:162-175.
12. 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. Developmental Psychobiology 2007, 49:243-257.
13. 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. Alcoholism, Clinical and Experimental Research 2008, 32:277-293.
14. Chasnoff I.J., Wells A.M., Telford E., Schmidt C., Messer G. Neurodevelopmental functioning in children with FAS, pFAS, and ARND. Journal of Developmental and Behavioral Pediatrics 2010, 31:192-201.
15. Christian K.M., Thompson R.F. Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory 2003, 11:427-455.
16. Coleman S.R., Gormezano I. Classical conditioning of the rabbit's (Oryctolagus cuniculus) nictitating membrane response under symmetrical CS-US interval shifts. Journal of Comparative & Physiological Psychology 1971, 77:447-455.
17. Dalla C., Shors T.J. Sex differences in learning processes of classical and operant conditioning. Physiology & Behavior 2009, 97:229-238.
18. Freeman J.H., Nicholson D.A. Developmental changes in eye-blink conditioning and neuronal activity in the cerebellar interpositus nucleus. The Journal of Neuroscience 2000, 20:813-819.
19. Freeman J.H., Steinmetz A.B. Neural circuitry and plasticity mechanisms underlying delay eyeblink conditioning. Learning & Memory 2011, 18:666-677.
20. Frey P.W., Ross L.E. Classical conditioning of the rabbit eyelid response as a function of interstimulus interval. Journal of Comparative & Physiological Psychology 1968, 65:246-250.
21. Garcia K.S., Steele P.M., Mauk M.D. Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. The Journal of Neuroscience 1999, 19:10940-10947.
22. Gil-Mohapel J., Boehme F., Kainer L., Christie B.R. Hippocampal cell loss and neurogenesis after fetal alcohol exposure: insights from different rodent models. Brain Research Reviews 2010, 64:283-303.
23. Goodlett C.R., Johnson T.B. Neonatal binge ethanol exposure using intubation: timing and dose effects on place learning. Neurotoxicology & Teratology 1997, 19:435-446.
24. Goodlett C.R., Johnson T.B. Temporal windows of vulnerability to alcohol during the third trimester equivalent: why "knowing when" matters. Alcohol and alcoholism: Effects on brain and development 1999, 59-91. Lawrence Erlbaum, Hillsdale, NJ. J.H. Hanningan, L.P. Spear, N.E. Spear, C.R. Goodlett (Eds.).
25. Gormezano I., Kehoe E.J., Marshall B.S. Twenty years to classical conditioning with the rabbit. Progress in Psychobiology and Physiological Psychology 1983, 10:197-275.
26. Green J.T. The effects of ethanol on the developing cerebellum and eyeblink classical conditioning. Cerebellum 2004, 3:178-187.
27. Green J.T., Arenos J.D., Dillon C.J. The effects of moderate neonatal ethanol exposure on eyeblink conditioning and deep cerebellar nuclei neuron numbers in the rat. Alcohol 2006, 39:135-150.
28. Green J.T., Johnson T.B., Goodlett C.R., Steinmetz J.E. Eyeblink classical conditioning and interpositus nucleus activity are disrupted in adult rats exposed to ethanol as neonates. Learning & Memory 2002, 9:304-320.
29. Green J.T., Rogers R.F., Goodlett C.R., Steinmetz J.E. Impairment in eyeblink classical conditioning in adult rats exposed to ethanol as neonates. Alcoholism, Clinical and Experimental Research 2000, 24:438-447.
30. Green J.T., Steinmetz J.E. Purkinje cell activity in the cerebellar anterior lobe after rabbit eyeblink conditioning. Learning & Memory 2005, 12:260-269.
31. Green J.T., Tran T., Steinmetz J.E., Goodlett C.R. Neonatal ethanol produces cerebellar deep nuclear cell loss and correlated disruption of eyeblink conditioning in adult rats. Brain Research 2002, 956:302-311.
32. Hamilton G.F., Whitcher L.T., Klintsova A.Y. Postnatal binge-like alcohol exposure decreases dendritic complexity while increasing the density of mature spines in mPFC Layer II/III pyramidal neurons. Synapse 2010, 64:127-135.
33. 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. Alcoholism, Clinical and Experimental Research 1993, 17:610-622.
34. Hesslow G., Ivarsson M. Suppression of cerebellar Purkinje cells during conditioned responses in ferrets. Neuroreport 1994, 5:649-652.
35. Hoehler F.K., Thompson R.F. Effect of the interstimulus (CS-UCS) interval on hippocampal unit activity during classical conditioning of the nictitating membrane response of the rabbit (Oryctolagus cuniculus). Journal of Comparative & Physiological Psychology 1980, 94:201-215.
36. Hong S., Optican L.M. Interaction between Purkinje cells and inhibitory interneurons may create adjustable output waveforms to generate timed cerebellar output. PLoS One 2008, 3:e2770.
37. Idrus N.M., Napper R.M. Acute and long-term Purkinje cell loss following a single ethanol binge during the early third trimester equivalent in the rat. Alcoholism, Clinical and Experimental Research 2012, 36:1365-1373.
38. Jacobson S.W., Stanton M.E., Dodge N.C., Pienaar M., Fuller D.S., Molteno C.D., et al. Impaired delay and trace eyeblink conditioning in school-age children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research 2011, 35:250-264.
39. Jacobson S.W., Stanton M.E., Molteno C.D., Burden M.J., Fuller D.S., Hoyme H.E., et al. Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research 2008, 32:365-372.
40. Jones K.L., Smith D.W. The fetal alcohol syndrome. Teratology 1975, 12:1-10.
41. Jones K.L., Smith D.W., Ulleland C.N., Streissguth A.P. Pattern of malformation in offspring of chronic alcoholic mothers. Lancet 1973, 1:1267-1271.
42. Kim J.J., Baxter M.G. Multiple brain-memory systems: the whole does not equal the sum of its parts. Trends in Neuroscience 2001, 24:324-330.
43. King D.A., Tracy J. DataMunch: A Matlab m-file collection for the analysis of trial-based spike and behavioral data 1999.
44. Kodituwakku P.W. Defining the behavioral phenotype in children with fetal alcohol spectrum disorders: a review. Neuroscience Biobehavioral Reviews 2007, 31:192-201.
45. Koekkoek S.K., Hulscher H.C., Dortland B.R., Hensbroek R.A., Elgersma Y., Ruigrok T.J., et al. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 2003, 301:1736-1739.
46. Kotani S., Kawahara S., Kirino Y. Purkinje cell activity during classical eyeblink conditioning in decerebrate guinea pigs. Brain Research 2006, 1068:70-81.
47. Lee T., Kim J.J. Differential effects of cerebellar, amygdalar, and hippocampal lesions on classical eyeblink conditioning in rats. The Journal of Neuroscience 2004, 24:3242-3250.
48. Lindquist D.H. Hippocampal-dependent Pavlovian conditioning in adult rats exposed to binge-like doses of ethanol as neonates. Behavioural Brain Research 2013, 242:191-199.
49. Lindquist D.H., Sokoloff G., Steinmetz J.E. Ethanol-exposed neonatal rats are impaired as adults in classical eyeblink conditioning at multiple unconditioned stimulus intensities. Brain Research 2007, 1150:155-166.
50. Lindquist D.H., Vogel R.W., Steinmetz J.E. Associative and non-associative blinking in classically conditioned adult rats. Physiology & Behavior 2009, 96:399-411.
51. 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 & Teratology 2003, 25:447-458.
52. Maren S. Central and basolateral amygdala neurons crash the aversive conditioning party: theoretical comment on Rorick-Kehn and Steinmetz (2005). Behavioral Neuroscience 2005, 119:1406-1410.
53. Mattson S.N., Crocker N., Nguyen T.T. Fetal alcohol spectrum disorders: neuropsychological and behavioral features. Neuropsychological Review 2011, 21:81-101.
54. May P.A., Gossage J.P. Estimating the prevalence of fetal alcohol syndrome: a summary. Alcohol Research & Health 2001, 25:159-167.
55. May P.A., Gossage J.P., Kalberg W.O., Robinson L.K., Buckley D., Manning M., et al. Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies. Developmental Disabilities Research Reviews 2009, 15:176-192.
56. McCormick D.A., Thompson R.F. Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. The Journal of Neuroscience 1984, 4:2811-2822.
57. Medina J.F., Nores W.L., Ohyama T., Mauk M.D. Mechanisms of cerebellar learning suggested by eyelid conditioning. Current Opinion in Neurobiology 2000, 10:717-724.
58. Murawski N.J., Jablonski S.A., Brown K.L., Stanton M.E. Effects of neonatal alcohol dose and exposure window on long delay and trace eyeblink conditioning in juvenile rats. Behavioural Brain Research 2013, 236:307-318.
59. Murawski N.J., Stanton M.E. Effects of dose and period of neonatal alcohol exposure on the context preexposure facilitation effect. Alcoholism, Clinical and Experimental Research 2011, 35:1160-1170.
60. Niccols A. Fetal alcohol syndrome and the developing socio-emotional brain. Brain and Cognition 2007, 65:135-142.
61. Penick S., Solomon P.R. Hippocampus, context, and conditioning. Behavioral Neuroscience 1991, 105:611-617.
62. Perrett S.P., Ruiz B.P., Mauk M.D. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. The Journal of Neuroscience 1993, 13:1708-1718.
63. Pierce D.R., Serbus D.C., Light K.E. Intragastric intubation of alcohol during postnatal development of rats results in selective cell loss in the cerebellum. Alcoholism, Clinical and Experimental Research 1993, 17:1275-1280.
64. Port R.L., Mikhail A.A., Patterson M.M. Differential effects of hippocampectomy on classically conditioned rabbit nictitating membrane response related to interstimulus interval. Behavioral Neuroscience 1985, 99:200-208.
65. Port R.L., Mikhail A.A., Patterson M.M. Failure of hippocampectomy to facilitate classical conditioning at an optimal interstimulus interval is not due to a "ceiling effect". Behavioral Neuroscience 1986, 100:161-164.
66. Richardson D.P., Byrnes M.L., Brien J.F., Reynolds J.N., Dringenberg H.C. Impaired acquisition in the water maze and hippocampal long-term potentiation after chronic prenatal ethanol exposure in the guinea-pig. European Journal of Neuroscience 2002, 16:1593-1598.
67. Riley E.P., McGee C.L. Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Experimental Biology and Medicine 2005, 2306:357-365.
68. Rogers R.F., Britton G.B., Steinmetz J.E. Learning-related interpositus activity is conserved across species as studied during eyeblink conditioning in the rat. Brain Research 2001, 905:171-177.
69. Rudy J.W. Context representations, context functions, and the parahippocampal-hippocampal system. Learning & Memory 2009, 16:573-585.
70. Sampson P.D., Streissguth A.P., Bookstein F.L., Little R.E., Clarren S.K., Dehaene P., et al. Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 1997, 56:317-326.
71. Schaefer G.B., Deere D. Recognition, diagnosis and treatment of fetal alcohol syndrome. The Journal of the Arkansas Medical Society 2011, 108:38-40.
72. Schmaltz L.W., Theios J. Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). Journal of Comparative & Physiological Psychology 1972, 79:328-333.
73. Schneiderman N. Interstimulus interval function of the nictitating membrane response of the rabbit under delay versus trace conditioning. Journal of Comparative & Physiological Psychology 1966, 62:397-402.
74. Servais L., Hourez R., Bearzatto B., Gall D., Schiffmann S.N., Cheron G. Purkinje cell dysfunction and alteration of long-term synaptic plasticity in fetal alcohol syndrome. Proceedings of the National Academy of Science, USA 2007, 104:9858-9863.
75. Smith M.C. CS-US interval and US intensity in classical conditioning of the rabbit's nictitating membrane response. Journal of Comparative & Physiological Psychology 1968, 66:679-687.
76. Stanton M.E., Goodlett C.R. Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcoholism, Clinical and Experimental Research 1998, 22:270-275.
77. Steinmetz J.E., Lindquist D.H. Neuronal basis of learning. Handbook of neuroscience for the behavioral sciences 2009, 507-527. John Wiley & Sons, Hoboken, NJ. G.G. Berntson, J.T. Cacioppo (Eds.).
78. Stratton K., Howe C., Battaglia F. Fetal alcohol syndrome: Diagnosis, epidemiology, prevention, and treatment 1996, National Academy Press, Washington, DC.
79. Streissguth A.P. Offspring effects of prenatal alcohol exposure from birth to 25 years: the Seattle Prospective Longitudinal Study. Clincal Psychology in Medical Settings 2007, 14:81-101.
80. Thomas J.D., Tran T.D. Choline supplementation mitigates trace, but not delay, eyeblink conditioning deficits in rats exposed to alcohol during development. Hippocampus 2012, 22:619-630.
81. Thompson R.F. In search of memory traces. Annual Review of Psychology 2005, 56:1-23.
82. Thompson R.F., Steinmetz J.E. The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 2009, 162:732-755.
83. Tran T.D., Jackson H.D., Horn K.H., Goodlett C.R. Vitamin E does not protect against neonatal ethanol-induced cerebellar damage or deficits in eyeblink classical conditioning in rats. Alcoholism, Clinical and Experimental Research 2005, 29:117-129.
84. Tran T.D., Kelly S.J. Critical periods for ethanol-induced cell loss in the hippocampal formation. Neurotoxicology & Teratology 2003, 25:519-528.
85. Tran T.D., Stanton M.E., Goodlett C.R. Binge-like ethanol exposure during the early postnatal period impairs eyeblink conditioning at short and long CS-US intervals in rats. Developmental Psychobiology 2007, 49:589-605.
86. Valenzuela C.F., Morton R.A., Diaz M.R., Topper L. Does moderate drinking harm the fetal brain? Insights from animal models. Trends in Neuroscience 2012, 35:284-292.
87. Villarreal R.P., Steinmetz J.E. Neuroscience and learning: lessons from studying the involvement of a region of cerebellar cortex in eyeblink classical conditioning. Journal of the Experimental Analysis of Behavior 2005, 84:631-652.
88. Vogel R.W., Amundson J.C., Lindquist D.H., Steinmetz J.E. Eyeblink conditioning during an interstimulus interval switch in rabbits (Oryctolagus cuniculus) using picrotoxin to disrupt cerebellar cortical input to the interpositus nucleus. Behavioral Neuroscience 2009, 123:62-74.
89. Wang L., Liu S.Q. Neural circuit and its functional roles in cerebellar cortex. Neuroscience Bulletin 2011, 27:173-184.
90. West J.R., Goodlett C.R., Bonthius D.J., Pierce D.R. Manipulating peak blood alcohol concentrations in neonatal rats: review of an animal model for alcohol-related developmental effects. Neurotoxicology 1989, 10:347-366.
91. West J.R., Hamre K.M., Pierce D.R. Delay in brain growth induced by alcohol in artificially reared rat pups. Alcohol 1984, 1:83-95.
92. Woodruff-Pak D.S., Disterhoft J.F. Where is the trace in trace conditioning?. Trends in Neuroscience 2008, 31:105-112.
93. Yamazaki T., Nagao S. Acomputational mechanism for unified gain and timing control in the cerebellum. PLoS One 2012, 7:e33319.
94. Young B.W., Sengelaub D.R., Steinmetz J.E. MK-801 administration during neonatal ethanol withdrawal attenuates interpositus cell loss and juvenile eyeblink conditioning deficits. Alcohol 2010, 44:359-369.