Methylphenidate regulates activity regulated cytoskeletal associated but not brain-derived neurotrophic factor gene expression in the developing rat striatum

Neuroscience

Volumn 144, Issue 3, 2007, Pages 969-984

  Chase, T ^b   Carrey, N ^a,b   Soo, E ^c   Wilkinson, M ^a,b  

^a IWK HEALTH CENTRE   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

attention deficit hyperactivity disorder; cortex; effector immediate early gene; oral treatment; Ritalin; striatum

Indexed keywords

ACTIVITY REGULATED CYTOSKELETAL PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; METHYLPHENIDATE; PROTEIN; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CINGULATE GYRUS; CONTROLLED STUDY; CORPUS STRIATUM; CYTOSKELETON; DESENSITIZATION; DRUG BLOOD LEVEL; FRONTAL CORTEX; GENE; GENE EXPRESSION; IMMATURITY; MALE; MASS SPECTROMETRY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPEATED DRUG DOSE; SINGLE DRUG DOSE;

ADMINISTRATION, ORAL; AGING; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CENTRAL NERVOUS SYSTEM STIMULANTS; CORPUS STRIATUM; CYTOSKELETAL PROTEINS; DRUG ADMINISTRATION SCHEDULE; GENE EXPRESSION REGULATION; MALE; METHYLPHENIDATE; NERVE TISSUE PROTEINS; NEURONS; RATS; RNA, MESSENGER; UP-REGULATION;

EID: 33845749581     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.10.035     Document Type: Article

References (98)

1. Alder J., Thakker-Varia S., Bangasser D.A., Kuroiwa M., Plummer M.R., Shors T.J., and Black I.B. Brain-derived neurotrophic factor-induced gene expression reveals novel actions of VGF in hippocampal synaptic plasticity. J Neurosci 23 (2003) 10800-10808
2. Andersen S.L. Stimulants and the developing brain. Trends Pharmacol Sci 26 (2005) 237-243
3. Aoyama T., Kotaki H., and Iga T. Dose-dependent kinetics of methylphenidate enantiomers after oral administration of racemic methylphenidate to rats. J Pharmacobiodyn 13 (1990) 647-652
4. Aoyama T., Yamamoto K., Kotaki H., Sawada Y., and Iga T. Pharmacodynamic modeling for change of locomotor activity by methylphenidate in rats. Pharm Res 14 (1997) 1601-1606
5. Arnsten A.F., and Dudley A.G. Methylphenidate improves prefrontal cortical cognitive function through alpha2 adrenoceptor and dopamine D1 receptor actions: Relevance to therapeutic effects in attention deficit hyperactivity disorder. Behav Brain Funct 1 (2005) 2
6. Bakhtiar R., and Tse F.L. Toxicokinetic assessment of methylphenidate (Ritalin(R)) in a 13-week oral (gavage) toxicity study in rats using an enantiomeric liquid chromatography/tandem mass spectrometry assay. Rapid Commun Mass Spectrom 17 (2003) 2160-2162
7. Biederman J., and Faraone S.V. Attention-deficit hyperactivity disorder. Lancet 366 (2005) 237-248
8. Bond B.C., Virley D.J., Cairns N.J., Hunter A.J., Moore G.B., Moss S.J., Mudge A.W., Walsh F.S., Jazin E., and Preece P. The quantification of gene expression in an animal model of brain ischaemia using TaqMan real-time RT-PCR. Brain Res Mol Brain Res 106 (2002) 101-116
9. Bramham C.R., and Messaoudi E. BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis. Prog Neurobiol 76 (2005) 99-125
10. Brandon C.L., Marinelli M., Baker L.K., and White F.J. Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats. Neuropsychopharmacology 25 (2001) 651-661
11. Carrey N., McFadyen M.P., and Brown R.E. Effects of subchronic methylphenidate hydrochloride administration on the locomotor and exploratory behavior of prepubertal mice. J Child Adolesc Psychopharmacol 10 (2000) 277-286
12. Carrey N.J., Wiggins D.M., and Milin R.P. Pharmacological treatment of psychiatric disorders in children and adolescents: focus on guidelines for the primary care practitioner. Drugs 51 (1996) 750-759
13. Chase T.D., Brown R.E., Carrey N., and Wilkinson M. Repeated methylphenidate attenuates c-fos expression in the striatum of prepubertal rats. Neuroreport 14 (2003) 769-772
14. Chase T.D., Carrey N., Brown R.E., and Wilkinson M. Methylphenidate regulates c-fos and fosB expression in multiple regions of the immature brain. Brain Res Dev Brain Res 156 (2005) 1-12
15. Chase T.D., Carrey N., Brown R.E., and Wilkinson M. Methylphenidate differentially regulates c-fos and fosB expression in the developing rat striatum. Brain Res Dev Brain Res 157 (2005) 181-191
16. Cyr M., Beaulieu J.M., Laakso A., Sotnikova T.D., Yao W.D., Bohn L.M., Gainetdinov R.R., and Caron M.G. Sustained elevation of extracellular dopamine causes motor dysfunction and selective degeneration of striatal GABAergic neurons. Proc Natl Acad Sci U S A 100 (2003) 11035-11040
17. Dassesse D., Vanderwinden J.M., Goldberg I., Vanderhaeghen J.J., and Schiffmann S.N. Caffeine-mediated induction of c-fos, zif-268 and arc expression through A1 receptors in the striatum: different interactions with the dopaminergic system. Eur J Neurosci 11 (1999) 3101-3114
18. De Foubert G., Carney S.L., Robinson C.S., Destexhe E.J., Tomlinson R., Hicks C.A., Murray T.K., Gaillard J.P., Deville C., Xhenseval V., Thomas C.E., O'Neill M.J., and Zetterstrom T.S. Fluoxetine-induced change in rat brain expression of brain-derived neurotrophic factor varies depending on length of treatment. Neuroscience 128 (2004) 597-604
19. Dickey C.A., Gordon M.N., Mason J.E., Wilson N.J., Diamond D.M., Guzowski J.F., and Morgan D. Amyloid suppresses induction of genes critical for memory consolidation in APP + PS1 transgenic mice. J Neurochem 88 (2004) 434-442
20. Dluzen D.E., Gao X., Story G.M., Anderson L.I., Kucera J., and Walro J.M. Evaluation of nigrostriatal dopaminergic function in adult +/+ and +/- BDNF mutant mice. Exp Neurol 170 (2001) 121-128
21. Fang H., Chartier J., Sodja C., Desbois A., Ribecco-Lutkiewicz M., Walker P.R., and Sikorska M. Transcriptional activation of the human brain-derived neurotrophic factor gene promoter III by dopamine signaling in NT2/N neurons. J Biol Chem 278 (2003) 26401-26409
22. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., and Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381 (1996) 706-709
23. Fone K.C., and Nutt D.J. Stimulants: use and abuse in the treatment of attention deficit hyperactivity disorder. Curr Opin Pharmacol 5 (2005) 87-93
24. Fosnaugh J.S., Bhat R.V., Yamagata K., Worley P.F., and Baraban J.M. Activation of arc, a putative "effector" immediate early gene, by cocaine in rat brain. J Neurochem 64 (1995) 2377-2380
25. Freeman W.M., Brebner K., Lynch W.J., Patel K.M., Robertson D.J., Roberts D.C., and Vrana K.E. Changes in rat frontal cortex gene expression following chronic cocaine. Brain Res Mol Brain Res 104 (2002) 11-20
26. Fujimoto T., Tanaka H., Kumamaru E., Okamura K., and Miki N. Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule-associated protein 2 immunoreactivity in the dendrites. J Neurosci Res 76 (2004) 51-63
27. Fujiyama K., Kajii Y., Hiraoka S., and Nishikawa T. Differential regulation by stimulants of neocortical expression of mrt1, arc, and homer1a mRNA in the rats treated with repeated methamphetamine. Synapse 49 (2003) 143-149
28. Gainetdinov R.R., Sotnikova T.D., and Caron M.G. Monoamine transporter pharmacology and mutant mice. Trends Pharmacol Sci 23 (2002) 367-373
29. Gainetdinov R.R., Wetsel W.C., Jones S.R., Levin E.D., Jaber M., and Caron M.G. Role of serotonin in the paradoxical calming effect of psychostimulants on hyperactivity. Science 283 (1999) 397-401
30. Gatley S.J., Volkow N.D., Gifford A.N., Fowler J.S., Dewey S.L., Ding Y.S., and Logan J. Dopamine-transporter occupancy after intravenous doses of cocaine and methylphenidate in mice and humans. Psychopharmacology (Berl) 146 (1999) 93-100
31. Gerasimov M.R., Franceschi M., Volkow N.D., Gifford A., Gatley S.J., Marsteller D., Molina P.E., and Dewey S.L. Comparison between intraperitoneal and oral methylphenidate administration: A microdialysis and locomotor activity study. J Pharmacol Exp Ther 295 (2000) 51-57
32. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., and Barnes C.A. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20 (2000) 3993-4001
33. Hawken C.M., Brown R.E., Carrey N., and Wilkinson M. Long-term methylphenidate treatment down-regulates c-fos in the striatum of male CD-1 mice. Neuroreport 15 (2004) 1045-1048
34. Huang E.J., and Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72 (2003) 609-642
35. Huff J.K., and Davies M.I. Microdialysis monitoring of methylphenidate in blood and brain correlated with changes in dopamine and rat activity. J Pharm Biomed Anal 29 (2002) 767-777
36. Hughes P., and Dragunow M. Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 47 (1995) 133-178
37. Husson I., Mesples B., Medja F., Leroux P., Kosofsky B., and Gressens P. Methylphenidate and MK-801, an N-methyl-d-aspartate receptor antagonist: shared biological properties. Neuroscience 125 (2004) 163-170
38. Hyman C., Hofer M., Barde Y.A., Juhasz M., Yancopoulos G.D., Squinto S.P., and Lindsay R.M. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350 (1991) 230-232
39. Hyman S.E., Kosofsky B.E., Nguyen T.V., Cohen B.M., and Comb M.J. Everything activates c-fos: how can it matter?. NIDA Res Monogr 125 (1993) 25-38
40. Kelz M.B., and Nestler E.J. deltaFosB: A molecular switch underlying long-term neural plasticity. Curr Opin Neurol 13 (2000) 715-720
41. Kernie S.G., Liebl D.J., and Parada L.F. BDNF regulates eating behavior and locomotor activity in mice. EMBO J 19 (2000) 1290-1300
42. Klebaur J.E., Ostrander M.M., Norton C.S., Watson S.J., Akil H., and Robinson T.E. The ability of amphetamine to evoke arc (Arg 3.1) mRNA expression in the caudate, nucleus accumbens and neocortex is modulated by environmental context. Brain Res 930 (2002) 30-36
43. Kodama M., Akiyama K., Ujike H., Shimizu Y., Tanaka Y., and Kuroda S. A robust increase in expression of arc gene, an effector immediate early gene, in the rat brain after acute and chronic methamphetamine administration. Brain Res 796 (1998) 273-283
44. Koya E., Spijker S., Homberg J.R., Voorn P., Schoffelmeer A.N., De Vries T.J., and Smit A.B. Molecular reactivity of mesocorticolimbic brain areas of high and low grooming rats after elevated plus maze exposure. Brain Res Mol Brain Res 137 (2005) 184-192
45. Kuczenski R., and Segal D.S. Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J Neurochem 68 (1997) 2032-2037
46. Kuczenski R., and Segal D.S. Exposure of adolescent rats to oral methylphenidate: preferential effects on extracellular norepinephrine and absence of sensitization and cross-sensitization to methamphetamine. J Neurosci 22 (2002) 7264-7271
47. Kuppers E., and Beyer C. Dopamine regulates brain-derived neurotrophic factor (BDNF) expression in cultured embryonic mouse striatal cells. Neuroreport 12 (2001) 1175-1179
48. Le Foll B., Diaz J., and Sokoloff P. A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning. Neuroreport 16 (2005) 175-178
49. Leblanc-Duchin D., and Taukulis H.K. Behavioral reactivity to a noradrenergic challenge after chronic oral methylphenidate (ritalin) in rats. Pharmacol Biochem Behav 79 (2004) 641-649
50. Liu D., Bei D., Parmar H., and Matus A. Activity-regulated, cytoskeleton-associated protein (Arc) is essential for visceral endoderm organization during early embryogenesis. Mech Dev 92 (2000) 207-215
51. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., Gilbert D.J., Jenkins N.A., Lanahan A.A., and Worley P.F. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14 (1995) 433-445
52. Marie-Claire C., Courtin C., Roques B.P., and Noble F. Cytoskeletal genes regulation by chronic morphine treatment in rat striatum. Neuropsychopharmacology 29 (2004) 2208-2215
53. McClung C.A., Ulery P.G., Perrotti L.I., Zachariou V., Berton O., and Nestler E.J. DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res Mol Brain Res 132 (2004) 146-154
54. McDougall S.A., Collins R.L., Karper P.E., Watson J.B., and Crawford C.A. Effects of repeated methylphenidate treatment in the young rat: sensitization of both locomotor activity and stereotyped sniffing. Exp Clin Psychopharmacol 7 (1999) 208-218
55. McFadyen M.P., Brown R.E., and Carrey N. Subchronic methylphenidate administration has no effect on locomotion, emotional behavior, or water maze learning in prepubertal mice. Dev Psychobiol 41 (2002) 123-132
56. Medhurst A.D., Harrison D.C., Read S.J., Campbell C.A., Robbins M.J., and Pangalos M.N. The use of TaqMan RT-PCR assays for semiquantitative analysis of gene expression in CNS tissues and disease models. J Neurosci Methods 98 (2000) 9-20
57. Meredith G.E., Callen S., and Scheuer D.A. Brain-derived neurotrophic factor expression is increased in the rat amygdala, piriform cortex and hypothalamus following repeated amphetamine administration. Brain Res 949 (2002) 218-227
58. Monteggia L.M., Barrot M., Powell C.M., Berton O., Galanis V., Gemelli T., Meuth S., Nagy A., Greene R.W., and Nestler E.J. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc Natl Acad Sci U S A 101 (2004) 10827-10832
59. Nishimura M., Yamagata K., Sugiura H., and Okamura H. The activity-regulated cytoskeleton-associated (Arc) gene is a new light-inducible early gene in the mouse suprachiasmatic nucleus. Neuroscience 116 (2003) 1141-1147
60. Oades R.D., Sadile A.G., Sagvolden T., Viggiano D., Zuddas A., Devoto P., Aase H., Johansen E.B., Ruocco L.A., and Russell V.A. The control of responsiveness in ADHD by catecholamines: evidence for dopaminergic, noradrenergic and interactive roles. Dev Sci 8 (2005) 122-131
61. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1986), Academic Press, New York
62. Pei Q., Sprakes M., Millan M.J., Rochat C., and Sharp T. The novel monoamine reuptake inhibitor and potential antidepressant, S33005, induces Arc gene expression in cerebral cortex. Eur J Pharmacol 495 (2004) 227-233
63. Pei Q., Zetterstrom T.S., Sprakes M., Tordera R., and Sharp T. Antidepressant drug treatment induces Arc gene expression in the rat brain. Neuroscience 121 (2003) 975-982
64. Penner M.R., McFadyen M.P., Carrey N., and Brown R.E. Effects of chronic and acute methylphenidate hydrochloride (Ritalin) administration on locomotor activity, ultrasonic vocalizations, and neuromotor development in 3- to 11-day-old CD-1 mouse pups. Dev Psychobiol 39 (2001) 216-228
65. Penner M.R., McFadyen M.P., Pinaud R., Carrey N., Robertson H.A., and Brown R.E. Age-related distribution of c-fos expression in the striatum of CD-1 mice after acute methylphenidate administration. Brain Res Dev Brain Res 135 (2002) 71-77
66. Pinaud R., Penner M.R., Robertson H.A., and Currie R.W. Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Res Mol Brain Res 91 (2001) 50-56
67. Porritt M.J., Batchelor P.E., and Howells D.W. Inhibiting BDNF expression by antisense oligonucleotide infusion causes loss of nigral dopaminergic neurons. Exp Neurol 192 (2005) 226-234
68. Rios M., Fan G., Fekete C., Kelly J., Bates B., Kuehn R., Lechan R.M., and Jaenisch R. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol Endocrinol 15 (2001) 1748-1757
69. Robinson T.E., and Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47 Suppl 1 (2004) 33-46
70. Rocha B.A., Fumagalli F., Gainetdinov R.R., Jones S.R., Ator R., Giros B., Miller G.W., and Caron M.G. Cocaine self-administration in dopamine-transporter knockout mice. Nat Neurosci 1 (1998) 132-137
71. Samaha A.N., Mallet N., Ferguson S.M., Gonon F., and Robinson T.E. The rate of cocaine administration alters gene regulation and behavioral plasticity: implications for addiction. J Neurosci 24 (2004) 6362-6370
72. Sato M., Ohguro H., Ohguro I., Mamiya K., Takano Y., Yamazaki H., Metoki T., Miyagawa Y., Ishikawa F., and Nakazawa M. Study of pharmacological effects of nilvadipine on RCS rat retinal degeneration by microarray analysis. Biochem Biophys Res Commun 306 (2003) 826-831
73. Schenk S., and Izenwasser S. Pretreatment with methylphenidate sensitizes rats to the reinforcing effects of cocaine. Pharmacol Biochem Behav 72 (2002) 651-657
74. Schochet T.L., Kelley A.E., and Landry C.F. Differential expression of arc mRNA and other plasticity-related genes induced by nicotine in adolescent rat forebrain. Neuroscience 135 (2005) 285-297
75. Sowell E.R., Peterson B.S., Thompson P.M., Welcome S.E., Henkenius A.L., and Toga A.W. Mapping cortical change across the human life span. Nat Neurosci 6 (2003) 309-315
76. Stanwood G.D., and Levitt P. Drug exposure early in life: functional repercussions of changing neuropharmacology during sensitive periods of brain development. Curr Opin Pharmacol 4 (2004) 65-71
77. Steward O., and Worley P. Local synthesis of proteins at synaptic sites on dendrites: role in synaptic plasticity and memory consolidation?. Neurobiol Learn Mem 78 (2002) 508-527
78. Steward O., and Worley P.F. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 30 (2001) 227-240
79. Sumner B.E., Cruise L.A., Slattery D.A., Hill D.R., Shahid M., and Henry B. Testing the validity of c-fos expression profiling to aid the therapeutic classification of psychoactive drugs. Psychopharmacology (Berl) 171 (2004) 306-321
80. Swanson J.M., and Volkow N.D. Pharmacokinetic and pharmacodynamic properties of stimulants: implications for the design of new treatments for ADHD. Behav Brain Res 130 (2002) 73-78
81. Tan A., Moratalla R., Lyford G.L., Worley P., and Graybiel A.M. The activity-regulated cytoskeletal-associated protein arc is expressed in different striosome-matrix patterns following exposure to amphetamine and cocaine. J Neurochem 74 (2000) 2074-2078
82. Thomas D.M., Francescutti-Verbeem D.M., Liu X., and Kuhn D.M. Identification of differentially regulated transcripts in mouse striatum following methamphetamine treatment: an oligonucleotide microarray approach. J Neurochem 88 (2004) 380-393
83. Torres-Reveron A., and Dow-Edwards D.L. Repeated administration of methylphenidate in young, adolescent, and mature rats affects the response to cocaine later in adulthood. Psychopharmacology (Berl) 181 (2005) 38-47
84. Trinh J.V., Nehrenberg D.L., Jacobsen J.P., Caron M.G., and Wetsel W.C. Differential psychostimulant-induced activation of neural circuits in dopamine transporter knockout and wild type mice. Neuroscience 118 (2003) 297-310
85. Tsai S.J. Attention-deficit hyperactivity disorder and brain-derived neurotrophic factor: a speculative hypothesis. Med Hypotheses 60 (2003) 849-851
86. Ujike H., Takaki M., Kodama M., and Kuroda S. Gene expression related to synaptogenesis, neuritogenesis, and MAP kinase in behavioral sensitization to psychostimulants. Ann N Y Acad Sci 965 (2002) 55-67
87. Volkow N.D., and Insel T.R. What are the long-term effects of methylphenidate treatment?. Biol Psychiatry 54 (2003) 1307-1309
88. Wang H., Cuzon V.C., and Pickel V.M. Postnatal development of mu-opioid receptors in the rat caudate-putamen nucleus parallels asymmetric synapse formation. Neuroscience 118 (2003) 695-708
89. Wang H., and Pickel V.M. Activity-regulated cytoskeleton-associated protein arc is targeted to dendrites and coexpressed with mu-opioid receptors in postnatal rat caudate-putamen nucleus. J Neurosci Res 77 (2004) 323-333
90. Wargin W., Patrick K., Kilts C., Gualtieri C.T., Ellington K., Mueller R.A., Kraemer G., and Breese G.R. Pharmacokinetics of methylphenidate in man, rat and monkey. J Pharmacol Exp Ther 226 (1983) 382-386
91. Wheeler T.L., Eppolito A.K., Smith L.N., Huff T.B., and Smith R.F. A novel method for oral stimulant administration in the neonate rat and similar species. J Neurosci Methods (2006) doi: 10.1016/j.jneumeth.2006.07.019.
92. Yamagata K., Suzuki K., Sugiura H., Kawashima N., and Okuyama S. Activation of an effector immediate-early gene arc by methamphetamine. Ann N Y Acad Sci 914 (2000) 22-32
93. Yin Y., Edelman G.M., and Vanderklish P.W. The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc Natl Acad Sci U S A 99 (2002) 2368-2373
94. Ying S.W., Futter M., Rosenblum K., Webber M.J., Hunt S.P., Bliss T.V., and Bramham C.R. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of arc synthesis. J Neurosci 22 (2002) 1532-1540
95. Yuferov V., Kroslak T., Laforge K.S., Zhou Y., Ho A., and Kreek M.J. Differential gene expression in the rat caudate putamen after "binge" cocaine administration: advantage of triplicate microarray analysis. Synapse 48 (2003) 157-169
96. Zhang D., Zhang L., Lou D.W., Nakabeppu Y., Zhang J., and Xu M. The dopamine D1 receptor is a critical mediator for cocaine-induced gene expression. J Neurochem 82 (2002) 1453-1464
97. Zito J.M., Safer D.J., dos Reis S., Gardner J.F., Boles M., and Lynch F. Trends in the prescribing of psychotropic medications to preschoolers. JAMA 283 (2000) 1025-1030
98. Zorner B., Wolfer D.P., Brandis D., Kretz O., Zacher C., Madani R., Grunwald I., Lipp H.P., Klein R., Henn F.A., and Gass P. Forebrain-specific trkB-receptor knockout mice: behaviorally more hyperactive than "depressive. " Biol Psychiatry 54 (2003) 972-982