Adolescent alcohol exposure persistently impacts adult neurobiology and behavior

Pharmacological Reviews

Volumn 68, Issue 4, 2016, Pages 1074-1109

  Crews, Fulton T ^a   Vetreno, Ryan P ^a   Broadwater, Margaret A ^a   Robinson, Donita L ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; DOPAMINE; SEROTONIN;

ADOLESCENCE; ADOLESCENT; ADULT; ADULTHOOD; ALCOHOLISM; ANXIETY; BINGE DRINKING; BRAIN DEVELOPMENT; BRAIN MATURATION; CHOLINERGIC SYSTEM; DRINKING BEHAVIOR; DRUG SELF ADMINISTRATION; ELECTROENCEPHALOGRAPHY; EPIGENETICS; EXPOSURE; GENE EXPRESSION; GENE INDUCTION; HIPPOCAMPUS; HUMAN; INSTRUMENTAL CONDITIONING; MODEL; MONOAMINERGIC SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NEUROBIOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RODENT MODEL; SLEEP; SOCIAL BEHAVIOR; SPATIAL LEARNING; UNDERAGE DRINKING;

EID: 85015087604     PISSN: 00316997     EISSN: 15210081     Source Type: Journal    
DOI: 10.1124/pr.115.012138     Document Type: Review

References (382)

1. Abrous DN, Koehl M, and Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523-569.
2. Acheson SK, Bearison C, Risher ML, Abdelwahab SH, Wilson WA, and Swartzwelder HS (2013) Effects of acute or chronic ethanol exposure during adolescence on behavioral inhibition and efficiency in a modified water maze task. PLoS One 8: e77768.
3. Acheson SK, Stein RM, and Swartzwelder HS (1998) Impairment of semantic and figural memory by acute ethanol: age-dependent effects. Alcohol Clin Exp Res 22: 1437-1442.
4. Agrawal A, Sartor CE, Lynskey MT, Grant JD, Pergadia ML, Grucza R, Bucholz KK, Nelson EC, Madden PA, Martin NG, et al. (2009) Evidence for an interaction between age at first drink and genetic influences on DSM-IV alcohol dependence symptoms. Alcohol Clin Exp Res 33:2047-2056.
5. Alaux-Cantin S, Warnault V, Legastelois R, Botia B, Pierrefiche O, Vilpoux C, and Naassila M (2013) Alcohol intoxications during adolescence increase motivation for alcohol in adult rats and induce neuroadaptations in the nucleus accumbens. Neuropharmacology 67:521-531.
6. Alfonso-Loeches S and Guerri C (2011) Molecular and behavioral aspects of the actions of alcohol on the adult and developing brain. Crit Rev Clin Lab Sci 48:19-47
7. Alfonso-Loeches S, Ureña-Peralta J, Morillo-Bargues MJ, Gómez-Pinedo U, and Guerri C (2016) Ethanol-induced TLR4/NLRP3 neuroinflammatory response in microglial cells promotes leukocyte infiltration across the BBB. Neurochem Res 41:193-209.
8. Altman J and Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
9. Alvarez-Buylla A and Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629-634.
10. Andero R, Choi DC, and Ressler KJ (2014) BDNF-TrkB receptor regulation of distributed adult neural plasticity, memory formation, and psychiatric disorders. Prog Mol Biol Transl Sci 122:169-192.
11. Andersen SL, Rutstein M, Benzo JM, Hostetter JC, and Teicher MH (1997) Sex differences in dopamine receptor overproduction and elimination. Neuroreport 8: 1495-1498.
12. Andersen SL and Teicher MH (2008) Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci 31:183-191.
13. Andersen SL, Thompson AT, Rutstein M, Hostetter JC, and Teicher MH (2000) Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167-169.
14. Anderson RI, Varlinskaya EI, and Spear LP (2010) Ethanol-induced conditioned taste aversion in male Sprague-Dawley rats: impact of age and stress. Alcohol Clin Exp Res 34:2106-2115.
15. Andersson B, Hansagi H, Damström Thakker K, and Hibell B (2002) Long-term trends in drinking habits among Swedish teenagers: National School Surveys 1971-1999. Drug Alcohol Rev 21:253-260.
16. Armstrong DM, Bruce G, Hersh LB, and Gage FH (1987) Development of cholinergic neurons in the septal/diagonal band complex of the rat. Brain Res 433:249-256
17. Asato MR, Sweeney JA, and Luna B (2006) Cognitive processes in the development of TOL performance. Neuropsychologia 44:2259-2269.
18. Badanich KA, Adler KJ, and Kirstein CL (2006) Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 550:95-106.
19. Banasr M and Duman RS (2007) Regulation of neurogenesis and gliogenesis by stress and antidepressant treatment. CNS Neurol Disord Drug Targets 6:311-320.
20. Barak B, Feldman N, and Okun E (2014) Toll-like receptors as developmental tools that regulate neurogenesis during development: an update. Front Neurosci 8:272
21. Bauer LO and Hesselbrock VM (1999) P300 decrements in teenagers with conduct problems: implications for substance abuse risk and brain development. Biol Psychiatry 46:263-272.
22. Bauer LO and Hesselbrock VM (2003) Brain maturation and subtypes of conduct disorder: interactive effects on p300 amplitude and topography in male adolescents. J Am Acad Child Adolesc Psychiatry 42:106-115.
23. Bava S and Tapert SF (2010) Adolescent brain development and the risk for alcohol and other drug problems. Neuropsychol Rev 20:398-413.
24. Bava S, Thayer R, Jacobus J, Ward M, Jernigan TL, and Tapert SF (2010) Longitudinal characterization of white matter maturation during adolescence. Brain Res 1327:38-46.
25. Berman SM, Noble EP, Antolin T, Sheen C, Conner BT, and Ritchie T (2006) P300 development during adolescence: effects of DRD2 genotype. Clin Neurophysiol 117: 649-659.
26. Berridge KC and Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369
27. Blakemore SJ and Robbins TW (2012) Decision-making in the adolescent brain. Nat Neurosci 15:1184-1191.
28. Blednov YA, Benavidez JM, Geil C, Perra S, Morikawa H, and Harris RA (2011) Activation of inflammatory signaling by lipopolysaccharide produces a prolonged increase of voluntary alcohol intake in mice. Brain Behav Immun 25 (Suppl 1): S92-S105.
29. Boulanger LM and Shatz CJ (2004) Immune signalling in neural development, synaptic plasticity and disease. Nat Rev Neurosci 5:521-531.
30. Bourin M and Hascoët M (2003) The mouse light/dark box test. Eur J Pharmacol 463: 55-65.
31. Boutros N, Semenova S, Liu W, Crews FT, and Markou A (2014) Adolescent intermittent ethanol exposure is associated with increased risky choice and decreased dopaminergic and cholinergic neuron markers in adult rats. Int J Neuropsychopharmacol 18: pyu003.
32. Boutros N, Semenova S, and Markou A (2016) Adolescent alcohol exposure decreased sensitivity to nicotine in adult Wistar rats. Addict Biol 21:826-834.
33. Brasser SM and Spear NE (2002) Physiological and behavioral effects of acute ethanol hangover in juvenile, adolescent, and adult rats. Behav Neurosci 116:305-320
34. Briones TL and Woods J (2013) Chronic binge-like alcohol consumption in adolescence causes depression-like symptoms possibly mediated by the effects of BDNF on neurogenesis. Neuroscience 254:324-334.
35. Broadwater M and Spear LP (2013a) Age differences in fear retention and extinction in male Sprague-Dawley rats: effects of ethanol challenge during conditioning. Behav Brain Res 252:377-387.
36. Broadwater M and Spear LP (2013b) Consequences of ethanol exposure on cued and contextual fear conditioning and extinction differ depending on timing of exposure during adolescence or adulthood. Behav Brain Res 256:10-19.
37. Broadwater MA and Spear LP (2014a) Tone conditioning potentiates rather than overshadows context fear in adult animals following adolescent ethanol exposure. Dev Psychobiol 56:1150-1155.
38. Broadwater M, Varlinskaya EI, and Spear LP (2013c) Effects of voluntary access to sweetened ethanol during adolescence on intake in adulthood. Alcohol Clin Exp Res 37:1048-1055.
39. Broadwater MA, Liu W, Crews FT, and Spear LP (2014b) Persistent loss of hippocampal neurogenesis and increased cell death following adolescent, but not adult, chronic ethanol exposure. Dev Neurosci 36:297-305.
40. Bromberg-Martin ES, Matsumoto M, and Hikosaka O (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834.
41. Brown RE, Basheer R, McKenna JT, Strecker RE, and McCarley RW (2012) Control of sleep and wakefulness. Physiol Rev 92:1087-1187.
42. Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, and Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
43. Brown SA, Tapert SF, Granholm E, and Delis DC (2000) Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin Exp Res 24:164-171
44. Brown SA, Vik PW, Patterson TL, Grant I, and Schuckit MA (1995) Stress, vulnerability and adult alcohol relapse. J Stud Alcohol 56:538-545.
45. Brunell SC and 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.
46. Calabrese E, Badea A, Watson C, and Johnson GA (2013) A quantitative magnetic resonance histology atlas of postnatal rat brain development with regional estimates of growth and variability. Neuroimage 71:196-206.
47. Casey BJ, Galvan A, and Hare TA (2005) Changes in cerebral functional organization during cognitive development. Curr Opin Neurobiol 15:239-244.
48. Casey, BJ, Getz S, and Galvan A (2008) The adolescent brain. Dev Rev 28:62-77
49. Casey BJ and Jones RM (2010) Neurobiology of the adolescent brain and behavior: implications for substance use disorders. J Am Acad Child Adolesc Psychiatry 49: 1189-1201, quiz 1285.
50. Caswell AJ, Celio MA, Morgan MJ, and Duka T (2016) Impulsivity as a multifaceted construct related to excessive drinking among UK students. Alcohol Alcohol 51: 77-83.
51. Celio MR and Blümcke I (1994) Perineuronal nets: a specialized form of extracellular matrix in the adult nervous system. Brain Res Brain Res Rev 19:128-145.
52. Celio MR, Spreafico R, De Biasi S, and Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21:510-515.
53. Centanni SW, Teppen T, Risher ML, Fleming RL, Moss JL, Acheson SK, Mulholland PJ, Pandey SC, Chandler LJ, and Swartzwelder HS (2014) Adolescent alcohol exposure alters GABAA receptor subunit expression in adult hippocampus. Alcohol Clin Exp Res 38:2800-2808.
54. Chesnokova V, Pechnick RN, and Wawrowsky K (2016) Chronic peripheral inflammation, hippocampal neurogenesis, and behavior. Brain Behav Immun DOI: 10.1016/j.bbi.2016.01.017 [published ahead of print].
55. Clark DB, Thatcher DL, and Tapert SF (2008) Alcohol, psychological dysregulation, and adolescent brain development. Alcohol Clin Exp Res 32:375-385.
56. Coleman LG Jr., He J, Lee J, Styner M, and Crews FT (2011) Adolescent binge drinking alters adult brain neurotransmitter gene expression, behavior, brain regional volumes, and neurochemistry in mice. Alcohol Clin Exp Res 35:671-688
57. Coleman LG Jr., Liu W, Oguz I, Styner M, and Crews FT (2014) Adolescent binge ethanol treatment alters adult brain regional volumes, cortical extracellular matrix protein and behavioral flexibility. Pharmacol Biochem Behav 116:142-151
58. Cooper-Kuhn CM, Winkler J, and Kuhn HG (2004) Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res 77:155-165
59. Cotman CW and Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295-301.
60. Crabbe JC, Bell RL, and Ehlers CL (2010) Human and laboratory rodent low response to alcohol: is better consilience possible? Addict Biol 15:125-144.
61. Crews F, He J, and Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86:189-199
62. Crews F, Nixon K, Kim D, Joseph J, Shukitt-Hale B, Qin L, and Zou J (2006a) BHT blocks NF-kappaB activation and ethanol-induced brain damage. Alcohol Clin Exp Res 30:1938-1949.
63. Crews FT and Boettiger CA (2009) Impulsivity, frontal lobes and risk for addiction. Pharmacol Biochem Behav 93:237-247.
64. Crews FT, Braun CJ, Hoplight B, Switzer RC 3rd, and Knapp DJ (2000) Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 24:1712-1723
65. Crews FT, Mdzinarishvili A, Kim D, He J, and Nixon K (2006b) Neurogenesis in adolescent brain is potently inhibited by ethanol. Neuroscience 137:437-445
66. Crews FT and Nixon K (2009) Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol 44:115-127.
67. Crews FT, Qin L, Sheedy D, Vetreno RP, and Zou J (2013) High mobility group box 1/Toll-like receptor danger signaling increases brain neuroimmune activation in alcohol dependence. Biol Psychiatry 73:602-612.
68. Crews FT and Vetreno RP (2016) Mechanisms of neuroimmune gene induction in alcoholism. Psychopharmacology 233:1543-1557.
69. Crews FT, Zou J, and Qin L (2011) Induction of innate immune genes in brain create the neurobiology of addiction. Brain Behav Immun 25 (Suppl 1):S4-S12.
70. Criado JR and Ehlers CL (2007) Electrophysiological responses to affective stimuli in Southwest California Indians: relationship to alcohol dependence. J Stud Alcohol Drugs 68:813-823.
71. Csikszentmihalyi M, Larson R, and Prescott S (1977) The ecology of adolescent activity and experience. J Youth Adolesc 6:281-294.
72. Cunningham MG, Bhattacharyya S, and Benes FM (2002) Amygdalo-cortical sprouting continues into early adulthood: implications for the development of normal and abnormal function during adolescence. J Comp Neurol 453:116-130
73. Daughters SB, Reynolds EK, MacPherson L, Kahler CW, Danielson CK, Zvolensky M, and Lejuez CW (2009) Distress tolerance and early adolescent externalizing and internalizing symptoms: the moderating role of gender and ethnicity. Behav Res Ther 47:198-205.
74. Davidson LL, Grigorenko EL, Boivin MJ, Rapa E, and Stein A (2015) A focus on adolescence to reduce neurological, mental health and substance-use disability. Nature 527:S161-S166.
75. Dawson DA, Goldstein RB, Chou SP, Ruan WJ, and Grant BF (2008) Age at first drink and the first incidence of adult-onset DSM-IV alcohol use disorders. Alcohol Clin Exp Res 32:2149-2160.
76. Day AM, Celio MA, Lisman SA, Johansen GE, and Spear LP (2013) Acute and chronic effects of alcohol on trail making test performance among underage drinkers in a field setting. J Stud Alcohol Drugs 74:635-641.
77. Demaster DM and Ghetti S (2013) Developmental differences in hippocampal and cortical contributions to episodic retrieval. Cortex 49:1482-1493.
78. Desikan A, Wills DN, and Ehlers CL (2014) Ontogeny and adolescent alcohol exposure in Wistar rats: open field conflict, light/dark box and forced swim test. Pharmacol Biochem Behav 122:279-285.
79. DeWit DJ, Adlaf EM, Offord DR, and Ogborne AC (2000) Age at first alcohol use: a risk factor for the development of alcohol disorders. Am J Psychiatry 157:745-750
80. Diaz-Granados JL and Graham DL (2007) The effects of continuous and intermittent ethanol exposure in adolesence on the aversive properties of ethanol during adulthood. Alcohol Clin Exp Res 31:2020-2027.
81. Dillon KA, Gross-Isseroff R, Israeli M, and Biegon A (1991) Autoradiographic analysis of serotonin 5-HT1A receptor binding in the human brain postmortem: effects of age and alcohol. Brain Res 554:56-64.
82. Dinopoulos A, Uylings HB, and Parnavelas JG (1992) The development of neurons in the nuclei of the horizontal and vertical limb of the diagonal band of Broca of the rat: a qualitative and quantitative analysis of Golgi preparations. Brain Res Dev Brain Res 65:65-74.
83. Donaldson ZR, Nautiyal KM, Ahmari SE, and Hen R (2013) Genetic approaches for understanding the role of serotoning receptors in mood and behavior. Curr Opin Neurobiol 23:339-406.
84. Doremus TL, Brunell SC, Rajendran P, and Spear LP (2005) Factors influencing elevated ethanol consumption in adolescent relative to adult rats. Alcohol Clin Exp Res 29:1796-1808.
85. Doremus TL, Brunell SC, Varlinskaya EI, and Spear LP (2003) Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats. Pharmacol Biochem Behav 75:411-418.
86. Dori I, Dinopoulos A, Blue ME, and Parnavelas JG (1996) Regional differences in the ontogeny of the serotonergic projection to the cerebral cortex. Exp Neurol 138:1-14
87. Douglas LA, Varlinskaya EI, and Spear LP (2003) Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation. Physiol Behav 80:317-325.
88. Douglas LA, Varlinskaya EI, and Spear LP (2004) Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45:153-162
89. Draski LJ, Bice PJ, and Deitrich RA (2001) Developmental alterations of ethanol sensitivity in selectively bred high and low alcohol sensitive rats. Pharmacol Biochem Behav 70:387-396.
90. Drummond SP, Gillin JC, Smith TL, and DeModena A (1998) The sleep of abstinent pure primary alcoholic patients: natural course and relationship to relapse. Alcohol Clin Exp Res 22:1796-1802.
91. Duman RS (2004) Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromolecular Med 5:11-25.
92. Duman RS and Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116-1127.
93. Eastwood SL, Weickert CS, Webster MJ, Herman MM, Kleinman JE, and Harrison PJ (2006) Synaptophysin protein and mRNA expression in the human hippocampal formation from birth to old age. Hippocampus 16:645-654.
94. Ehardt C and Bernstein I (1987) Patterns of affiliation among immature rhesus monkeys (macaca mulatta). Am J Primatol 13:255-269.
95. Ehlers CL and Criado JR (2010) Adolescent ethanol exposure: does it produce longlasting electrophysiological effects? Alcohol 44:27-37.
96. Ehlers CL, Criado JR, Wills DN, Liu W, and Crews FT (2011) Periadolescent ethanol exposure reduces adult forebrain ChAT+IR neurons: correlation with behavioral pathology. Neuroscience 199:333-345.
97. Ehlers CL, Desikan A, and Wills DN (2013a) Developmental differences in EEG and sleep responses to acute ethanol administration and its withdrawal (hangover) in adolescent and adult Wistar rats. Alcohol 47:601-610.
98. Ehlers CL, Desikan A, and Wills DN (2014a) Event-related potential responses to the acute and chronic effects of alcohol in adolescent and adult Wistar rats. Alcohol Clin Exp Res 38:749-759.
99. Ehlers CL, Liu W, Wills DN, and Crews FT (2013b) Periadolescent ethanol vapor exposure persistently reduces measures of hippocampal neurogenesis that are associated with behavioral outcomes in adulthood. Neuroscience 244:1-15
100. Ehlers CL, Phillips E, Finnerman G, Gilder D, Lau P, and Criado J (2007) P3 components and adolescent binge drinking in Southwest California Indians. Neurotoxicol Teratol 29:153-163.
101. Ehlers CL, Wills DN, Desikan A, Phillips E, and Havstad J (2014b) Decreases in energy and increases in phase locking of event-related oscillations to auditory stimuli occur during adolescence in human and rodent brain. Dev Neurosci 36: 175-195.
102. Engleman EA, Ingraham CM, McBride WJ, Lumeng L, and Murphy JM (2006) Extracellular dopamine levels are lower in the medial prefrontal cortex of alcoholpreferring rats compared to Wistar rats. Alcohol 38:5-12.
103. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, and Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317.
104. Ernst M and Fudge JL (2009) A developmental neurobiological model of motivated behavior: anatomy, connectivity and ontogeny of the triadic nodes. Neurosci Biobehav Rev 33:367-382.
105. Evrard SG, Duhalde-Vega M, Tagliaferro P, Mirochnic S, Caltana LR, and Brusco A (2006) A low chronic ethanol exposure induces morphological changes in the adolescent rat brain that are not fully recovered even after a long abstinence: an immunohistochemical study. Exp Neurol 200:438-459.
106. Fagen RM (1976) Exercise, play, and physical training in animals, in Perspectives in Ethology pp 189-219, Springer US, New York.
107. Feinberg I and Campbell IG (2010) Sleep EEG changes during adolescence: an index of a fundamental brain reorganization. Brain Cogn 72:56-65.
108. Field RH, Gossen A, and Cunningham C (2012) Prior pathology in the basal forebrain cholinergic system predisposes to inflammation-induced working memory deficits: reconciling inflammatory and cholinergic hypotheses of delirium. J Neurosci 32:6288-6294
109. File SE and Seth P (2003) A review of 25 years of the social interaction test. Eur J Pharmacol 463:35-53.
110. Fleming RL, Acheson SK, Moore SD, Wilson WA, and Swartzwelder HS (2012) In the rat, chronic intermittent ethanol exposure during adolescence alters the ethanol sensitivity of tonic inhibition in adulthood. Alcohol Clin Exp Res 36:279-285
111. Fleming RL, Li Q, Risher ML, Sexton HG, Moore SD, Wilson WA, Acheson SK, and Swartzwelder HS (2013) Binge-pattern ethanol exposure during adolescence, but not adulthood, causes persistent changes in GABAA receptor-mediated tonic inhibition in dentate granule cells. Alcohol Clin Exp Res 37:1154-1160.
112. Fowler SW, Walker JM, Klakotskaia D, Will MJ, Serfozo P, Simonyi A, and Schachtman TR (2013) Effects of a metabotropic glutamate receptor 5 positive allosteric modulator, CDPPB, on spatial learning task performance in rodents. Neurobiol Learn Mem 99:25-31.
113. Frankle WG, Laruelle M, and Haber SN (2006) Prefrontal cortical projections to the midbrain in primates: evidence for a sparse connection. Neuropsychopharmacology 31:1627-1636.
114. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, and Gundelfinger ED (2009) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12:897-904.
115. Galef JB (1977) Mechanisms for the social transmission of food preferences from adult to weaning rats, in Learning Mechanisms in Food Selection (Barker LM, Best M, and Domjan M eds) pp 123-148, Baylor University Press, Waco, TX
116. Gao M, Liu CL, Yang S, Jin GZ, Bunney BS, and Shi WX (2007) Functional coupling between the prefrontal cortex and dopamine neurons in the ventral tegmental area. J Neurosci 27:5414-5421.
117. Gariano RF and Groves PM (1988) Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Res 462:194-198.
118. Gass JT, Glen Jr. WB, McGonigal JT, Trantham-Davidson H, Lopez MF, Randall PK, Yaxley R, Floresco SB, and Chandler LJ (2014) Adolescent alcohol exposure reduces behavioral flexibility, promotes disinhibition, and increases resistance to extinction of ethanol self-administration in adulthood. Neuropsychopharmacology 39:2570-2583.
119. Gessa GL, Muntoni F, Collu M, Vargiu L, and Mereu G (1985) Low doses of ethanol activate dopaminergic neurons in the ventral tegmental area. Brain Res 348: 201-203.
120. Giedd JN (2004) Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 1021:77-85.
121. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, and Rapoport JL (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861-863.
122. Giedd JN, Snell JW, Lange N, Rajapakse JC, Casey BJ, Kozuch PL, Vaituzis AC, Vauss YC, Hamburger SD, Kaysen D, et al. (1996) Quantitative magnetic resonance imaging of human brain development: ages 4-18. Cereb Cortex 6:551-560
123. Gilpin NW, Karanikas CA, and Richardson HN (2012) Adolescent binge drinking leads to changes in alcohol drinking, anxiety, and amygdalar corticotropin releasing factor cells in adulthood in male rats. PLoS One 7:e31466.
124. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF 3rd, Herman DH, Clasen LS, Toga AW, et al. (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101:8174-8179.
125. Gogtay N, Nugent TF 3rd, Herman DH, Ordonez A, Greenstein D, Hayashi KM, Clasen L, Toga AW, Giedd JN, Rapoport JL, et al. (2006) Dynamic mapping of normal human hippocampal development. Hippocampus 16:664-672
126. Gordon JA and Stryker MP (1996) Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 16:3274-3286
127. Goto Y and Grace AA (2005) Dopamine-dependent interactions between limbic and prefrontal cortical plasticity in the nucleus accumbens: disruption by cocaine sensitization. Neuron 47:255-266.
128. Goudriaan AE, Grekin ER, and Sher KJ (2007) Decision making and binge drinking: a longitudinal study. Alcohol Clin Exp Res 31:928-938.
129. Gould E, Farris TW, and Butcher LL (1989) Basal forebrain neurons undergo somatal and dendritic remodeling during postnatal development: a single-section Golgi and choline acetyltransferase analysis. Brain Res Dev Brain Res 46:297-302
130. Gould E, Reeves AJ, Fallah M, Tanapat P, Gross CG, and Fuchs E (1999) Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96: 5263-5267.
131. Gould E, Woolf NJ, and Butcher LL (1991) Postnatal development of cholinergic neurons in the rat: I. Forebrain. Brain Res Bull 27:767-789.
132. Grant BF and Dawson DA (1997) Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse 9:103-110.
133. Gratton G, Coles MG, Sirevaag EJ, Eriksen CW, and Donchin E (1988) Preand poststimulus activation of response channels: a psychophysiological analysis. J Exp Psychol Hum Percept Perform 14:331-344.
134. Guerri C and Pascual M (2010) Mechanisms involved in the neurotoxic, cognitive, and neurobehavioral effects of alcohol consumption during adolescence. Alcohol 44: 15-26.
135. Gümüştekín K, Seven B, Karabulut N, Aktaş O, Gürsan N, Aslan S, Keleş M, Varoglu E, and Dane S (2004) Effects of sleep deprivation, nicotine, and selenium on wound healing in rats. Int J Neurosci 114:1433-1442.
136. Hakim F, Wang Y, Zhang SX, Zheng J, Yolcu ES, Carreras A, Khalyfa A, Shirwan H, Almendros I, and Gozal D (2014) Fragmented sleep accelerates tumor growth and progression through recruitment of tumor-associated macrophages and TLR4 signaling. Cancer Res 74:1329-1337.
137. Handy TC (2005) Event Related Potentials: A Methods Handbook, MIT Press, Bradford, Cambridge, MA.
138. Hansson AC, Nixon K, Rimondini R, Damadzic R, Sommer WH, Eskay R, Crews FT, and Heilig M (2010) Long-term suppression of forebrain neurogenesis and loss of neuronal progenitor cells following prolonged alcohol dependence in rats. Int J Neuropsychopharmacol 13:583-593.
139. Harry GJ and Kraft AD (2012) Microglia in the developing brain: a potential target with lifetime effects. Neurotoxicology 33:191-206.
140. Hartup WW and Stevens N (1997) Friendships and adaptation in the life course. Psychol Bull 121:355-370.
141. Hartzler B and Fromme K (2003) Fragmentary and en bloc blackouts: similarity and distinction among episodes of alcohol-induced memory loss. J Stud Alcohol 64: 547-550.
142. Hasin DS, Stinson FS, Ogburn E, and Grant BF (2007) Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Arch Gen Psychiatry 64:830-842.
143. Hauser SR, Getachew B, Taylor RE, and Tizabi Y (2011) Alcohol induced depressivelike behavior is associated with a reduction in hippocampal BDNF. Pharmacol Biochem Behav 100:253-258.
144. He J and Crews FT (2007) Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 86:327-333.
145. He J, Nixon K, Shetty AK, and Crews FT (2005) Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. Eur J Neurosci 21:2711-2720.
146. Helms CM, Rau A, Shaw J, Stull C, Gonzales SW, and Grant KA (2014) The effects of age at the onset of drinking to intoxication and chronic ethanol self-administration in male rhesus macaques. Psychopharmacology 231:1853-1861
147. Hensler JG (2006) Serotonergic modulation of the limbic system. Neurosci Biobehav Rev 30:203-214.
148. Herrera DG, Yague AG, Johnsen-Soriano S, Bosch-Morell F, Collado-Morente L, Muriach M, Romero FJ, and Garcia-Verdugo JM (2003) Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci USA 100:7919-7924.
149. Herting MM, Colby JB, Sowell ER, and Nagel BJ (2014) White matter connectivity and aerobic fitness in male adolescents. Dev Cogn Neurosci 7:65-75.
150. Hill SY and Shen S (2002) Neurodevelopmental patterns of visual P3b in association with familial risk for alcohol dependence and childhood diagnosis. Biol Psychiatry 51:621-631.
151. Hingson RW, Edwards EM, Heeren T, and Rosenbloom D (2009) Age of drinking onset and injuries, motor vehicle crashes, and physical fights after drinking and when not drinking. Alcohol Clin Exp Res 33:783-790.
152. Hollstedt C, Olsson O, and Rydberg U (1980) Effects of ethanol on the developing rat. II. Coordination as measured by the tilting-plane test. Med Biol 58:164-168.
153. Hunsaker MR, Scott JA, Bauman MD, Schumann CM, and Amaral DG (2014) Postnatal development of the hippocampus in the Rhesus macaque (Macaca mulatta): a longitudinal magnetic resonance imaging study. Hippocampus 24: 794-807.
154. Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE, Ye T, Colantuoni C, Herman MM, et al. (2011) Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 31:11088-11095.
155. Imperato A and Di Chiara G (1986) Preferential stimulation of dopamine release in the nucleus accumbens of freely moving rats by ethanol. J Pharmacol Exp Ther 239:219-228.
156. Insel TR, Miller LP, and Gelhard RE (1990) The ontogeny of excitatory amino acid receptors in rat forebrain. I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 35:31-43.
157. Irwin M, Miller C, Gillin JC, Demodena A, and Ehlers CL (2000) Polysomnographic and spectral sleep EEG in primary alcoholics: an interaction between alcohol dependence and African-American ethnicity. Alcohol Clin Exp Res 24:1376-1384
158. Irwin MR, Olmstead R, Valladares EM, Breen EC, and Ehlers CL (2009) Tumor necrosis factor antagonism normalizes rapid eye movement sleep in alcohol dependence. Biol Psychiatry 66:191-195.
159. Iwata M, Ota KT, and Duman RS (2013) The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain Behav Immun 31: 105-114.
160. Jackson KM, Barnett NP, Colby SM, and Rogers ML (2015) The prospective association between sipping alcohol by the sixth grade and later substance use. J Stud Alcohol Drugs 76:212-221.
161. Jang MH, Shin MC, Jung SB, Lee TH, Bahn GH, Kwon YK, Kim EH, and Kim CJ (2002a) Alcohol and nicotine reduce cell proliferation and enhance apoptosis in dentate gyrus. Neuroreport 13:1509-1513.
162. Jang MH, Shin MC, Kim EH, and Kim CJ (2002b) Acute alcohol intoxication decreases cell proliferation and nitric oxide synthase expression in dentate gyrus of rats. Toxicol Lett 133:255-262.
163. Jo YS, Lee J, and Mizumori SJ (2013) Effects of prefrontal cortical inactivation on neural activity in the ventral tegmental area. J Neurosci 33:8159-8171.
164. Johnston LD, O’Malley PM, Meich RA, Bachman JG, and Shulenberg JE (2015) Monitoring the Future National Survey Results on Drug Use: 1975-2014: Overview, Key Findings on Adolescent Drug Use, Institute for Social Research, The University of Michigan, Ann Arbor, MI.
165. Kalant H (1971) Absorption, diffusion, distribution and elimination of ethanol: effects on biological membranes, in The Biology of Alcoholism (Kissin B, Begleiter H eds) vol 1, pp 1-62, Plenum Press, New York.
166. Kalkhoven E (2004) CBP and p300: HATs for different occasions. Biochem Pharmacol 68:1145-1155.
167. Kaneko N, Okano H, and Sawamoto K (2006) Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 11:1145-1159.
168. Karlsgodt KH, John M, Ikuta T, Rigoard P, Peters BD, Derosse P, Malhotra AK, and Szeszko PR (2015) The accumbofrontal tract: diffusion tensor imaging characterization and developmental change from childhood to adulthood. Hum Brain Mapp 36:4954-4963.
169. Kaul D, Habbel P, Derkow K, Krüger C, Franzoni E, Wulczyn FG, Bereswill S, Nitsch R, Schott E, Veh R, et al. (2012) Expression of Toll-like receptors in the developing brain. PLoS One 7:e37767.
170. Kelly SJ, Bonthius DJ, and West JR (1987) Developmental changes in alcohol pharmacokinetics in rats. Alcohol Clin Exp Res 11:281-286.
171. Kempermann G (2002) Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22:635-638.
172. Kempermann G, Kuhn HG, and Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
173. Klempin F and Kempermann G (2007) Adult hippocampal neurogenesis and aging. Eur Arch Psychiatry Clin Neurosci 257:271-280.
174. Kofink D, Boks MP, Timmers HT, and Kas MJ (2013) Epigenetic dynamics in psychiatric disorders: environmental programming of neurodevelopmental processes. Neurosci Biobehav Rev 37:831-845.
175. Koob GF and Le Moal M (1997) Drug abuse: hedonic homeostatic dysregulation. Science 278:52-58.
176. Krishnan HR, Sakharkar AJ, Teppen TL, Berkel TD, and Pandey SC (2014) The epigenetic landscape of alcoholism. Int Rev Neurobiol 115:75-116.
177. Krueger JM and Majde JA (1990) Sleep as a host defense: its regulation by microbial products and cytokines. Clin Immunol Immunopathol 57:188-199
178. Kuhn HG, Dickinson-Anson H, and Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
179. Land C and Spear NE (2004) Ethanol impairs memory of a simple discrimination in adolescent rats at doses that leave adult memory unaffected. Neurobiol Learn Mem 81:75-81.
180. Laviola G, Macrì S, Morley-Fletcher S, and Adriani W (2003) Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev 27:19-31.
181. Leeman RF, Heilig M, Cunningham CL, Stephens DN, Duka T, and O’Malley SS (2010) Ethanol consumption: how should we measure it? Achieving consilience between human and animal phenotypes. Addict Biol 15:109-124
182. Lebel C, Walker L, Leemans A, Phillips L, and Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40: 1044-1055.
183. Lenroot RK and Giedd JN (2006) Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev 30: 718-729.
184. Leuner B, Gould E, and Shors TJ (2006) Is there a link between adult neurogenesis and learning? Hippocampus 16:216-224.
185. Li Q, Wilson WA, and Swartzwelder HS (2003) Developmental differences in the sensitivity of hippocampal GABAA receptor-mediated IPSCS to ethanol. Alcohol Clin Exp Res 27:2017-2022.
186. Li Q, Wilson WA, and Swartzwelder HS (2006) Developmental differences in the sensitivity of spontaneous and miniature IPSCs to ethanol. Alcohol Clin Exp Res 30:119-126.
187. Liappas J, Paparrigopoulos T, Tzavellas E, and Christodoulou G (2002) Impact of alcohol detoxification on anxiety and depressive symptoms. Drug Alcohol Depend 68:215-220.
188. Lilja T, Heldring N, and Hermanson O (2013) Like a rolling histone: epigenetic regulation of neural stem cells and brain development by factors controlling histone acetylation and methylation. Biochim Biophys Acta 1830:2354-2360
189. Lim CS, Hwang YK, Kim D, Cho SH, Bañuelos C, Bizon JL, and Han JS (2011) Increased interactions between PKA and NF-kB signaling in the hippocampus following loss of cholinergic input. Neuroscience 192:485-493.
190. Linke R and Frotscher M (1993) Development of the rat septohippocampal projection: tracing with DiI and electron microscopy of identified growth cones. J Comp Neurol 332:69-88.
191. Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92:180-185.
192. Liu W and Crews FT (2015) Adolescent intermittent ethanol exposure enhances ethanol activation of the nucleus accumbens while blunting the prefrotnal cortex responses in adult rat. Neuroscience 293:92-108.
193. Loizou LA (1972) The postnatal ontogeny of monoamine-containing neurones in the central nervous system of the albino rat. Brain Res 40:395-418.
194. Madsen TM, Kristjansen PE, Bolwig TG, and Wörtwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119:635-642.
195. Malberg JE, Eisch AJ, Nestler EJ, and Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110
196. Maldonado-Devincci AM, Alipour KK, Michael LA, and Kirstein CL (2010) Repeated binge ethanol administration during adolescence enhances voluntary sweetened ethanol intake in young adulthood in male and female rats. Pharmacol Biochem Behav 96:476-487.
197. Malter Cohen M, Tottenham N, and Casey BJ (2013) Translational developmental studies of stress on brain and behavior: implications for adolescent mental health and illness? Neuroscience 249:53-62.
198. Markham JA, Morris JR, and Juraska JM (2007) Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood. Neuroscience 144:961-968.
199. Markwiese BJ, Acheson SK, Levin ED, Wilson WA, and Swartzwelder HS (1998) Differential effects of ethanol on memory in adolescent and adult rats. Alcohol Clin Exp Res 22:416-421.
200. Matthews DA, Nadler JV, Lynch GS, and Cotman CW (1974) Development of cholinergic innervation in the hippocampal formation of the rat. I. Histochemical demonstration of acetylcholinesterase activity. Dev Biol 36:130-141
201. Matthews DB, Tinsley KL, Diaz-Granados JL, Tokunaga S, and Silvers JM (2008) Chronic intermittent exposure to ethanol during adolescence produces tolerance to the hypnotic effects of ethanol in male rats: a dose-dependent analysis. Alcohol 42: 617-621.
202. McCutcheon JE and Marinelli M (2009) Age matters. Eur J Neurosci 29:997-1014
203. McHugh SB, Deacon RM, Rawlins JN, and Bannerman DM (2004) Amygdala and ventral hippocampus contribute differentially to mechanisms of fear and anxiety. Behav Neurosci 118:63-78.
204. Mejia-Toiber J, Boutros N, Markou A, and Semenova S (2014) Impulsive choice and anxiety-like behavior in adult rats exposed to chronic intermittent ethanol during adolescence and adulthood. Behav Brain Res 266:19-28.
205. Mengler L, Khmelinskii A, Diedenhofen M, Po C, Staring M, Lelieveldt BP, and Hoehn M (2014) Brain maturation of the adolescent rat cortex and striatum: changes in volume and myelination. Neuroimage 84:35-44.
206. Mesulam MM, Mufson EJ, Wainer BH, and Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
207. Michelsen KA, Schmitz C, and Steinbusch HW (2007) The dorsal raphe nucleus: from silver stainings to a role in depression. Brain Res Brain Res Rev 55:329-342.
208. Milivojevic V and Covault J (2013) Alcohol exposure during late adolescence increases drinking in adult Wistar rats, an effect that is not reduced by finasteride. Alcohol Alcohol 48:28-38.
209. Miller EK and Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167-202.
210. Monje ML, Toda H, and Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-1765.
211. Montesinos J, Pascual M, Pla A, Maldonado C, Rodríguez-Arias M, Miñarro J, and Guerri C (2015) TLR4 elimination prevents synaptic and myelin alterations and long-term cognitive dysfunctions in adolescent mice with intermittent ethanol treatment. Brain Behav Immun 45:233-244.
212. Montesinos J, Pascual M, Rodríguez-Arias M, Miñarro J, and Guerri C (2016) Involvement of TLR4 in the long-term epigenetic changes, rewarding and anxiety effects induced by intermittent ethanol treatment in adolescence. Brain Behav Immun 53:159-171.
213. Moonat S, Sakharkar AJ, Zhang H, Tang L, and Pandey SC (2013) Aberrant histone deacetylase2-mediated histone modifications and synaptic plasticity in the amygdala predisposes to anxiety and alcoholism. Biol Psychiatry 73:763-773
214. Moy SS, Duncan GE, Knapp DJ, and Breese GR (1998) Sensitivity to ethanol across development in rats: comparison to [3H]zolpidem binding. Alcohol Clin Exp Res 22: 1485-1492.
215. Müller CP and Homberg JR (2015) The role of serotonin in drug use and addiction. Behav Brain Res 277:146-192.
216. Nadler JV, Matthews DA, Cotman CW, and Lynch GS (1974) Development of cholinergic innervation in the hippocampal formation of the rat. II. Quantitative changes in choline acetyltransferase and acetylcholinesterase activities. Dev Biol 36:142-154.
217. Naneix F, Marchand AR, Di Scala G, Pape JR, and Coutureau E (2012) Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence. J Neurosci 32:16223-16232.
218. Nasrallah NA, Clark JJ, Collins AL, Akers CA, Phillips PE, and Bernstein IL (2011) Risk preference following adolescent alcohol use is associated with corrupted encoding of costs but not rewards by mesolimbic dopamine. Proc Natl Acad Sci USA 108:5466-5471.
219. Nautiyal KM, Tanaka KF, Barr MM, Tritschler L, Le Dantec Y, David DJ, Gardier AM, Blanco C, Hen R, and Ahmari SE (2015) Distinct circuits underlie the effects of 5-HT1B receptors on aggression and impulsivity. Neuron 86:813-826
220. Niedermeyer E and Lopes da Silva FH (1999) Electroencephalography: Basic Principles, Clinical Applications, and Related Fields, 4th ed, Lippincott Williams and Wilkins, Baltimore, MD.
221. Nixon K and Crews FT (2002) Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83:1087-1093.
222. Novier A, Diaz-Granados JL, and Matthews DB (2015) Alcohol use across the lifespan: an analysis of adolescent and aged rodents and humans. Pharmacol Biochem Behav 133:65-82.
223. Nurse S and Lacaille JC (1999) Late maturation of GABA(B) synaptic transmission in area CA1 of the rat hippocampus. Neuropharmacology 38:1733-1742.
224. Oguz I, Yaxley R, Budin F, Hoogstoel M, Lee J, Maltbie E, Liu W, and Crews FT (2013) Comparison of magnetic resonance imaging in live vs. post mortem rat brains. PLoS One 8:e71027.
225. Onaivi ES and Martin BR (1989) Neuropharmacological and physiological validation of a computer-controlled two-compartment black and white box for the assessment of anxiety. Prog Neuropsychopharmacol Biol Psychiatry 13:963-976
226. Opp MR (2009) Sleeping to fuel the immune system: mammalian sleep and resistance to parasites. BMC Evol Biol 9:8.
227. Orłowski D, Sołtys Z, and Janeczko K (2003) Morphological development of microglia in the postnatal rat brain: a quantitative study. Int J Dev Neurosci 21:445-450
228. Pandey SC, Sakharkar AJ, Tang L, and Zhang H (2015) Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood. Neurobiol Dis 82:607-619.
229. Pandey SC, Zhang H, Ugale R, Prakash A, Xu T, and Misra K (2008) Effector immediate-early gene arc in the amygdala plays a critical role in alcoholism. J Neurosci 28:2589-2600.
230. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, et al. (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458
231. Paolicelli RC and Gross CT (2011) Microglia in development: linking brain wiring to brain environment. Neuron Glia Biol 7:77-83.
232. Pascual M, Blanco AM, Cauli O, Miñarro J, and Guerri C (2007) Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats. Eur J Neurosci 25:541-550.
233. Pascual M, Boix J, Felipo V, and Guerri C (2009) Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat. J Neurochem 108:920-931.
234. Pascual M, Do Couto BR, Alfonso-Loeches S, Aguilar MA, Rodriguez-Arias M, and Guerri C (2012) Changes in histone acetylation in the prefrontal cortex of ethanol-exposed adolescent rats are associated with ethanol-induced place conditioning. Neuropharmacology 62:2309-2319.
235. Pascual M, Pla A, Miñarro J, and Guerri C (2014) Neuroimmune activation and myelin changes in adolescent rats exposed to high-dose alcohol and associated cognitive dysfunction: a review with reference to human adolescent drinking. Alcohol Alcohol 49:187-192.
236. Patrick ME and Schulenberg JE (2013) Prevalence and predictors of adolescent alcohol use and binge drinking in the United States. Alcohol Res 35:193-200.
237. Patrick ME, Schulenberg JE, Martz ME, Maggs JL, O’Malley PM, and Johnston LD (2013) Extreme binge drinking among 12th-grade students in the United States: prevalence and predictors. JAMA Pediatr 167:1019-1025.
238. Pattwell SS, Duhoux S, Hartley CA, Johnson DC, Jing D, Elliott MD, Ruberry EJ, Powers A, Mehta N, Yang RR, et al. (2012) Altered fear learning across development in both mouse and human. Proc Natl Acad Sci USA 109:16318-16323
239. Paus T, Keshavan M, and Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9:947-957.
240. Pautassi RM, Myers M, Spear LP, Molina JC, and Spear NE (2008) Adolescent but not adult rats exhibit ethanol-mediated appetitive second-order conditioning. Alcohol Clin Exp Res 32:2016-2027.
241. Pedersen W and Skrondal A (1998) Alcohol consumption debut: predictors and consequences. J Stud Alcohol 59:32-42.
242. Pedrazzi M, Raiteri L, Bonanno G, Patrone M, Ledda S, Passalacqua M, Milanese M, Melloni E, Raiteri M, Pontremoli S, et al. (2006) Stimulation of excitatory amino acid release from adult mouse brain glia subcellular particles by high mobility group box 1 protein. J Neurochem 99:827-838.
243. Pellow S, Chopin P, File SE, and Briley M (1985) Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149-167.
244. Petanjek Z, Judas M, Simic G, Rasin MR, Uylings HB, Rakic P, and Kostovic I (2011) Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA 108:13281-13286.
245. Philpot R and Kirstein C (2004) Developmental differences in the accumbal dopaminergic response to repeated ethanol exposure. Ann N Y Acad Sci 1021:422-426
246. Philpot RM, Wecker L, and Kirstein CL (2009) Repeated ethanol exposure during adolescence alters the developmental trajectory of dopaminergic output from the nucleus accumbens septi. Int J Dev Neurosci 27:805-815.
247. Pian JP, Criado JR, Milner R, and Ehlers CL (2010) N-methyl-D-aspartate receptor subunit expression in adult and adolescent brain following chronic ethanol exposure. Neuroscience 170:645-654.
248. Polich J, Ladish C, and Burns T (1990) Normal variation of P300 in children: age, memory span, and head size. Int J Psychophysiol 9:237-248.
249. Porjesz B, Rangaswamy M, Kamarajan C, Jones KA, Padmanabhapillai A, and Begleiter H (2005) The utility of neurophysiological markers in the study of alcoholism. Clin Neurophysiol 116:993-1018.
250. Prescott CA and Kendler KS (1999) Age at first drink and risk for alcoholism: a noncausal association. Alcohol Clin Exp Res 23:101-107.
251. Prut L and Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463:3-33.
252. Qin L, Liu Y, Hong JS, and Crews FT (2013) NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration. Glia 61:855-868.
253. Quartz SR and Sejnowski TJ (1997) The neural basis of cognitive development: a constructivist manifesto. Behav Brain Sci 20:537-556, discussion 556-596.
254. Quoilin C, Didone V, Tirelli E, and Quertemont E (2012) Chronic ethanol exposure during adolescence alters the behavioral responsiveness to ethanol in adult mice. Behav Brain Res 229:1-9.
255. Rachdaoui N and Sarkar DK (2014) Transgenerational epigenetics and brain disorders. Int Rev Neurobiol 115:51-73.
256. Renthal W and Nestler EJ (2008) Epigenetic mechanisms in drug addiction. Trends Mol Med 14:341-350.
257. Richardson RM, Sun D, and Bullock MR (2007) Neurogenesis after traumatic brain injury. Neurosurg Clin N Am 18: 169-181, xi.
258. Risher ML, Fleming RL, Boutros N, Semenova S, Wilson WA, Levin ED, Markou A, Swartzwelder HS, and Acheson SK (2013) Long-term effects of chronic intermittent ethanol exposure in adolescent and adult rats: radial-arm maze performance and operant food reinforced responding. PLoS One 8:e62940.
259. Risher ML, Fleming RL, Risher WC, Miller KM, Klein RC, Wills T, Acheson SK, Moore SD, Wilson WA, Eroglu C, et al. (2015) Adolescent intermittent alcohol exposure: persistence of structural and functional hippocampal abnormalities into adulthood. Alcohol Clin Exp Res 39:989-997.
260. Robinson DL, Howard EC, McConnell S, Gonzales RA, and Wightman RM (2009) Disparity between tonic and phasic ethanol-induced dopamine increases in the nucleus accumbens of rats. Alcohol Clin Exp Res 33:1187-1196
261. Roehrs T and Roth T (2001) Sleep, sleepiness, and alcohol use. Alcohol Res Health 25: 101-109.
262. Rolls A, Shechter R, London A, Ziv Y, Ronen A, Levy R, and Schwartz M (2007) Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 9:1081-1088.
263. Rose ME and Grant JE (2010) Alcohol-induced blackout: phenomenology, biological basis, and gender differences. J Addict Med 4:61-73.
264. Rosenberg DR and Lewis DA (1995) Postnatal maturation of the dopaminergic innervation of monkey prefrontal and motor cortices: a tyrosine hydroxylase immunohistochemical analysis. J Comp Neurol 358:383-400.
265. Rubenstein JL (1998) Development of serotonergic neurons and their projections. Biol Psychiatry 44:145-150.
266. Saalfield J and Spear L (2015) Consequences of repeated ethanol exposure during early or late adolescence on conditioned taste aversions in rats. Dev Cogn Neurosci 16:174-182.
267. Sakharkar AJ, Vetreno RP, Zhang H, Kokare DM, Crews FT, and Pandey SC (2016) A role for histone acetylation mechanisms in adolescent alcohol exposure-induced deficits in hippocampal brain-derived neurotrophic factor expression and neurogenesis markers in adulthood. Brain Struct Funct DOI: 10.1007/s00429-016-1196-y [published ahead of print].
268. Sakharkar AJ, Zhang H, Tang L, Baxstrom K, Shi G, Moonat S, and Pandey SC (2014) Effects of histone deacetylase inhibitors on amygdaloid histone acetylation and neuropeptide Y expression: a role in anxiety-like and alcohol-drinking behaviours. Int J Neuropsychopharmacol 17:1207-1220.
269. Sakharkar AJ, Zhang H, Tang L, Shi G, and Pandey SC (2012) Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol. Alcohol Clin Exp Res 36:61-71
270. Sanchez-Roige S, Baro V, Trick L, Peña-Oliver Y, Stephens DN, and Duka T (2014a) Exaggerated waiting impulsivity associated with human binge drinking, and high alcohol consumption in mice. Neuropsychopharmacology 39:2919-2927.
271. Sanchez-Roige S, Peña-Oliver Y, Ripley TL, and Stephens DN (2014b) Repeated ethanol exposure during early and late adolescence: double dissociation of effects on waiting and choice impulsivity. Alcohol Clin Exp Res 38:2579-2589.
272. Sarkar DK (2016) Male germline transmits fetal alcohol epigenetic marks for multiple generations: a review. Addict Biol 21:23-34.
273. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, and Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74:691-705.
274. Schier CJ, Dilly GA, and Gonzales RA (2013) Intravenous ethanol increases extracellular dopamine in the medial prefrontal cortex of the Long-Evans rat. Alcohol Clin Exp Res 37:740-747.
275. Schindler AG, Tsutsui KT, and Clark JJ (2014) Chronic alcohol intake during adolescence, but not adulthood, promotes persistent deficits in risk-based decision making. Alcohol Clin Exp Res 38:1622-1629.
276. Schoenfeld TJ and Cameron HA (2015) Adult neurogenesis and mental illness. Neuropsychopharmacology 40:113-128.
277. Schramm-Sapyta NL, DiFeliceantonio AG, Foscue E, Glowacz S, Haseeb N, Wang N, Zhou C, and Kuhn CM (2010) Aversive effects of ethanol in adolescent versus adult rats: potential causes and implication for future drinking. Alcohol Clin Exp Res 34: 2061-2069.
278. Schuckit MA, Smith TL, Danko GP, Bucholz KK, Agrawal A, Dick DM, Nurnberger JI, Kramer J, Hesselbrock M, Saunders G, et al. (2014) Predictors of subgroups based on maximum drinks per occasion over six years for 833 adolescents and young adults in COGA. J Stud Alcohol Drugs 75:24-34.
279. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27.
280. Semenova S (2012) Attention, impulsivity, and cognitive flexibility in adult male rats exposed to ethanol binge during adolescence as measured in the five-choice serial reaction time task: the effects of task and ethanol challenges. Psychopharmacology 219:433-442.
281. Sesack SR and Pickel VM (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320: 145-160.
282. Shah AA, Sjovold T, and Treit D (2004) Inactivation of the medial prefrontal cortex with the GABAA receptor agonist muscimol increases open-arm activity in the elevated plus-maze and attenuates shock-probe burying in rats. Brain Res 1028: 112-115.
283. Sheikh BN (2014) Crafting the brain: role of histone acetyltransferases in neural development and disease. Cell Tissue Res 356:553-573.
284. Sher KJ and Gotham HJ (1999) Pathological alcohol involvement: a developmental disorder of young adulthood. Dev Psychopathol 11:933-956.
285. Sherrill LK, Berthold C, Koss WA, Juraska JM, and Gulley JM (2011) Sex differences in the effects of ethanol pre-exposure during adolescence on ethanol-induced conditioned taste aversion in adult rats. Behav Brain Res 225:104-109
286. Shnitko TA, Kennerly LC, Spear LP, and Robinson DL (2014) Ethanol reduces evoked dopamine release and slows clearance in the rat medial prefrontal cortex. Alcohol Clin Exp Res 38:2969-2977.
287. Shnitko TA, Spear LP, and Robinson DL (2016) Adolescent binge-like alcohol alters sensitivity to acute alcohol effects on dopamine release in the nucleus accumbens of adult rats. Psychopharmacology 233:361-371.
288. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, and Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376
289. Silveri MM, Cohen-Gilbert J, Crowley DJ, Rosso IM, Jensen JE, and Sneider JT (2014) Altered anterior cingulate neurochemistry in emerging adult binge drinkers with a history of alcohol-induced blackouts. Alcohol Clin Exp Res 38:969-979.
290. Silveri MM and Spear LP (1998) Decreased sensitivity to the hypnotic effects of ethanol early in ontogeny. Alcohol Clin Exp Res 22:670-676.
291. Silveri MM and Spear LP (2000) Ontogeny of ethanol elimination and ethanolinduced hypothermia. Alcohol 20:45-53.
292. Silveri MM and Spear LP (2001) Acute, rapid, and chronic tolerance during ontogeny: observations when equating ethanol perturbation across age. Alcohol Clin Exp Res 25:1301-1308.
293. Siqueira L and Smith VC; Committee on Substance Abuse (2015) Binge drinking. Pediatrics 136:e718-e726.
294. Sitapara RA, Antoine DJ, Sharma L, Patel VS, Ashby CR Jr., Gorasiya S, Yang H, Zur M, and Mantell LL (2014) The a7 nicotinic acetylcholine receptor agonist GTS-21 improves bacterial clearance in mice by restoring hyperoxia-compromised macrophage function. Mol Med 20:238-247.
295. Slawecki CJ, Thorsell A, and Ehlers CL (2004) Long-term neurobehavioral effects of alcohol or nicotine exposure in adolescent animal models. Ann N Y Acad Sci 1021: 448-452.
296. Smith HR and Pang KC (2005) Orexin-saporin lesions of the medial septum impair spatial memory. Neuroscience 132:261-271.
297. Smith P (1982) Does play matter? Functional and evolutionary aspects of animal and human play. Behav Brain Sci 5:139-184.
298. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, and Toga AW (1999) In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859-861.
299. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, Buchholz BA, et al. (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219-1227.
300. Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417-463.
301. Spear L, editor (2010) The Behavioral Neuroscience of Adolescence, W.W. Norton & Company, New York.
302. Spear LP (2011) Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data. Dev Cogn Neurosci 1:392-400
303. Spear LP (2014) Adolescents and alcohol: acute sensitivities, enhanced intake, and later consequences. Neurotoxicol and Teratol 0:51-59.
304. Spear LP (2015) Adolescent alcohol exposure: are there separable vulnerable periods within adolescence? Physiol Behav 148:122-130.
305. Spear LP and Swartzwelder HS (2014) Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neurosci Biobehav Rev 45:1-8.
306. Spear LP and Varlinskaya EI (2005) Adolescence: alcohol sensitivity, tolerance, and intake. Recent Dev Alcohol 17:143-159.
307. Steinberg L (1989) Pubertal maturation and parent-adolescent distance: an evolutionary perspective, in Advances in Adolescent Behavior and Development (Adams GR, Montemayor R, and Gullotta TP eds) pp 71-97, Sage Publications, Thousand Oaks, CA.
308. Steinberg L and Morris AS (2001) Adolescent development. Annu Rev Psychol 52: 83-110.
309. Stephens DN, Duka T, Crombag HS, Cunningham CL, Heilig M, and Crabbe JC (2010) Reward sensitivity: issues of measurement, and achieving consilience between human and animal phenotypes. Addict Biol 15:145-168
310. Su X, Lee JW, Matthay ZA, Mednick G, Uchida T, Fang X, Gupta N, and Matthay MA (2007) Activation of the alpha7 nAChR reduces acid-induced acute lung injury in mice and rats. Am J Respir Cell Mol Biol 37:186-192.
311. Su X, Matthay MA, and Malik AB (2010) Requisite role of the cholinergic alpha7 nicotinic acetylcholine receptor pathway in suppressing Gram-negative sepsisinduced acute lung inflammatory injury. J Immunol 184:401-410
312. Substance Abuse and Mental Health Services Administration (SAMHSA) (2006) Results from the 2005 National Survey on Drug Use and Health: National Findings (DHHS Publication No. SMA 06-4194), Substance Abuse and Mental Health Services Administration, Rockville, MD.
313. Suzuki M, Hagino H, Nohara S, Zhou S-Y, Kawasaki Y, Takahashi T, Matsui M, Seto H, Ono T, and Kurachi M (2005) Male-specific volume expansion of the human hippocampus during adolescence. Cereb Cortex 15:187-193.
314. Svensson TH and Tung CS (1989) Local cooling of pre-frontal cortex induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo. Acta Physiol Scand 136:135-136.
315. Swaminathan A, Kumar M, Halder Sinha S, Schneider-Anthony A, Boutillier AL, and Kundu TK (2014) Modulation of neurogenesis by targeting epigenetic enzymes using small molecules: an overview. ACS Chem Neurosci 5:1164-1177
316. Swartzwelder HS, Acheson SK, Miller KM, Sexton HG, Liu W, Crews FT, and Risher ML (2015) Adolescent intermittent alcohol exposure: deficits in object recognition memory and forebrain cholinergic markers. PLoS One 10:e0140042.
317. Swartzwelder HS, Wilson WA, and Tayyeb MI (1995a) Differential sensitivity of NMDA receptor-mediated synaptic potentials to ethanol in immature versus mature. Alcohol Clin Exp Res 19:320-323.
318. Swartzwelder HS, Wilson WA, and Tayyeb MI (1995b) Age-dependent inhibition of long-term potentiation by ethanol in immature versus mature hippocampus. Alcohol Clin Exp Res 19:1480-1485.
319. Szyf M (2013) The genomeand system-wide response of DNA methylation to early life adversity and its implication on mental health. Can J Psychiatry 58:697-704
320. Taffe MA, Kotzebue RW, Crean RD, Crawford EF, Edwards S, and Mandyam CD (2010) Long-lasting reduction in hippocampal neurogenesis by alcohol consumption in adolescent nonhuman primates. Proc Natl Acad Sci USA 107:11104-11109.
321. Taliaz D, Stall N, Dar DE, and Zangen A (2010) Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 15:80-92.
322. Tapia-Arancibia L, Rage F, Givalois L, Dingeon P, Arancibia S, and Beaugé F (2001) Effects of alcohol on brain-derived neurotrophic factor mRNA expression in discrete regions of the rat hippocampus and hypothalamus. J Neurosci Res 63: 200-208.
323. Tarazi FI and Baldessarini RJ (2000) Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 18:29-37
324. Tarokh L, Carskadon MA, and Achermann P (2010) Developmental changes in brain connectivity assessed using the sleep EEG. Neuroscience 171:622-634
325. Toscano CD, McGlothan JL, and Guilarte TR (2003) Lead exposure alters cyclic-AMP response element binding protein phosphorylation and binding activity in the developing rat brain. Brain Res Dev Brain Res 145:219-228.
326. Trantham-Davidson H, Centanni S, and Chandler LJ (2015) Binge-like alcohol exposure during adolescence disrupts dopaminergic neurotransmission in the adult prefrontal cortex, in Proceedings of the Annual Conference of the Society for Neuroscience; 2015 Oct 17-21. Chicago, IL; Abstract 777.10.
327. Tremblay ME, Lowery RL, and Majewska AK (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8:e1000527.
328. Tremere LA and Pinaud R (2006) Disparity for disinhibitory and excitatory effects during cortical reorganization. Int J Neurosci 116:547-564.
329. Uematsu A, Matsui M, Tanaka C, Takahashi T, Noguchi K, Suzuki M, and Nishijo H (2012) Developmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. PLoS One 7:e46970.
330. Valor LM, Viosca J, Lopez-Atalaya JP, and Barco A (2013) Lysine acetyltransferases CBP and p300 as therapeutic targets in cognitive and neurodegenerative disorders. Curr Pharm Des 19:5051-5064.
331. Van Kampen JM and Eckman CB (2010) Agonist-induced restoration of hippocampal neurogenesis and cognitive improvement in a model of cholinergic denervation. Neuropharmacology 58:921-929.
332. van Praag H, Shubert T, Zhao C, and Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25:8680-8685.
333. Vanderschuren LJ, Niesink RJ, and Van Ree JM (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21:309-326.
334. Varlinskaya EI and Spear LP (2002) Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol Clin Exp Res 26:1502-1511.
335. Varlinskaya EI and Spear LP (2004) Acute ethanol withdrawal (hangover) and social behavior in adolescent and adult male and female Sprague-Dawley rats. Alcohol Clin Exp Res 28:40-50.
336. Varlinskaya EI and Spear LP (2008) Social interactions in adolescent and adult Sprague-Dawley rats: Impact of social deprivation and test context familiarity. Behav Brain Res 188:398-405.
337. Varlinskaya EI and Spear LP (2006) Differences in the social consequences of ethanol emerge during the course of adolescence in rats: social facilitation, social inhibition, and anxiolysis. Dev Psychobiol 48:146-161.
338. Varlinskaya EI and Spear LP (2007) Chronic tolerance to the social consequences of ethanol in adolescent and adult Sprague-Dawley rats. Neurotoxicol Teratol 29: 23-30.
339. Varlinskaya EI, Spear LP, and Spear NE (1999) Social behavior and social motivation in adolescent rats: role of housing conditions and partner’s activity. Physiol Behav 67:475-482.
340. Varlinskaya EI, Truxell E, and Spear LP (2014) Chronic intermittent ethanol exposure during adolescence: effects on social behavior and ethanol sensitivity in adulthood. Alcohol 48:433-444.
341. Varlinskaya EI, Vetter-O’Hagen CS, and Spear LP (2013) Puberty and gonadal hormones: role in adolescent-typical behavioral alterations. Horm Behav 64: 343-349.
342. Veldhuis JD, Roemmich JN, Richmond EJ, Rogol AD, Lovejoy JC, Sheffield-Moore M, Mauras N, and Bowers CY (2005) Endocrine control of body composition in infancy, childhood, and puberty. Endocr Rev 26:114-146.
343. Vetreno RP, Broadwater M, Liu W, Spear LP, and Crews FT (2014) Adolescent, but not adult, binge ethanol exposure leads to persistent global reductions of choline acetyltransferase expressing neurons in brain. PLoS One 9:e113421
344. Vetreno RP and Crews FT (2012) Adolescent binge drinking increases expression of the danger signal receptor agonist HMGB1 and Toll-like receptors in the adult prefrontal cortex. Neuroscience 226:475-488.
345. Vetreno RP and Crews FT (2015) Binge ethanol exposure during adolescence leads to a persistent loss of neurogenesis in the dorsal and ventral hippocampus that is associated with impaired adult cognitive functioning. Front Neurosci 9:35
346. Vetreno RP, Qin L, and Crews FT (2013) Increased receptor for advanced glycation end product expression in the human alcoholic prefrontal cortex is linked to adolescent drinking. Neurobiol Dis 59:52-62.
347. Vetreno RP, Yaxley R, Paniagua B, and Crews FT (2016a) Diffusion tensor imaging reveals adolescent binge ethanol-induced brain structural integrity alterations in adult rats that correlate with behavioral dysfunction. Addict Biol 21:939-953
348. Vetreno RP, Yaxley R, Paniagua B, Johnson GA, and Crews FT (2016b) Adult rat cortical thickness changes across age and following adolescent intermittent ethanol treatment. Addict Biol DOI: [published ahead of print].
349. Vetter CS, Doremus-Fitzwater TL, and Spear LP (2007) Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntaryaccess conditions. Alcohol Clin Exp Res 31:1159-1168.
350. Vetter-O’Hagen CS and Spear LP (2012) Hormonal and physical markers of puberty and their relationship to adolescent-typical novelty-directed behavior. Dev Psychobiol 54:523-535.
351. Wahlstrom D, Collins P, White T, and Luciana M (2010) Developmental changes in dopamine neurotransmission in adolescence: behavioral implications and issues in assessment. Brain Cogn 72:146-159.
352. Wallace JA and Lauder JM (1983) Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 10:459-479.
353. Ward RJ, Lallemand F, and de Witte P (2014) Influence of adolescent heavy session drinking on the systemic and brain innate immune system. Alcohol Alcohol 49: 193-197.
354. Watanabe M and Sakagami M (2007) Integration of cognitive and motivational context information in the primate prefrontal cortex. Cereb Cortex 17 (Suppl 1): i101-i109.
355. Wetherill RR and Fromme K (2009) Subjective responses to alcohol prime eventspecific alcohol consumption and predict blackouts and hangover. J Stud Alcohol Drugs 70:593-600.
356. White AM, Bae JG, Truesdale MC, Ahmad S, Wilson WA, and Swartzwelder HS (2002a) Chronic-intermittent ethanol exposure during adolescence prevents normal developmental changes in sensitivity to ethanol-induced motor impairments. Alcohol Clin Exp Res 26:960-968.
357. White AM, Ghia AJ, Levin ED, and 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.
358. White AM, Jamieson-Drake DW, and Swartzwelder HS (2002b) Prevalence and correlates of alcohol-induced blackouts among college students: results of an e-mail survey. J Am Coll Health 51:117-119, 122-131.
359. White AM and Swartzwelder HS (2004) Hippocampal function during adolescence: a unique target of ethanol effects. Ann N Y Acad Sci 1021:206-220.
360. White HR, Marmorstein NR, Crews FT, Bates ME, Mun EY, and Loeber R (2011) Associations between heavy drinking and changes in impulsive behavior among adolescent boys. Alcohol Clin Exp Res 35:295-303.
361. Willey AR, Varlinskaya EI, and Spear LP (2009) Social interactions and 50 kHz ultrasonic vocalizations in adolescent and adult rats. Behav Brain Res 202:122-129
362. Williams SM and Goldman-Rakic PS (1998) Widespread origin of the primate mesofrontal dopamine system. Cereb Cortex 8:321-345.
363. Winward JL, Bekman NM, Hanson KL, Lejuez CW, and Brown SA (2014) Changes in emotional reactivity and distress tolerance among heavy drinking adolescents during sustained abstinence. Alcohol Clin Exp Res 38:1761-1769
364. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494
365. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O’Donnell J, Christensen DJ, Nicholson C, Iliff JJ, et al. (2013) Sleep drives metabolite clearance from the adult brain. Science 342:373-377.
366. Xu Z, Seidler FJ, Ali SF, Slikker W Jr., and Slotkin TA (2001) Fetal and adolescent nicotine administration: effects on CNS serotonergic systems. Brain Res 914:166-178
367. Yan H, Li Q, Fleming R, Madison RD, Wilson WA, and Swartzwelder HS (2009) Developmental sensitivity of hippocampal interneurons to ethanol: involvement of the hyperpolarization-activated current, Ih. J Neurophysiol 101:67-83.
368. Yan H, Li Q, Madison R, Wilson WA, and Swartzwelder HS (2010) Differential sensitivity of hippocampal interneurons to ethanol in adolescent and adult rats. J Pharmacol Exp Ther 335:51-60.
369. Yu ZY, Wang W, Fritschy JM, Witte OW, and Redecker C (2006) Changes in neocortical and hippocampal GABAA receptor subunit distribution during brain maturation and aging. Brain Res 1099:73-81.
370. Zager A, Andersen ML, Ruiz FS, Antunes IB, and Tufik S (2007) Effects of acute and chronic sleep loss on immune modulation of rats. Am J Physiol Regul Integr Comp Physiol 293:R504-R509.
371. Zahalka EA, Seidler FJ, Lappi SE, Yanai J, and Slotkin TA (1993) Differential development of cholinergic nerve terminal markers in rat brain regions: implications for nerve terminal density, impulse activity and specific gene expression. Brain Res 601:221-229
372. Zeigler DW, Wang CC, Yoast RA, Dickinson BD, McCaffree MA, Robinowitz CB, and Sterling ML; Council on Scientific Affairs, American Medical Association (2005) The neurocognitive effects of alcohol on adolescents and college students. Prev Med 40:23-32.
373. Zhao C, Teng EM, Summers RG Jr., Ming GL, and Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11.
374. Zhao C, Deng W, and Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.
375. Zhou G, Hu S, Lv Y, Song Q, Zou X, and Sheng Z (2011) Carbachol alleviates rat cytokine release and organ dysfunction induced by lipopolysaccharide. J Trauma 71:157-162.
376. Zhu H, Zhao L, Wang E, Dimova N, Liu G, Feng Y, and Cambi F (2012) The QKI-PLP pathway controls SIRT2 abundance in CNS myelin. Glia 60:69-82.
377. Zou J and Crews F (2005) TNF alpha potentiates glutamate neurotoxicity by inhibiting glutamate uptake in organotypic brain slice cultures: neuroprotection by NF kappa B inhibition. Brain Res 1034:11-24.
378. Zou J and Crews F (2006) CREB and NF-kappaB transcription factors regulate sensitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell Mol Neurobiol 26:385-405.
379. Zou J and Crews F (2010) Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-kB and proinflammatory cytokines. Alcohol Clin Exp Res 34:777-789.
380. Zou J and Crews FT (2012) Inflammasome-IL-1b signaling mediates ethanol inhibition of hippocampal neurogenesis. Front Neurosci 6:77.
381. Zou JY and Crews FT (2014) Release of neuronal HMGB1 by ethanol through decreased HDAC activity activates brain neuroimmune signaling. PLoS One 9: e87915.
382. Zurolo E, Iyer A, Maroso M, Carbonell C, Anink JJ, Ravizza T, Fluiter K, Spliet WG, van Rijen PC, Vezzani A, et al. (2011) Activation of Toll-like receptor, RAGE and HMGB1 signalling in malformations of cortical development. Brain 134: 1015-1032.