The effects of rearing environment and chronic methylphenidate administration on behavior and dopamine receptors in adolescent rats

Brain Research

Volumn 1527, Issue , 2013, Pages 67-78

  Gill, Kathryn E ^a   Beveridge, Thomas J R ^a   Smith, Hilary R ^a   Porrino, Linda J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; Enrichment; Environment; Isolation; Methylphenidate

Indexed keywords

DOPAMINE RECEPTOR; METHYLPHENIDATE;

ANIMAL BEHAVIOR; ANIMAL TISSUE; ANXIETY; ARTICLE; AUTORADIOGRAPHY; DOPAMINERGIC SYSTEM; DRUG EFFECT; IN VITRO STUDY; LOCOMOTION; LONG TERM CARE; MALE; NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; RAT; REARING; SOCIAL ENVIRONMENT;

ANIMALIA; RATTUS; RODENTIA;

DOPAMINE; ENRICHMENT; ENVIRONMENT; ISOLATION; METHYLPHENIDATE;

AGING; ANIMALS; AUTORADIOGRAPHY; BEHAVIOR, ANIMAL; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; HOUSING, ANIMAL; MALE; METHYLPHENIDATE; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE; SOCIAL ISOLATION;

EID: 84881178936     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.06.021     Document Type: Article

References (120)

1. K.M. Alvers, J.A. Marusich, C.D. Gipson, J.S. Beckmann, and M.T. Bardo Environmental enrichment during development decreases intravenous self-administration of methylphenidate at low unit doses in rats Behav. Pharmacol. 23 2012 650 657
2. P.J. Baarendse, G. van Grootheest, R.F. Jansen, A.W. Pieneman, S.O. Ogren, M. Verhage, and O. Stiedl Differential involvement of the dorsal hippocampus in passive avoidance in C57bl/6J and DBA/2J mice Hippocampus 18 2008 11 19
3. M.T. Bardo, and R.P. Hammer Jr. Autoradiographic localization of dopamine D1 and D2 receptors in rat nucleus accumbens: resistance to differential rearing conditions Neuroscience 45 1991 281 290
4. M.T. Bardo, S.L. Bowling, J.K. Rowlett, P. Manderscheid, S.T. Buxton, and L.P. Dwoskin Environmental enrichment attenuates locomotor sensitization, but not in vitro dopamine release, induced by amphetamine Pharmacol. Biochem. Behav. 51 1995 397 405
5. M.T. Bardo, J.E. Klebaur, J.M. Valone, and C. Deaton Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats Psychopharmacology (Berlin) 155 2001 278 284
6. J.A. Bethancourt, C.E. Vasquez, and G.B. Britton Sex-dependent effects of long-term oral methylphenidate treatment on spontaneous and learned fear behaviors Neurosci. Lett. 496 2011 30 34
7. T.J. Beveridge, H.R. Smith, M.A. Nader, and L.J. Porrino Abstinence from chronic cocaine self-administration alters striatal dopamine systems in rhesus monkeys Neuropsychopharmacology 34 2009 1162 1171
8. M.J. Bickerdike, I.K. Wright, and C.A. Marsden Social isolation attenuates rat forebrain 5-HT release induced by KCI stimulation and exposure to a novel environment Behav. Pharmacol. 4 1993 231 236
9. J. Biederman Attention-deficit/hyperactivity disorder: a selective overview Biol. Psychiatry 57 2005 1215 1220
10. C.A. Bolanos, M. Barrot, O. Berton, D. Wallace-Black, and E.J. Nestler Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood Biol. Psychiatry 54 2003 1317 1329
11. S.L. Bowling, J.K. Rowlett, and M.T. Bardo The effect of environmental enrichment on amphetamine-stimulated locomotor activity, dopamine synthesis and dopamine release Neuropharmacology 32 1993 885 893
12. J.C. Brenes, M. Padilla, and J. Fornaguera A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats Behav. Brain Res 197 2008 125 127
13. J.C. Brenes, O. Rodriguez, and J. Fornaguera Differential effect of environment enrichment and social isolation on depressive-like behavior, spontaneous activity and serotonin and norepinephrine concentration in prefrontal cortex and ventral striatum Pharmacol. Biochem. Behav. 89 2008 85 93
14. J.C. Brenes Saenz, O.R. Villagra, and J. Fornaguera Trias Factor analysis of Forced Swimming test, Sucrose Preference test and Open Field test on enriched, social and isolated reared rats Behav. Brain Res. 169 2006 57 65
15. M.E. Cain, T.A. Green, and M.T. Bardo Environmental enrichment decreases responding for visual novelty Behav. Processes 73 2006 360 366
16. A.M. Chappell, E. Carter, B.A. McCool, and J.L. Weiner Adolescent rearing conditions influence the relationship between initial anxiety-like behavior and ethanol drinking in male Long Evans rats Alcohol. Clin. Exp. Res. 37 Suppl. 1 2013 E394 E403
17. S. Charntikov, T. Der-Ghazarian, M.S. Herbert, L.R. Horn, C.B. Widarma, A. Gutierrez, F.A. Varela, and S.A. McDougall Importance of D1 and D2 receptors in the dorsal caudate-putamen for the locomotor activity and stereotyped behaviors of preweanling rats Neuroscience 183 2011 121 133
18. J.W. Dalley, T.D. Fryer, L. Brichard, E.S. Robinson, D.E. Theobald, K. Laane, Y. Pena, E.R. Murphy, Y. Shah, K. Probst, I. Abakumova, F.I. Aigbirhio, H.K. Richards, Y. Hong, J.C. Baron, B.J. Everitt, and T.W. Robbins Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement Science 315 2007 1267 1270
19. M.D. De Bellis Developmental traumatology: a contributory mechanism for alcohol and substance use disorders Psychoneuroendocrinology 27 2002 155 170
20. G.A. Deehan Jr., M.E. Cain, and S.W. Kiefer Differential rearing conditions alter operant responding for ethanol in outbred rats Alcohol. Clin. Exp. Res. 31 2007 1692 1698
21. G.A. Deehan Jr., M.I. Palmatier, M.E. Cain, and S.W. Kiefer Differential rearing conditions and alcohol-preferring rats: consumption of and operant responding for ethanol Behav. Neurosci. 125 2011 184 193
22. A. Del Arco, S. Zhu, A. Terasmaa, A.H. Mohammed, and K. Fuxe Hyperactivity to novelty induced by social isolation is not correlated with changes in D2 receptor function and binding in striatum Psychopharmacology (Berlin) 171 2004 148 155
23. A. Del Arco, G. Segovia, J.J. Canales, P. Garrido, M. de Blas, J.M. Garcia-Verdugo, and F. Mora Environmental enrichment reduces the function of D1 dopamine receptors in the prefrontal cortex of the rat J. Neural. Transm. 114 2007 43 48
24. R.I. Desai, P. Terry, and J.L. Katz A comparison of the locomotor stimulant effects of D1-like receptor agonists in mice Pharmacol. Biochem. Behav. 81 2005 843 848
25. E. Djouma, K. Card, D.J. Lodge, and A.J. Lawrence The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D2 receptors in the amygdala and nucleus accumbens of fawn-hooded rats Eur. J. Neurosci. 23 2006 3319 3327
26. B.M. Elliott, and N.E. Grunberg Effects of social and physical enrichment on open field activity differ in male and female Sprague-Dawley rats Behav. Brain Res. 165 2005 187 196
27. K. Fabricius, L. Helboe, A. Fink-Jensen, G. Wortwein, and B. Steiniger-Brach Pharmacological characterization of social isolation-induced hyperactivity Psychopharmacology (Berlin) 215 2011 257 266
28. R.P. Fares, A. Belmeguenai, P.E. Sanchez, H.Y. Kouchi, J. Bodennec, A. Morales, B. Georges, C. Bonnet, S. Bouvard, R.S. Sloviter, and L. Bezin Standardized environmental enrichment supports enhanced brain plasticity in healthy rats and prevents cognitive impairment in epileptic rats PLoS One 8 2013 e53888
29. C. Fehr, I. Yakushev, N. Hohmann, H.G. Buchholz, C. Landvogt, H. Deckers, A. Eberhardt, M. Klager, M.N. Smolka, A. Scheurich, T. Dielentheis, L.G. Schmidt, F. Rosch, P. Bartenstein, G. Grunder, and M. Schreckenberger Association of low striatal dopamine d2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse Am. J. Psychiatry 165 2008 507 514
30. R. Galani, M.C. Berthel, C. Lazarus, M. Majchrzak, A. Barbelivien, C. Kelche, and J.C. Cassel The behavioral effects of enriched housing are not altered by serotonin depletion but enrichment alters hippocampal neurochemistry Neurobiol. Learn. Mem. 88 2007 1 10
31. J.L. Gariepy, P.L. Gendreau, R.B. Mailman, M. Tancer, and M.H. Lewis Rearing conditions alter social reactivity and D1 dopamine receptors in high- and low-aggressive mice Pharmacol. Biochem. Behav. 51 1995 767 773
32. K.E. Gill, P.J. Pierre, J. Daunais, A.J. Bennett, S. Martelle, H.D. Gage, J.M. Swanson, M.A. Nader, and L.J. Porrino Chronic treatment with extended release methylphenidate does not alter dopamine systems or increase vulnerability for cocaine self-administration: a study in nonhuman primates Neuropsychopharmacology 37 2012 2555 2565
33. C.D. Gipson, J.S. Beckmann, S. El-Maraghi, J.A. Marusich, and M.T. Bardo Effect of environmental enrichment on escalation of cocaine self-administration in rats Psychopharmacology (Berlin) 214 2011 557 566
34. J.D. Gray, M. Punsoni, N.E. Tabori, J.T. Melton, V. Fanslow, M.J. Ward, B. Zupan, D. Menzer, J. Rice, C.T. Drake, R.D. Romeo, W.G. Brake, A. Torres-Reveron, and T.A. Milner Methylphenidate administration to juvenile rats alters brain areas involved in cognition, motivated behaviors, appetite, and stress J. Neurosci. 27 2007 7196 7207
35. R. Griggs, C. Weir, W. Wayman, and T.E. Koeltzow Intermittent methylphenidate during adolescent development produces locomotor hyperactivity and an enhanced response to cocaine compared to continuous treatment in rats Pharmacol. Biochem. Behav. 96 2010 166 174
36. F.S. Hall, L.S. Wilkinson, T. Humby, W. Inglis, D.A. Kendall, C.A. Marsden, and T.W. Robbins Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems Pharmacol. Biochem. Behav. 59 1998 859 872
37. X. Han, W. Wang, F. Shao, and N. Li Isolation rearing alters social behaviors and monoamine neurotransmission in the medial prefrontal cortex and nucleus accumbens of adult rats Brain Res. 1385 2011 175 181
38. Harlan Industries, 2008. Sprague Dawley Growth Curve 〈 http://www.harlan.com/products-and-services/research-models-and-services/ research-models/sprague-dawley-outbred-rat.hlâŒ.
39. R.C. Harvey, S. Sen, A. Deaciuc, L.P. Dwoskin, and K.M. Kantak Methylphenidate treatment in adolescent rats with an attention deficit/hyperactivity disorder phenotype: cocaine addiction vulnerability and dopamine transporter function Neuropsychopharmacology 36 2011 837 847
40. C.A. Heidbreder, I.C. Weiss, A.M. Domeney, C. Pryce, J. Homberg, G. Hedou, J. Feldon, M.C. Moran, and P. Nelson Behavioral, neurochemical and endocrinological characterization of the early social isolation syndrome Neuroscience 100 2000 749 768
41. K.G. Hellemans, L.C. Benge, and M.C. Olmstead Adolescent enrichment partially reverses the social isolation syndrome Brain Res. Dev. Brain Res. 150 2004 103 115
42. L.C. Hoffmann, S.R. Schutte, M. Koch, and K. Schwabe Effect of "enriched environment" during development on adult rat behavior and response to the dopamine receptor agonist apomorphine Neuroscience 158 2009 1589 1598
43. S.R. Jaffee, K.B. Hanscombe, C.M. Haworth, O.S. Davis, and R. Plomin Chaotic homes and children's disruptive behavior: a longitudinal cross-lagged twin study Psychol. Sci. 23 2012 643 650
44. G.H. Jones Social isolation and individual differences: behavioural and dopaminergic responses to psychomotor stimulants Clin. Neuropharmacol. 15 Suppl. 1, Pt A 1992 253A 254A
45. Y. Kim, M.A. Teylan, M. Baron, A. Sands, A.C. Nairn, and P. Greengard Methylphenidate-induced dendritic spine formation and DeltaFosB expression in nucleus accumbens Proc. Natl. Acad. Sci. USA 106 2009 2915 2920
46. M.V. King, P. Seeman, C.A. Marsden, and K.C. Fone Increased dopamine D2High receptors in rats reared in social isolation Synapse 63 2009 476 483
47. M.S. Kleven, B.D. Perry, W.L. Woolverton, and L.S. Seiden Effects of repeated injections of cocaine on D1 and D2 dopamine receptors in rat brain Brain Res. 532 1990 265 270
48. K. Koda, Y. Ago, Y. Cong, Y. Kita, K. Takuma, and T. Matsuda Effects of acute and chronic administration of atomoxetine and methylphenidate on extracellular levels of noradrenaline, dopamine and serotonin in the prefrontal cortex and striatum of mice J. Neurochem. 114 2010 259 270
49. H. Koike, D. Ibi, H. Mizoguchi, T. Nagai, A. Nitta, K. Takuma, T. Nabeshima, Y. Yoneda, and K. Yamada Behavioral abnormality and pharmacologic response in social isolation-reared mice Behav. Brain Res. 202 2009 114 121
50. T.A. Kosten, M.J. Miserendino, and P. Kehoe Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience Brain Res. 875 2000 44 50
51. A.K. Lack, K.E. Gill, and L.J. Porrino Local cerebral glucose utilization in rats exposed to an enriched environment: a comparison to impoverishment Pharmacol. Biochem. Behav 96 2010 521 525
52. K. Latimer, P. Wilson, J. Kemp, L. Thompson, F. Sim, C. Gillberg, C. Puckering, and H. Minnis Disruptive behaviour disorders: a systematic review of environmental antenatal and early years risk factors Child Care Health Dev. 38 2012 611 628
53. M.S. Lidow, P.S. Goldman-Rakic, D.W. Gallager, and P. Rakic Distribution of dopaminergic receptors in the primate cerebral cortex: quantitative autoradiographic analysis using [3H]raclopride, [3H]spiperone and [3H]SCH23390 Neuroscience 40 1991 657 671
54. D.J. Lodge, and A.J. Lawrence The effect of isolation rearing on volitional ethanol consumption and central CCK/dopamine systems in Fawn-Hooded rats Behav. Brain Res. 141 2003 113 122
55. V. Lovic, D. Keen, P.J. Fletcher, and A.S. Fleming Early-life maternal separation and social isolation produce an increase in impulsive action but not impulsive choice Behav. Neurosci. 125 2011 481 491
56. J.L. Lukkes, M.V. Mokin, J.L. Scholl, and G.L. Forster Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses Horm. Behav. 55 2009 248 256
57. W.J. Lynch, L.D. Mangini, and J.R. Taylor Neonatal isolation stress potentiates cocaine seeking behavior in adult male and female rats Neuropsychopharmacology 30 2005 322 329
58. L. MacGillivray, K.B. Reynolds, P.I. Rosebush, and M.F. Mazurek The comparative effects of environmental enrichment with exercise and serotonin transporter blockade on serotonergic neurons in the dorsal raphe nucleus Synapse 66 2012 465 470
59. B.K. Madras, G.M. Miller, and A.J. Fischman The dopamine transporter and attention-deficit/hyperactivity disorder Biol. Psychiatry 57 2005 1397 1409
60. D.T. Malone, C.S. Kearn, L. Chongue, K. Mackie, and D.A. Taylor Effect of social isolation on CB1 and D2 receptor and fatty acid amide hydrolase expression in rats Neuroscience 152 2008 265 272
61. B.A. McCool, and A.M. Chappell Early social isolation in male Long-Evans rats alters both appetitive and consummatory behaviors expressed during operant ethanol self-administration Alcohol. Clin. Exp. Res. 33 2009 273 282
62. S. Miachon, T. Rochet, B. Mathian, B. Barbagli, and B. Claustrat Long-term isolation of Wistar rats alters brain monoamine turnover, blood corticosterone, and ACTH Brain Res. Bull. 32 1993 611 614
63. H. Miura, H. Qiao, and T. Ohta Attenuating effects of the isolated rearing condition on increased brain serotonin and dopamine turnover elicited by novelty stress Brain Res. 926 2002 10 17
64. K. Mizoguchi, M. Yuzurihara, A. Ishige, H. Sasaki, D.H. Chui, and T. Tabira Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction J. Neurosci. 20 2000 1568 1574
65. D. Morgan, K.A. Grant, H.D. Gage, R.H. Mach, J.R. Kaplan, O. Prioleau, S.H. Nader, N. Buchheimer, R.L. Ehrenkaufer, and M.A. Nader Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration Nat. Neurosci. 5 2002 169 174
66. M.A. Nader, J.B. Daunais, T. Moore, S.H. Nader, R.J. Moore, H.R. Smith, D.P. Friedman, and L.J. Porrino Effects of cocaine self-administration on striatal dopamine systems in rhesus monkeys: initial and chronic exposure Neuropsychopharmacology 27 2002 35 46
67. F. Naka, T. Shiga, M. Yaguchi, and N. Okado An enriched environment increases noradrenaline concentration in the mouse brain Brain Res. 924 2002 124 126
68. L.R. Nelson, and G. Ellison Enhanced stereotypies after repeated injections but not continuous amphetamines Neuropharmacology 17 1978 1081 1084
69. N.M. Neugebauer, S.T. Cunningham, J. Zhu, R.I. Bryant, L.S. Middleton, and L.P. Dwoskin Effects of environmental enrichment on behavior and dopamine transporter function in medial prefrontal cortex in adult rats prenatally treated with cocaine Brain Res. Dev. Brain Res. 153 2004 213 223
70. H. Ouchi, K. Ono, Y. Murakami, and K. Matsumoto Social isolation induces deficit of latent learning performance in mice: a putative animal model of attention deficit/hyperactivity disorder Behav. Brain Res. 238 2013 146 153
71. F.A. Pamplona, P. Pandolfo, R. Savoldi, R.D. Prediger, and R.N. Takahashi Environmental enrichment improves cognitive deficits in spontaneously hypertensive rats (SHR): relevance for attention deficit/hyperactivity disorder (ADHD) Prog. Neuropsychopharmacol. Biol. Psychiatry 33 2009 1153 1160
72. B.A. Pappas, S.J. Murtha, G.A. Park, K.T. Condon, R.M. Szirtes, S.I. Laventure, and A. Ally Neonatal brain dopamine depletion and the cortical and behavioral consequences of enriched postweaning environment Pharmacol. Biochem. Behav. 42 1992 741 748
73. W.E. Pelham, E.M. Gnagy, L. Burrows-Maclean, A. Williams, G.A. Fabiano, S.M. Morrisey, A.M. Chronis, G.L. Forehand, C.A. Nguyen, M.T. Hoffman, T.M. Lock, K. Fielbelkorn, E.K. Coles, C.J. Panahon, R.L. Steiner, D.L. Meichenbaum, A.N. Onyango, and G.D. Morse Once-a-day concerta methylphenidate versus three-times-daily methylphenidate in laboratory and natural settings Pediatrics 107 2001 E105
74. J.L. Perry, D.J. Stairs, and M.T. Bardo Impulsive choice and environmental enrichment: effects of d-amphetamine and methylphenidate Behav. Brain Res. 193 2008 48 54
75. J.R. Peters, B. Vallie, M. Difronzo, and S.T. Donaldson Role of dopamine D1 receptors in novelty seeking in adult female Long-Evans rats Brain Res. Bull. 74 2007 232 236
76. L.M. Pritchard, T.A. Van Kempen, and B. Zimmerberg Behavioral effects of repeated handling differ in rats reared in social isolation and environmental enrichment Neurosci. Lett. 536 2013 47 51
77. M.D. Puhl, J.S. Blum, S. Acosta-Torres, and P.S. Grigson Environmental enrichment protects against the acquisition of cocaine self-administration in adult male rats, but does not eliminate avoidance of a drug-associated saccharin cue Behav. Pharmacol. 23 2012 43 53
78. O. Rilke, M. Jahkel, and J. Oehler Dopaminergic parameters during social isolation in low- and high-active mice Pharmacol. Biochem. Behav. 60 1998 499 505
79. C. Rivier, and W. Vale Diminished responsiveness of the hypothalamic-pituitary-adrenal axis of the rat during exposure to prolonged stress: a pituitary-mediated mechanism Endocrinology 121 1987 1320 1328
80. S. Sadasivan, B.B. Pond, A.K. Pani, C. Qu, Y. Jiao, and R.J. Smeyne Methylphenidate exposure induces dopamine neuron loss and activation of microglia in the basal ganglia of mice PLoS One 7 2012 e33693
81. D.J. Safer, J.M. Zito, and E.M. Fine Increased methylphenidate usage for attention deficit disorder in the 1990s Pediatrics 98 1996 1084 1088
82. N.J. Sandstrom, and S.R. Hart Isolation stress during the third postnatal week alters radial arm maze performance and corticosterone levels in adulthood Behav. Brain Res. 156 2005 289 296
83. S. Schenk, T. Hunt, R. Malovechko, A. Robertson, G. Klukowski, and Z. Amit Differential effects of isolation housing on the conditioned place preference produced by cocaine and amphetamine Pharmacol. Biochem. Behav. 24 1986 1793 1796
84. S. Schenk, G. Lacelle, K. Gorman, and Z. Amit Cocaine self-administration in rats influenced by environmental conditions: implications for the etiology of drug abuse Neurosci. Lett. 81 1987 227 231
85. S. Schenk, K. Gorman, and Z. Amit Age-dependent effects of isolation housing on the self-administration of ethanol in laboratory rats Alcohol 7 1990 321 326
86. C.W. Schindler, and G.N. Carmona Effects of dopamine agonists and antagonists on locomotor activity in male and female rats Pharmacol. Biochem. Behav. 72 2002 857 863
87. N.C. Schrijver, and H. Wurbel Early social deprivation disrupts attentional, but not affective, shifts in rats Behav. Neurosci. 115 2001 437 442
88. F. Shao, J. Jin, Q. Meng, M. Liu, X. Xie, W. Lin, and W. Wang Pubertal isolation alters latent inhibition and DA in nucleus accumbens of adult rats Physiol. Behav. 98 2009 251 257
89. Y. Simchon, A. Weizman, and M. Rehavi The effect of chronic methylphenidate administration on presynaptic dopaminergic parameters in a rat model for ADHD Eur. Neuropsychopharmacol. 20 2010 714 720
90. J.K. Smith, J.C. Neill, and B. Costall Post-weaning housing conditions influence the behavioural effects of cocaine and d-amphetamine Psychopharmacology (Berlin) 131 1997 23 33
91. M. Solinas, N. Thiriet, C. Chauvet, and M. Jaber Prevention and treatment of drug addiction by environmental enrichment Prog. Neurobiol. 92 2010 572 592
92. P.L. Soto, K.M. Wilcox, Y. Zhou, N.A. Ator, M.A. Riddle, D.F. Wong, and M.R. Weed Long-term exposure to oral methylphenidate or dl-amphetamine mixture in peri-adolescent rhesus monkeys: effects on physiology, behavior, and dopamine system development Neuropsychopharmacology 37 2012 2566 2579
93. T. Spencer, J. Biederman, and T. Wilens Pharmacotherapy of attention deficit hyperactivity disorder Child Adolesc. Psychiatr. Clin. N. Am. 9 2000 77 97
94. T.J. Spencer, J. Biederman, P.E. Ciccone, B.K. Madras, D.D. Dougherty, A.A. Bonab, E. Livni, D.A. Parasrampuria, and A.J. Fischman PET study examining pharmacokinetics, detection and likeability, and dopamine transporter receptor occupancy of short- and long-acting oral methylphenidate Am. J. Psychiatry. 163 2006 387 395
95. E.J. Sproson, J. Chantrey, C. Hollis, C.A. Marsden, and K.C. Fonel Effect of repeated methylphenidate administration on presynaptic dopamine and behaviour in young adult rats J. Psychopharmacol. 15 2001 67 75
96. D.J. Stairs, and M.T. Bardo Neurobehavioral effects of environmental enrichment and drug abuse vulnerability Pharmacol. Biochem. Behav. 92 2009 377 382
97. J.M. Swanson, S.B. Wigal, T. Wigal, E. Sonuga-Barke, L.L. Greenhill, J. Biederman, S. Kollins, A.S. Nguyen, H.H. DeCory, S.J. Hirshe Dirksen, and S.J. Hatch A comparison of once-daily extended-release methylphenidate formulations in children with attention-deficit/hyperactivity disorder in the laboratory school (the Comacs Study) Pediatrics 113 2004 e206 e216
98. P.K. Thanos, N.D. Volkow, P. Freimuth, H. Umegaki, H. Ikari, G. Roth, D.K. Ingram, and R. Hitzemann Overexpression of dopamine D2 receptors reduces alcohol self-administration J. Neurochem. 78 2001 1094 1103
99. P.K. Thanos, N.B. Taintor, S.N. Rivera, H. Umegaki, H. Ikari, G. Roth, D.K. Ingram, R. Hitzemann, J.S. Fowler, S.J. Gatley, G.J. Wang, and N.D. Volkow DRD2 gene transfer into the nucleus accumbens core of the alcohol preferring and nonpreferring rats attenuates alcohol drinking Alcohol. Clin. Exp. Res. 28 2004 720 728
100. P.K. Thanos, M. Michaelides, H. Benveniste, G.J. Wang, and N.D. Volkow Effects of chronic oral methylphenidate on cocaine self-administration and striatal dopamine D2 receptors in rodents Pharmacol. Biochem. Behav. 87 2007 426 433
101. A.H. Tran, R. Tamura, T. Uwano, T. Kobayashi, M. Katsuki, and T. Ono Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place Proc. Natl. Acad. Sci. USA 102 2005 2117 2122
102. S. Ueda, S. Sakakibara, and K. Yoshimoto Effect of long-lasting serotonin depletion on environmental enrichment-induced neurogenesis in adult rat hippocampus and spatial learning Neuroscience 135 2005 395 402
103. E.M. Unterwald, J. Fillmore, and M.J. Kreek Chronic repeated cocaine administration increases dopamine D1 receptor-mediated signal transduction Eur. J. Pharmacol. 318 1996 31 35
104. S. Urakawa, K. Takamoto, E. Hori, N. Sakai, T. Ono, and H. Nishijo Rearing in enriched environment increases parvalbumin-positive small neurons in the amygdala and decreases anxiety-like behavior of male rats BMC Neurosci. 14 2013 13
105. G.B. Varty, M.P. Paulus, D.L. Braff, and M.A. Geyer Environmental enrichment and isolation rearing in the rat: effects on locomotor behavior and startle response plasticity Biol. Psychiatry 47 2000 864 873
106. N.D. Volkow, G.J. Wang, J.S. Fowler, J. Logan, R. Hitzemann, Y.S. Ding, N. Pappas, C. Shea, and K. Piscani Decreases in dopamine receptors but not in dopamine transporters in alcoholics Alcohol. Clin. Exp. Res. 20 1996 1594 1598
107. N.D. Volkow, G.J. Wang, J.S. Fowler, S.J. Gatley, J. Logan, Y.S. Ding, R. Hitzemann, and N. Pappas Dopamine transporter occupancies in the human brain induced by therapeutic doses of oral methylphenidate Am. J. Psychiatry. 155 1998 1325 1331
108. N.D. Volkow, L. Chang, G.J. Wang, J.S. Fowler, Y.S. Ding, M. Sedler, J. Logan, D. Franceschi, J. Gatley, R. Hitzemann, A. Gifford, C. Wong, and N. Pappas Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex Am. J. Psychiatry 158 2001 2015 2021
109. N.D. Volkow, and J.M. Swanson Variables that affect the clinical use and abuse of methylphenidate in the treatment of ADHD Am. J. Psychiatry 160 2003 1909 1918
110. N.D. Volkow, G.J. Wang, H. Begleiter, B. Porjesz, J.S. Fowler, F. Telang, C. Wong, Y. Ma, J. Logan, R. Goldstein, D. Alexoff, and P.K. Thanos High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors Arch. Gen. Psychiatry 63 2006 999 1008
111. G.J. Wang, N.D. Volkow, J.S. Fowler, J. Logan, N.N. Abumrad, R.J. Hitzemann, N.S. Pappas, and K. Pascani Dopamine D2 receptor availability in opiate-dependent subjects before and after naloxone-precipitated withdrawal Neuropsychopharmacology 16 1997 174 182
112. Y.C. Wang, U.C. Ho, M.C. Ko, C.C. Liao, and L.J. Lee Differential neuronal changes in medial prefrontal cortex, basolateral amygdala and nucleus accumbens after postweaning social isolation Brain Struct. Funct. 217 2012 337 351
113. J. Wolffgramm Free choice ethanol intake of laboratory rats under different social conditions Psychopharmacology (Berlin) 101 1990 233 239
114. T.E. Wooters, M.T. Bardo, L.P. Dwoskin, N.M. Midde, A.M. Gomez, C.F. Mactutus, R.M. Booze, and J. Zhu Effect of environmental enrichment on methylphenidate-induced locomotion and dopamine transporter dynamics Behav. Brain Res. 219 2011 98 107
115. I.K. Wright, N. Upton, and C.A. Marsden Resocialisation of isolation-reared rats does not alter their anxiogenic profile on the elevated X-maze model of anxiety Physiol. Behav. 50 1991 1129 1132
116. J.R. Yates, M. Darna, C.D. Gipson, L.P. Dwoskin, and M.T. Bardo Isolation rearing as a preclinical model of attention/deficit-hyperactivity disorder Behav. Brain Res. 234 2012 292 298
117. J.T. Yorgason, R.A. Espana, J.K. Konstantopoulos, J.L. Weiner, and S.R. Jones Enduring increases in anxiety-like behavior and rapid nucleus accumbens dopamine signaling in socially isolated rats Eur. J. Neurosci. 37 2013 1022 1031
118. S. Zeigler, J. Lipton, A. Toga, and G. Ellison Continuous cocaine administration produces persisting changes in brain neurochemistry and behavior Brain Res. 552 1991 27 35
119. N. Zhu, J. Weedon, and D.L. Dow-Edwards The multifaceted effects of oral administration of methylphenidate in juvenile rats: anxiety, activity, and attention Eur. Neuropsychopharmacol. 20 2010 236 244
120. J.M. Zito, D.J. Safer, S. dosReis, J.F. Gardner, M. Boles, and F. Lynch Trends in the prescribing of psychotropic medications to preschoolers JAMA 283 2000 1025 1030