Age- and sex-dependent effects of footshock stress on subsequent alcohol drinking and acoustic startle behavior in mice selectively bred for high-alcohol preference

Alcoholism: Clinical and Experimental Research

Volumn 32, Issue 10, 2008, Pages 1782-1794

  Chester, Julia A ^a   Barrenha, Gustavo D ^a   Hughes, Matthew L ^a   Keuneke, Kelly J ^a  

^a PURDUE UNIVERSITY   (United States)

Author keywords

Acoustic startle; Adolescence; Alcoholism; Anxiety; Genetics

Indexed keywords

ALCOHOL;

AGE; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DRINKING BEHAVIOR; FEMALE; FLUID INTAKE; FOOTSHOCK; GENETIC PREDISPOSITION; MALE; MOUSE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SEX DIFFERENCE; STARTLE REFLEX; WEIGHT CHANGE;

AGE FACTORS; ALCOHOL DRINKING; ANIMALS; ANXIETY; BODY WEIGHT; DRINKING; FEMALE; MALE; MICE; SENSORY GATING; SEX FACTORS; STARTLE REACTION; STRESS, PSYCHOLOGICAL;

MUS;

EID: 52149083738     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2008.00763.x     Document Type: Article

References (76)

1. Adamec R, Head D, Blundell J, Burton P, Berton O (2006) Lasting anxiogenic effects of feline predator stress in mice: sex differences in vulnerability to stress and predicting severity of anxiogenic response from the stress experience. Physiol Behav 88 : 12 29.
2. Adriani W, Macri S, Pacifici R, Laviola G (2002) Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology 27 : 212 224.
3. Anisman H, Zaharia MD, Meaney MJ, Merali Z (1998) Do early-life events permanently alter behavioral and hormonal responses to stressors? Int J Dev Neurosci 16 : 149 164.
4. Arnsten AF, Shansky RM (2004) Adolescence: vulnerable period for stress-induced prefrontal cortical function? Introduction to part IV. Ann N Y Acad Sci 1021 : 143 147.
5. Baker S, Bielajew C (2007) Influence of housing on the consequences of chronic mild stress in female rats. Stress 10 : 283 293.
6. Baker SL, Kentner AC, Konkle AT, Santa-Maria Barbagallo L, Bielajew C (2006) Behavioral and physiological effects of chronic mild stress in female rats. Physiol Behav 87 : 314 322.
7. Bakshi VP, Geyer MA (1999) Ontogeny of isolation rearing-induced deficits in sensorimotor gating in rats. Physiol Behav 67 : 385 392.
8. Barrenha GD, Chester JA (2007) Genetic correlation between innate alcohol preference and fear-potentiated startle in selected mouse lines. Alcohol Clin Exp Res 31 : 1081 1088.
9. Blaszczyk J, Tajchert K (1996) Sex and strain differences of acoustic startle reaction development in adolescent albino Wistar and hooded rats. Acta Neurobiol Exp (Wars) 56 : 919 925.
10. Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978) Prestimulus effects on human startle reflex in normals and schizophrenics. Psychophysiology 15 : 339 343.
11. Brunell SC, Spear LP (2005) Effect of stress on the voluntary intake of a sweetened ethanol solution in pair-housed adolescent and adult rats. Alcohol Clin Exp Res 29 : 1641 1653.
12. Cappell H, Herman CP (1972) Alcohol and tension reduction. A review. Q J Stud Alcohol 33 : 33 64.
13. 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.
14. Chester JA, de Paula Barrenha G, DeMaria A, Finegan A (2006) Different effects of stress on alcohol drinking behaviour in male and female mice selectively bred for high alcohol preference. Alcohol Alcohol 41 : 44 53.
15. Colombo G, Agabio R, Lobina C, Reali R, Zocchi A, Fadda F, Gessa GL (1995) Sardinian alcohol-preferring rats: a genetic animal model of anxiety. Physiol Behav 57 : 1181 1185.
16. Conger JJ (1956) Alcoholism: theory, problem and challenge. II. Reinforcement theory and the dynamics of alcoholism. Q J Stud Alcohol 17 : 296 305.
17. Conti LH, Printz MP (2003) Rat strain-dependent effects of repeated stress on the acoustic startle response. Behav Brain Res 144 : 11 18.
18. Coplan JD, Andrews MW, Rosenblum LA, Owens MJ, Friedman S, Gorban JM, Nemeroff CB (1996) Persistent elevations of cerebrospinal fluid concentrations of corticotrophin-releasing factor in adult non-human primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc Natl Acad Sci U S A 93 : 1619 1623.
19. Davis M (1989) Sensitization of the acoustic startle reflex by footshock. Behav Neurosci 103 : 495 503.
20. Davis M (1990) Animal models of anxiety based on classical conditioning: the conditioned emotional response (CER) and the fear-potentiated startle effect. Pharmacol Ther 47 : 147 165.
21. Davis M (1998) Are different parts of the extended amygdala involved in fear versus anxiety? Biol Psychiatry 44 : 1239 1247.
22. Dixon WJ (1950) Analysis of extreme values. Ann Math Stat 21 : 488 506.
23. Doremus TL, Brunell SC, Rajendran P, Spear LP (2005) Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 29 : 1796 1808.
24. Dubovicky M, Paton S, Morris M, Mach M, Lucot JB (2007) Effects of combined exposure to pyridostigmine bromide and shaker stress on acoustic startle response, pre-pulse inhibition and open field behavior in mice. J Appl Toxicol 27 : 276 283.
25. Ellenbroek BA, van den Kroonenberg PT, Cools AR (1998) The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 30 : 251 260.
26. Enoch MA (2006) Genetic and environmental influences on the development of alcoholism: resilience vs. risk. Ann N Y Acad Sci 1094 : 193 201.
27. Faraday MM (2002) Rat sex and strain differences in responses to stress. Physiol Behav 75 : 507 522.
28. Farr SA, Flood JF, Scherrer JF, Kaiser FE, Taylor GT, Morley JE (1995) Effect of ovarian steroids on footshock avoidance learning and retention in female mice. Physiol Behav 58 : 715 723.
29. Garrick T, Morrow N, Shalev AY, Eth S (2001) Stress-induced enhancement of auditory startle: an animal model of posttraumatic stress disorder. Psychiatry 64 : 346 354.
30. Goldman L, Winget C, Hollingshead GW, Levine S (1973) Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 12 : 199 211.
31. Grahame NJ, Li TK, Lumeng L (1999) Selective breeding for high and low alcohol preference in mice. Behav Genet 29 : 47 57.
32. Grant BF, Dawson DA (1998) Age of onset of drug use and its association with DSM-IV drug abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 10 : 163 173.
33. Grant JD, Scherrer JF, Lynskey MT, Lyons MJ, Eisen SA, Tsuang MT, True WR, Bucholz KK (2006) Adolescent alcohol use is a risk factor for adult alcohol and drug dependence: evidence from a twin design. Psychol Med 36 : 109 118.
34. Grillon C, Davis M (1997) Effects of stress and shock anticipation on prepulse inhibition of the startle reflex. Psychophysiology 34 : 511 517.
35. Hall FS (1998) Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit Rev Neurobiol 12 : 129 162.
36. Hascoet M, Colombel MC, Bourin M (1999) Influence of age on behavioural response in the light/dark paradigm. Physiol Behav 66 : 567 570.
37. Hefner K, Holmes A (2007) Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 176 : 210 215.
38. Heim C, Nemeroff CB (1999) The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biol Psychiatry 46 : 1509 1522.
39. Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM (2001) Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology (Berl) 158 : 366 373.
40. Johnson JL, Leff M (1999) Children of substance abusers: overview of research findings. Pediatrics 103 : 1085 1099.
41. Keppel G (1991) Design and Analysis: A Researcher's Handbook. 3rd ed. Prentice-Hall, Upper Saddle River.
42. Kessler RC, Crum RM, Warner LA, Nelson CB, Schulenberg J, Anthony JC (1997) Lifetime co-occurrence of DSM-III-R alcohol abuse and dependence with other psychiatric disorders in the National Comorbidity Survey. Arch Gen Psychiatry 54 : 313 321.
43. King KM, Chassin L (2007) A prospective study of the effects of age of initiation of alcohol and drug use on young adult substance dependence. J Stud Alcohol Drugs 68 : 256 265.
44. Kinkead B, Yan F, Owens MJ, Nemeroff CB (2008) Endogenous neurotensin is involved in estrous cycle related alterations in prepulse inhibition of the acoustic startle reflex in female rats. Psychoneuroendocrinology 33 : 178 187.
45. Koch M (1998) Sensorimotor gating changes across the estrous cycle in female rats. Physiol Behav 64 : 625 628.
46. Koehl M, Lemaire V, Mayo W, Abrous DN, Maccari S, Piazza PV, Le MM, Vallee M (2002) Individual vulnerability to substance abuse and affective disorders: role of early environmental influences. Neurotox Res 4 : 281 296.
47. Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24 : 97 129.
48. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM (2000) Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122 : 81 103.
49. Laviola G, Adriani W, Morley-Fletcher S, Terranova ML (2002) Peculiar response of adolescent mice to acute and chronic stress and to amphetamine: evidence of sex differences. Behav Brain Res 130 : 117 125.
50. Marcondes FK, Miguel KJ, Melo LL, Spadari-Bratfisch RC (2001) Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74 : 435 440.
51. Mathews IZ, Wilton A, Styles A, McCormick CM (2008) Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats. Behav Brain Res 190 : 33 40.
52. McCormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86 : 220 233.
53. Meziane H, Ouagazzal AM, Aubert L, Wietrzych M, Krezel W (2007) Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav 6 : 192 200.
54. Millstein RA, Ralph RJ, Yang RJ, Holmes A (2006) Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes Brain Behav 5 : 346 354.
55. Phillips TJ, Roberts AJ, Lessov CN (1997) Behavioral sensitization to ethanol: genetics and the effects of stress. Pharmacol Biochem Behav 57 : 487 493.
56. Piazza PV, Le Moal M (1998) The role of stress in drug self-administration. Trends Pharmacol Sci 19 : 67 74.
57. Pijlman FT, Herremans AH, van de KJ, Kruse CG, van Ree JM (2003) Behavioural changes after different stress paradigms: prepulse inhibition increased after physical, but not emotional stress. Eur Neuropsychopharmacol 13 : 369 380.
58. Plappert CF, Rodenbucher AM, Pilz PK (2005) Effects of sex and estrous cycle on modulation of the acoustic startle response in mice. Physiol Behav 84 : 585 594.
59. Pohl J, Olmstead MC, Wynne-Edwards KE, Harkness K, Menard JL (2007) Repeated exposure to stress across the childhood-adolescent period alters rats' anxiety- and depression-like behaviors in adulthood: the importance of stressor type and gender. Behav Neurosci 121 : 462 474.
60. Roman E, Nylander I (2005) The impact of emotional stress early in life on adult voluntary ethanol intake-results of maternal separation in rats. Stress 8 : 157 174.
61. Roman E, Ploj K, Nylander I (2004) Maternal separation has no effect on voluntary ethanol intake in female Wistar rats. Alcohol 33 : 31 39.
62. Romeo RD, Bellani R, Karatsoreos IN, Chhua N, Vernov M, Conrad CD, McEwen BS (2006) Stress history and pubertal development interact to shape hypothalamic-pituitary-adrenal axis plasticity. Endocrinology 147 : 1664 1674.
63. Romeo RD, McEwen BS (2006) Stress and the adolescent brain. Ann N Y Acad Sci 1094 : 202 214.
64. Schneider T, Popik P (2007) Attenuation of estrous cycle-dependent marble burying in female rats by acute treatment with progesterone and antidepressants. Psychoneuroendocrinology 32 : 651 659.
65. Servatius RJ, Ottenweller JE, Bergen MT, Soldan S, Natelson BH (1994) Persistent stress-induced sensitization of adrenocortical and startle responses. Physiol Behav 56 : 945 954.
66. Sher KJ (1987) Stress response dampening, in Psychological Theories of Drinking and Alcoholism (Blane HT, Leonard KE eds pp 227 271. Guilford Press, New York.
67. Shors TJ, Leuner B (2003) Estrogen-mediated effects on depression and memory formation in females. J Affect Disord 74 : 85 96.
68. Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158 : 343 359.
69. Song M, Wang XY, Zhao M, Wang XY, Zhai HF, Lu L (2007) Role of stress in acquisition of alcohol-conditioned place preference in adolescent and adult mice. Alcohol Clin Exp Res 31 : 2001 2005.
70. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24 : 417 463.
71. Stone EA, Quartermain D (1997) Greater behavioral effects of stress in immature as compared to mature male mice. Physiol Behav 63 : 143 145.
72. Tabakoff B, Jafee RC, Ritzmann RF (1978) Corticosterone concentrations in mice during ethanol drinking and withdrawal. J Pharm Pharmacol 30 : 371 374.
73. Varty GB, Powell SB, Lehmann-Masten V, Buell MR, Geyer MA (2006) Isolation rearing of mice induces deficits in prepulse inhibition of the startle response. Behav Brain Res 169 : 162 167.
74. Wagner EF (1993) Delay of gratification, coping with stress, and substance use in adolescence. Exp Clin Psychopharmacol 1 : 27 43.
75. Weiss F, Lorang MT, Bloom FE, Koob GF (1993) Oral alcohol self-administration stimulates dopamine release in the rat nucleus accumbens: genetic and motivational determinants. J Pharmacol Exp Ther 267 : 250 258.
76. Zimmermann US, Blomeyer D, Laucht M, Mann KF (2007) How gene-stress-behavior interactions can promote adolescent alcohol use: the roles of predrinking allostatic load and childhood behavior disorders. Pharmacol Biochem Behav 86 : 246 262.