Long-term oral methylphenidate treatment in adolescent and adult rats: Differential effects on brain morphology and function

Neuropsychopharmacology

Volumn 39, Issue 2, 2014, Pages 263-273

  Van Der Marel, Kajo ^a   Klomp, Anne ^b   Meerhoff, Gideon F ^c   Schipper, Pieter ^d   Lucassen, Paul J ^c   Homberg, Judith R ^d   Dijkhuizen, Rick M ^a   Reneman, Liesbeth ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d RADBOUD UNIVERSITY   (Netherlands)

Author keywords

attention deficit hyperactivity disorder; clinical or preclinical; development developmental disorders; methylphenidate; MRI; rats

Indexed keywords

DEXAMPHETAMINE; METHYLPHENIDATE;

ADOLESCENT; AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ANTERIOR COMMISSURE; ARTICLE; ATTENTION DEFICIT DISORDER; BRAIN; BRAIN FUNCTION; BRAIN MATURATION; BRAIN SIZE; CEREBELLUM; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORPUS CALLOSUM; CORPUS STRIATUM; CORTICAL THICKNESS (BRAIN); DIFFUSION TENSOR IMAGING; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GRAY MATTER; INDEPENDENT COMPONENT ANALYSIS; LONG TERM CARE; LOW DRUG DOSE; MALE; MOTOR CORTEX; MYELINATION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; SUPERIOR COLLICULUS; TREATMENT DURATION; WHITE MATTER;

ADMINISTRATION, ORAL; AGING; ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; DRUG ADMINISTRATION SCHEDULE; MALE; METHYLPHENIDATE; RATS; RATS, WISTAR; TREATMENT OUTCOME;

EID: 84890568023     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.169     Document Type: Article

References (55)

1. Andersen SL, Arvanitogiannis A, Pliakas AM, LeBlanc C, CarlezonWA (2002). Altered responsiveness to cocaine in rats exposed to methylphenidate during development. Nat Neurosci 5: 13-14.
2. Andersen SL, Navalta CP (2004). Altering the course of neurodevelopment: a framework for understanding the enduring effects of psychotropic drugs. Int J Dev Neurosci 22: 423-440.
3. Ashburner J, Friston KJ (2000). Voxel-based morphometry. The methods. NeuroImage 11: 805-821.
4. Ashtari M, Kumra S, Bhaskar SL, Clarke T, Thaden E, Cervellione KL et al (2005). Attention-deficit/hyperactivity disorder: a preliminary diffusion tensor imaging study. Biol Psychiatr 57: 448-455.
5. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011). A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage 54: 2033-2044.
6. Beckmann CF, Smith SM (2005). Tensorial extensions of independent component analysis for multisubject FMRI analysis. NeuroImage 25: 294-311.
7. Brandon CL, Marinelli M, White FJ (2003). Adolescent exposure to methylphenidate alters the activity of rat midbrain dopamine neurons. Biol Psychiatr 54: 1338-1344.
8. Brenhouse HC, Andersen SL (2011). Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci Biobehav Rev 35: 1687-1703.
9. Britton GB, Bethancourt JA (2009). Characterization of anxietyrelated responses in male rats following prolonged exposure to therapeutic doses of oral methylphenidate. Pharmacol Biochem Behav 93: 451-459.
10. Carmona S, Vilarroya O, Bielsa A, Trèmols V, Soliva JC, Rovira M et al (2005). Global and regional gray matter reductions in ADHD: a voxel-based morphometric study. Neurosci Lett 389: 88-93.
11. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK Clasen LS et al (2002). Developmental trajectories of brain volume abnormalities in children and adolescents with attention deficit/hyperactivity disorder. JAMA 288: 1740-1748.
12. Chen YI, Choi J-K, Xu H, Ren J, Andersen SL, Jenkins BG (2010). Pharmacologic neuroimaging of the ontogeny of dopamine receptor function. Dev Neurosci 32: 125-138.
13. Cox RW (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29: 162-173.
14. Elder TE (2010). The importance of relative standards in ADHD diagnoses: evidence based on exact birth dates. J Health Econ 29: 641-656.
15. Faraone SV, Biederman J, Morley CP, Spencer TJ (2008). Effect of stimulants on height and weight: a review of the literature. J Am Acad Child Adolesc Psychiatr 47: 994-1009.
16. Fearnley JM, Lees AJ (1991). Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114(Pt 5): 2283-2301.
17. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB Smith SM et al (2009). Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci USA 106: 7209-7214.
18. Fleckenstein AE, Volz TJ, Riddle EL, Gibb JW, Hanson GR (2007). New insights into the mechanism of action of amphetamines. Annu Rev Pharmacol Toxicol 47: 681-698.
19. Gerasimov MR, Franceschi M, Volkow ND, Gifford A, Gatley SJ Marsteller D et al (2000). Comparison between intraperitoneal and oral methylphenidate administration: a microdialysis and locomotor activity study. J Pharmacol Exp Ther 295: 51-57.
20. Gerfen CR (2004). Basal Ganglia. In: Paxinos G (ed) The Rat Nervous System. 3rd edn. Elsevier Academic Press: San Diego CA, pp 455-508.
21. Giedd JN, Castellanos FX, Casey BJ, Kozuch P, King AC Hamburger SD et al (1994). Quantitative morphology of the corpus callosum in attention deficit hyperactivity disorder. Am J Psychiatr 151: 665-669.
22. Gill KE, Pierre PJ, Daunais J, Bennett AJ, Martelle S, Gage HD et al (2012). Chronic treatment with extended release methylphenidate does not alter dopamine systems or increase vulnerability for cocaine self-administration: a study in nonhuman primates. Neuropsychopharmacology 37: 2555-2565.
23. Gray JD, Punsoni M, Tabori NE, Melton JT, Fanslow V, Ward MJ et al (2007). Methylphenidate administration to juvenile rats alters brain areas involved in cognition, motivated behaviors appetite, and stress. J Neurosci 27: 7196-7207.
24. Grund T, Teuchert-Noodt G, Busche A, Neddens J, Brummelte S Moll GH et al (2007). Administration of oral methylphenidate during adolescence prevents suppressive development of dopamine projections into prefrontal cortex and amygdala after an early pharmacological challenge in gerbils. Brain Res 1176: 124-132.
25. Jenkinson M, Bannister P, Brady M, Smith S (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17: 825-841.
26. Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012). FSL. NeuroImage 62: 782-790.
27. Jensen PS, Arnold LE, Swanson JM, Vitiello B, Abikoff HB Greenhill LL et al (2007). 3-Year follow-up of the NIMH MTA study. J Am Acad Child Adolesc Psychiatr 46: 989-1002.
28. Jones SR, Gainetdinov RR, Wightman RM, Caron MG (1998). Mechanisms of amphetamine action revealed in mice lacking the dopamine transporter. J Neurosci 18: 1979-1986.
29. Klein S, Staring M, Murphy K, Viergever MA, Pluim JPW (2010). Elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imag 29: 196-205.
30. Lakhan SE, Kirchgessner A (2012). Prescription stimulants in individuals with and without attention deficit hyperactivity disorder: misuse, cognitive impact, and adverse effects. Brain Behav 2: 661-677.
31. Le Bihan D (2003). Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4: 469-480.
32. Lerch JP, Carroll JB, Dorr A, Spring S, Evans AC, Hayden MR et al (2008). Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease. NeuroImage 41: 243-251.
33. McCutcheon JE, Marinelli M (2009). Age matters. Eur J Neurosci 29: 997-1014.
34. Moll GH, Hause S, Rüther E, Rothenberger A, Huether G (2001). Early methylphenidate administration to young rats causes a persistent reduction in the density of striatal dopamine transporters. J Child Adolesc Psychopharmacol 11: 15-24.
35. Nakao T, Radua J, Rubia K, Mataix-Cols D (2011). Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry 168: 1154-1163.
36. Papadopulos F, Spinelli M, Valente S, Foroni L, Orrico C, Alviano F et al (2007). Common tasks in microscopic and ultrastructural image analysis using ImageJ. Ultrastruct Pathol 31: 401-407.
37. Pastor PN, Reuben CA (2008). Diagnosed attention deficit hyperactivity disorder and learning disability: United States 2004-2006. Vital Health Stat 10: 1-14.
38. Ren J, Xu H, Choi J-K, Jenkins BG, Chen YI (2009). Dopaminergic response to graded dopamine concentration elicited by four amphetamine doses. Synapse 63: 764-772.
39. Schwarz A, Gozzi A, Reese T, Bertani S, Crestan V, Hagan J et al (2004). Selective dopamine D(3) receptor antagonist SB-277011 A potentiates phMRI response to acute amphetamine challenge in the rat brain. Synapse 54: 1-10.
40. Semrud-Clikeman M, Pliśzka SR, Lancaster J, Liotti M (2006). Volumetric MRI differences in treatment-na?̈ve vs chronically treated children with ADHD. Neurology 67: 1023-1027.
41. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP Greenstein D et al (2007). Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci USA 104: 19649-19654.
42. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N et al (2008). Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28: 3586-3594.
43. Shaw P, Sharp WS, Morrison M, Eckstrand K, Greenstein DK Clasen LS et al (2009). Psychostimulant treatment and the developing cortex in attention deficit hyperactivity disorder. Am J Psychiatr 166: 58-63.
44. Silk TJ, Vance A, Rinehart N, Bradshaw JL, Cunnington R (2009). White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Hum Brain Mapp 30: 2757-2765.
45. Sled JG, Zijdenbos P, Evans AC (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imag 17: 87-97.
46. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE Mackay CE et al (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 31: 1487-1505.
47. Sobel LJ, Bansal R, Maia TV, Sanchez J, Mazzone L, Durkin K et al (2010). Basal ganglia surface morphology and the effects of stimulant medications in youth with attention deficit hyperactivity disorder. Am J Psychiatr 167: 977-986.
48. Soto PL, Wilcox KM, Zhou Y, Ator NA, Riddle MA, Wong DF et al (2012). Long-term exposure to oral methylphenidate or dlamphetamine mixture in peri-adolescent rhesus monkeys: effects on physiology, behavior, and dopamine system development. Neuropsychopharmacology 37: 2566-2579.
49. Spear LP (2000). The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24: 417-463.
50. Teicher MH, Andersen SL, Hostetter JC (1995). Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Brain Res Dev Brain Res 89: 167-172.
51. van Meer MPA, Otte WM, van der Marel K, Nijboer CH Kavelaars A, Berkelbach van der Sprenkel JW et al (2012). Extent of bilateral neuronal network reorganization and functional recovery in relation to stroke severity. J Neurosci 32: 4495-4507.
52. Volkow ND, Wang GJ, Fowler JS, Gatley SJ, Logan J, Ding YS et al (1998). Dopamine transporter occupancies in the human brain induced by therapeutic doses of oral methylphenidate. Am J Psychiatr 155: 1325-1331.
53. Wang R, Benner T, Sorensen AG, Wedeen VJ (2007). Diffusion toolkit: a software package for diffusion imaging data processing and tractography. Proc Intl Soc Mag Reson Med 15: 3720.
54. Ward BD (2000): Simultaneous inference for fMRI data http://afni.nimh. nih.gov/afni/doc/manual/AlphaSim.
55. Woods RP (2003). Characterizing volume and surface deformations in an atlas framework. Theory, applications and implementation. NeuroImage 18: 769-788.