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Neuroadaptations Involved in Long-Term Exposure to ADHD Pharmacotherapies: Alterations That Support Dependence Liability of These Medications

  • Dela Pena, Ike C. (Uimyung Research Institute for Neuroscience, Sahmyook University) ;
  • Ahn, Hyung-Seok (Uimyung Research Institute for Neuroscience, Sahmyook University) ;
  • Shin, Chan-Young (Center for Geriatric Neuroscience Research, Institute of Biomedical Science and Technology, Konkuk University) ;
  • Cheong, Jae-Hoon (Uimyung Research Institute for Neuroscience, Sahmyook University)
  • Received : 2010.10.18
  • Accepted : 2010.11.24
  • Published : 2011.01.31

Abstract

Repeated administration of addictive drugs causes cellular and molecular changes believed to be the mechanism of pro-addictive behaviors. Neuroadaptations also take place with repeated administration of amphetamine, methylphenidate and atomoxetine, drugs for Attention Deficit Hyperactivity Disorders (ADHD), and it is speculated that these changes may serve as markers to demonstrate the dependence liability of these therapies. In this review, we enumerate the neuroadaptive changes in molecules associated with neuronal signaling and plasticity, as well as neuronal morphology wrought by repeated administration of ADHD medications. We provide the current perspective on the dependence liability of these therapies, and also suggest of some factors that need to be considered in future investigations, so that what is drawn from animal studies would be better consolidated with those known clinically.

Keywords

References

  1. Ackerman, J. M. and White, F. J. (1990) A10 somatodendritic dopamineautoreceptor sensitivity following withdrawal from repeatedcocaine treatment. Neurosci. Lett. 117, 181-187. https://doi.org/10.1016/0304-3940(90)90141-U
  2. Adriani, W., Leo, D., Greco, D., Rea, M., di Porzio, U., Laviola, G.and Perrone-Capano, C. (2006) Methylphenidate administration toadolescent rats determines plastic changes in reward-related behaviorand striatal gene expression. Neuropsychopharmacol. 31,1946-1956. https://doi.org/10.1038/sj.npp.1300962
  3. Amini, B., Yang, P. B., Swann, A. C. and Dafny, N. (2004) Differentiallocomotor responses in male rats from three strains to acute methylphenidate.Int. J. Neurosci. 114, 1063-1083. https://doi.org/10.1080/00207450490475526
  4. Andersen, S. L., LeBlanc, C. J. and Lyss, P. J. (2001) Maturationalincreases in c-fos expression in the ascending dopamine systems.Synapse 41, 345-350. https://doi.org/10.1002/syn.1091
  5. Andersen, S. L., Arvanitogiannis, A., Pliakas, A. M., LeBlanc, C. andCarlezon, W. A. Jr. (2002) Altered responsiveness to cocaine inrats exposed to methylphenidate during development. Nat. Neurosci.5, 13-14. https://doi.org/10.1038/nn777
  6. Arnsten A. F. (2006) Stimulants: therapeutic actions in ADHD. Neuropsychopharmacol.31, 2376-2383. https://doi.org/10.1038/sj.npp.1301164
  7. Askenasy, E. P., Taber, K. H., Yang, P. B. and Dafny, N. (2007) Methylphenidate(Ritalin): behavioral studies in the rat. Intern. J. Neurosci. 117, 757-794. https://doi.org/10.1080/00207450600910176
  8. Banerjee, P. S., Aston, J., Khundakar, A. A. and Zetterstrom, T. S.(2009) Differential regulation of psychostimulant-induced gene expressionof brain derived neurotrophic factor and the immediateearlygene arc in the juvenile and adult brain Eur. J. Neurosci. 29,465-476. https://doi.org/10.1111/j.1460-9568.2008.06601.x
  9. Barkley, R. A., Fischer, M., Smallish, L. and Fletcher, K. (2003) Doesthe treatment of attention-defi cit/hyperactivity disorder with stimulantscontribute to drug use/abuse? A 13-year prospective study.Pediatrics 111, 97-109. https://doi.org/10.1542/peds.111.1.97
  10. Barron, E., Yang, P. B., Swann, A. C. and Dafny, N. (2009) Adolescentand adult male spontaneous hyperactive rats (SHR) respond differentlyto acute and chronic methylphenidate (Ritalin). Int. J. Neurosci.119, 40-58. https://doi.org/10.1080/00207450802330546
  11. Beitner-Johnson, D., Guitart, X. and Nestler, E. J. (1992) Neurofi lamentproteins and the mesolimbic dopamine system: common regulationby chronic morphine and chronic cocaine in the rat ventraltegmental area. J. Neurosci. 12, 2165-2176.
  12. Berke, J. D. and Hyman, S. E. (2000) Addiction, dopamine, and themolecular mechanisms of memory. Neuron 25, 515-532. https://doi.org/10.1016/S0896-6273(00)81056-9
  13. Biederman, J. and Faraone, S. V. (2005) Attention-deficit hyperactivitydisorder. Lancet. 366, 237-248. https://doi.org/10.1016/S0140-6736(05)66915-2
  14. Biederman, J., Wigal, S. B., Spencer, T. J., McGough, J. J. and Mays,D. A. (2006) A post hoc subgroup analysis of an 18-day randomizedcontrolled trial comparing the tolerability and effi cacy of mixedamphetamine salts extended release and atomoxetine in school-agegirls with attention-deficit/hyperactivity disorder. Clin. Ther. 28,280-293. https://doi.org/10.1016/j.clinthera.2006.02.008
  15. Bonci, A., Bernardi, G., Grillner, P. and Mercuri, N. B. (2003) The dopamine-containing neuron: maestro or simple musician in the orchestraof addiction. Trends Pharmacol. Sci. 24, 172-177. https://doi.org/10.1016/S0165-6147(03)00068-3
  16. Bramham, C. R. and Messaoudi, E. (2005). BDNF function in adultsynaptic plasticity: the synaptic consolidation hypothesis. Prog.Neurobiol. 76, 99-125. https://doi.org/10.1016/j.pneurobio.2005.06.003
  17. Brandon, C. L. and Steiner, H. (2003) Repeated methylphenidatetreatment in adolescent rats alters gene regulation in the striatum.Eur. J. Neurosci. 18, 1584-1592. https://doi.org/10.1046/j.1460-9568.2003.02892.x
  18. Bymaster, F. P., Katner, J. S., Nelson, D. L., Hemrick-Luecke, S. K.,Threlkeld, P. G., Heiligenstein, J. H., Morin, S. M., Gehlert, D. R.and Perry, K. W. (2002) Atomoxetine increases extracellular levelsof norepinephrine and dopamine in prefrontal cortex of rat: apotential mechanism for efficacy in attention deficit/hyperactivitydisorder. Neuropsychopharmacol. 27, 699-711. https://doi.org/10.1016/S0893-133X(02)00346-9
  19. Carlezon, W. A. Jr. and Nestler, E. J. (2002) Elevated levels of GluR1in the midbrain: a trigger for sensitization to drugs of abuse? TrendsNeurosci. 25, 610-615. https://doi.org/10.1016/S0166-2236(02)02289-0
  20. Chao, J. and Nestler, E. J. (2004) Molecular neurobiology of drug addiction.Annu. Rev. Med. 55, 113-132. https://doi.org/10.1146/annurev.med.55.091902.103730
  21. Chase, T. D., Brown, R. E., Carrey, N., Wilkinson, M., Chase, T. D.,Brown, R. E., Carrey, N. and Wilkinson, M. (2003) Daily methylphenidateadministration attenuates c-fos expression in the striatum ofprepubertal rats. Neuroreport 14, 769-772. https://doi.org/10.1097/00001756-200304150-00022
  22. Chase, T. D., Carrey, N., Brown, R. E. and Wilkinson, M. (2005a) Methylphenidateregulates c-fos and fosB expression in multiple regionsof the immature rat brain. Brain Res. Dev. Brain Res. 156, 1-12. https://doi.org/10.1016/j.devbrainres.2005.01.011
  23. Chase, T. D., Carrey, N., Brown, R. E. and Wilkinson, M. (2005b)Methylphenidate differentially regulates c-fos and fosB expressionin the developing rat striatum. Dev. Brain Res. 157, 181-191. https://doi.org/10.1016/j.devbrainres.2005.04.003
  24. Chase, T., Carrey, N., Soo, E. and Wilkinson, M. (2007) Methylphenidateregulates activity regulated cytoskeletal associated but notbrain-derived neurotrophic factor gene expression in the developingrat striatum. Neurosci. 144, 969-984. https://doi.org/10.1016/j.neuroscience.2006.10.035
  25. Commons, K. G. (2010) Neuronal pathways linking substance P todrug addiction and stress. Brain Res. 1314, 175-182. https://doi.org/10.1016/j.brainres.2009.11.014
  26. Cotterly, L., Beverley, J. A., Yano, M. and Steiner, H. (2007) Dysregulationof gene induction in corticostriatal circuits after repeated methylphenidatetreatment in adolescent rats: Differential effects on zif268 and homer 1a. Eur. J. Neurosci. 25, 3617-3628. https://doi.org/10.1111/j.1460-9568.2007.05570.x
  27. Daunais, J. B. and McGinty, J. F. (1994) Acute and chronic cocaineadministration differentially alters striatal opioid and nuclear transcriptionfactor mRNAs. Synapse 18, 35-45. https://doi.org/10.1002/syn.890180106
  28. de la Pena, I. C., Ahn, H. S., Choi, J. Y., Shin, C. Y., Ryu, J. H. andCheong, J. H. (2011) Methylphenidate self-adminstration and conditionedplace preference in an animal model of attention deficithyperactivity disorder-the spontaneously hypertensive rat. Behav.Pharmacol. 22, 31-39. https://doi.org/10.1097/FBP.0b013e328342503a
  29. Everitt, B. J. and Robbins,T. W. (2005) Neural systems of reinforcementfor drug addiction: From actions to habits to compulsion. Nat.Neurosci. 8, 1481-1489. https://doi.org/10.1038/nn1579
  30. Evans, C., Blackburn, D. and Butt, P. (2004) Use and abuse of methylphenidatein attention-deficit hyperactivity disorder. CPJ/RPC 137,30-33.
  31. Faraone, S. V. and Biederman, J. (2005) What is the prevalence ofadult ADHD? Results of a population screen of 966 adults. J. Atten.Dissord. 9, 384-391. https://doi.org/10.1177/1087054705281478
  32. Faraone, S. V., Wigal, S. B. and Hodgkins, P. (2007) Forecastingthree-month outcomes in a laboratory school comparison of mixedamphetamine salts extended release (Adderall XR) and atomoxetine(Strattera) in school-aged children with ADHD. J. Atten. Disord.11, 74-82. https://doi.org/10.1177/1087054706292196
  33. Fumagalli, F., Cattaneo, A., Caffi no, L., Ibba, M., Racagni, G., Carboni,E., Gennarelli, M. and Riva, M. A. (2010) Sub-chronic exposure toatomoxetine up-regulates BDNF expression and signalling in thebrain of adolescent spontaneously hypertensive rats: Comparisonwith methylphenidate. Pharmacol. Res. 62, 523-529. https://doi.org/10.1016/j.phrs.2010.07.009
  34. Gao, W. Y., Lee, T. H., King, G. R. and Ellinwood, E. H. (1998) Alterationsin baseline activity and quinpirole sensitivity in putative dopamineneurons in the substantia nigra and ventral tegmental areaafter withdrawal from cocaine pretreatment. Neuropsychophamacol.18, 222-232. https://doi.org/10.1016/S0893-133X(97)00132-2
  35. Gardier, A. M., Moratalla, R., Cuellar, B., Sacerdote, M., Guibert, B.,Lebrec, H. and Graybiel, A. M. (2000) Interaction between the serotoninergicand dopaminergic systems in d-fenfl uramine-inducedactivation of cfos and jun B genes in rat striatal neurons. J. Neurochem.74, 1363-1373.
  36. Gasior, M., Bergman, J., Kallman, M. J. and Paronis, C. A. (2005) Evaluationof the reinforcing effects of monoamine reuptake inhibitorsunder a concurrent schedule of food and i.v. drug delivery in rhesusmonkeys. Neuropsychopharmacol. 30, 758-764.
  37. Goldman-Rakic, P. S. (1996) Cellular basis of working memory. Neuron14, 477-485.
  38. Grimes, C. A. and Jope, R. S. (2001) The multifaceted roles of glycogensynthase kinase 3beta in cellular signaling. Prog. Neurobiol.65, 391-426. https://doi.org/10.1016/S0301-0082(01)00011-9
  39. Grimm, J. W., Lu, L., Hayashi, T., Hope, B. T., Su, T. P. and Shaham,Y. (2003) Time-dependent increases in brain-derived neurotrophicfactor protein levels within the mesolimbic dopamine system afterwithdrawal from cocaine: implications for incubation of cocainecraving. J. Neurosci. 23, 742-747.
  40. Guillin, O., Diaz, J., Carroll, P., Griffon, N., Schwartz, J. C. and Sokoloff,P. (2001) BDNF controls dopamine D3 receptor expression andtriggers behavioural sensitization. Nature. 411, 86-89. https://doi.org/10.1038/35075076
  41. Heal, D. J., Cheetham, S. C. and Smith, S. L. (2009) The neuropharmacologyof ADHD drugs in vivo: Insights on effi cacy and safety.Neuropharmacol. 57, 7-8.
  42. Hechtman, L. and Greenfi eld, B. (2003) Long-term use of stimulants inchildren with attention defi cit hyperactivity disorder: safety, efficacy,and long-term outcome. Paediatr. Drugs 5, 787-794. https://doi.org/10.2165/00148581-200305120-00002
  43. Heil, S. H., Holmes, H. W., Bickel, W. K., Higgins, S. T., Badger, G. J.,Laws, H. F. and Faries, D. E. (2002) Comparison of the subjective,physiological, and psychomotor effects of atomoxetine and methylphenidatein light drug users. Drug Alcohol Depend. 67, 149-156. https://doi.org/10.1016/S0376-8716(02)00053-4
  44. Herges, S. and Taylor, D. A. (1998) Involvement of serotonin in themodulation of cocaine-induced locomotor activity in the rat. Pharmacol.Biochem. Behav. 59, 595-611. https://doi.org/10.1016/S0091-3057(97)00473-5
  45. Himelstein, J., Newcorn, J. H. and Halperin, J. M. (2000) The neurobiologyof attention-deficit hyperactivity disorder. Front. Biosci. 5,D461-D478. https://doi.org/10.2741/Himelste
  46. Hiroi, N., Brown, J. R., Haile, C. N., Ye, H., Greenberg, M. E. andNestler, E. J. (1997) FosB mutant mice: Loss of chronic cocaineinduction of Fos-related proteins and heightened sensitivity to cocaine'spsychomotor and rewarding effects. Proc. Natl. Acad. Sci.USA. 94, 10397-10402. https://doi.org/10.1073/pnas.94.19.10397
  47. Hooks, M. S., Jones, G. H., Neill, D. B. and Justice, J. B. (1991) Individualdifferences in amphetamine sensitization: dose-dependenteffects. Pharmacol. Biochem. Behav. 41, 203-210.
  48. Hope, B., Kosofsky, B., Hyman, S. E. and Nestler, E. J. (1992) Regulationof immediate early gene expression and AP-1 binding in therat nucleus accumbens by chronic cocaine. Proc. Natl. Acad. Sci.USA. 89, 5764-5768. https://doi.org/10.1073/pnas.89.13.5764
  49. Horner, K. A., Adams, D. H., Hanson, G. R. and Keefe, K. A. (2005)Blockade of stimulant-induced preprodynorphin mRNA expressionin the striatal matrix by serotonin depletion. Neurosci. 131, 67-77. https://doi.org/10.1016/j.neuroscience.2004.10.030
  50. Hyman, S. E. (1996) Addiction to cocaine and amphetamine. Neuron16, 901-904. https://doi.org/10.1016/S0896-6273(00)80111-7
  51. Hyman, S. E. and Malenka, R. C. (2001) Addiction and the brain: theneurobiology of compulsion and its persistence. Nat. Rev. Neurosci.2, 695-703. https://doi.org/10.1038/35094560
  52. Jasinski, D. R., Faries, D. E., Moore, R. J., Schuh, L. M. and Allen, A. J.(2008) Abuse liability assessment of atomoxetine in a drug-abusingpopulation. Drug Alcohol Depend. 95, 140-146. https://doi.org/10.1016/j.drugalcdep.2008.01.008
  53. Kalivas, P. W. (1993) Neurotransmitter regulation of dopamine neuronsin ventral tegmental area. Brain Res. Rev. 18, 75-113. https://doi.org/10.1016/0165-0173(93)90008-N
  54. Kalivas, P. W. and Duffy, T. (1998) Repeated cocaine administrationalters extracellular glutamate levels in the ventral tegmental area.J. Neurochem. 70, 1497-1502.
  55. Kalivas, P. W. and O’Brien, C. (2008) Drug addiction as a pathology ofstaged neuroplasticity. Neuropsychopharmacol. 33, 166-180. https://doi.org/10.1038/sj.npp.1301564
  56. Kankaanpaa, A., Meririnne, E. and Seppala, T. (2002) 5-HT3 receptorantagonist MDL 72222 attenuates cocaine- and mazindol-, but notmethylphenidate-induced neurochemical and behavioral effects inthe rat. Psychopharmacol. (Ber) 159, 341-350. https://doi.org/10.1007/s00213-001-0939-4
  57. Katusic, S. K., Barbaresi, W. J., Colligan, R. C., Weaver, A. L., Leibson,C. L. and Jacobsen, S. J. (2005) Psychostimulant treatmentand risk for substance abuse among young adults with a historyof attentiondefi cit/hyperactivity disorder: a population-based, birthcohort study. J. Child. Adolesc. Psychopharmacol. 15, 764-776. https://doi.org/10.1089/cap.2005.15.764
  58. Kemner, J. E., Starr, H. L., Ciccone, P. E., Hooper-Wood, C. G. andCrockett, R. S. (2005) Outcomes of OROSmethylphenidate comparedwith atomoxetine in childrenwith ADHD: a multi-center, randomizedprospective study. Adv. Ther. 22, 498-512. https://doi.org/10.1007/BF02849870
  59. Kim, H. J., Park, S. H., Kyeong M. K., Ryu, J. H., Cheong, J. H. andShin, C. Y. (2008) Ever increasing number of animal model systemsfor attention defi cit/hyperactivity disorder: attention please.Biomol. and Ther. 16, 312-319. https://doi.org/10.4062/biomolther.2008.16.4.312
  60. Kim, Y., Teylan, M. A., baron, M., Sands, A., Nairn, A. C. and Greengard,P. (2008) Methylphenidate-induced dendritic spine formationand fosB expression in nucleus accumbens. PNAS. 106, 2915-2920.
  61. Kiyatkin, E. A. and Rebec, G. V. (1996) Dopaminergic modulation ofglutamate-induced excitations of neurons in the neostriatum andnucleus accumbens of awake, unrestrained rats. J. Neurophysiol.75, 142-153.
  62. Koda, K., Ago, Y., Cong, Y., Kita, Y., Takuma, K. and Matsuda, T.(2010) Effects of acute and chronic administration of atomoxetineand methylphenidate on extracellular levels of noradrenaline, dopamineand serotonin in the prefrontal cortex and striatum of mice.J. Neurochem. 114, 259-270.
  63. Kollins, S. H., MacDonald, E. K. and Rush, C. R. (2001) Assessingthe abuse potential of methylphenidate in nonhuman and humansubjects: review. Pharmacol. Biochem. Behav. 68, 611-627. https://doi.org/10.1016/S0091-3057(01)00464-6
  64. Kollins, S. H. (2003) Comparing the abuse potential of methylphenidateversus other stimulants: a review of available evidence andrelevance to the ADHD patient. J. Clin. Psych. 64, 14-18. https://doi.org/10.4088/JCP.v64n0105
  65. Koob, G. F., Sanna, P. P. and Bloom, F. E. (1998) Neuroscience of addiction.Neuron 21, 467-476. https://doi.org/10.1016/S0896-6273(00)80557-7
  66. Koob, G. F. and LeMoal, M. (2001) Drug addiction, dysregulation ofreward, and allostasis. Neuropsychopharmacol. 24, 97-129. https://doi.org/10.1016/S0893-133X(00)00195-0
  67. Kopnisky, K. L. and Hyman, S. E. (2002) Molecular and cellular biologyof addiction. In Neuropsychopharmacology: The Fifth Generationof Progress (K. L. Davis, D. Charney, J. T. Coyle, C. Nemeroff,Eds.), pp. 1368-1379. Lippincott Williams and Wilkins, Philadelphia.
  68. Kostrzewa, R. M., Reader, T. A. and Descarries, L. (1998) Serotoninneural adaptations to ontogenetic loss of dopamine neurons in ratbrain. J. Neurochem. 70, 889-898.
  69. Korsching, S., Turgeon, S. M., Pollack, A. E. and Fink, J. S. (1993)The neurotrophic factor concept: a reexamination. J. Neurosci. 13,2739-2748.
  70. Kuczenski, R. and Segal, D. S. (1997) Effects of methylphenidate onextracellular dopamine, serotonin, and norepinephrine: comparisonwith amphetamine. J. Neurochem. 68, 2032-2037.
  71. Kuczenski, R. and Segal, D. S. (2002) Exposure of adolescent rats tooral methylphenidate: preferential effects on extracellular norepinephrineand absence of sensitization and cross-sensitization tomethamphetamine. J. Neurosci. 22, 7264-7271.
  72. Kuczenski, R. and Segal, D. S. (2005) Stimulant actions in rodents: implicationsfor attention-defi cit/hyperactivity disorder treatment andpotential substance abuse. Biol. Psychiatry. 57, 1391-1396. https://doi.org/10.1016/j.biopsych.2004.12.036
  73. Lagace, D. C., Yee, J. K., Bolanos, C. A. and Eisch, A. J. (2006) Juvenileadministration of methylphenidate attenuates adult hippocampalneurogenesis. Biol. Psychiatry 60, 1121-1130. https://doi.org/10.1016/j.biopsych.2006.04.009
  74. Lambert, N. M. and Hartsong, C. S. (1998) Prospective study of tobaccosmoking and substance dependencies among samples ofADHD and non-ADHD participants. J. Learn. Diabil. 31, 533-544. https://doi.org/10.1177/002221949803100603
  75. Li, Y., Kolb, B. and Robinson, T. E. (2003) The location of persistentamphetamine-induced changes in the density of dendritic spineson medium spiny neurons in the nucleus accumbens and caudate-putamen.Neuropsychopharmacol. 28, 1082-5.
  76. Lile, J. A., Stoops, W. W., Durell, T. M., Glaser, P. E. and Rush, C.R. (2006) Discriminative-stimulus, self-reported, performance andcardiovascular effects of atomoxetine in methylphenidate-trainedhumans. Exp. Clin. Psychopharmacol. 14, 136-147. https://doi.org/10.1037/1064-1297.14.2.136
  77. Lin, J. S., Hou, Y. and Jouvet, M. (1996) Potential brain neuronal targetsfor amphetamine-, methylphenidate-, and modafi nil-inducedwakefulness, evidenced by c-fos immunocytochemistry in the cat.Proc. Natl. Acad. Sci. USA. 93, 14128-14133. https://doi.org/10.1073/pnas.93.24.14128
  78. Lu, B. and Figurov, A. (1997) Role of neurotrophins in synapse developmentand plasticity. Rev. Neurosci. 8, 1-12. https://doi.org/10.1515/REVNEURO.1997.8.1.1
  79. Maganti, R. (2004) Neuroscience of psychoactive substance abuseand dependence. Annals of Pharmacother. 38, 1-264.
  80. Mandyam, C. D., Wee, S., Crawford, E. F., Eisch, A. J., Richardson, H.N. and Koob, G. F. (2008) Varied access to intravenous methamphetamineself-administration differentially alters adult hippocampalneurogenesis. Biol. Psych. 64, 958-965. https://doi.org/10.1016/j.biopsych.2008.04.010
  81. Meredith, G. E., Callen, S. and Scheuer D. A. (2002) Brain-derivedneurotrophic factor expression is increased in the rat amygdale,piriform cortex and hypothalamus following repeated amphetamineadministration. Brain Res. 949, 218-227. https://doi.org/10.1016/S0006-8993(02)03160-8
  82. Mijnster, M. J., Galis-de Graaf Y. and Voorn, P. (1998) Serotonergicregulation of neuropeptide and glutamic acid decarboxylase mRNAlevels in the rat striatum and globus pallidus: studies with fl uoxetineand DOI. Brain Res. Mol. Brain Res. 54, 64-73. https://doi.org/10.1016/S0169-328X(97)00321-5
  83. Nestler, E. J. (1996) Under siege: the brain on opiates. Neuron. 16,897-900. https://doi.org/10.1016/S0896-6273(00)80110-5
  84. Nestler E. J. (2001) Molecular basis of long-term plasticity underlyingaddiction. Nat. Rev Neurosci. 2, 119-128. https://doi.org/10.1038/35053570
  85. Nestler, E. J., Terwilliger, R. Z., Walker, J. R., Sevarino, K. A. and Duman,R. S. (1990) Chronic cocaine treatment decreases levels ofthe G protein subunits $Gi{\alpha}$ and Goα in discrete regions of rat brain.J. Neurochem. 55, 1079-1082. https://doi.org/10.1111/j.1471-4159.1990.tb04602.x
  86. Newcorn, J. H., Kratochvil, C. J., Allen, A. J., Casat, C. D., Ruff, D. D.,Moore, R. J. and Michelson, D. (2008) Atomoxetine and osmoticallyreleased methylphenidate for the treatment of attention deficithyperactivity disorder: acute comparison and differential response.Am. J. Psych. 165, 721-730. https://doi.org/10.1176/appi.ajp.2007.05091676
  87. Norrholm, S. D., Bibb, J. A., Nestler, E. J. Ouimet, C. C., Taylor. J.R. and Greengard, P. (2003) Cocaine-induced proliferation of dendriticspines in the nucleus accumbens is dependent on the activityof cyclin-dependent kinase-5. Neurosci. 26, 12308-12313.
  88. Okamoto, K. and Aoki, K. (1963) Development of a strain of spontaneouslyhypertensive rats. Jpn. Circ. J. 27, 282-293. https://doi.org/10.1253/jcj.27.282
  89. Pandolfo, P., Pamplona, F., Prediger, R. and Takahashi, R. (2007) Increasedsensitivity of adolescent spontaneously hypertensive rats,an animal model of attention defi cit hyperactivity disorder, to the locomotorstimulation induced by cannabinoid receptor agonist WIN55,212-2. Eur. Jour. Pharmacol. 563, 141-148. https://doi.org/10.1016/j.ejphar.2007.02.013
  90. Pandolfo, P., Vendruscolo, L., Sordi, R. and Takahashi, R. (2009)Cannabinoid-induced conditioned place preference in the spontaneouslyhypertensive rat-an animal model of attention deficit hyperactivitydisorder. Psychopharmacol. 205, 319-326. https://doi.org/10.1007/s00213-009-1542-3
  91. Piazza, P. V., Deminie`re, J. M., Le Moal, M. and Simon, H. (1989)Factors that predict individual vulnerability to amphetamine self-administration,Science 245, 1511-1513. https://doi.org/10.1126/science.2781295
  92. Pierce, R. C. and Kalivas, P. W. (1997) A circuitry model of the expressionof behavioral sensitization to amphetamine-like psychostimulants.Brain Res. Rev. 25, 192-216. https://doi.org/10.1016/S0165-0173(97)00021-0
  93. Pierce, R. C., Bell, K., Duffy, P. and Kalivas, P. W. (1996) Repeated cocaineaugments excitatory amino acid transmission in the nucleusaccumbens only in rats having developed behavioral sensitization.J. Neurosci. 16, 1550-1560.
  94. Prasad, S. and Steer, S. (2008) Switching from neurostimulant therapyto atomoxetine in children and adolescents with attention-deficithyperactivity disorder: clinical approaches and review of currentavailable evidence. Ped. Drugs 10, 39-47. https://doi.org/10.2165/00148581-200810010-00005
  95. Pulvirenti, L., Maldonado-Lopez, R. and Koob, G. F. (1992) NMDA receptorsin the nucleus accumbens modulate intravenous cocainebut not heroin self-administration in the rat. Brain Res. 594, 327-330. https://doi.org/10.1016/0006-8993(92)91145-5
  96. Pulvirenti, L., Berrier, R., Kreifeldt, M. and Koob, G. F. (1994) Modulationof locomotor activity by NMDA receptors in the nucleus accumbenscore and shell regions of the rat. Brain Res. 664, 231-236. https://doi.org/10.1016/0006-8993(94)91977-1
  97. Rat Genome Database: 2008 (http://rgd.mcw.edu).
  98. Reid, M. S. and Berger, S. P. (1996) Evidence for sensitization ofcocaine-induced mucleus accumbens glutamate release. Neuroreport7, 1325-1329. https://doi.org/10.1097/00001756-199605170-00022
  99. Robinson, L. M., Sclar, D. A., Skaer, T. L. and Galin, R. S. (1999) Nationaltrends in the prevalence of attention-defi cit/hyperactivity disorderand the prescribing of methylphenidate among school-agechildren: 1990-1995. Clin. Pediatr. (Phila). 38, 209-217. https://doi.org/10.1177/000992289903800402
  100. Robinson, T. E. and Kolb, B. (1997) Persistent structural modifi cationsin nucleus accumbens and prefrontal cortex neurons produced byprevious experience with amphetamine. J. Neurosci. 21, 8491-8497.
  101. Robinson, T. E. and Kolb, B. (2004) Structural plasticity associatedwith exposure to drugs of abuse. Neuropharmacol. 47, 33-46. https://doi.org/10.1016/j.neuropharm.2004.06.025
  102. Robinson, T. E. and Berridge, K. C. (1993) The neural basis of drugcraving: an incentive-sensitization theory of addiction. Brain Res.Rev. 18, 247-291. https://doi.org/10.1016/0165-0173(93)90013-P
  103. Robinson, T. E. and Kolb, B. (1999) Alterations in the morphology ofdendrites and dendritic spines in the nucleus accumbens and prefrontalcortex following repeated treatment with amphetamine orcocaine. Eur. J. Neurosci. 11, 1598-1604. https://doi.org/10.1046/j.1460-9568.1999.00576.x
  104. Russell, V. A., Sagvolden, T. and Johansen, E. B. (2005) Animal modelsof attention-defi cit hyperactivity disorder. Behav. Brain Funct.1, 9. https://doi.org/10.1186/1744-9081-1-9
  105. Sagvolden, T. and Sergeant, J. A. (1998) Attention defi cit/hyperactivitydisorder--from brain dysfunctions to behaviour. Behav. Brain Res.94, 1-10. https://doi.org/10.1016/S0166-4328(97)00164-2
  106. Sagvolden, T., Russell, V. A., Aase, H., Johansen, E. B. and Farshbaf,M. (2005a) Rodent models of attention-deficit/hyperactivity disorder.Biol. Psychiatry 57, 1239-1247. https://doi.org/10.1016/j.biopsych.2005.02.002
  107. Sagvolden, T., Johansen, E. B., Aase, H. and Russell, V. A. (2005b) A dynamic developmental theory of Attention- Deficit/Hyperactivity Disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav. Brain. Sci. 28, 397-419.
  108. Sagvolden, T., Johansen, E. B., Wøien, G., Walaas, S. I., Storm-Mathisen,J., Bergersen, L. H., Hvalby, O., Jensen, V., Aase, H., Russell,V. A., Killeen, P. R., Dasbanerjee, T., Middleton, F. A. and FaraoneS. V. (2009) The spontaneously hypertensive rat model of ADHD--the importance of selecting the appropriate reference strain. Neuropharmacol.57, 619-626. https://doi.org/10.1016/j.neuropharm.2009.08.004
  109. See, R. E. and Kalivas, P. W. (2008) Neuroscience of substance abuseand dependence. In Kaplan & Sadock's Comprehensive Textbookof Psychiatry (B. J. Sadock, V. A. Sadock, P. Ruiz, Eds.), pp. 387-393. Williams & Wilkins, Lippincott.
  110. Segal, D. S. and Kuczenski, R. (1999) Escalating dose-binge treatmentwith methylphenidate: role of serotonin in the emergent behavioralprolife profile. J. Pharmacol. Exp. Ther. 291, 19-30.
  111. Segal, D. S. and Kuczenski, R. (1987) Individual differences in responsiveness to single and repeated amphetamine administration:behavioral characteristics and neurochemical correlates. J. Pharmacol.Exp. Ther. 242, 917-926.
  112. Self, D. W. and Nestler, E. J. (1995) Molecular mechanisms of drugreinforcement and addiction. Annu. Rev. Neurosci. 18, 463-495. https://doi.org/10.1146/annurev.ne.18.030195.002335
  113. Sontag, T., Tucha, O., Walitza, S. and Lange, K. W. (2010) Animalmodels of attention defi cit/hyperactivity disorder (ADHD): a criticalreview. ADHD Atten. Def. Hyp. Disord. 2, 1-20. https://doi.org/10.1007/s12402-010-0019-x
  114. Sorg, B. A., Davidson, D. L., Kalivas, P. W. and Prasad, B. M. (1997)Repeated daily cocaine alters subsequent cocaine-induced increaseof extracellular dopamine in the medial prefrontal cortex. J.Pharmacol. Exp. Ther. 281, 54-61.
  115. Spangler, R., Zhou, Y., Maggos, C. E., Schlussman, S. D., Ho, A. andKreek, M. J. (1997) Prodynorphin, proenkephalin and kappa opioidreceptor mRNA responses to acute ‘‘binge’’ cocaine. Brain Res.Mol. Brain Res. 44, 139-142. https://doi.org/10.1016/S0169-328X(96)00249-5
  116. Starr, H. L. and Kemner, J. (2005) Multicenter, randomized, open-labelstudy of OROS methylphenidate versus atomoxetine: treatmentoutcomes in African American children with ADHD. J. Natl. Med.Assoc. 97, 11S-16S.
  117. Steiner, H. and Gerfen, C. R. (1993) Cocaine-induced c-fos messengerRNA is inversely related to dynorphin expression in striatum. J.Neurosci. 13, 5066-5081.
  118. Steiner, H. and Gerfen, C. R. (1998) Role of dynorphin and enkephalinin the regulation of striatal output pathways and behavior. Exp.Brain Res. 123, 60-76. https://doi.org/10.1007/s002210050545
  119. Steketee, J. D. (2005) Cortical mechanisms of cocaine sensitization.Crit. Rev. Neurobiol. 17, 69-86. https://doi.org/10.1615/CritRevNeurobiol.v17.i2.20
  120. Striplin, C. D. and Kalivas, P. W. (1993) Robustness of G proteinchanges in cocaine sensitization shown with immunoblotting. Synapse14, 10-15. https://doi.org/10.1002/syn.890140103
  121. Swanson, J., McBurnett, K., Christian, D. and Wigal, T. (1995) Stimulantmedications and the treatment of children with ADHD. In Advancesin Clinical Psychology (T. Ollendick, R. Prinz, Eds.), pp.265-322. Plenum Press, New York, NY.
  122. Swanson, J. M., Sergeant, J. A., Taylor, E., Sonuga-Barke, E. J. S.,Jensen, P. S. and Cantwell, D. P. (1998) Attention defi cit disorderand hyperkinetic disorder. Lancet. 351, 429-433. https://doi.org/10.1016/S0140-6736(97)11450-7
  123. Swanson, C. J., Perry, K. W., Koch-Krueger, S., Katner, J., Svensson,K. A. and Bymaster, F. P. (2006) Effect of the attention deficit/hyperactivitydisorder drug atomoxetine on extracellular concentrationsof norepinephrine and dopamine in several brain regions of the rat.Neuropharmacol. 50, 755-760. https://doi.org/10.1016/j.neuropharm.2005.11.022
  124. Szumlinski, K., Ary, A. W. and Lominac K. D. (2008) Homers regulatedrug-induced neuroplasticity: Implications for addiction. Biochem.Pharmacol. 75, 112-133. https://doi.org/10.1016/j.bcp.2007.07.031
  125. Teicher, M. H., Andersen, S. L. and Hostetter, J. C. (1995) Evidence fordopamine receptor pruning between adolescence and adulthood instriatum but not nucleus accumbens. Dev. Brain. Res. 89, 167-172. https://doi.org/10.1016/0165-3806(95)00109-Q
  126. Teicher, M. H., Andersen, S. L. and Hostetter, J. C. (1995) Evidence fordopamine receptor pruning between adolescence and adulthood instriatum but not nucleus accumbens. Dev. Brain. Res. 89, 167-172. https://doi.org/10.1016/0165-3806(95)00109-Q
  127. Teicher, M. H., Anderson, C. M., Polcari, A., Glod, C. A., Maas, L. C.and Renshaw, P. F. (2000). Functional deficits in basal ganglia ofchildren with attention-deficit hyperactivity disorder shown withfunctional magnetic resonance imaging relaxometry. Nat. Med. 6,470-473. https://doi.org/10.1038/74737
  128. Thomas, U. (2002) Modulation of synaptic signalling complexes byHomer proteins. J. Neurochem. 81, 407-413. https://doi.org/10.1046/j.1471-4159.2002.00869.x
  129. Toda, S., Shen, H. W., Peters, J., Cagle, S. and Kalivas, P. W. (2006)Cocaine increases actin cycling: Effects in the reinstatement modelof drug seeking. J. Neurosci. 26, 1579. https://doi.org/10.1523/JNEUROSCI.4132-05.2006
  130. Todtenkopf, M. S., Parsegian, A., Naydenov, A., Neve, R. L., Konradi,C. and Carlezon, Jr. W. A. (2006) Brain reward regulated by AMPAreceptor subunits in nucleus accumbens shell. J. Neurosci. 26,11665-11669. https://doi.org/10.1523/JNEUROSCI.3070-06.2006
  131. Unal, C. T., Beverley, J. A., Willuhn, I. and Steiner, H. (2009) Longlastingdysregulation of gene expression in corticostriatal circuitsafter repeated cocaine treatment in adult rats: effects on zif 268and homer 1a. Eur J. Neurosci. 21, 1615-1626. https://doi.org/10.1016/j.neubiorev.2006.12.002
  132. van der Kooij, M. A. and Glennon, J. C. (2007) Animal models concerningthe role of dopamine in attention-deficit hyperactivity disorder.Neurosci. Biobehav. Rev. 31, 597-618. https://doi.org/10.1016/j.neubiorev.2006.12.002
  133. Vanderschuren, L. J. and Kalivas, P. W. (2000) Alterations in dopaminergicand glutamatergic transmission in the induction and expression of behavioral sensitization: A critical review of preclinicalstudies. Psychopharmacol. 151, 99-120. https://doi.org/10.1007/s002130000493
  134. Vendruscolo, L. F., Izidio, G. S. and Takahashi, R. N. (2009) Drug reinforcementin a rat model of attention deficit/hyperactivity disorderthespontaneously hypertensive rat (SHR). Curr. Drug Abuse Rev.2, 177-183. https://doi.org/10.2174/1874473710902020177
  135. Vezina, P. (2004) Sensitization of midbrain dopamine neuron reactivityand the self-administration of psychomotor stimulant drugs. Neurosci.Biobehav. Rev. 27, 827-839. https://doi.org/10.1016/j.neubiorev.2003.11.001
  136. Volkow N. D. and Swanson, J. M. (2003) Variables that affect the clinicaluse and abuse of methylphenidate in the treatment of ADHD.Am. J. Psychiatry. 160, 1909-1918. https://doi.org/10.1176/appi.ajp.160.11.1909
  137. Volkow, N. D., Fowler, J. S., Wang, G. J., Ding, Y. S. and Gatley, S. J.,(2002a) Role of dopamine in the therapeutic and reinforcing effectsof methylphenidate in humans: results from imaging studies. Eur.J. Neuropsychopharmacol. 12, 557-566. https://doi.org/10.1016/S0924-977X(02)00104-9
  138. Volkow, N. D., Wang, G. J., Fowler, J. S., Logan, J., Gatley, S. J.,Wong, C., Hitzemann, R. and Pappas, N. R. (1999) Reinforcing effectsof psychostimulants in humans are associated with increasesin brain dopamine and occupancy of D(2) receptors. J. Pharmacol.Exp. Ther. 291, 409-415. https://doi.org/10.1002/syn.10137
  139. Volkow, N. D., Wang, G. J., Fowler, J. S., Thanos, P. P., Logan, J.and Gatley, S. J., (2002b) Brain DA D2 receptors predict reinforcingeffects of stimulants in humans: replication study. Synapse 46,79-82. https://doi.org/10.1002/syn.10137
  140. Walker, P. D., Capodilupo J. G., Wolf W. A. and Carlock, L. R. (1996)Preprotachykinin and preproenkephalin mRNA expression withinstriatal subregions in response to altered serotonin transmission.Brain Res. 732, 25-35. https://doi.org/10.1016/0006-8993(96)00483-0
  141. Wee, S. and Woolverton, W. L. (2004) Evaluation of the reinforcingeffects of atomoxetine in monkeys: comparison to methylphenidateand desipramine. Drug and Alc. Dep. 75, 271-276. https://doi.org/10.1016/j.drugalcdep.2004.03.010
  142. White, F. J. and Kalivas, P. W. (1998) Neuroadaptations involved inamphetamine and cocaine addiction. Drug and Alc. Dep. 51, 141-153. https://doi.org/10.1016/S0376-8716(98)00072-6
  143. White, F. J. and Wang, R. Y. (1984) Electrophysiological evidence forA10 dopamine autoreceptor subsensitivity following chronic d-amphetaminetreatment. Brain Res. 309, 283-292. https://doi.org/10.1016/0006-8993(84)90595-X
  144. White, F. J., Hu, X. T., Henry, D. J. and Zhang, X. F. (1995) Neurophysiologicalalterations in the mesocorticolimbic dopamine systemduring repeated cocaine administration. In The Neurobiologyof Cocaine: Cellular and Molecular Mechanisms (R. P. Jr. Hammer,Ed.), pp. 95-115. CRC Press, Boca Raton.
  145. White, F. J., Hu, X. T., Zhang, X. F. and Wolf, M. E. (1995) Repeatedadministration of cocaine or amphetamine alters neuronal responsesto glutamate in the mesoaccumbens dopamine system. J. Pharmacol.Exp. Ther. 273, 445-454.
  146. White, F. J. and Wolf, M. E. (1991) Psychomotor stimulants. In TheBiological Basis of Drug Tolerance and Dependence (J. A. Pratt,Ed.), pp. 153-197. Academic Press, London, https://doi.org/10.1177/1087054705281121
  147. Wigal, S. B., McGough, J. J., McCracken, J. T., Biederman, J., Spencer,T. J., Posner, K. L., Wigal, T. L., Kollins, S. H., Clark, T. M.,Mays, D. A., Zhang, Y. and Tulloch, S. J. (2005) A laboratory schoolcomparison of mixed amphetamine salts extended release (AdderallXR) and atomoxetine (Strattera) in school-aged children withattention deficit/hyperactivity disorder. J. Atten. Disord. 9, 275-289. https://doi.org/10.1177/1087054705281121
  148. Wilens, T. E., Faraone, S. V., Biederman, J. and Gunawardene, S.(2003) Does stimulant therapy of attention-deficit/hyperactivity disorderbeget later substance abuse? A meta-analytic review of theliterature. Pediatrics 111, 179-185. https://doi.org/10.1542/peds.111.1.179
  149. Wilens, T. E., Adler, L. A., Adams, J., Sgambati, S., Rotrosen, J., Sawtelle,R., Utzinger, L. and Fusillo, S. (2008) Misuse and diversion ofstimulants prescribed for ADHD: a systematic review of the literature.J Am. Acad. Child. Adolesc. Psychiatry 47, 21-31. https://doi.org/10.1097/chi.0b013e31815a56f1
  150. Willuhn, I., Sun, W. and Steiner, H. (2003) Topography of cocaine-inducedgene regulation in the rat striatum: relationship to corticalinputs and role of behavioral context. Eur. J. Neurosci. 17, 1053-1066. https://doi.org/10.1046/j.1460-9568.2003.02525.x
  151. Xiao, B., Tu, J. C. and Worley. P. (2000) Homer: a link between neuralactivity and glutamate receptor function. Curr. Opin. Neurobiol. 10,370-374. https://doi.org/10.1016/S0959-4388(00)00087-8
  152. Xue, C. J., Ng, J. P., Li, Y. and Wolf, M. E. (1996) Acute and repeatedsystemic amphetamine administration: Effects on extracellular glutamate,aspartate, and serine levels in rat ventral tegmental areaand nucleus accumbens. J. Neurochem. 67, 352-363. https://doi.org/10.1016/S0006-8993(02)04240-3
  153. Yang, P., Behrang, A., Swann, A. and Nachum, D. (2003) Strain differencesin the behavioral responses of male rats to chronicallyadministered methylphenidate. Brain Res. 971, 139-152. https://doi.org/10.1016/S0006-8993(02)04240-3
  154. Yano, M. and Steiner, H. (2005a) Methylphenidate (Ritalin) inducesHomer 1a and zif 268 expression in specific corticostriatal circuits.Neurosci. 132, 855-865. https://doi.org/10.1016/j.neuroscience.2004.12.019
  155. Yano, M. and Steiner, H. (2005b) Topography of methylphenidate(Ritalin)-induced gene regulation in the striatum: differential effectson c-fos, substance P and opioid peptides. Neuropsychopharmacol.30, 901-915. https://doi.org/10.1038/sj.npp.1300613
  156. Yano, M., Beverley, J. A. and Steiner, H. (2006) Inhibition of methylphenidate-induced gene expression in the striatum by local blockadeof D1 receptors: Interhemispheric effects. Neurosci. 140, 699-709. https://doi.org/10.1016/j.neuroscience.2006.02.017
  157. Yano, M. and Steiner, H. (2007) Methylphenidate and cocaine:thesame effects on gene regulation. Trends in Pharmacol Sci. 28,588-596. https://doi.org/10.1016/j.tips.2007.10.004
  158. Zhang, X. F., Hu, X. T., White, F. J. and Wolf, M. E. (1997) Increased responsiveness of ventral tegmental area dopamine neurons to glutamateafter repeated administration of cocaine or amphetamine istransient and selectively involves AMPA receptors. J. Pharmacol.Exp. Ther. 281, 699-706.

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