Juvenile methylphenidate reduces prefrontal cortex plasticity via D3 receptor and BDNF in adulthood

Frontiers in Synaptic Neuroscience

Volumn 6, Issue JAN, 2014, Pages

  Andersen, Susan L ^a   Sonntag, Kai C ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

ADHD; Adolescence; Child; Methylphenidate; Ritalin; Sensitive period

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COCAINE; DOPAMINE 3 RECEPTOR; MESSENGER RNA; METHYLPHENIDATE; NAFADOTRIDE;

ADULTHOOD; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; EXON; FEMALE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PREFRONTAL CORTEX; PREFRONTAL CORTEX PLASTICITY; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

EID: 84904724005     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2014.00001     Document Type: Article

References (47)

1. Aid, T., Kazantseva, A., Piirsoo, M., Palm, K., and Timmusk, T. (2007). Mouse and rat BDNF gene structure and expression revisited. J. Neurosci. Res. 85, 525-535. doi: 10.1002/jnr.21139
2. Altar, C. A., Fritsche, M., and Lindsay, R. M. (1998). Cell body infusions of brain-derived neurotrophic factor increase forebrain dopamine release and serotonin metabolism determined within vivo microdialysis. Adv. Pharmacol. 42, 915-921. doi: 10.1016/S1054-3589(08)60896-0
3. Andersen, S. L. (2005). Stimulants and the developing brain. Trends Pharmacol. Sci. 26, 237-243. doi: 10.1016/j.tips.2005.03.009
4. Andersen, S. L., Arvanitogiannis, A., Pliakas, A. M., Leblanc, C., and Carlezon, W. A. Jr. (2002). Altered responsiveness to cocaine in rats exposed to methylphenidate during development. Nat. Neurosci. 5, 13-14. doi: 10.1038/nn777
5. Andersen, S. L., Dumont, N. L., and Teicher, M. H. (1997). Developmental differences in dopamine synthesis inhibition by 7-OHDPAT. Naunyn Schmiedebergs Arch. Pharmacol. 356, 173-181. doi: 10.1007/PL00005038
6. Andersen, S. L., Napierata, L., Brenhouse, H. C., and Sonntag, K. C. (2008). Juvenile methylphenidate modulates reward-related behaviors and cerebral blood flow by decreasing cortical D3 receptors. Eur. J. Neurosci. 27, 2962-2972. doi: 10.1111/j.1460-9568.2008.06254.x
7. Argento, J. K., Arvanitogiannis, A., and Flores, C. (2012). Juvenile exposure to methylphenidate reduces cocaine reward and alters netrin-1 receptor expression in adulthood. Behav. Brain Res. 229, 202-207. doi: 10.1016/j.bbr.2012.01.008
8. Asai, N., Abe, T., Saito, T., Sato, H., Ishiguro, S., and Nishida, K. (2007). Temporal and spatial differences in expression of TrkB isoforms in rat retina during constant light exposure. Exp. Eye Res. 85, 346-355. doi: 10.1016/j.exer.2007.05.010
9. Barth, V., Need, A. B., Tzavara, E. T., Giros, B., Overshiner, C., Gleason, S. D., et al. (2013). In vivo occupancy of dopamine D3 receptors by antagonists produces neurochemical and behavioral effects of potential relevance to attention-deficit-hyperactivity disorder. J. Pharmacol. Exp. Ther. 344, 501-510. doi: 10.1124/jpet.112.198895
10. Berglind, W. J., See, R. E., Fuchs, R. A., Ghee, S. M., Whitfield, T. W. Jr., Miller, S. W., et al. (2007). A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats. Eur. J. Neurosci. 26, 757-766. doi: 10.1111/j.1460-9568.2007.05692.x
11. Bolanos, C. A., Barrot, M., Berton, O., Wallace-Black, D., and Nestler, E. J. (2003). Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol. Psychiatry 54, 1317-1329. doi: 10.1016/S0006-3223(03)00570-5
12. Booth, R. G., Baldessarini, R. J., Marsh, E., and Owens, C. E. (1994). Actions of (+/-)-7-hydroxy-N,N-dipropylaminotetralin (7-OH-DPAT) on dopamine synthesis in limbic and extrapyramidal regions of rat brain. Brain Res. 662, 283-288. doi: 10.1016/0006-8993(94)90827-3
13. Boulle, F., Van Den Hove, D. L., Jakob, S. B., Rutten, B. P., Hamon, M., Van Os, J., et al. (2012). Epigenetic regulation of the BDNF gene: implications for psychiatric disorders. Mol. Psychiatry 17, 584-596. doi: 10.1038/mp.2011.107
14. Brandon, C. L., Marinelli, M., Baker, L. K., and White, F. J. (2001). Enhanced reactivity and vulnerability to cocaine following methylphenidate treatment in adolescent rats. Neuropsychopharmacology 25, 651-661. doi: 10.1016/S0893-133X(01)00281-0
15. Brenhouse, H. C., and Andersen, S. L. (2011). Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci. Biobehav. Rev. 35, 1687-1703. doi: 10.1016/j.neubiorev.2011.04.013
16. Brenhouse, H. C., Napierata, L., Kussmaul, L., Leussis, M., and Andersen, S. L. (2009). Juvenile methylphenidate exposure and factors that influence incentive processing. Dev. Neurosci. 31, 95-106. doi: 10.1159/000207498
17. Caputo, V., Sinibaldi, L., Fiorentino, A., Parisi, C., Catalanotto, C., Pasini, A., et al. (2011). Brain derived neurotrophic factor (BDNF) expression is regulated by microRNAs miR-26a and miR-26b allele-specific binding. PLoS ONE 6:e28656. doi: 10.1371/journal.pone.0028656
18. Carlezon, W. A. Jr., Mague, S. D., and Andersen, S. L. (2003). Enduring behavioral effects of early exposure to methylphenidate in rats. Biol. Psychiatry 54, 1330-1337. doi: 10.1016/j.biopsych.2003.08.020
19. Chase, T., Carrey, N., Soo, E., and Wilkinson, M. (2007). Methylphenidate regulates activity regulated cytoskeletal associated but not brain-derived neurotrophic factor gene expression in the developing rat striatum. Neuroscience 144, 969-984. doi: 10.1016/j.neuroscience.2006.10.035
20. Dalsgaard, S., Nielsen, H. S., and Simonsen, M. (2013). Five-fold increase in national prevalence rates of attention-deficit/hyperactivity disorder medications for children and adolescents with autism spectrum disorder, attention-deficit/hyperactivity disorder, and other psychiatric disorders: a danish register-based study. J. Child Adolesc. Psychopharmacol. 23, 432-439. doi: 10.1089/cap.2012.0111
21. Dow-Edwards, D. L., and Busidan, Y. (2001). Behavioral responses to dopamine agonists in adult rats exposed to cocaine during the preweaning period. Pharmacol. Biochem. Behav. 70, 23-30. doi: 10.1016/S0091-3057(01)00582-2
22. Dumont, N. L., Andersen, S. L., Thompson, A. P., and Teicher, M. H. (2004). Transient dopamine synthesis modulation in prefrontal cortex: in vitro studies. Brain Res. Dev. Brain Res. 150, 163-166. doi: 10.1016/j.devbrainres.2004.02.010
23. Everitt, B. J., and Robbins, T. W. (2000). Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology 153, 17-30. doi: 10.1007/s002130000566
24. Fumagalli, F., Cattaneo, A., Caffino, L., Ibba, M., Racagni, G., Carboni, E., et al. (2010). Sub-chronic exposure to atomoxetine up-regulates BDNF expression and signalling in the brain of adolescent spontaneously hypertensive rats: comparison with methylphenidate. Pharmacol. Res. 62, 523-529. doi: 10.1016/j.phrs.2010.07.009
25. Gal, K., and Gyertyan, I. (2005). Dopamine D3 as well as D2 receptor ligands attenuate the cue-induced cocaine-seeking in a relapse model in rats. Drug Alcohol Depend. 81, 63-70. doi: 10.1016/j.drugalcdep.2005.05.011
26. Kuczenski, R., and Segal, D. S. (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.
27. Leal, G., Comprido, D., and Duarte, C. B. (2014). BDNF-induced local protein synthesis and synaptic plasticity. Neuropharmacology 76, 639-656. doi: 10.1016/j.neuropharm.2013.04.005
28. Leblanc-Duchin, D., and Taukulis, H. K. (2007). Chronic oral methylphenidate administration to periadolescent rats yields prolonged impairment of memory for objects. Neurobiol. Learn. Mem. 88, 312-320. doi: 10.1016/j.nlm.2007.04.010
29. Le Foll, B., Diaz, J., and Sokoloff, P. (2005). A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning. Neuroreport 16, 175-178. doi: 10.1097/00001756-200502080-00022
30. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
31. Lu, H., Cheng, P. L., Lim, B. K., Khoshnevisrad, N., and Poo, M. M. (2010). Elevated BDNF after cocaine withdrawal facilitates LTP in medial prefrontal cortex by suppressing GABA inhibition. Neuron 67, 821-833. doi: 10.1016/j.neuron.2010.08.012
32. Mannuzza, S., Klein, R. G., Truong, N. L., Moulton, J. L. 3rd., Roizen, E. R., Howell, K. H., et al. (2008). Age of methylphenidate treatment initiation in children with ADHD and later substance abuse: prospective follow-up into adulthood. Am. J. Psychiatry 165, 604-609. doi: 10.1176/appi.ajp.2008.07091465
33. McCarthy, D. M., Brown, A. N., and Bhide, P. G. (2012). Regulation of BDNF expression by cocaine. Yale J. Biol. Med. 85, 437-446.
34. Mellios, N., Huang, H. S., Grigorenko, A., Rogaev, E., and Akbarian, S. (2008). A set of differentially expressed miRNAs, including miR-30a-5p, act as post-transcriptional inhibitors of BDNF in prefrontal cortex. Hum. Mol. Genet. 17, 3030-3042. doi: 10.1093/hmg/ddn201
35. Nakayama, M., Gahara, Y., Kitamura, T., and Ohara, O. (1994). Distinctive four promoters collectively direct expression of brain-derived neurotrophic factor gene. Brain Res. Mol. Brain Res. 21, 206-218. doi: 10.1016/0169-328X(94)90251-8
36. Pattabiraman, P. P., Tropea, D., Chiaruttini, C., Tongiorgi, E., Cattaneo, A., and Domenici, L. (2005). Neuronal activity regulates the developmental expression and subcellular localization of cortical BDNF mRNA isoforms in vivo. Mol. Cell. Neurosci. 28, 556-570. doi: 10.1016/j.mcn.2004.11.010
37. Sadri-Vakili, G., Kumaresan, V., Schmidt, H. D., Famous, K. R., Chawla, P., Vassoler, F. M., et al. (2010). Cocaine-induced chromatin remodeling increases brain-derived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine. J. Neurosci. 30, 11735-11744. doi: 10.1523/JNEUROSCI.2328-10.2010
38. Schmidt, H. D., McGinty, J. F., West, A. E., and Sadri-Vakili, G. (2013). Epigenetics and psychostimulant addiction. Cold Spring Harb. Perspect. Med. 3:a012047. doi: 10.1101/cshperspect.a012047
39. Shaw, P., Eckstrand, K., Sharp, W., Blumenthal, J., Lerch, J. P., Greenstein, D., et al. (2007). Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc. Natl. Acad. Sci. U.S.A. 104, 19649-19654. doi: 10.1073/pnas.0707741104
40. Sokoloff, P., Le Foll, B., Perachon, S., Bordet, R., Ridray, S., and Schwartz, J. C. (2001). The dopamine D3 receptor and drug addiction. Neurotox. Res. 3, 433-441. doi: 10.1007/BF03033202
41. Stanwood, G. D., Artymyshyn, R. P., Kung, M. P., Kung, H. F., Lucki, I., and McGonigle, P. (2000). Quantitative autoradiographic mapping of rat brain dopamine D3 binding with [(125)I]7-OH-PIPAT: evidence for the presence of D3 receptors on dopaminergic and nondopaminergic cell bodies and terminals. J. Pharmacol. Exp. Ther. 295, 1223-1231.
42. Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., and Nestler, E. J. (2006). Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9, 519-525. doi: 10.1038/nn1659
43. Tseng, K. Y., and O'Donnell, P. (2007). Dopamine modulation of prefrontal cortical interneurons changes during adolescence. Cereb. Cortex 17, 1235-1240. doi: 10.1093/cercor/bhl034
44. Urban, K. R., Waterhouse, B. D., and Gao, W. J. (2012). Distinct age-dependent effects of methylphenidate on developing and adult prefrontal neurons. Biol. Psychiatry 72, 880-888. doi: 10.1016/j.biopsych.2012.04.018
45. Wargin, W., Patrick, K., Kilts, C., Gualtieri, C. T., Ellington, K., Mueller, R. A., et al. (1983). Pharmacokinetics of methylphenidate in man, rat and monkey. J. Pharmacol. Exp. Ther. 226, 382-386.
46. Warren, B. L., Iniguez, S. D., Alcantara, L. F., Wright, K. N., Parise, E. M., Weakley, S. K., et al. (2011). Juvenile administration of concomitant methylphenidate and fluoxetine alters behavioral reactivity to reward- and mood-related stimuli and disrupts ventral tegmental area gene expression in adulthood. J. Neurosci. 31, 10347-10358. doi: 10.1523/JNEUROSCI.1470-11.2011
47. Watson, D. J., Loiseau, F., Ingallinesi, M., Millan, M. J., Marsden, C. A., and Fone, K. C. (2012). Selective blockade of dopamine D3 receptors enhances while D2 receptor antagonism impairs social novelty discrimination and novel object recognition in rats: a key role for the prefrontal cortex. Neuropsychopharmacology 37, 770-786. doi: 10.1038/npp.2011.254