Prenatal exposure to methylphenidate affects the dopamine system and the reactivity to natural reward in adulthood in rats

International Journal of Neuropsychopharmacology

Volumn 18, Issue 4, 2014, Pages 1-11

  Lepelletier, François Xavier ^a   Tauber, Clovis ^a   Nicolas, Céline ^b,c   Solinas, Marcello ^b,c   Castelnau, Pierre ^a   Belzung, Catherine ^a   Emond, Patrick ^a   Cortese, Samuele ^a,d   Faraone, Stephen V ^e   Chalon, Sylvie ^a   Galineau, Laurent ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE POITIERS   (France)

^d NEW YORK UNIVERSITY CHILD STUDY CENTER   (United States)

^e SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

Dopamine; Methylphenidate; Motivation; Prenatal; Rat; Sucrose

Indexed keywords

COCAINE; DEXMETHYLPHENIDATE; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; PROTEIN C FOS; SUCROSE; CENTRAL STIMULANT AGENT; DOPAMINE UPTAKE INHIBITOR; METHYLPHENIDATE; SUGAR INTAKE;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL BODY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC ACTIVITY; DOPAMINERGIC SYSTEM; DRUG BLOOD LEVEL; FEMALE; LOCOMOTION; LONG TERM EXPOSURE; MALE; MESOLIMBIC DOPAMINERGIC SYSTEM; MOTIVATION; NEUROBIOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; PRENATAL EXPOSURE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REWARD; SIGNAL NOISE RATIO; SUCROSE PREFERENCE TEST; ADMINISTRATION AND DOSAGE; ANIMAL; BRAIN; DISEASE MODEL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; RANDOMIZATION; SUGAR INTAKE; WISTAR RAT;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; COCAINE; DIETARY SUCROSE; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; FEMALE; MALE; METHYLPHENIDATE; MOTIVATION; MOTOR ACTIVITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; RATS; RATS, WISTAR; REWARD;

EID: 84939162847     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu044     Document Type: Article

References (69)

1. American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Washington, DC: American Psychiatric Press.
2. Aoyama T, Kotaki H, Iga T (1990) Dose-dependent kinetics of methylphenidate enantiomers after oral administration of racemic methylphenidate to rats. J Pharmacobiodyn 13:647- 652.
3. Bakhtiar R, Tse FL (2004) Toxicokinetic assessment of methylphenidate (Ritalin) enantiomers in pregnant rats and rabbits. Biomed Chrom 18:275-281.
4. Banaschewski T, Coghill D, Santosh P, Zuddas A, Asherson P, Buitelaar J, Danckaerts M, Döpfner M, Faraone SV, Rothenberger A, Sergeant J, Steinhausen HC, Sonuga-Barke EJ, Taylor E (2006) Eur Child Adolesc Psychiatry 15:476-495.
5. Billiard M (2008) Narcolepsy: current treatment options and future approaches. Neuropsychiatr Dis Treat 4:557-566.
6. Bolanos CA, Barrot M, Berton O, Wallace-Black D, Nestler EJ (2003) Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatry 54:1317-1329.
7. Bolea-Alamanac BM, Green A, Verma G, Maxwell P, Davies SJ (2014) Methylphenidate use in pregnancy and lactation, a systematic review of evidence. Br J Clin Pharmacol 77:96-101.
8. Bouchez G, Sensebé L, Vourc'h P, Garreau L, Bodard S, Rico A, Guilloteau D, Charbord P, Besnard JC, Chalon S (2008) Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson's disease. Neurochem Int 52:1332-1342.
9. Brown EE, Robertson GS, Fibiger HC (1992) Evidence for conditional neuronal activation following exposure to a cocainepaired environment: role of forebrain limbic structures. J Neurosci 12:4112-4121.
10. Bubenikova-Valesova V, Kacer P, Syslova K, Rambousek L, Janovsky M, Schutova B, Hruba L, Slamberova R (2009) Prenatal methamphetamine exposure affects the mesolimbic dopaminergic system and behavior in adult offspring. Int J Dev Neurosci 27:525-530.
11. Burchfield DJ, Lucas VW, Abrams RM, Miller RL, De-Vane CL (1991) Disposition and pharmacodynamics of methamphetamine in pregnant sheep. JAMA 265:1968-1973.
12. Carlezon WA Jr, Mague SD, Andersen SL (2003) Enduring behavioral effects of early exposure to methylphenidate during development. Biol Psychiatry 54:1330-1337.
13. Chalon S, Garreau L, Emond P, Zimmer L, Vilar MP, Besnard JC, Guilloteau D (1999) Pharmacological characterization of (E)-N- (3-iodoprop-2-enyl)-2beta-carbomethoxy-3beta-(4'-methylphenyl) n ortropane as a selective and potent inhibitor of the neuronal dopamine transporter. J Pharm Exp Ther 291:648- 654.
14. Chefer VI, Thompson AC, Zapata A, Shippenberg TS (2009) Overview of brain microdialysis. Curr Protoc Neurosci Chapter 47: 7.1.1-7.1.28.
15. Cirelli C, Tononi G (2000) On the functional significance of c-fos induction during the sleep-waking cycle. Sleep 23:453-469.
16. Cochran SM, McKerchar CE, Morris BJ, Pratt JA (2002) Induction of differential patterns of local cerebral glucose metabolism and immediate-early genes by acute clozapine and haloperidol. Neuropharmacology 43:394-407.
17. De Zwaan M, Gruss B, Müller A, Graap H, Martin A, Glaesmer H, Hilbert A, Philipsen A (2012) The estimated prevalence and correlates of adult ADHD in a German community sample. Eur Arch Psychiatry Clin Neurosci 262:79-86.
18. Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137:75-114.
19. Dideriksen D, Pottegård A, Hallas J, Aagaard L, Damkier P (2013) First trimester in utero exposure to methylphenidate. Basic Clin Pharmacol Toxicol 112:73-76.
20. Ding YS, Fowler JS, Volkow ND, Dewey SL, Wang GJ, Logan J, Gatley SJ, Pappas N (1997) Chiral drugs: comparison of the pharmacokinetics of [11C]d-threo and L-threo-methylphenidate in the human and baboon brain. Psychopharmacology (Berl) 131:71-78.
21. Estelles J, Rodríguez-Arias M, Maldonado C, Aguilar MA, Miñarro J (2006) Gestational exposure to cocaine alters cocaine reward. Behav Pharmacol 17:509-515.
22. Faraone SV, Biederman J, Spencer T, Wilens T, Seidman LJ, Mick E, Doyle AE (2000) Attention-deficit/hyperactivity disorder in adults: an overview. Biol Psychiatry 48:9-20.
23. Faraone SV, Buitelaar J (2010) Comparing the efficacy of stimulants for ADHD in children and adolescents using meta-analysis. Eur Child Adolesc Psychiatry 19:353-364.
24. Fone KC, Nutt DJ (2005) Stimulants: use and abuse in the treatment of attention deficit hyperactivity disorder. Curr Opin Pharmacol 5:87-93.
25. Frank ST, Krumm B, Spanagel R (2008) Cocaine-induced dopamine overflow within the nucleus accumbens measured by in vivo microdialysis: a meta-analysis. Synapse 62:243-252.
26. Gatley SJ, Pan D, Chen R, Chaturvedi G, Ding YS (1996) Affinities of methylphenidate derivatives for dopamine, norepinephrine and serotonin transporters. Life Sci 58:231-239.
27. Gerasimov MR, Franceschi M, Volkow ND, Gifford A, Gatley SJ, Marsteller D, Molina PE, Dewey SL (2000) Comparison between intraperitoneal and oral methylphenidate administration: A microdialysis and locomotor activity study. J Pharm Exp Ther 295:51-57.
28. Gozzi A, Colavito V, Seke Etet PF, Montanari D, Fiorini S, Tambalo S, Bifone A, Zucconi GG, Bentivoglio M (2012) Modulation of fronto-cortical activity by modafinil: a functional imaging and fos study in the rat. Neuropsychopharmacology 37:822-837.
29. Grace AA, Floresco SB, Goto Y, Lodge DJ (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220-227.
30. Graybiel AM, Moratalla R, Robertson HA (1990) Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc Natl Acad Sci USA 87:6912-6916.
31. Hajnal A, Smith GP, Norgren R (2004) Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 286:R31-R37.
32. Han DD, Gu HH (2006) Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol 6:6-13.
33. Herlenius E, Lagercrantz H (2004) Development of neurotransmitter systems during critical periods. Exp Neurol 190:S8-S21.
34. Heyser CJ, Miller JS, Spear NE, Spear LP (1992) Prenatal exposure to cocaine disrupts cocaine-induced conditioned place preference in rats. Neurotoxicol Teratol 14:57-64.
35. Hysek CM, Simmler LD, Schillinger N, Meyer N, Schmid Y, Donzelli M, Grouzmann E, Liechti ME (2014) Pharmacokinetic and pharmacodynamic effects of methylphenidate and MDMA administered alone or in combination. Int J Neuropsychop 17:371-381.
36. Keller RW Jr, LeFevre R, Raucci J, Carlson JN, Glick SD (1996) Enhanced cocaine self-administration in adult rats prenatally exposed to cocaine. Neurosci Lett 205:153-156.
37. Komatsu DE, Thanos PK, Mary MN, Janda HA, John CM, Robison L, Ananth M, Swanson JM, Volkow ND, Hadjiargyrou M (2012) Chronic exposure to methylphenidate impairs appendicular bone quality in young rats. Bone 50:1214-1222.
38. Kuczenski R, Segal DS (2002) Exposure of adolescent rats to oral methylphenidate: preferential effects on extracellular norepinephrine and absence of sensitization and cross-sensitization to methamphetamine. J Neurosci 22:7264-7271.
39. Levitt P, Harvey JA, Friedman E, Simansky K, Murphy EH (1997) New evidence for neurotransmitter influences on brain development. Trends Neurosci 20:269-274.
40. Lin D, Kellogg CK (1996) Neonatal exposure to cocaine enhances the reward-potentiating properties of the drug in young adult animals. Behav Neurosci 110:791-801.
41. Lloyd SA, Oltean C, Pass H, Phillips B, Staton K, Robertson CL, Shanks RA (2013) Prenatal exposure to psychostimulants increases impulsivity, compulsivity, and motivation for rewards in adult mice. Physiol Behav 119:43-51.
42. Maeno H (1982) Dopamine receptors in canine caudate nucleus. Mol Cell Biochem 43:65-80.
43. Maiya R, Mayfield RD (2004) Dopamine transporter network and pathways. Int Rev Neurobiol 61:79-96.
44. Malanga CJ, Riday TT, Carlezon WA Jr, Kosofsky BE (2007) Prenatal exposure to cocaine increases the rewarding potency of cocaine and selective dopaminergic agonists in adult mice. Biol Psychiatry 63:214-221.
45. Malanga CJ1, Ren JQ, Guerriero RM, Kosofsky BE (2009) Augmentation of cocaine-sensitized dopamine release in the nucleus accumbens of adult mice following prenatal cocaine exposure. Dev Neurosci 31:76-89.
46. McFadyen-Leussis MP, Lewis SP, Bond TL, Carrey N, Brown RE (2004) Prenatal exposure to methylphenidate hydrochloride decreases anxiety and increases exploration in mice. Pharmacol Biochem Behav 7 7:491-500.
47. Meador-Woodruff JH, Mansour A, Bunzow JR, Van Tol HH, Watson SJ Jr, Civelli O (1989) Distribution of D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA 86:7625-7628.
48. Olson L, Seiger A (1972) Early prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z Anat Entwicklungsgesch 137:301-316.
49. Panos JJ, Law CD, Ferguson SA (2014) Effects of perinatal methylphenidate (MPH) treatment in male and female Sprague- Dawley offspring. Neurotoxicol Teratol 42:9-16.
50. Patrick KS, Ellington KR, Breese GR (1984) Distribution of methylphenidate and p-hydroxymethylphenidate in rats. J Pharm Exp Ther 231:61-65.
51. Paxinos G, Watson C (2008) The rat brain in stereotaxic coordinates, 6th ed. San Diego, CA: Elsevier.
52. Phelps ME, Huang SC, Hoffman EJ, Selin C, Sokoloff L, Kuhl DE (1979) Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: validation of method. Ann Neurol 6:371-388.
53. Polanczyc G, De-Lima MS, Horta BL, Biederman J, Rohde LA (2007) The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psych 164:942- 948.
54. Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108 (Suppl 3):511-533.
55. Richfield EK, Penney JB, Young AB (1989) Anatomical and affinity state comparisons between dopamineD1 and D2 receptors in the rat central nervous system. Neuroscience 30:767-777.
56. Rocha BA, Mead AN, Kosofsky BE (2002) Increased vulnerability to self-administer cocaine in mice prenatally exposed to cocaine. Psychopharmacology (Berl) 163:221-229.
57. Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76:470-485.
58. Schiffer WK, Lee DE, Alexoff DL, Ferrieri R, Brodie JD, Dewey SL (2006) Metabolic correlates of toluene abuse: decline and recovery of function in adolescent animals. Psychopharmacology (Berl) 186:159-167.
59. Shah NS, Yates JD (1978) Placental transfer and tissue distribution of dextro-amphetamine in the mouse. Arch Int Pharmacodyn Ther 233:200-208.
60. Simon V, Czobor P, Balint S, Mészaros A, Bitter I (2009) Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis. Br J Psychiatry 194:204-211.
61. Šlamberová R, Pometlová M, Schutová B, Hrubá L, Macúchová E, Nová E, Rokyta R (2012) Do prenatally methamphetamineexposed adult male rats display general predisposition to drug abuse in the conditioned place preference test? Physiol Res 61(Suppl 2):S129-S138.
62. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28:897-916.
63. Solinas M, Goldberg SR (2005) Motivational effects of cannabinoids and opioids on food reinforcement depend on simultaneous activation of cannabinoid and opioid systems. Neuropsychopharmacology 30:2035-2045.
64. Spencer TJ, Biederman J, Ciccone PE, Madras BK, Dougherty DD, Bonab AA, Livni E, Parasrampuria DA, Fischman AJ (2006) PET study examining pharmacokinetics, detection and likeability, and dopamine transporter receptor occupancy of short- and long-acting oral methylphenidate. Am J Psych 163:387-395.
65. Surmeier DJ, Ding J, Day M, Wang Z, Shen W (2007) D1 and D2 dopamine- receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 30:228-235.
66. Swanson JM, Volkow ND (2003) Serum and brain concentrations of methylphenidate: implications for use and abuse. Neurosci Biobehav Rev 27:615-621.
67. Wargin W, Patrick K, Kilts C, Gualtieri CT, Ellington K, Mueller RA, Kraemer G, Breese GR (1983) Pharmacokinetics of methylphenidate in man, rat and monkey. J Pharm Exp Ther 226:382-386.
68. Wilens TE (2008) Effects of methylphenidate on the catecholaminergic system in attention-deficit/hyperactivity disorder. J Clin Psychopharmacol 28:S46-S53.
69. Yamada H, Kuroki T, Nakahara T, Hashimoto K, Tsutsumi T, Hirano M, Maeda H (2007) The dopamine D1 receptor agonist, but not the D2 receptor agonist, induces gene expression of Homer 1a in rat striatum and nucleus accumbens. Brain Res 1131:88-96.