Mapping the central effects of methylphenidate in the rat using pharmacological MRI BOLD contrast

Neuropharmacology

Volumn 57, Issue 7-8, 2009, Pages 653-664

  Easton, Neil ^a   Marshall, Fiona H ^b   Marsden, Charles A ^a   Fone, Kevin C F ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b Heptares Therapeutics Ltd   (United Kingdom)

Author keywords

Attention deficit hyperactivity disorder; BOLD; Dopamine reuptake transporter; fMRI; Methylphenidate; Pharmacological MRI

Indexed keywords

AMPHETAMINE; ATOMOXETINE; DOPAMINE; DOPAMINE TRANSPORTER; GUANFACINE; METHYLPHENIDATE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; ATTENTION DEFICIT DISORDER; BLOOD PRESSURE; BRAIN ELECTROPHYSIOLOGY; BREATHING RATE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DRUG EFFECT; DRUG MECHANISM; ENTORHINAL CORTEX; GLOBUS PALLIDUS; MALE; MOTOR CORTEX; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEUS ACCUMBENS; ORBITAL CORTEX; OXYGEN BLOOD LEVEL; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PUTAMEN; RAT; SOMATOSENSORY CORTEX; STRIA TERMINALIS; SUBSTANTIA NIGRA; TEMPORAL LOBE;

ANIMALS; BLOOD PRESSURE; BRAIN; DOPAMINE UPTAKE INHIBITORS; MAGNETIC RESONANCE IMAGING; MALE; METHYLPHENIDATE; OXYGEN; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY RATE;

EID: 70350416456     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2009.08.018     Document Type: Article

References (91)

1. Allison J.D., Meador K.J., Loring D.W., Figueroa R.E., and Wright J.C. Functional MRI cerebral activation and deactivation during finger movement. Neurology 54 (2000) 135-142
2. Andersen S.L., Napierata L., Brenhouse H.C., and Sonntag K.C. Juvenile methylphenidate modulates reward-related behaviors and cerebral blood flow by decreasing cortical D3 receptors. Eur. J. Neurosci. 27 (2008) 2962-2972
3. Andrews G.D., and Lavin A. Methylphenidate increases cortical excitability via activation of alpha-2 noradrenergic receptors. Neuropsychopharmacology 31 (2006) 594-601
4. Arnsten A.F.T. Stimulants: therapeutic actions in ADHD. Neuropsychopharmacology 31 (2006) 2376-2383
5. Barkley R.A., Grodzinsky G., and DuPaul G.J. Frontal lobe functions in attention deficit disorder with and without hyperactivity: a review and research report. J. Abnorm Child. Psychol. 20 (1992) 163-188
6. Bell R.D., Alexander G.M., and Schwartzman R.J. Methylphenidate decreases local glucose metabolism in the motor cortex. Pharmacol. Biochem. Behav. 18 (1983) 1-5
7. Berridge C.W., Devilbiss D.M., Andrzejewski M.E., Arnsten A.F., Kelley A.E., Schmeichel B., Hamilton C., and Spencer R.C. Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function. Biol. Psychiatry 60 (2006) 1111-1120
8. Best M., Williams J.M., and Coccaro E.F. Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder. Proc. Natl. Acad. Sci. U.S.A 99 (2002) 8448-8453
9. Biederman J. Attention-deficit/hyperactivity disorder: a selective overview. Biol. Psychiatry 57 (2005) 1215-1220
10. Bobb A.J., Castellanos F.X., Addington A.M., and Rapoport J.L. Molecular genetic studies of ADHD: 1991 to 2004. Am. J. Med. Genet. Part B-Neuropsychiatric Genet. 132B (2005) 109-125
11. Brandon C.L., and Steiner H. Repeated methylphenidate treatment in adolescent rats alters gene regulation in the striatum. Eur. J. Neurosci. 18 (2003) 1584-1592
12. 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. Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 27 (2002) 699-711
13. Canese R., Adriani W., Marco E., Pasquale F., Lorenzini P., De Luca N., Fabi F., Podo F., and Laviola G. Peculiar response to methylphenidate in adolescent compared to adult rats: a phMRI study. Psychopharmacology 203 (2009) 143-153
14. Carboni E., Rolando M.T., Silvagni A., and Di Chiara G. Increase of dialysate dopamine in the bed nucleus of stria terminalis by clozapine and related neuroleptics. Neuropsychopharmacology 22 (2000) 140-147
15. Cash D., Lowe A.S., Roberts T.J., Ireland M.D., and Williams S.C.R. In vivo mapping of mouse brain response to d-amphetamine using bold contrast FMRI. J. Psychopharmacol. 16 (2002) A62
16. 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
17. Chase T.D., Carrey N., Brown R.E., and Wilkinson M. Methylphenidate regulates c-fos and fosB expression in multiple regions of the immature rat brain. Brain Res. Dev. Brain Res. 156 (2005) 1-12
18. Ciliax B.J., Heilman C., Demchyshyn L.L., Pristupa Z.B., Ince E., Hersch S.M., Niznik H.B., and Levey A.I. The dopamine transporter - immunocytochemical characterization and localization in brain. J. Neurosci. 15 (1995) 1714-1723
19. Coulter C.L., Happe H.K., Bergman D.A., and Murrin L.C. Localization and quantification of the dopamine transporter: comparison of [3H]WIN 35,428 and [125I]RTI-55. Brain Res. 690 (1995) 217-224
20. Dodds C.M., Mueller U., Clark L., van Loon A., Cools R., and Robbins T.W. Methylphenidate has differential effects on blood oxygenation level-dependent signal related to cognitive subprocesses of reversal learning. J. Neurosci. 28 (2008) 5976-5982
21. Dougherty D.D., Bonab A.A., Spencer T.J., Rauch S.L., Madras B.K., and Fischman A.J. Dopamine transporter density in patients with attention deficit hyperactivity disorder. Lancet 354 (1999) 2132-2133
22. Drouin C., Page M., and Waterhouse B. Methylphenidate enhances noradrenergic transmission and suppresses mid- and long-latency sensory responses in the primary somatosensory cortex of awake rats. J. Neurophysiol. 96 (2006) 622-632
23. Easton N., Marshall F., Fone K., and Marsden C. Atomoxetine produces changes in cortico-basal thalamic loop circuits: assessed by phMRI BOLD contrast. Neuropharmacology 52 (2007) 812-826
24. Easton N., Marshall F., Fone K.C.F., and Marsden C.A. Differential effects of the d- and l-isomers of amphetamine on pharmacological MRI BOLD contrast in the rat. Psychopharmacology 193 (2007) 11-30
25. Easton N., Steward C., Marshall F., Fone K., and Marsden C. Effects of amphetamine isomers, methylphenidate and atomoxetine on synaptosomal and synaptic vesicle accumulation and release of dopamine and noradrenaline in vitro in the rat brain. Neuropharmacology 52 (2007) 405-414
26. Easton N., Shah Y.B., Marshall F.H., Fone K.C., and Marsden C.A. Guanfacine produces differential effects in frontal cortex compared with striatum: assessed by phMRI BOLD contrast. Psychopharmacology 189 (2006) 369-385
27. Ernst M., Zametkin A.J., Matochik J.A., Jons P.H., and Cohen R.M. DOPA decarboxylase activity in attention deficit hyperactivity disorder adults. A [fluorine-18]fluorodopa positron emission tomographic study. J. Neurosci. 18 (1998) 5901-5907
28. Fassbender C., and Schweitzer J.B. Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature. Clin. Psychol. Rev. 26 (2006) 445-465
29. Febo M., Segarra A.C., Nair G., Schmidt K., Duong T.Q., and Ferris C.F. The neural consequences of repeated cocaine exposure revealed by functional MRI in awake rats. Neuropsychopharmacology 30 (2005) 936-943
30. Fone K.C.F., and Nutt D.J. Stimulants: use and abuse in the treatment of attention deficit hyperactivity disorder. Curr. Opin. Pharmacol. 5 (2005) 87-93
31. Friston K.J., Ashburner J., Poline J.B., Frith C.D., Heather J.D., and Frackowiak R.S.J. Spatial registration and normalization of images. Hum. Brain Mapp. 3 (1995) 165-189
32. Friston K.J., Holmes A.P., Worsely K.J., Poline J.B., Frith C.D., and Frackowiak R.S.J. [SPM_3] statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2 (1995) 189-210
33. Gatley S.J., Pan D., Chen R., Chaturvedi G., and Ding Y.S. Affinities of methylphenidate derivatives for dopamine, norepinephrine and serotonin transporters. Life Sci. 58 (1996) 231-239
34. Grace A.A., Solanto M.V., and Arnsten A.F. Psychostimulant Actions on Dopamine and Limbic System Function: Relevance to the Pathophysiology and Treatment of ADHD. Stimulant Drugs and ADHD: Basic and Clinical Neuroscience (2001), Oxford University Press, New York pp. 134-155
35. Graziano M.S., Taylor C.S., Moore T., and Cooke D.F. The cortical control of movement revisited. Neuron 36 (2002) 349-362
36. Greenhill L.L., Muniz R., Ball R.R., Levine A., Pestreich L., and Jiang H. Efficacy and safety of dexmethylphenidate extended-release capsules in children with attention-deficit/hyperactivity disorder. J. Am. Acad. Child. Adolesc. Psychiatry 45 (2006) 817-823
37. Harel N., Lee S.P., Nagaoka T., Kim D.S., and Kim S.G. Origin of negative blood oxygenation level-dependent fMRI signals. J. Cereb. Blood Flow Metab. 22 (2002) 908-917
38. Herregodts P., Ebinger G., and Michotte Y. Distribution of monoamine in human brain - evidence for neurochemical heterogeneity in subcortical as well as cortical areas. Brain Res. 542 (1991) 300-306
39. Hewitt K.N., Shah Y.B., Prior M.J., Morris P.G., Hollis C.P., Fone K.C., and Marsden C.A. Behavioural and pharmacological magnetic resonance imaging assessment of the effects of methylphenidate in a potential new rat model of attention deficit hyperactivity disorder. Psychopharmacology (Berl) 180 (2005) 716-723
40. Isaac W., and Kallman W.M. Stimulants and lesions of the substantia nigra and red nucleus. Physiol. Behav. 15 (1975) 471-474
41. Jones M., Berwick J., Hewson-Stoate N., Gias C., and Mayhew J. The effect of hypercapnia on the neural and hemodynamic responses to somatosensory stimulation. Neuroimage 27 (2005) 609-623
42. Kohler C., and Sundberg H. Locomotor-activity and exploratory-behavior after medial entorhinal cortex lesions in albino-rat. Behav. Biol. 20 (1977) 419-432
43. Krause K.H., Dresel S., Krause J., Kung H.F., Tatsch K., and Lochmuller H. Elevated striatal dopamine transporter in a drug naive patient with Tourette syndrome and attention deficit/hyperactivity disorder: positive effect of methylphenidate. J. Neurol. 249 (2002) 1116-1118
44. Kuczenski R., and Segal D.S. Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J. Neurochem. 68 (1997) 2032-2037
45. Kuczenski R., and Segal D.S. Dynamic changes in sensitivity occur during the acute response to cocaine and methylphenidate. Psychopharmacology (Berl) 147 (1999) 96-103
46. Kuczenski R., and Segal D.S. Locomotor effects of acute and repeated threshold doses of amphetamine and methylphenidate: relative roles of dopamine and norepinephrine. J. Pharmacol. Exp. Ther. 296 (2001) 876-883
47. Kutcher S., Aman M., Brooks S.J., Buitelaar J., van Daalen E., Fegert J., Findling R.L., Fisman S., Greenhill L.L., Huss M., Kusumakar V., Pine D., Taylor E., and Tyano S. International consensus statement on attention- deficit/hyperactivity disorder (ADHD) and disruptive behaviour disorders (DBDs): clinical implications and treatment practice suggestions. Eur. Neuropsychopharmacol. 14 (2004) 11-28
48. Lee J.S., Kim B.N., Kang E., Lee D.S., Kim Y.K., Chung J.K., Lee M.C., and Cho S.C. Regional cerebral blood flow in children with attention deficit hyperactivity disorder: comparison before and after methylphenidate treatment. Hum. Brain Map 24 (2005) 157-164
49. Liu Z.M., Schmidt K.F., Sicard K.M., and Duong T.Q. Imaging oxygen consumption in forepaw somatosensory stimulation in rats under isoflurane anesthesia. Magn. Reson. Med. 52 (2004) 277-285
50. Ma C.L., Arnsten A.F., and Li B.M. Locomotor hyperactivity induced by blockade of prefrontal cortical alpha2-adrenoceptors in monkeys. Biol. Psychiatry 57 (2005) 192-195
51. Makris N., Biederman J., Valera E.M., Bush G., Kaiser J., Kennedy D.N., Caviness V.S., Faraone S.V., and Seidman L.J. Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. Cereb. Cortex 17 (2007) 1364-1375
52. Mandeville J.B., Jenkins B.G., Chen Y.C., Choi J.K., Kim Y.R., Belen D., Liu C., Kosofsky B.E., and Marota J.J. Exogenous contrast agent improves sensitivity of gradient-echo functional magnetic resonance imaging at 9.4 T. Magn. Reson. Med. 52 (2004) 1272-1281
53. Meador-Woodruff J.H., Damask S.P., and Watson Jr. S.J. Differential expression of autoreceptors in the ascending dopamine systems of the human brain. Proc. Natl. Acad. Sci. 91 (1994) 8297-8301
54. Mehta M.A., Calloway P., and Sahakian B.J. Amelioration of specific working memory deficits by methylphenidate in a case of adult attention deficit/hyperactivity disorder. J. Psychopharmacol. 14 (2000) 299-302
55. Moll G.H., Heinrich H., and Rothenberger A. Methylphenidate and intracortical excitability: opposite effects in healthy subjects and attention-deficit hyperactivity disorder. Acta Psychiatr. Scand. 107 (2003) 69-72
56. Moll G.H., Heinrich H., Trott G.E., Wirth S., and Rothenberger A. Deficient intracortical inhibition in drug-naive children with attention-deficit hyperactivity disorder is enhanced by methylphenidate. Neurosci. Lett. 284 (2000) 121-125
57. Newton J.M., Sunderland A., and Gowland P.A. fMRI signal decreases in ipsilateral primary motor cortex during unilateral hand movements are related to duration and side of movement. Neuroimage 24 (2005) 1080-1087
58. NICE. Attention deficit hyperactivity disorder. Diagnosis and management of ADHD in children, young people and adults. Natl. Inst. for Health Clin. Excell. Clinical Guideline 72 (2008)
59. Nutt D.J., Fone K., Asherson P., Bramble D., Hill P., Matthews K., Morris K.A., Santosh P., Sonuga-Barke E., Taylor E., Weiss M., Young S., and Consensus G. Evidence-based guidelines for management of attention-deficit/hyperactivity disorder in adolescents in transition to adult services and in adults: recommendations from the British Association for Psychopharmacology. J. Psychopharmacol. 21 (2007) 10-41
60. Ojemann J.G., Akbudak E., Snyder A.Z., McKinstry R.C., Raichle M.E., and Conturo T.E. Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. Neuroimage 6 (1997) 156-167
61. Parush S., Sohmer H., Steinberg A., and Kaitz M. Somatosensory functioning in children with attention deficit hyperactivity disorder. Dev. Med. Child. Neurol. 39 (1997) 464-468
62. Porrino L.J., and Lucignani G. Different patterns of local brain energy metabolism associated with high and low doses of methylphenidate. Relevance to its action in hyperactive children. Biol. Psychiatry 22 (1987) 126-138
63. Preuss M. Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J. Cog Neurosci. 7 (1995) 1-23
64. Qiu A.Q., Crocetti D., Adler M., Mahone E.M., Denckla M.B., Miller M.I., and Mostofsky S.H. Basal ganglia volume and shape in children with attention deficit hyperactivity disorder. Am. J. Psychiatry 166 (2009) 74-82
65. Rubia K., Overmeyer S., Taylor E., Brammer M., Williams S.C.R., Simmons A., and Bullmore E.T. Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. Am. J. Psychiatry 156 (1999) 891-896
66. Sanders J.D., Happe H.K., Bylund D.B., and Murrin L.C. Development of the norepinephrine transporter in the rat CNS. Neuroscience 130 (2005) 107-117
67. Sanes J.N. Neocortical mechanisms in motor learning. Curr. Opin. Neurobiol. 13 (2003) 225-231
68. Schiffer W.K., Volkow N.D., Fowler J.S., Alexoff D.L., Logan J., and Dewey S.L. Therapeutic doses of amphetamine or methylphenidate differentially increase synaptic and extracellular dopamine. Synapse 59 (2006) 243-251
69. Schroeter S., Apparsundaram S., Wiley R.G., Miner L.H., Sesack S.R., and Blakely R.D. Immunolocalization of the cocaine- and antidepressant-sensitive 1-norepinephrine transporter. J. Comp. Neurol. 420 (2000) 211-232
70. Scott S.H. Role of motor cortex in coordinating multi-joint movements: is it time for a new paradigm?. Can. J. Physiol. Pharmacol. 78 (2000) 923-933
71. Seeman P., and Madras B. Methylphenidate elevates resting dopamine which lowers the impulse-triggered release of dopamine: a hypothesis. Behav. Brain Res. 130 (2002) 79-83
72. Seidman L.J., Valera E.M., Makris N., Monuteaux M.C., Boriel D.L., Kelkar K., Kennedy D.N., Caviness V.S., Bush G., Aleardi M., Faraone S.V., and Biederman J. Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biol. Psychiatry 60 (2006) 1071-1080
73. Sellings L.H., and Clarke P.B. Segregation of amphetamine reward and locomotor stimulation between nucleus accumbens medial shell and core. J. Neurosci. 23 (2003) 6295-6303
74. Shah Y.B., and Marsden C.A. The application of functional magnetic resonance imaging to neuropharmacology. Curr. Opin. Pharmacol. 4 (2004) 517-521
75. Shmuel A., Augath M., Oeltermann A., and Logothetis N.K. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat. Neurosci. 9 (2006) 569-577
76. Shmuel A., Yacoub E., Pfeuffer J., Van de Moortele P.F., Adriany G., Hu X., and Ugurbil K. Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36 (2002) 1195-1210
77. Shumsky J.S., Danley J.E., Bertrand L., Drouin C., Nissanov J., and Waterhouse B.D. Low dose methylphenidate improves vigilance performance in a sustained attention task. Soc. Neurosci. Abstr. (2006) 800-804
78. Sicard K., Shen Q., Brevard M.E., Sullivan R., Ferris C.F., King J.A., and Duong T.Q. Regional cerebral blood flow and BOLD responses in conscious and anesthetized rats under basal and hypercapnic conditions: implications for functional MRI studies. J. Cereb. Blood Flow Metab. 23 (2003) 472-481
79. Sicard K.M., and Duong T.Q. Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. Neuroimage 25 (2005) 850-858
80. Skoubis P.D., Hradil V., Chin C.L., Luo Y., Fox G.B., and McGaraughty S. Mapping brain activity following administration of a nicotinic acetylcholine receptor agonist, ABT-594, using functional magnetic resonance imaging in awake rats. Neuroscience 137 (2006) 583-591
81. Smith A.T., Williams A.L., and Singh K.D. Negative BOLD in the visual cortex: evidence against blood stealing. Hum. Brain Mapp. 21 (2004) 213-220
82. Steward C.A., Marsden C.A., Prior M.J., Morris P.G., and Shah Y.B. Methodological considerations in rat brain BOLD contrast pharmacological MRI. Psychopharmacology (Berl) 180 (2005) 687-704
83. Swanson J.M., Kinsbourne M., Nigg J., Lanphear B., Stefanatos G.A., Volkow N., Taylor E., Casey B.J., Castellanos F.X., and Wadhwa P.D. Etiologic subtypes of attention-deficit/hyperactivity disorder: brain imaging, molecular genetic and environmental factors and the dopamine hypothesis. Neuropsychol. Rev. 17 (2007) 39-59
84. 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
85. Teicher M.H., Tomoda A., and Andersen S.L. Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable?. Ann. N. Y Acad. Sci. 1071 (2006) 313-323
86. Vaidya C.J., Austin G., Kirkorian G., Ridlehuber H.W., Desmond J.E., Glover G.H., and Gabrieli J.D. Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc. Natl. Acad. Sci. 95 (1998) 14494-14499
87. Volkow N.D., Wang G.J., Fowler J.S., and Ding Y.S. Imaging the effect of methylphenidate on brain dopamine: new model on its therapeutic actions for attention-deficit/hyperactivity disorder. Biol. Psychiatry 57 (2005) 1410-1415
88. Volkow N.D., Wang G.J., Fowler J.S., Logan J., Gerasimov M., Maynard L., Ding Y.S., Gatley S.J., Gifford A., and Franceschi D. Therapeutic doses of oral methylphenidate significantly increase extracellular dopamine in the human brain. J. Neurosci. 21 (2001) U1-U5
89. Wang G.J., Volkow N.D., Fowler J.S., Logan J., Pappas N.R., Wong C.T., Hitzemann R.J., and Netusil N. Reproducibility of repeated measures of endogenous dopamine competition with [11C]raclopride in the human brain in response to methylphenidate. J. Nucl. Med. 40 (1999) 1285-1291
90. Yang B.R., Chan R.C.K., Jing J., Li T., Sham P., and Chen R.Y.L. A meta-analysis of association studies between the 10-repeat allele of a VNTR polymorphism in the 3'-UTR of dopamine transporter gene and attention deficit hyperactivity disorder. Am. J. Med. Genet. Part B-Neuropsychiatric Genet. 144B (2007) 541-550
91. Zang Y.F., Jin Z., Weng X.C., Zhang L., Zeng Y.W., Yang L., Wang Y.F., Seidman L.J., and Faraone S.V. Functional MRI in attention-deficit hyperactivity disorder: evidence for hypofrontality. Brain Dev. 27 (2005) 544-550