Pattern classification of working memory networks reveals differential effects of methylphenidate, atomoxetine, and placebo in healthy volunteers

Neuropsychopharmacology

Volumn 36, Issue 6, 2011, Pages 1237-1247

  Marquand, Andre F ^a   De Simoni, Sara ^a   O'Daly, Owen G ^a   Williams, Steven C R ^a   Mouro Miranda, Janaina ^a,b   Mehta, Mitul A ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

atomoxetine; methylphenidate; pattern recognition; reward; working memory

Indexed keywords

ATOMOXETINE; METHYLPHENIDATE; PLACEBO;

ADULT; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; DOUBLE BLIND PROCEDURE; DROWSINESS; DRUG EFFECT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MOTIVATION; NAUSEA; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; REWARD; TASK PERFORMANCE; VOLUNTEER; WORKING MEMORY;

ADRENERGIC UPTAKE INHIBITORS; ADULT; CENTRAL NERVOUS SYSTEM STIMULANTS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; METHYLPHENIDATE; NEUROPSYCHOLOGICAL TESTS; PLACEBO EFFECT; PROPYLAMINES; REWARD; TASK PERFORMANCE AND ANALYSIS; YOUNG ADULT;

EID: 79954589579     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2011.9     Document Type: Article

References (72)

1. Alexander GE, Delong MR, Strick PL (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357-381. (Pubitemid 16055790)
2. Andreou P, Neale BM, Chen W, Christiansen H, Gabriels I, Heise A et al (2007). Reaction time performance in ADHD: improvement under fast-incentive condition and familial effects. Psychol Med 37: 1703-1715. (Pubitemid 350100437)
3. Arnsten A, Dudley A (2005). Methylphenidate improves prefrontal cortical cognitive function through a2 adrenoreceptors and dopamine D1 receptor actions: relevance to therapeutic effects in attention-deficit hyperactivity disorder. Behav Brain Funct 1: 2-10.
4. Arnsten AFT (2006). Stimulants: therapeutic actions in ADHD. Neuropsychopharmacology 31: 2376-2383.
5. Arnsten AFT (2007). Catecholamine and second messenger influences on prefrontal cortical networks of 'representational knowledge': a rational bridge between genetics and the symptoms of mental illness. Cerebral Cortex 17: I6-I15.
6. Arnsten AFT, Goldman-Rakic PS (1985). Alpha-2-adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged non-human primates. Science 230: 1273-1276. (Pubitemid 16194533)
7. Bedard AC, Martinussen R, Ickowicz A, Tannock R (2004). Methylphenidate improves visual-spatial memory in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 43: 260-268. (Pubitemid 41615004)
8. Berridge CW, Devilbiss DM, Andrzejewski ME, Arnsten AFT, Kelley AE, Schmeichel B et al (2006). Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function. Biol Psychiatry 60: 1111-1120. (Pubitemid 44647216)
9. Bolden-Watson C, Richelson E (1993). Blockade by newly-developed antidepressants of biogenic-amine uptake into rat-brain synaptosomes. Life Sci 52: 1023-1029.
10. Bond AJ, Lader MH (1974). The use of analogue scales in rating subjective feelings. Br J Med Psychol 47: 211-218.
11. Brozoski TJ, Brown RM, Rosvold HE, Goldman PS (1979). Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205: 929-932. (Pubitemid 10243358)
12. Bymaster FP, Katner JS, Nelson DL, Hemrick-Luecke SK, Threlkeld PG, Heiligenstein JH et al (2002). Atomoxetine increases extracellular levels of norepinephrine and dopamine in pre-frontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 27: 699-711. (Pubitemid 35335888)
13. Ciliax BJ, Drash GW, Staley JK, Haber S, Mobley CJ, Miller GW et al (1999). Immunocytochemical localization of the dopamine transporter in human brain. J Comp Neurol 409: 38-56. (Pubitemid 29242784)
14. 0Esposito M (2004). Maintenance of spatial and motor codes during oculomotor delayed response tasks. J Neurosci 24: 3944-3952. (Pubitemid 38544221)
15. De Martino F, Valente G, Staeren N, Ashburner J, Goebel R, Formisano E (2008). Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns. NeuroImage 43: 44-58.
16. Durstewitz D, Seamans JK, Sejnowski TJ (2000). Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. Jo Neurophysiol 83: 1733-1750. (Pubitemid 30159594)
17. Eichele T, Debener S, Calhoun VD, Specht K, Engel AK, Hugdahl K et al (2008). Prediction of human errors by maladaptive changes in event-related brain networks. Proc Natl Acad Sci USA 105: 6173-6178. (Pubitemid 351758418)
18. Elliott R, Sahakian BJ, Matthews K, Bannerjea A, Rimmer J, Robbins TW (1997). Effects of methylphenidate on spatial working memory and planning in healthy young adults. Psychopharmacology 131: 196-206. (Pubitemid 27261609)
19. Faraone SV, Biederman J, Spencer T, Michelson D, Adler L, Reimherr F et al (2005). Efficacy of atomoxetine in adult attention-deficit/hyperactivity disorder: a drug-placebo response curve analysis. Behav Brain Funct 1: 16.
20. Fassbender C, Zhang H, Buzy WM, Cortes CR, Mizuiri D, Beckett L et al. (2009). A lack of default network suppression is linked to increased distractibility in ADHD. Brain Res 1273: 114-128.
21. Foote S, Freedman R, Oliver AP. (1975). Effects of putative neurotransmitters on neuronal activity in monkey auditory cortex. Brain Res 86: 229-242.
22. Formisano E, De Martino F, Bonte M, Goebel R (2008). 'Who' Is Saying 'What'? Brain-based decoding of human voice and speech. Science 322: 970-973.
23. Gamo NJ, Wamg M, Arnsten AF (2010). Methylphenidate and atomoxetine enhance prefrontal function through alpha-2 adrenergic and dopamine D1 receptors. J Am Acad Child Adolesc Psychiatry 49: 1011-1023.
24. Gibbs SEB, D'Esposito M (2005). A functional MRI study of the effects of bromocriptine, a dopamine receptor agonist, on component processes of working memory. Psychopharmacology 180: 644-653. (Pubitemid 41317861)
25. Gilbert DL, Ridel KR, Sallee FR, Zhang J, Lipps TD, Wassermann EM (2006). Comparison of the inhibitory and excitatory effects of ADHD medications methylphenidate and atomoxetine on motor cortex. Neuropsychopharmacology 31: 442-449. (Pubitemid 43113408)
26. Guyon I, Weston J, Barnhill S, Vapnik V (2002). Gene selection for cancer classification using support vector machines. Mach Learn 46: 389-422. (Pubitemid 34129977)
27. Han DD, Gu HH (2006). Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacology 6 Article No. 6. pp 1-7.
28. Hanson SJ, Halchenko YO (2008). Brain reading using full brain support vector machines for object recognition: there is no 'Face' identification area. Neural Comput 20: 486-503.
29. Haynes JD, Rees G (2006). Decoding mental states from brain activity in humans. Nat Rev Neurosci 7: 523-534. (Pubitemid 43989773)
30. Herbert M, Johns MW, Dore C (1976). Factor-analysis of analog scales measuring subjective feelings before and after sleep. Br J Med Psychol 49: 373-379.
31. Ichihara-Takeda S, Takeda K, Funahashi S (2010). Reward acts as a signal to control delay-period activity in delayed-response tasks. Neuroreport 21: 367-370.
32. Kelly C, de Zubicaray G, Di Martino A, Copland DA, Reiss PT, Klein DF et al (2009). -Dopa modulates functional connectivity in striatal cognitive and motor networks: a Double-Blind Placebo-Controlled Study. J Neurosci 29: 7364-7378.
33. Kemner JE, Starr HL, Ciccone PE, Hooper-Wood CG, Crockett RS (2005). Outcomes of OROS (R) methylphenidate compared with atomoxetine in children with ADHD: a multicenter, randomized prospective study. Adv Ther 22: 498-512. (Pubitemid 43130867)
34. Kriegeskorte N, Goebel R, Bandettini P (2006). Information-based functional brain mapping. Proc Natl Acad Sci USA 103: 3863-3868. (Pubitemid 43376646)
35. Levy F (2009). Dopamine vs noradrenaline: inverted-U effects and ADHD theories. Austr NZ J Psychiatry 43: 101-108.
36. Marquand A, De Simoni S, O'Daly O, Mourao-Miranda J, Mehta M (2010a). Quantifying the information content of brain voxels using target information, Gaussian processes and recursive feature elimination Qu. In: International Conference on Pattern Recognition. Istanbul, Turkey.
37. Marquand A, et al (2010b). Quantitative prediction of subjective pain intensity from whole-brain fMRI data using Gaussian processes. NeuroImage 49: 2178-2189.
38. Martinussen R, Hayden J, Hogg-Johnson S, Tannock R (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 44: 377-384. (Pubitemid 40393276)
39. Mattay VS, Callicott JH, Bertolino A, Heaton I, Frank JA, Coppola R et al (2000). Effects of dextroamphetamine on cognitive performance and cortical activation. NeuroImage 12: 268-275.
40. Mattay VS, Goldberg TE, Fera F, Hariri AR, Tessitore A, Egan MF et al (2003). Catechol O-methyltransferase val(158)-met genotype and individual variation in the brain response to amphetamine. Proc Natl Acad Sci USA 100: 6186-6191. (Pubitemid 36576952)
41. Mehta MA, Goodyer IM, Sahakian BJ (2004). Methylphenidate improves working memory and set-shifting in AD/HD: relationships to baseline memory capacity. J Child Psychol Psychiatry 45: 293-305. (Pubitemid 38240276)
42. Mehta MA, Owen AM, Sahakian BJ, Mavaddat N, Pickard JD, Robbins TW (2000). Methylphenidate enhances working memory by modulating discrete frontal and parietal lobe regions in the human brain. J Neurosci 20: 6.
43. Michelson D, Faries D, Wernicke J, Kelsey D, Kendrick K, Sallee FR et al (2001). Atomoxetine in the treatment of children and adolescents with attention-deficit/hyperactivity disorder: a randomized, placebo-controlled, dose-response study. Pediatrics 108: E83.
44. Mourao-Miranda J, Bokde AL, Born C, Hampel H, Stetter M (2005). Classifying brain states and determining the discriminating activation patterns: support vector machine on functional MRI data. NeuroImage 28: 980-995. (Pubitemid 41713632)
45. Newcorn JH, Kratochvil CJ, Allen AJ, Casat CD, Ruff DD, Moore RJ et al (2008). Atomoxetine and osmotically released methylphe-nidate for the treatment of attention deficit hyperactivity disorder: acute comparison and differential response. Am J Psychiatry 165: 721-730. (Pubitemid 351810541)
46. Norman KA, Polyn SM, Detre GJ, Haxby JV (2006). Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10: 424-430. (Pubitemid 44308461)
47. Pessoa L, Engelmann J (2010). Embedding reward signals into perception and cognition. Front Neurosci 4: 1-8.
48. Peterson BS, Potenza MN, Wang ZS, Zhu HT, Martin A, Marsh R et al (2009). An fMRI study of the effects of psychostimulants on default-mode processing during stroop task performance in youths with ADHD. Am J Psychiatry 166: 1286-1294.
49. Pochon JB, Levy R, Fossati P, Lehericy S, Poline JB, Pillon B et al (2002). The neural system that bridges reward and cognition in humans: an fMRI study. Proc Natl Acad Sci USA 99: 5669-5674. (Pubitemid 34411608)
50. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001). A default mode of brain function. Proc Natl Acad Sci USA 98: 676-682. (Pubitemid 32105102)
51. Rasmussen C, Williams CKI (2006). Gaussian Processes for Machine Learning. The MIT Press: Cambridge, MA.
52. Sauer JM, Ring BJ, Witcher JW (2005). Clinical pharmacokinetics of atomoxetine. Clin Pharmacokinet 44: 571-590. (Pubitemid 40994086)
53. Schou M, Halldin C, Pike VW, Mozley PD, Dobson D, Innis RB. et al (2005). Post-mortem human brain autoradiography of the norepinephrine transporter using (S,S)-F-18 FMeNER-D-2. Eur Neuropsychopharmacol 15: 517-520. (Pubitemid 41219622)
54. Schultz W, Apicella P, Ljungberg T (1993). Responses of monkey dopamine neurons to reward and conditioned-stimuli during successive steps of learning a delayed-response task. J Neurosci 13: 900-913. (Pubitemid 23067580)
55. Schultz W, Romo R (1990). Dopamine neurons of the monkey midbrainFcontingencies of responses to stimuli eliciting immediate behavioural reactions. J Neurophysiol 63: 607-624. (Pubitemid 20115487)
56. Schweitzer JB, Lee DO, Hanford RB, Zink CF, Ely TD, Tagamets MA et al (2004). Effect of methylphenidate on executive functioning in adults with attention-deficit/hyperactivity disorder: normalization of behavior but not related brain activity. Biol Psychiatry 56: 597-606. (Pubitemid 39336408)
57. Seamans JK, Gorelova N, Durstewitz D, Yang CR (2001). Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21: 3628-3638. (Pubitemid 32422827)
58. Seeman P, Madras BK (1998). Anti-hyperactivity medication: methylphenidate and amphetamine. Mol Psychiatry 3: 386-396. (Pubitemid 28442411)
59. Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Raichle ME et al (1997). Common blood flow changes across visual tasks.2. Decreases in cerebral cortex. J Cogn Neurosci 9: 648-663. (Pubitemid 27455556)
60. Spencer T, Biederman J, Wilens T, Prince J, Hatch M, Jones J et al (1998). Effectiveness and tolerability of tomoxetine in adults with attention deficit hyperactivity disorder. Am J Psychiatry 155: 693-695. (Pubitemid 28225414)
61. Starr HL, Kemner J (2005). Multicenter, randomized, open-label study of OROS methylphenidate versus atomoxetine: treatment outcomes in African-American children with ADHD. J Natl Med Assoc 97: 11S-16S. (Pubitemid 41429050)
62. Taylor SF, Welsh RC, Wager TD, Phan KL, Fitzgerald KD, Gehring WJ (2004). A functional neuroimaging study of motivation and executive function. NeuroImage 21: 1045-1054. (Pubitemid 38314967)
63. Tomasi D, Volkow ND, Wang RL, Telang F, Wang GJ, Chang L et al (2009). Dopamine transporters in striatum correlate with deactivation in the default mode network during visuospatial attention. PLoS One 4.
64. Trommer BL, Hoeppner JAB, Zecker SG (1991). The go-no go test in attention-deficit disorder is sensitive to methylphenidate. J Child Neurol 6: S128-S131.
65. 2O PET study in healthy volunteers. Hum Brain Mapp 28: 625-635. (Pubitemid 47052616)
66. Vijayraghavan S, Wang M, Birnbaum SG, Williams GV, Arnsten AFT (2007). Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat Neurosci 10: 376-384.
67. Volkow ND, Wang GJ, Fowler JS, Telang F, Maynard L, Logan J et al (2004). Evidence that methylphenidate enhances the saliency of a mathematical task by increasing dopamine in the human brain. Am J Psychiatry 161: 1173-1180. (Pubitemid 38859165)
68. Wargin W, Patrick K, Kilts C, Gualtieri CT, Ellington K, Mueller RA et al (1983). Pharmacokinetics of methylphenidate in man, rat and monkey. J Pharmacol Exp Therap 226: 382-386. (Pubitemid 13041511)
69. Weissman DH, Roberts KC, Visscher KM, Woldorff MG (2006). The neural bases of momentary lapses in attention. Nat Neurosci 9: 971-978. (Pubitemid 43980513)
70. Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 57: 1336-1346. (Pubitemid 40798553)
71. Wong DT, Threlkeld PG, Best KL, Bymaster FP (1982). A new inhibitor of norepinephrine uptake devoid of affinity for receptors in rat-brain. J Pharmacol Exp Therap 222: 61-65. (Pubitemid 12096999)
72. Yu AJ, Dayan P (2005). Uncertainty, neuromodulation, and attention. Neuron 46: 681-692. (Pubitemid 40797391)