Immunization with DAT fragments is associated with long-term striatal impairment, hyperactivity and reduced cognitive flexibility in mice

Behavioral and Brain Functions

Volumn 8, Issue , 2012, Pages

  Adriani, Walter ^a   Koot, Susanne ^a,b   Columba Cabezas, Sandra ^a   Romano, Emilia ^a   Travaglini, Domenica ^a   van den Bos, Ruud ^b   Granstrem, Oleg ^c   Ali, Syed F ^d   Laviola, Giovanni ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c PAVLOV FIRST SAINT PETERSBURG STATE MEDICAL UNIVERSITY   (Russian Federation)

^d NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

ADHD; Auto antibodies to neuro receptors; DAT; Delay of reward; Flexibility of choice behaviour; OCD

Indexed keywords

AUTOANTIBODY; DOPAMINE TRANSPORTER; MONOAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENTION DEFICIT DISORDER; AUTOIMMUNITY; BEHAVIOR; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; FOOD INTAKE; HYPERACTIVITY; MALE; MOUSE; NONHUMAN; OBSESSIVE COMPULSIVE DISORDER; PRIORITY JOURNAL; TASK PERFORMANCE;

ANIMALS; BEHAVIOR, ANIMAL; COGNITION; CORPUS STRIATUM; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; EXPLORATORY BEHAVIOR; HYPERKINESIS; IMMUNIZATION; MALE; MICE; PEPTIDE FRAGMENTS; REWARD;

EID: 84870057385     PISSN: None     EISSN: 17449081     Source Type: Journal    
DOI: 10.1186/1744-9081-8-54     Document Type: Article

References (87)

1. Snyder R, Turgay A, Aman M, Binder C, Fisman S, Carroll A. Risperidone conduct study group. Effects of risperidone on conduct and disruptive behavior disorders in children with subaverage IQs. J Am Acad Child Adolesc Psychiatr 2002, 41:1026-1036.
2. Doyle AE. Executive functions in attention-deficit/hyperactivity disorder. J Clin Psychiatr 2006, 67:21-26.
3. Castellanos FX, Sonuga-Barke EJ, Milham MP, Tannock R. Characterizing of cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 2006, 10:117-123. 10.1016/j.tics.2006.01.011, 16460990.
4. Sonuga-Barke EJ. Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biol Psychiatry 2005, 57:1231-1238. 10.1016/j.biopsych.2004.09.008, 15949993.
5. Sagvolden T, Sergeant JA. Attention deficit/hyperactivity disorder - from brain dysfunctions to behaviour. Behav Brain Res 1998, 94:1-10.
6. Oades RD. Frontal, temporal and lateralized brain function in children with attention-deficit hyperactivity disorder: a psycho-physiological and neuro-psychological viewpoint on development. Behav Brain Res 1998, 94:83-95. 10.1016/S0166-4328(97)00172-1, 9708842.
7. Geller D, Biederman J, Jones J, Park K, Schwartz S, Shapiro S, Coffey B. Is juvenile obsessive-compulsive disorder a developmental subtype of the disorder? A review of the pediatric literature. J Am Acad Child Adolesc Psychiatr 1998, 37:420-427.
8. Sheppard DM, Bradshaw JL, Purcell R, Pantelis C. Tourette's and comorbid syndromes: obsessive compulsive and attention deficit hyperactivity disorder. A common etiology?. Clin Psychol Rev 1999, 19:531-552. 10.1016/S0272-7358(98)00059-2, 10467490.
9. Lowengrub K, Iancu I, Aizer A, Kotler M, Dannon PN. Pharmacotherapy of the pathological gambling: review of new treatment modalities. Expert Rev Neurother 2006, 6:1845-1851. 10.1586/14737175.6.12.1845, 17181431.
10. Hollander E, Buchalter AJ, DeCaria CM. Pathological gambling. Psychiatr Clin North Am 2000, 23:629-642. 10.1016/S0193-953X(05)70185-4, 10986732.
11. Hollander E, Sood E, Pallanti S, Baldini-Rossi N, Baker B. Pharmacological treatments of pathological gambling. J Gambl Stud 2005, 21:99-110. 10.1007/s10899-004-1932-8, 15789195.
12. Zuckerman M, Kuhlman DM. Personality and risk-taking: common biosocial factors. J Pers 2000, 68:999-1029. 10.1111/1467-6494.00124, 11130742.
13. Ebstein RP, Novick O, Umansky R, Priel B, Osher Y, Blaine D, Bennett ER, Nemanov L, Katz M, Belmaker RH. Dopamine D4 receptor (D4DR) exon III polymorphism associated with the human personality trait of Novelty Seeking. Nat Genet 1996, 12:78-80. 10.1038/ng0196-78, 8528256.
14. Comings DE, Gonzalez N, Wu S, Gade R, Muhleman D, Saucier G, Johnson P, Verde R, Rosenthal RJ, Lesieur HR, Rugle LJ, Miller WB, MacMurray JP. Studies of the 48 bp repeat polymorphism of DRD4 gene in impulsive, compulsive, addictive behaviors: Tourette syndrome, ADHD, pathological gambling, and substance abuse. Am J Med Genet 1999, 88:358-368. 10.1002/(SICI)1096-8628(19990820)88:4<358::AID-AJMG13>3.0.CO;2-G, 10402503.
15. Laucht M, Becker K, El-Faddagh M, Hohm E, Schmidt MH. Association of the DRD4 exon III polymorphism with smoking in fifteen-year-olds: a mediating role for novelty seeking?. J Am Acad Child Adolesc Psychiatr 2005, 44:477-484.
16. Faraone SV, Perlis RH, Doyle AE, Smoller JW, Goralnick JJ, Holmgren MA, Sklar P. Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry 2005, 57:1313-1323. 10.1016/j.biopsych.2004.11.024, 15950004.
17. Millet B, Chabane N, Delorme R, Leboyer M, Leroy S, Poirier MF, Bourdel MC, Mouren-Simeoni MC, Rouillon F, Loo H, Krebs MO. Association between the dopamine receptor D4 gene and obsessive-compulsive disorder. Am J Med Genet B (Neuropsychiatr) 2003, 116:55-59.
18. Camarena B, Loyzaga C, Aguilar A, Weissbecker K, Nicolini H. Association study between the dopamine receptor D(4) gene and obsessive-compulsive disorder. Eur Neuro-psycho-pharmacol 2007, 17:406-409.
19. Jucaite A, Fernell E, Halldin C, Forssberg H, Farde L. Reduced midbrain dopamine transporter binding in male adolescents with attention-deficit/hyperactivity disorder: association between striatal dopamine markers and motor hyperactivity. Biol Psychiatry 2005, 57:229-238. 10.1016/j.biopsych.2004.11.009, 15691523.
20. Bannon MJ. The dopamine transporter: role in neurotoxicity and human disease. Toxicol Appl Pharmacol 2005, 204:355-360. 10.1016/j.taap.2004.08.013, 15845424.
21. Hesse S, Müller U, Lincke T, Barthel H, Villmann T, Angermeyer MC, Sabri O, Stengler-Wenzke K. Serotonin and dopamine transporter imaging in patients with obsessive-compulsive disorder. Psychiatr Res 2005, 140:63-72.
22. Berridge KC, Aldridge JW, Houchard KR, Zhuang X. Sequential super-stereotypy of an instinctive fixed action pattern in hyper-dopaminergic mutant mice: a model of obsessive compulsive disorder and Tourette's. BMC Biol 2005, 3:4. 10.1186/1741-7007-3-4, 552313, 15710042.
23. Hoekstra PJ, Minderaa RB. Tic disorders and obsessive-compulsive disorder: is autoimmunity involved?. Int Rev Psychiatr 2005, 17:497-502.
24. Shulman ST. Pediatric autoimmune neuropsychiatric disorders associated with streptococci (PANDAS): update. Curr Opin Pediatr 2009, 21:127-130. 10.1097/MOP.0b013e32831db2c4, 19242249.
25. Graus F, Saiz A, Dalmau J. Antibodies and neuronal autoimmune disorders of the CNS. J Neurol 2010, 257:509-517. 10.1007/s00415-009-5431-9, 20035430.
26. Pachter JS, de Vries HE, Fabry Z. The blood-brain barrier and its role in immune privilege in the central nervous system. J Neuropathol Exp Neurol 2003, 62:593-604.
27. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178-201. 10.1016/j.neuron.2008.01.003, 18215617.
28. Diamond B, Huerta PT, Mina-osorio P, Kowal C, Volpe BT. Losing your nerves? maybe it's the antibodies. Nat Rev Immunol 2009, 9:449-456. 10.1038/nri2529, 2783680, 19424277.
29. Levin EC, Acharya NK, Han M, Zavareh SB, Sedeyn JC, Venkataraman V, Nagele RG. Brain-reactive autoantibodies are nearly ubiquitous in human sera and may be linked to pathology in the context of blood-brain barrier breakdown. Brain Res 2010, 1345:221-232.
30. Kuang F, Wang BR, Zhang P, Fei LL, Jia Y, Duan XL, Wang X, Xu Z, Li GL, Jiao XY, Ju G. Extravasation of blood-borne immunoglobulin G through blood-brain barrier during adrenaline-induced transient hypertension in the rat. Int J Neurosci 2004, 114:575-591.
31. Ankeny DP, Popovich PG. B cells and autoantibodies: complex roles in CNS injury. Trends Immunol 2010, 31:332-338. 10.1016/j.it.2010.06.006, 2933277, 20691635.
32. Davies AL, Hayes KC, Dekaban GA. Clinical correlates of the elevated serum concentrations of cytokines and autoantibodies in patients with spinal cord injury. Arch Phys Med Rehabil 2007, 88:1384-1393. 10.1016/j.apmr.2007.08.004, 17964877.
33. Cohen-Solal JF, Diamond B. Neuropsychiatric lupus and autoantibodies against ionotropic glutamate receptor (NMDAR). Rev Med Intern 2011, 32:130-132.
34. Rogers SW, Andrews PI, Gahring LC, Whisenand T, Cauley K, Crain B. Auto-antibodies to glutamate receptor GluR3 in Rasmussen's encephalitis. Science 1994, 265:648-651. 10.1126/science.8036512, 8036512.
35. Twyman RE, Gahring LC, Spiess J, Rogers SW. Glutamate receptor antibodies activate a subset of receptors and reveal an agonist binding site. Neuron 1995, 14:755-762. 10.1016/0896-6273(95)90219-8, 7718238.
36. Dambinova SA, Khounteev GA, Izykenova GA, Zavolokov IG, Ilyukhina AY, Skoromets AA. Blood test detecting autoantibodies to NMDA neuroreceptors for evaluation of patients with transient ischemic attack and stroke. Clin Chem 2003, 49:1752-1762. 10.1373/49.10.1752, 14500616.
37. Roy BF, Bowen WD, Frazier JS, Rose JW, McFarland HF, McFarlin DE, Murphy DL, Morihisa JM. Human anti-idiotypic antibody against the opiate receptors. Ann Neurol 1988, 24:57-63. 10.1002/ana.410240111, 2843077.
38. Singer HS, Giuliano JD, Hansen BH, Hallett JJ, Laurino JP, Benson M, Kiessling LS. Antibodies against human putamen in children with Tourette syndrome. Neurology 1998, 50:1618-1624. 10.1212/WNL.50.6.1618, 9633702.
39. Morshed SA, Parveen S, Leckman JF, Mercadante MT, Bittencourt Kiss MH, Miguel EC, Arman A, Yazgan Y, Fujii T, Paul S, Peterson BS, Zhang H, King RA, Scahill L, Lombroso PJ. Antibodies against neural, nuclear, cytoskeletal, and streptococcal epitopes in children and adults with Tourette's syndrome, Sydenham's chorea, and autoimmune disorders. Biol Psychiatry 2001, 50:566-577. 10.1016/S0006-3223(01)01096-4, 11690591.
40. Loiselle CR, Wendlandt JT, Rohde CA, Singer HS. Antistreptococcal, neuronal, and nuclear antibodies in Tourette syndrome. Pediatr Neurol 2003, 28:119-125. 10.1016/S0887-8994(02)00507-6, 12699862.
41. Dambinova SA, Izykenova GA, Burov SV, Grigorenko EV, Gromov SA. The presence of autoantibodies to N-terminus domain of GluR1 subunit of AMPA receptor in the blood serum of patients with epilepsy. J Neurol Sci 1997, 152:93-97. 10.1016/S0022-510X(97)00150-0, 9395130.
42. Dambinova SA, Granstrem O, Tourov A, Salluzzo R, Castello F, Izykenova GA. Monitoring brain spiking activity and autoantibodies to N-terminus domain of GluR1 subunit of AMPA receptors in blood serum of rats with cobalt-induced epilepsy. J Neurochem 1998, 71:2088-2093.
43. Vincent A, Lily O, Palace J. Pathogenic autoantibodies to neuronal proteins in neurological disorders. J Neuroimmunol 1999, 100:169-180. 10.1016/S0165-5728(99)00210-6, 10695727.
44. Kowal C, Degiorgio LA, Lee JY, Edgar MA, Huerta PT, Volpe BT, Diamond B. Human lupus autoantibodies against NMDA receptors mediate cognitive impairment. Proc Natl Acad Sci USA 2006, 103:19854-19859. 10.1073/pnas.0608397104, 1702320, 17170137.
45. Knight JG, Menkes DB, Highton J, Adams DD. Rationale for a trial of immuno-suppressive therapy in acute schizophrenia. Mol Psychiatr 2007, 12:424-431.
46. Colasanti T, Delunardo F, Margutti P, Vacirca D, Piro E, Siracusano A, Ortona E. Autoantibodies involved in neuropsychiatric manifestations associated with systemic lupus erythematosus. J Neuroimmunol 2009, 212:3-9. 10.1016/j.jneuroim.2009.05.003, 19500858.
47. Granstrem O, Adriani W, Shumilina M, Izykenova G, Dambinova S, Laviola G. Specific changes in levels of auto-antibodies to glutamate and opiate receptors induced by morphine administration in rats. Neurosci Lett 2006, 403:1-5. 10.1016/j.neulet.2006.04.017, 16687214.
48. Levite M, Fleidervish IA, Schwarz A, Pelled D, Futerman AH. Autoantibodies to the glutamate receptor kill neurons via activation of the receptor ion channel. J Autoimmun 1999, 13:61-72. 10.1006/jaut.1999.0301, 10441169.
49. Capone F, Adriani W, Shumilina M, Izykenova G, Granstrem O, Dambinova S, Laviola G. Auto-antibodies against opioid or glutamate receptors are associated with changes in morphine reward and physical dependence in mice. Psychopharmacology 2008, 197:535-548. 10.1007/s00213-007-1062-y, 18265961.
50. Adriani W, Boyer F, Gioiosa L, Macrì S, Dreyer J-L, Laviola G. Increased impulsive behavior and risk proneness following lentivirus-mediated DAT over-expression in rats' nucleus accumbens. Neuroscience 2009, 159:47-58. 10.1016/j.neuroscience.2008.11.042, 19135135.
51. Van den Bos R, Lasthuis W, den Heijer E, van der Harst J, Spruijt B. Towards a rodent model of the Iowa gambling task. Beh Res Meth 2006, 38:470-478.
52. Van den Bos R, van der Harst J, Jonkman S, Schilders M, Spruijt B. Rats assess costs and benefits according to an internal standard. Behav Brain Res 2006, 171:350-354. 10.1016/j.bbr.2006.03.035, 16697474.
53. Koot S, Van den Bos R, Adriani W, Laviola G. Gender differences in delay-discounting under mild food restriction. Behav Brain Res 2009, 200:134-43. 10.1016/j.bbr.2009.01.006, 19373979.
54. Sagvolden T. Behavioral validation of the spontaneously hypertensive rat (SHR) as an animal model of attention deficit/hyperactivity disorder (AD/HD). Neurosci Biobehav Rev 2000, 24:31-39. 10.1016/S0149-7634(99)00058-5, 10654658.
55. Adriani W, Caprioli A, Granstrem O, Carli M, Laviola G. The spontaneously-hypertensive-rat as an animal model of ADHD: evidence for impulsive and non-impulsive subpopulations. Neurosci Biobehav Rev 2003, 27:639-651. 10.1016/j.neubiorev.2003.08.007, 14624808.
56. Adriani W, Zoratto F, Romano E, Laviola G. Cognitive impulsivity in animal models: role of response time and reinforcing rate in delay intolerance with Two-choice operant tasks. Neuropharmacology 2010, 58:694-701. 10.1016/j.neuropharm.2009.11.007, 19945469.
57. Evenden JL, Ryan CN. The pharmacology of impulsive behaviour in rats VI: the effects of ethanol and selective serotonergic drugs on response choice with varying delays of reinforcement. Psychopharmacology 1999, 146:413-421. 10.1007/PL00005486, 10550491.
58. Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Rev 1998, 28:309-369. 10.1016/S0165-0173(98)00019-8, 9858756.
59. Ragozzino ME, Ragozzino KE, Mizumori SJ, Kesner RP. Role of the dorsomedial striatum in the behavioral flexibility for response and visual cue discrimination learning. Behav Neurosci 2002, 116:105-115. 3273324, 11898801.
60. Salamone JD, Correa M, Mingote S, Weber SM. Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 2003, 305:1-8. 10.1124/jpet.102.035063, 12649346.
61. Yin HH, Knowlton BJ, Balleine BW. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 2004, 19:181-189. 10.1111/j.1460-9568.2004.03095.x, 14750976.
62. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW. The role of the dorsomedial striatum in instrumental conditioning. 4. Eur J Neurosci 2005, 22:513-523. 10.1111/j.1460-9568.2005.04218.x, 16045504.
63. Faure A, Haberland U, Condé F, El MN. Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J Neurosci 2005, 25:2771-2780. 10.1523/JNEUROSCI.3894-04.2005, 15772337.
64. Berridge KC. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 2007, 191:391-431. 10.1007/s00213-006-0578-x, 17072591.
65. Ali SF, Newport GD, Holson RR, Slikker W, Bowyer JF. Low environmental temperatures or pharmacological agents which produce hypothermia decreases methamphetamine neurotoxicity in mice. Brain Res 1994, 658:33-38. 10.1016/S0006-8993(09)90007-5, 7530580.
66. Ognibene E, Adriani W, Caprioli A, Ghirardi O, Ali SF, Aloe L, Laviola G. The effect of early maternal separation on brain derived neurotrophic factor and monoamine levels in adult heterozygous reeler mice. Prog Neuropsychopharmacol Biol Psychiatr 2008, 32:1269-1276.
67. Abdi H, Williams LJ. Honestly significant difference (HSD) test. Encyclopedia of research design 2010, 583-585. Thousand Oaks, CA, USA: Sage, Salkind NJ, Dougherty DM, Frey B.
68. Piazza PV, Maccari S, Deminiere JM, Le Moal M, Mormede P, Simon H. Corticosterone levels determine individual vulnerability to amphetamine self-administration. Proc Natl Acad Sci USA 1991, 88:2088-2092. 10.1073/pnas.88.6.2088, 51174, 2006148.
69. Harlow ED, Lane D. Antibodies laboratory manual 1988, Cold Spring Harbor: CSH.
70. Adriani W, Laviola G. Elevated levels of impulsivity and reduced place conditioning with amphetamine: two behavioral features of adolescence in mice. Behav Neurosci 2003, 117:695-703.
71. Evenden JL, Ryan CN. The pharmacology of impulsive behaviour in rats: the effects of drugs on response choice with varying delays of reinforcement. Psychopharmacology 1996, 128:161-170. 10.1007/s002130050121, 8956377.
72. Qi Z, Miller GW, Voit EO. A mathematical model of presynaptic dopamine homeostasis: implications for schizophrenia. Pharmaco-psychiatry 2008, 41:S89-S98.
73. Rolls ET, Loh M, Deco G, Winterer G. Computational models of schizophrenia and dopamine modulation in the prefrontal cortex. Nat Rev Neurosci 2008, 9:696-709. 10.1038/nrn2462, 18714326.
74. Ragozzino ME. The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Ann N Y Acad Sci 2007, 1121:355-375. 10.1196/annals.1401.013, 17698989.
75. Snider LA, Swedo SE. Post-streptococcal autoimmune disorders of the central nervous system. Curr Opin Neurol 2003, 16:359-365. 10.1097/00019052-200306000-00017, 12858074.
76. Cohen-Kashi-Malina K, Ganor Y, Levite M, Teichberg VI. Auto-antibodies against an extracellular peptide of the GluR3 subtype of AMPA receptors activate both homomeric and heteromeric AMPA receptor channels. Neurochem Res 2006, 31:1181-1190. 10.1007/s11064-006-9143-6, 16967334.
77. Ganor Y, Teichberg VI, Levite M. TCR activation eliminates glutamate receptor GluR3 from the cell surface of normal human T cells, via an autocrine/paracrine granzyme B-mediated proteolytic cleavage. J Immunol 2007, 178:683-692.
78. Ciliax BJ, Heilman C, Demchyshyn LL, Pristupa ZB, Ince E, Hersch SM, Niznik HB, Levey AI. The dopamine transporter: immunochemical characterization and localization in brain. J Neurosci 1995, 15:1714-1723.
79. Ciliax BJ, Drash GW, Staley JK, Haber S, Mobley CJ, Miller GW, Mufson EJ, Mash DC, Levey AI. Immunocytochemical localization of the dopamine transporter in human brain. J Comp Neurol 1999, 409:38-56. 10.1002/(SICI)1096-9861(19990621)409:1<38::AID-CNE4>3.0.CO;2-1, 10363710.
80. Rite I, Machado A, Cano J, Venero JL. Blood-brain barrier disruption induces in vivo degeneration of nigral dopaminergic neurons. J Neurochem 2007, 101:1567-1582. 10.1111/j.1471-4159.2007.04567.x, 17437543.
81. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res Bull 1999, 49:377-391. 10.1016/S0361-9230(99)00072-6, 10483914.
82. Herrera AJ, Castano A, Venero JL, et al. The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiol Dis 2000, 7:429-447. 10.1006/nbdi.2000.0289, 10964613.
83. Vizuete ML, Merino M, Venero JL, et al. Histamine infusion induces a selective dopaminergic neuronal death along with an inflammatory reaction in rat substantia nigra. J Neurochem 2000, 75:540-552.
84. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 2000, 20:6309-6316.
85. Ji KA, Eu MY, Kang SH, Gwag BJ, Jou I, Joe EH. Differential neutrophil infiltration contributes to regional differences in brain inflammation in the substantia nigra pars compacta and cortex. Glia 2008, 56:1039-1047. 10.1002/glia.20677, 18381656.
86. Dougherty DD, Bonab AA, Spencer TJ, Rauch SL, Madras BK, Fischman AJ. Dopamine transporter density in patients of attention deficit hyperactivity disorder. Lancet 1999, 354:2132-2133. 10.1016/S0140-6736(99)04030-1, 10609822.
87. Sharma HS, Ali SF. Alterations in blood-brain barrier function by morphine and methamphetamine. Ann NY Acad Sci 2006, 1074:198-224. 10.1196/annals.1369.020, 17105918.