Dissociable effects of methylphenidate, atomoxetine and placebo on regional cerebral blood flow in healthy volunteers at rest: A multi-class pattern recognition approach

NeuroImage

Volumn 60, Issue 2, 2012, Pages 1015-1024

  Marquand, Andre F ^a   O'Daly, Owen G ^a   De Simoni, Sara ^a   Alsop, David C ^b   Maguire, R Paul ^c   Williams, Steven C R ^a   Zelaya, Fernando O ^a   Mehta, Mitul A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c PFIZER INC   (United States)

Author keywords

Arterial spin labeling; Atomoxetine; Methylphenidate; Multi class pattern recognition

Indexed keywords

ATOMOXETINE; METHYLPHENIDATE; PLACEBO;

ACCURACY; ADULT; ARTERIAL SPIN LABELING; ARTICLE; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN REGION; CAUDATE NUCLEUS; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG MECHANISM; HUMAN; HUMAN EXPERIMENT; MALE; MESENCEPHALON; NERVE CELL NETWORK; NON INVASIVE MEASUREMENT; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATTERN RECOGNITION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REST; SPIN LABELING; SUBCORTEX; SUBSTANTIA NIGRA; THALAMUS; VOLUNTEER;

ADRENERGIC UPTAKE INHIBITORS; ADULT; BRAIN; CENTRAL NERVOUS SYSTEM STIMULANTS; CEREBROVASCULAR CIRCULATION; HUMANS; MALE; METHYLPHENIDATE; PATTERN RECOGNITION, AUTOMATED; PROPYLAMINES; REGIONAL BLOOD FLOW; REST; YOUNG ADULT;

EID: 84863406628     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.01.058     Document Type: Article

References (71)

1. Alsop D.C., Detre J.A. Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J. Cereb. Blood Flow Metab. 1996, 16:1236-1249.
2. Biederman J., Spencer T., Wilens T. Evidence-based pharmacotherapy for attention-deficit hyperactivity disorder. Int. J. Neuropsychopharmacol. 2004, 7:77-97.
3. Bolden-Watson C., Richelson E. Blockade by newly-developed antidepressants of biogenic-amine uptake into rat-brain synaptosomes. Life Sci. 1993, 52:1023-1029.
4. Borghammer P., Cumming P., Aanerud J., Gjedde A. Artefactual subcortical hyperperfusion in PET studies normalized to global mean: lessons from Parkinson's disease. NeuroImage 2009, 45:249-257.
5. Buxton R.B. Interpreting oxygenation-based neuroimaging signals: the importance and the challenge of understanding brain oxygen metabolism. Front. Neuroenergetics 2010, 2:8.
6. Buxton R.B., Frank L.R., Wong E.C., Siewert B., Warach S., Edelman R.R. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn. Reson. Med. 1998, 40:383-396.
7. Buxton R.B., Uludag K., Dubowitz D.J., Liu T.T. Modeling the hemodynamic response to brain activation. NeuroImage 2004, 23:S220-S233.
8. 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., 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 2002, 27:699-711.
9. Carroll M.K., Cecchi G.A., Rish I., Garg R., Rao A.R. Prediction and interpretation of distributed neural activity with sparse models. NeuroImage 2009, 44:112-122.
10. Chamberlain S.R., Hampshire A., Muller U., Rubia K., del Campo N., Craig K., Regenthal R., Suckling J., Roiser J.P., Grant J.E., Bullmore E.T., Robbins T.W., Sahakian B.J. Atomoxetine modulates right inferior frontal activation during inhibitory control: a pharmacological functional magnetic resonance imaging study. Biol. Psychiatry 2009, 65:550-555.
11. Ciliax B.J., Drash G.W., Staley J.K., Haber S., Mobley C.J., Miller G.W., Mufson E.J., Mash D.C., Levey A.I. Immunocytochemical localization of the dopamine transporter in human brain. J. Comp. Neurol. 1999, 409:38-56.
12. Cunningham E.T., Sawchenko P.E. Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J. Comp. Neurol. 1988, 274:60-76.
13. Dai W.Y., Garcia D., de Bazelaire C., Alsop D.C. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn. Reson. Med. 2008, 60:1488-1497.
14. Detre J.A., Leigh J.S., Williams D.S., Koretsky A.P. Perfusion imaging. Magn. Reson. Med. 1992, 23:37-45.
15. Dodds C.M., Mueller U., Clark L., van Loon A., Cools R., Robbins T.W. Methylphenidate has differential effects on blood oxygenation level-dependent signal related to cognitive subprocesses of reversal learning. J. Neurosci. 2008, 28:5976-5982.
16. Faraone S.V., Biederman J., Spencer T., Michelson D., Adler L., Reimherr F., Glatt S.J. Efficacy of atomoxetine in adult attention-deficit/hyperactivity disorder: a drug-placebo response curve analysis. Behav. Brain Funct. 2005, 1:16.
17. Garcia D., Duhamel G., Alsop D. Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn. Reson. Med. 2005, 54:366-372.
18. Garcia-Cabezas M.A., Rico B., Sanchez-Gonzalez M.A., Cavada C. Distribution of the dopamine innervation in the macaque and human thalamus. NeuroImage 2007, 34:965-984.
19. Ghose S., Fujita M., Morrison P., Uhl G., Murphy D.L., Mozley P.D., Schou M., Halldin C., Innis R. Specific in vitro binding of (S, S)-H-3 MeNER to norepinephrine transporters. Synapse 2005, 56:100-104.
20. Gilbert D.L., Ridel K.R., Sallee F.R., Zhang J., Lipps T.D., Wassermann E.M. Comparison of the inhibitory and excitatory effects of ADHD medications methylphenidate and atomoxetine on motor cortex. Neuropsychopharmacology 2006, 31:442-449.
21. Graf H., Abler B., Freudenmann R., Beschoner P., Schaeffeler E., Spitzer M., Schwab M., Gron G. Neural correlates of error monitoring modulated by atomoxetine in healthy volunteers. Biol. Psychiatry 2011, 69:890-897.
22. Grenhoff J., Nisell M., Ferre S., Astonjones G., Svensson T.H. Noradrenergic modulation of midbrain dopamine cell firing elicited by stimulation of the locus-ceruleus in the rat. J. Neural Transm. Gen. Sect. 1993, 93:11-25.
23. Guyon I., Weston J., Barnhill S., Vapnik V. Gene selection for cancer classification using support vector machines. Mach. Learn. 2002, 46:389-422.
24. Han D.D., Gu H.H. Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol. 2006, 6. (Article No.: 6).
25. Hannestad J., Gallezot J.D., Planeta-Wilson B., Lin S.F., Williams W.A., van Dyck C.H., Malison R.T., Carson R.E., Ding Y.S. Clinically relevant doses of methylphenidate significantly occupy norepinephrine transporters in humans in vivo. Biol. Psychiatry 2010, 68:854-860.
26. Hanson S.J., Halchenko Y.O. Brain reading using full brain support vector machines for object recognition: there is no "face" identification area. Neural Comput. 2008, 20:486-503.
27. Herscovitch P., Raichle M.E. What is the correct value for the brain-blood partition coefficient for water?. J. Cereb. Blood Flow Metab. 1985, 5:65-69.
28. Kaenmaki M., Tammimaki A., Myohanen T., Pakarinen K., Amberg C., Karayiorgou M., Gogos J.A., Mannisto P.T. Quantitative role of COMT in dopamine clearance in the prefrontal cortex of freely moving mice. J. Neurochem. 2010, 114:1745-1755.
29. Kemner J.E., Starr H.L., Ciccone P.E., Hooper-Wood C.G., Crockett R.S. Outcomes of OROS (R) methylphenidate compared with atomoxetine in children with ADHD: a multicenter, randomized prospective study. Adv. Ther. 2005, 22:498-512.
30. Krimer L.S., Muly E.C., Williams G.V., Goldman-Rakic P.S. Dopaminergic regulation of cerebral cortical microcirculation. Nat. Neurosci. 1998, 1:286-289.
31. Krishnapuram B., Carin L., Figueiredo M.A.T., Hartemink A.J. Sparse multinomial logistic regression: fast algorithms and generalization bounds. IEEE Trans. Pattern Anal. Mach. Intell. 2005, 27:957-968.
32. Lategan A.J., Marien M.R., Colpaert F.C. Effects of locus-ceruleus lesions on the release of endogenous dopamine in the rat nucleus-accumbens and caudate-nucleus as determined by intracerebral microdialysis. Brain Res. 1990, 523:134-138.
33. Lategan A.J., Marien M.R., Colpaert F.C. Suppression of nigrostriatal and mesolimbic dopamine release invivo following noradrenaline depletion by DSP-4 - a microdialysis study. Life Sci. 1992, 50:995-999.
34. Lu H.Z., Clingman C., Golay X., van Zijl P.C.M. Determining the longitudinal relaxation time (T-1) of blood at 3.0tesla. Magn. Reson. Med. 2004, 52:679-682.
35. Ma Y.L., Tang C.K., Moeller J.R., Eidelberg D. Abnormal regional brain function in Parkinson's disease: truth or fiction?. NeuroImage 2009, 45:260-266.
36. Marien M.R., Colpaert F.C., Rosenquist A.C. Noradrenergic mechanisms in neurodegenerative diseases: a theory. Brain Res. Rev. 2004, 45:38-78.
37. Marquand A., De Simoni S., O'Daly O., Mourao-Miranda J., Mehta M. Quantifying the information content of brain voxels using target information, Gaussian processes and recursive feature elimination. International Conference on Pattern Recognition. Istanbul, Turkey 2010.
38. Marquand A., De Simoni S., O'Daly O., Williams S., Mourão-Miranda J., Mehta M. Pattern classification of working memory networks reveals differential effects of methylphenidate, atomoxetine, and placebo in healthy volunteers. Neuropsychopharmacology 2011, 36:1237-1247.
39. Mehta M.A., Owen A.M., Sahakian B.J., Mavaddat N., Pickard J.D., Robbins T.W. Methylphenidate enhances working memory by modulating discrete frontal and parietal lobe regions in the human brain. J. Neurosci. 2000, 20:6.
40. Melchitzky D.S., Lewis D.A. Tyrosine hydroxylase- and dopamine transporter-immunoreactive axons in the primate cerebellum - evidence for a lobular- and laminar-specific dopamine innervation. Neuropsychopharmacology 2000, 22:466-472.
41. Michelson D., Faries D., Wernicke J., Kelsey D., Kendrick K., Sallee F.R., Spencer T., Atomoxetine A.S.G. Atomoxetine in the treatment of children and adolescents with attention-deficit/hyperactivity disorder: a randomized, placebo-controlled, dose-response study. Pediatrics 2001, 108.
42. Moore R.Y., Bloom F.E. Central catecholamine neuron systems - anatomy and physiology of the norepinephrine and epinephrine systems. Annu. Rev. Neurosci. 1979, 2:113-168.
43. Moron J.A., Brockington A., Wise R.A., Rocha B.A., Hope B.T. Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: evidence from knock-out mouse lines. J. Neurosci. 2002, 22:389-395.
44. Mourao-Miranda J., Bokde A.L., Born C., Hampel H., Stetter M. Classifying brain states and determining the discriminating activation patterns: support vector machine on functional MRI data. NeuroImage 2005, 28:980-995.
45. Mulligan S.J., MacVicar B.A. Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 2004, 431:195-199.
46. Newcorn J.H., Kratochvil C.J., Allen A.J., Casat C.D., Ruff D.D., Moore R.J., Michelson D., Atomoxetine Methylphenidate C. Atomoxetine and osmotically released methylphenidate for the treatment of attention deficit hyperactivity disorder: acute comparison and differential response. Am. J. Psychiatry 2008, 165:721-730.
47. Powers R.E., Oconnor D.T., Price D.L. Noradrenergic systems in human cerebellum. Brain Res. 1989, 481:194-199.
48. Raichle M.E., Hartman B.K., Eichling J.O., Sharpe L.G. Central noradrenergic regulation of cerebral blood-flow and vascular-permeability. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:3726-3730.
49. Rubia K., Halari R., Cubillo A., Smith A.B., Mohammad A.M., Brammer M., Taylor E. Methylphenidate normalizes fronto-striatal underactivation during interference inhibition in medication-naive boys with attention-deficit hyperactivity disorder. Neuropsychopharmacology 2011, 36:1575-1586.
50. Ryali S., Supekar K., Abrams D.A., Menon V. Sparse logistic regression for whole-brain classification of fMRI data. NeuroImage 2010, 51:752-764.
51. Sanchez-Gonzalez M.A., Garcia-Cabezas M.A., Rico B., Cavada C. The primate thalamus is a key target for brain dopamine. J. Neurosci. 2005, 25:6076-6083.
52. Sauer J.M., Ring B.J., Witcher J.W. Clinical pharmacokinetics of atomoxetine. Clin. Pharmacokinet. 2005, 44:571-590.
53. Scholkopf B., Smola A. Learning with kernels. Support vector machines, regularization, optimization and beyond 2002, MIT Press, Cambridge, Massachusetts.
54. Schou M., Halldin C., Pike V.W., Mozley P.D., Dobson D., Innis R.B., Farde L., Hall H. Post-mortem human brain autoradiography of the norepinephrine transporter using (S, S)-F-18 FMeNER-D-2. Eur. Neuropsychopharmacol. 2005, 15:517-520.
55. Schweitzer J.B., Lee D.O., Hanford R.B., Zink C.F., Ely T.D., Tagamets M.A., Hoffman J.M., Grafton S.T., Kilts C.D. Effect of methylphenidate on executive functioning in adults with attention-deficit/hyperactivity disorder: normalization of behavior but not related brain activity. Biol. Psychiatry 2004, 56:597-606.
56. Seeman P., Madras B.K. Anti-hyperactivity medication: methylphenidate and amphetamine. Mol. Psychiatry 1998, 3:386-396.
57. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
58. Spencer T., Biederman J., Wilens T., Prince J., Hatch M., Jones J., Harding M., Faraone S.V., Seidman L. Effectiveness and tolerability of tomoxetine in adults with attention deficit hyperactivity disorder. Am. J. Psychiatry 1998, 155:693-695.
59. Starr H.L., Kemner J. Multicenter, randomized, open-label study of OROS methylphenidate versus atomoxetine: treatment outcomes in African-American children with ADHD. J. Natl. Med. Assoc. 2005, 97:11S-16S.
60. Swanson L.W., Hartman B.K. Central adrenergic system - immunofluorescence study of location of cell bodies and their efferent connections in rat utilizing dopamine-beta-hydroxylase as a marker. J. Comp. Neurol. 1975, 163:467-505.
61. Tejani-Butt S.M. [3H] Nisoxetine - a radioligand for quantitation of norepinephrine uptake sites by autoradiography or by homogenate binding. J. Pharmacol. Exp. Ther. 1992, 260:427-436.
62. Telang F.W., Volkow N.D., Levy A., Logan J., Fowler J.S., Felder C., Wong C., Wang G.J. Distribution of tracer levels of cocaine in the human brain as assessed with averaged 11C cocaine images. Synapse 1999, 31:290-296.
63. Udo de Haes J.I., Maguire R.P., Jager P.L., Paans A.M.J., den Boer J.A. Methylphenidate-induced activation of the anterior cingulate but not the striatum: a 15O H2O PET study in healthy volunteers. Hum. Brain Mapp. 2007, 28:625-635.
64. Vaidya C.J., Austin G., Kirkorian G., Ridlehuber H.W., Desmond J.E., Glover G.H., Gabrieli J.D.E. Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14494-14499.
65. Volkow N.D., Wang G.J., Fowler J.S., Logan J., Schlyer D., Hitzemann R., Lieberman J., Angrist B., Pappas N., Macgregor R., Burr G., Cooper T., Wolf A.P. Imaging endogenous dopamine competition with C-11 raclopride in the human brain. Synapse 1994, 16:255-262.
66. Volkow N.D., Wang G.J., Fowler J.S., Logan J., Angrist B., Hitzemann R., Lieberman J., Pappas N. Effects of methylphenidate on regional brain glucose metabolism in humans: relationship to dopamine D-2 receptors. Am. J. Psychiatry 1997, 154:50-55.
67. Volkow N.D., Wang G.J., Fowler J.S., Gatley S.J., Logan J., Ding Y.S., Hitzemann R., Pappas N. Dopamine transporter occupancies in the human brain induced by therapeutic doses of oral methylphenidate. Am. J. Psychiatry 1998, 155:1325-1331.
68. Wargin W., Patrick K., Kilts C., Gualtieri C.T., Ellington K., Mueller R.A., Kraemer G., Breese G.R. Pharmacokinetics of methylphenidate in man, rat and monkey. J. Pharmacol. Exp. Ther. 1983, 226:382-386.
69. Williams D.S., Detre J.A., Leigh J.S., Koretsky A.P. Magnetic-resonance-imaging of perfusion using spin inversion of arterial water. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:212-216.
70. Wong D.T., Threlkeld P.G., Best K.L., Bymaster F.P. A new inhibitor of norepinephrine uptake devoid of affinity for receptors in rat-brain. J. Pharmacol. Exp. Ther. 1982, 222:61-65.
71. Yamashita O., Sato M., Yoshioka T., Tong F., Kamitani Y. Sparse estimation automatically selects voxels relevant for the decoding of fMRI activity patterns. NeuroImage 2008, 42:1414-1429.