Differential effects of acute alcohol on prepulse inhibition and event-related potentials in adolescent and adult Wistar rats

Alcoholism: Clinical and Experimental Research

Volumn 32, Issue 12, 2008, Pages 2062-2073

  Pian, Jerry P ^a   Criado, Jose R ^a   Ehlers, Cindy L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Adolescence; Alcohol; ERP; Ethanol; PPI

Indexed keywords

ALCOHOL;

ADOLESCENT; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN CORTEX; COGNITION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ELECTROENCEPHALOGRAM; EVENT RELATED POTENTIAL; FRONTAL CORTEX; MALE; NEUROPHYSIOLOGY; NONHUMAN; PARIETAL LOBE; PREPULSE INHIBITION; PRIORITY JOURNAL; RAT;

ACOUSTIC STIMULATION; AGE FACTORS; ANIMALS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; ETHANOL; EVOKED POTENTIALS; EVOKED POTENTIALS, AUDITORY; MALE; NERVE NET; RATS; RATS, WISTAR; STARTLE REACTION;

RATTUS; RATTUS NORVEGICUS;

EID: 57249105132     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2008.00794.x     Document Type: Article

References (90)

1. Adler LE, Pachtman E, Franks RD, Pecevich M, Waldo MC, Freedman R (1982) Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biol Psychiatry 17 : 639 654.
2. Boutros NN, Korzyukov O, Jansen B, Feingold A, Bell M (2004) Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Res 126 : 203 215.
3. Bowirrat A, Oscar-Berman M (2005) Relationship between dopaminergic neurotransmission, alcoholism, and reward deficiency syndrome. Am J Med Genet B Neuropsychiatr Genet 132B : 29 37.
4. Brenowitz S, David J, Trussell L (1998) Enhancement of synaptic efficacy by presynaptic GABA(B) receptors. Neuron 20 : 135 141.
5. Brunell SC, Spear LP (2006) Effects of acute ethanol or amphetamine administration on the acoustic startle response and prepulse inhibition in adolescent and adult rats. Psychopharmacology (Berl) 186 : 579 586.
6. van den Buuse M (2003) Deficient prepulse inhibition of acoustic startle in Hooded-Wistar rats compared with Sprague-Dawley rats. Clin Exp Pharmacol Physiol 30 : 254 261.
7. van den Buuse M, Garner B, Koch M (2003) Neurodevelopmental animal models of schizophrenia: effects on prepulse inhibition. Curr Mol Med 3 : 459 471.
8. Chester JA, Barrenha GD (2007) Acoustic startle at baseline and during acute alcohol withdrawal in replicate mouse lines selectively bred for high or low alcohol preference. Alcohol Clin Exp Res 31 : 1633 1644.
9. Chester JA, Mullins AJ, Nguyen CH, Watts VJ, Meisel RL (2006) Repeated quinpirole treatments produce neurochemical sensitization and associated behavioral changes in female hamsters. Psychopharmacology (Berl) 188 : 53 62.
10. Chugani HT, Phelps ME, Mazziotta JC (1987) Positron emission tomography study of human brain functional development. Ann Neurol 22 : 487 497.
11. Cicero TJ (1979) A critique of animal analogs in alcoholism, in Biochemistry and Pharmacology of Ethanol (Majchrowicz E, Noble EP eds pp 553 560. Plenum Press, New York.
12. Crews F, He J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86 : 189 199.
13. Curtin JJ, Lang AR, Patrick CJ, Stritzke WG (1998) Alcohol and fear-potentiated startle: the role of competing cognitive demands in the stress-reducing effects of intoxication. J Abnorm Psychol 107 : 547 557.
14. Davis M, Gendelman DS, Tischler MD, Gendelman PM (1982) A primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 2 : 791 805.
15. Ehlers CL (1988) ERP responses to ethanol and diazepam administration in squirrel monkeys. Alcohol 5 : 315 320.
16. Ehlers CL, Chaplin RI, Lumeng L, Li TK (1991) Electrophysiological response to ethanol in P and NP rats. Alcohol Clin Exp Res 15 : 739 744.
17. Ehlers CL, Kaneko WM, Wall TL, Chaplin RI (1992) Effects of dizocilpine (MK-801) and ethanol on the EEG and event-related potentials (ERPS) in rats. Neuropharmacology 31 : 369 378.
18. Ehlers CL, Li TK, Lumeng L, Hwang BH, Somes C, Jimenez P, Mathe AA (1998a) Neuropeptide Y levels in ethanol-naive alcohol-preferring and nonpreferring rats and in Wistar rats after ethanol exposure. Alcohol Clin Exp Res 22 : 1778 1782.
19. Ehlers CL, Slutske WS, Gilder DA, Lau P, Wilhelmsen KC (2006) Age at first intoxication and alcohol use disorders in Southwest California Indians. Alcohol Clin Exp Res 30 : 1856 1865.
20. Ehlers CL, Somes C, Cloutier D (1998b) Are some of the effects of ethanol mediated through NPY? Psychopharmacology (Berl) 139 : 136 144.
21. Ehlers CL, Somes C, Lopez A, Kirby D, Rivier JE (1997) Electrophysiological actions of neuropeptide Y and its analogs: new measures for anxiolytic therapy? Neuropsychopharmacology 17 : 34 43.
22. Ellwanger J, Geyer MA, Braff DL (2003) The relationship of age to prepulse inhibition and habituation of the acoustic startle response. Biol Psychol 62 : 175 195.
23. Engel AK, Konig P, Kreiter AK, Schillen TB, Singer W (1992) Temporal coding in the visual cortex: new vistas on integration in the nervous system. Trends Neurosci 15 : 218 226.
24. Farid M, Martinez ZA, Geyer MA, Swerdlow NR (2000) Regulation of sensorimotor gating of the startle reflex by serotonin 2A receptors. Ontogeny and strain differences. Neuropsychopharmacology 23 : 623 632.
25. Gomez Gonzalez CM, Clark VP, Fan S, Luck SJ, Hillyard SA (1994) Sources of attention-sensitive visual event-related potentials. Brain Topogr 7 : 41 51.
26. Grant BF, Stinson FS, Harford TC (2001) Age at onset of alcohol use and DSM-IV alcohol abuse and dependence: a 12-year follow-up. J Subst Abuse 13 : 493 504.
27. Grillon C, Sinha R, Ameli R, O'Malley SS (2000) Effects of alcohol on baseline startle and prepulse inhibition in young men at risk for alcoholism and/or anxiety disorders. J Stud Alcohol 61 : 46 54.
28. Hansen JC, Hillyard SA (1980) Endogenous brain potentials associated with selective auditory attention. Electroencephalogr Clin Neurophysiol 49 : 277 290.
29. Herrmann CS, Demiralp T (2005) Human EEG gamma oscillations in neuropsychiatric disorders. Clin Neurophysiol 116 : 2719 2733.
30. Herrmann CS, Knight RT (2001) Mechanisms of human attention: event-related potentials and oscillations. Neurosci Biobehav Rev 25 : 465 476.
31. Hillyard SA, Hansen JC (1986) Attention: electrophysiological approaches, in Psychophysiology: Systems, Processes, and Applications (Coles MGH, Donchin E, Porges SW eds pp 227 243. Guilford Press, New York.
32. Hillyard SA, Kutas M (1983) Electrophysiology of cognitive processing. Annu Rev Psychol 34 : 33 61.
33. Hince DA, Martin-Iverson MT (2005) Differences in prepulse inhibition (PPI) between Wistar and Sprague-Dawley rats clarified by a new method of PPI standardization. Behav Neurosci 119 : 66 77.
34. Hoffman DC, Donovan H (1994) D1 and D2 dopamine receptor antagonists reverse prepulse inhibition deficits in an animal model of schizophrenia. Psychopharmacology (Berl) 115 : 447 453.
35. Hollstedt C, Olsson O, Rydberg U (1980) Effects of ethanol on the developing rat. II. Coordination as measured by the tilting-plane test. Med Biol 58 : 164 168.
36. Hsieh MH, Swerdlow NR, Braff DL (2006) Effects of background and prepulse characteristics on prepulse inhibition and facilitation: implications for neuropsychiatric research. Biol Psychiatry 59 : 555 559.
37. Hutchison KE, Rohsenow D, Monti P, Palfai T, Swift R (1997) Prepulse inhibition of the startle reflex: preliminary study of the effects of a low dose of alcohol in humans. Alcohol Clin Exp Res 21 : 1312 1319.
38. Huttenlocher PR (1979) Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res 163 : 195 205.
39. Huttenlocher PR (1984) Synapse elimination and plasticity in developing human cerebral cortex. Am J Ment Defic 88 : 488 496.
40. Jaaskelainen IP, Lehtokoski A, Alho K, Kujala T, Pekkonen E, Sinclair JD, Naatanen R, Sillanaukee P (1995) Low dose of ethanol suppresses mismatch negativity of auditory event-related potentials. Alcohol Clin Exp Res 19 : 607 610.
41. Jones AE, McBride WJ, Murphy JM, Lumeng L, Li T, Shekhar A, McKinzie DL (2000) Effects of ethanol on startle responding in alcohol-preferring and -non-preferring rats. Pharmacol Biochem Behav 67 : 313 318.
42. Kaneko WM, Phillips EL, Riley EP, Ehlers CL (1996) EEG findings in fetal alcohol syndrome and Down syndrome children. Electroencephalogr Clin Neurophysiol 98 : 20 28.
43. Kaneko WM, Riley EP, Ehlers CL (1993) Electrophysiological and behavioral findings in rats prenatally exposed to alcohol. Alcohol 10 : 169 178.
44. Kinney GG, Wilkinson LO, Saywell KL, Tricklebank MD (1999) Rat strain differences in the ability to disrupt sensorimotor gating are limited to the dopaminergic system, specific to prepulse inhibition, and unrelated to changes in startle amplitude or nucleus accumbens dopamine receptor sensitivity. J Neurosci 19 : 5644 5653.
45. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59 : 107 128.
46. Koch M, Friauf E (1995) Glycine receptors in the caudal pontine reticular formation: are they important for the inhibition of the acoustic startle response? Brain Res 671 : 63 72.
47. Koch M, Schnitzler HU (1997) The acoustic startle response in rats - circuits mediating evocation, inhibition and potentiation. Behav Brain Res 89 : 35 49.
48. Kodsi MH, Swerdlow NR (1995) Prepulse inhibition in the rat is regulated by ventral and caudodorsal striato-pallidal circuitry. Behav Neurosci 109 : 912 928.
49. Light GA, Braff DL (2005) Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. Arch Gen Psychiatry 62 : 127 136.
50. Little PJ, Kuhn CM, Wilson WA, Swartzwelder HS (1996) Differential effects of ethanol in adolescent and adult rats. Alcohol Clin Exp Res 20 : 1346 1351.
51. Lovinger DM, Homanics GE (2007) Tonic for what ails us? high-affinity GABAA receptors and alcohol. Alcohol 41 : 139 143.
52. Lumeng L, Hawkins TD, Li TK (1977) New strains of rats with alcohol preference and non-preference, in Alcohol and Aldehyde Metabolizing Systems III. Intermediary Metabolism and Neurochemistry (Thurman RG, Williamson JR, Drott H, Chance B eds pp 537 544. Academic Press, New York.
53. Martin-Iverson MT, Stevenson KN (2005) Apomorphine effects on emotional modulation of the startle reflex in rats. Psychopharmacology (Berl) 181 : 60 70.
54. Merica H, Fortune RD (2004) State transitions between wake and sleep, and within the ultradian cycle, with focus on the link to neuronal activity. Sleep Med Rev 8 : 473 485.
55. Merica H, Gaillard JM (1992) The EEG of the sleep onset period in insomnia: a discriminant analysis. Physiol Behav 52 : 199 204.
56. Moy SS, Duncan GE, Knapp DJ, Breese GR (1998) Sensitivity to ethanol across development in rats: comparison to [3H]zolpidem binding. Alcohol Clin Exp Res 22 : 1485 1492.
57. Noldy NE, Carlen PL (1990) Acute, withdrawal, and chronic alcohol effects in man: event-related potential and quantitative EEG techniques. Ann Med 22 : 333 339.
58. Ouagazzal A, Grottick AJ, Moreau J, Higgins GA (2001) Effect of LSD on prepulse inhibition and spontaneous behavior in the rat. A pharmacological analysis and comparison between two rat strains. Neuropsychopharmacology 25 : 565 575.
59. Padmanabhapillai A, Tang Y, Ranganathan M, Rangaswamy M, Jones KA, Chorlian DB, Kamarajan C, Stimus A, Kuperman S, Rohrbaugh J, O'Connor SJ, Bauer LO, Schuckit MA, Begleiter H, Porjesz B (2006) Evoked gamma band response in male adolescent subjects at high risk for alcoholism during a visual oddball task. Int J Psychophysiol 62 : 262 271.
60. Palmer AA, Dulawa SC, Mottiwala AA, Conti LH, Geyer MA, Printz MP (2000) Prepulse startle deficit in the Brown Norway rat: a potential genetic model. Behav Neurosci 114 : 374 388.
61. Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates. 2nd edn. Academic Press, Sydney.
62. Perrin RG, Hockman CH, Kalant H, Livingston KE (1974) Acute effects of ethanol on spontaneous and auditory evoked electrical activity in cat brain. Electroencephalogr Clin Neurophysiol 36 : 19 31.
63. Pian JP, Criado JR, Walker BM, Ehlers CL (2008) Differential effects of acute alcohol on EEG and sedative responses in adolescent and adult Wistar rats. Brain Res 1194 : 28 36.
64. Picton TW, Taylor MJ (2007) Electrophysiological evaluation of human brain development. Dev Neuropsychol 31 : 249 278.
65. Pohorecky LA, Cagan M, Brick J, Jaffe SL (1976) The startle response in rats: effect of ethanol. Pharmacol Biochem Behav 4 : 311 316.
66. Rigdon GC (1990) Differential effects of apomorphine on prepulse inhibition of acoustic startle reflex in two rat strains. Psychopharmacology (Berl) 102 : 419 421.
67. Rodd ZA, Bell RL, McKinzie DL, Webster AA, Murphy JM, Lumeng L, Li TK, McBride WJ (2004) Low-dose stimulatory effects of ethanol during adolescence in rat lines selectively bred for high alcohol intake. Alcohol Clin Exp Res 28 : 535 543.
68. Salamy A, Williams HL (1973) The effects of alcohol on sensory evoked and spontaneous cerebral potentials in man. Electroencephalogr Clin Neurophysiol 35 : 3 11.
69. Silveri MM, Spear LP (1998) Decreased sensitivity to the hypnotic effects of ethanol early in ontogeny. Alcohol Clin Exp Res 22 : 670 676.
70. Silveri MM, Spear LP (2000) Ontogeny of ethanol elimination and ethanol-induced hypothermia. Alcohol 20 : 45 53.
71. Sipes TE, Geyer MA (1995) DOI disruption of prepulse inhibition of startle in the rat is mediated by 5-HT(2A) and not by 5-HT(2C) receptors. Behav Pharmacol 6 : 839 842.
72. Slawecki CJ (2002) Altered EEG responses to ethanol in adult rats exposed to ethanol during adolescence. Alcohol Clin Exp Res 26 : 246 254.
73. Slawecki CJ, Betancourt M, Li TK, Ehlers CL (2000a) Neurophysiological findings and drinking levels in high alcohol drinking (HAD) and low alcohol drinking (LAD) rats. Alcohol Clin Exp Res 24 : 1492 1499.
74. Slawecki CJ, Ehlers CL (2005) Enhanced prepulse inhibition following adolescent ethanol exposure in Sprague-Dawley rats. Alcohol Clin Exp Res 29 : 1829 1836.
75. Slawecki CJ, Roth J, Gilder A (2006) Neurobehavioral profiles during the acute phase of ethanol withdrawal in adolescent and adult Sprague-Dawley rats. Behav Brain Res 170 : 41 51.
76. Slawecki CJ, Thorsell A, Ehlers CL (2004) Long-term neurobehavioral effects of alcohol or nicotine exposure in adolescent animal models. Ann N Y Acad Sci 1021 : 448 452.
77. Slawecki CJ, Walpole T, Purdy RH, Ehlers CL (2000b) Comparison of the neurophysiological effects of allopregnanolone and ethanol in rats. Psychopharmacology (Berl) 149 : 351 359.
78. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24 : 417 463.
79. Swerdlow NR, Geyer MA, Braff DL (2001) Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 156 : 194 215.
80. Swerdlow NR, Geyer MA, Shoemaker JM, Light GA, Braff DL, Stevens KE, Sharp R, Breier M, Neary A, Auerbach PP (2006) Convergence and divergence in the neurochemical regulation of prepulse inhibition of startle and N40 suppression in rats. Neuropsychopharmacology 31 : 506 515.
81. Swerdlow NR, Shoemaker JM, Auerbach PP, Pitcher L, Goins J, Platten A (2004) Heritable differences in the dopaminergic regulation of sensorimotor gating. II. Temporal, pharmacologic and generational analyses of apomorphine effects on prepulse inhibition. Psychopharmacology (Berl) 174 : 452 462.
82. Swerdlow NR, Varty GB, Geyer MA (1998) Discrepant findings of clozapine effects on prepulse inhibition of startle: is it the route or the rat? Neuropsychopharmacology 18 : 50 56.
83. Teicher MH, Anderson SL, Hostetter JC Jr. (1995) Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Brain Res Dev Brain Res 89 : 167 172.
84. Thatcher RW, Walker RA, Giudice S (1987) Human cerebral hemispheres develop at different rates and ages. Science 236 : 1110 1113.
85. Varty GB, Bakshi VP, Geyer MA (1999) M100907, a serotonin 5-HT2A receptor antagonist and putative antipsychotic, blocks dizocilpine-induced prepulse inhibition deficits in Sprague-Dawley and Wistar rats. Neuropsychopharmacology 20 : 311 321.
86. Wagner T, Pilz PK, Fendt M (2000) The superior olivary complex is necessary for the full expression of the acoustic but not tactile startle response in rats. Behav Brain Res 108 : 181 188.
87. Wan FJ, Geyer MA, Swerdlow NR (1995) Presynaptic dopamine-glutamate interactions in the nucleus accumbens regulate sensorimotor gating. Psychopharmacology (Berl) 120 : 433 441.
88. Wan FJ, Taaid N, Swerdlow NR (1996) Do D1/D2 interactions regulate prepulse inhibition in rats? Neuropsychopharmacology 14 : 265 274.
89. Weber M, Swerdlow NR (2008) Rat strain differences in startle gating-disruptive effects of apomorphine occur with both acoustic and visual prepulses. Pharmacol Biochem Behav 88 : 306 311.
90. White AM, Ghia AJ, Levin ED, Swartzwelder HS (2000) Binge pattern ethanol exposure in adolescent and adult rats: differential impact on subsequent responsiveness to ethanol. Alcohol Clin Exp Res 24 : 1251 1256.