L-dopa modulates functional connectivity in striatal cognitive and motor networks: A double-blind placebo-controlled study

Journal of Neuroscience

Volumn 29, Issue 22, 2009, Pages 7364-7378

  Kelly, Clare ^a   De Zubicaray, Greig ^b   Di Martino, Adriana ^a,c   Copland, David A ^b   Reiss, Philip T ^a,d   Klein, Donald F ^a,d,e   Castellanos, F Xavier ^a,d   Milham, Michael P ^a   McMahon, Katie ^b  

^a NEW YORK UNIVERSITY CHILD STUDY CENTER   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF CAGLIARI   (Italy)

^d NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^e New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENSERAZIDE PLUS LEVODOPA; DOPAMINE; LEVODOPA; PLACEBO;

ADULT; ARTICLE; BLOOD SAMPLING; CAUDATE NUCLEUS; CLINICAL ARTICLE; CLINICAL TRIAL; COGNITION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BLOOD LEVEL; DOPAMINERGIC TRANSMISSION; DOUBLE BLIND PROCEDURE; DRUG EFFECT; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN TISSUE; MALE; MOTIVATION; MOTONEURON; MOTOR ACTIVITY; MOTOR PERFORMANCE; NERVE CELL NETWORK; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUTAMEN; RANDOMIZED CONTROLLED TRIAL;

ADULT; BENSERAZIDE; BRAIN MAPPING; COGNITION; CORPUS STRIATUM; DOPAMINE AGENTS; DOUBLE-BLIND METHOD; DRUG COMBINATIONS; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LEVODOPA; MAGNETIC RESONANCE IMAGING; MALE; MOVEMENT; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PROBABILITY;

EID: 66749127280     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0810-09.2009     Document Type: Article

References (78)

1. Achard S, Bullmore ET (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:e17. (Pubitemid 46318379)
2. 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)
3. Andersson JLR, Jenkinson M, Smith SM (2007a) Non-linear optimisation. FMRIB technical report TR07JA1.
4. Andersson JLR, Jenkinson M, Smith SM (2007b) Non-linear registration, aka spatial normalisation. FMRIB technical report TR07JA2.
5. Andrews-Hanna JR, Snyder AZ, Vincent JL, Lustig C, Head D, Raichle ME, Buckner RL (2007) Disruption of large-scale brain systems in advanced aging. Neuron 56:924-935. (Pubitemid 350181355)
6. Angwin AJ, Chenery HJ, Copland DA, Arnott WL, Murdoch BE, Silburn PA (2004) Dopamine and semantic activation: an investigation of masked direct and indirect priming. J Int Neuropsychol Soc 10:15-25. (Pubitemid 38128458)
7. Arnsten AF (2007) Catecholamine and second messenger influences on prefrontal cortical networks of "representational knowledge": a rational bridge between genetics and the symptoms of mental illness. Cereb Cortex 17 [Suppl 1]:i6-i15.
8. Asanuma K, Tang C, Ma Y, Dhawan V, Mattis P, Edwards C, Kaplitt MG, Feigin A, Eidelberg D (2006) Network modulation in the treatment of Parkinson's disease. Brain 129:2667-2678. (Pubitemid 44522100)
9. Bäckman L, Nyberg L, Lindenberger U, Li SC, Farde L (2006) The correlative triad among aging, dopamine, and cognition: current status and future prospects. Neurosci Biobehav Rev 30:791-807. (Pubitemid 44389711)
10. Bamford NS, Zhang H, Schmitz Y, Wu NP, Cepeda C, Levine MS, Schmauss C, Zakharenko SS, Zablow L, Sulzer D (2004a) Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42:653-663. (Pubitemid 38639883)
11. Bamford NS, Robinson S, Palmiter RD, Joyce JA, Moore C, Meshul CK (2004b) Dopamine modulates release from corticostriatal terminals. J Neurosci 24:9541-9552. (Pubitemid 39441508)
12. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
13. Bond A, Lader M (1974) The use of analog scales in rating subjects feelings. Br J Med Psychol 47:211-218.
14. Brennan AR, Arnsten AF (2008) Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function. Ann N Y Acad Sci 1129:236-245.
15. Buhmann C, Glauche V, Stürenburg HJ, Oechsner M, Weiller C, Büchel C (2003) Pharmacologically modulated fMRI-cortical responsiveness to levodopa in drug-naive hemiparkinsonian patients. Brain 126:451-461. (Pubitemid 36172749)
16. Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, Kirsch A, Shaw D, Shehzad Z, Di Martino A, Biswal BB, Sonuga-Barke EJS, Rotrosen J, Adler LA, Milham MP (2008) Cingulate-precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 63:332-337.
17. Cepeda C, Levine MS (1998) Dopamine and N-methyl-D-aspartate receptor interactions in the neostriatum. Dev Neurosci 20:1-18.
18. Cools R (2006) Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 30:1-23. (Pubitemid 41779404)
19. Cools R, Frank MJ, Gibbs SE, Miyakawa A, Jagust W, D'Esposito M (2009) Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J Neurosci 29:1538-1543.
20. Copland DA, McMahon KL, Silburn PA, de Zubicaray GI (2009) Dopaminergic neuromodulation of semantic processing: a 4-T fMRI study with levodopa. Cereb Cortex, in press.
21. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162-173. (Pubitemid 26266657)
22. Damoiseaux JS, Beckmann CF, Arigita EJ, Barkhof F, Scheltens P, Stam CJ, Smith SM, Rombouts SA (2008) Reduced resting-state brain activity in the "default network" in normal aging. Cereb Cortex 18:1856-1864.
23. Di Martino A, Scheres A, Margulies DS, Kelly AM, Uddin LQ, Shehzad Z, Biswal B, Walters JR, Castellanos FX, Milham MP (2008) Functional connectivity of human striatum: a resting state FMRI study. Cereb Cortex 18:2735-2747.
24. Drevets WC, Price JC, Kupfer DJ, Kinahan PE, Lopresti B, Holt D, Mathis C (1999) PET measures of amphetamine-induced dopamine release in ventral versus dorsal striatum. Neuropsychopharmacology 21:694-709.
25. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102:9673-9678. (Pubitemid 40981739)
26. Fransson P (2005) Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp 26:15-29. (Pubitemid 41232552)
27. Fransson P (2006) How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations. Neuropsychologia 44:2836-2845. (Pubitemid 44511969)
28. Ghosh A, Rho Y, McIntosh AR, Kötter R, Jirsa VK (2008) Noise during rest enables the exploration of the brain's dynamic repertoire. PLoS Comput Biol 4:e1000196.
29. Gonon F (2009) The dopaminergic hypothesis of attention-deficit/ hyperactivity disorder needs re-examining. Trends Neurosci 32:2-8.
30. Graybiel AM (2008) Habits, rituals, and the evaluative brain. Annu Rev Neurosci 31:359-387.
31. Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A 101:4637-4642. (Pubitemid 38437463)
32. Haber SN (2003) The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317-330. (Pubitemid 38077155)
33. Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT (2006) Brain connectivity related to working memory performance. J Neurosci 26:13338-13343. (Pubitemid 46011644)
34. Haslinger B, Erhard P, Kämpfe N, Boecker H, Rummeny E, Schwaiger M, Conrad B, Ceballos-Baumann AO (2001) Event-related functional magnetic resonance imaging in Parkinson's disease before and after levodopa. Brain 124:558-570. (Pubitemid 32221323)
35. Heimer L, Alheid GF (1991) Piecing together the puzzle of basal forebrain anatomy. Adv Exp Med Biol 295:1-42.
36. Hershey T, Black KJ, Hartlein J, Braver TS, Barch DM, Carl JL, Perlmutter JS (2004) Dopaminergic modulation of response inhibition: an fMRI study. Brain Res Cogn Brain Res 20:438-448. (Pubitemid 38960676)
37. Honey GD, Suckling J, Zelaya F, Long C, Routledge C, Jackson S, Ng V, Fletcher PC, Williams SC, Brown J, Bullmore ET (2003) Dopaminergic drug effects on physiological connectivity in a human cortico-striatothalamic system. Brain 126:1767-1781. (Pubitemid 36917336)
38. Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL (2005) The cerebellum communicates with the basal ganglia. Nat Neurosci 8:1491-1493. (Pubitemid 41573660)
39. Ichinohe N, Mori F, Shoumura K (2000) A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat. Brain Res 880:191-197.
40. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143-156. (Pubitemid 35282800)
41. 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. (Pubitemid 35317016)
42. Kahn I, Andrews-Hanna JR, Vincent JL, Snyder AZ, Buckner RL (2008) Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. J Neurophysiol 100:129-139.
43. Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2008) Competition between functional brain networks mediates behavioral variability. Neuroimage 39:527-537. (Pubitemid 350102198)
44. Kennedy DN, Lange N, Makris N, Bates J, Meyer J, Caviness VS Jr (1998) Gyri of the human neocortex: an MRI-based analysis of volume and variance. Cereb Cortex 8:372-384. (Pubitemid 28280741)
45. Kischka U, Kammer T, Maier S, Weisbrod M, Thimm M, Spitzer M (1996) Dopaminergic modulation of semantic network activation. Neuropsychologia 34:1107-1113. (Pubitemid 26345288)
46. Krain AL, Castellanos FX (2006) Brain development and ADHD. Clin Psychol Rev 26:433-444.
47. Laruelle M, Kegeles LS, Abi-Dargham A (2003) Glutamate, dopamine, and schizophrenia: from pathophysiology to treatment. Ann N Y Acad Sci 1003:138-158. (Pubitemid 38083052)
48. Li SJ, Biswal B, Li Z, Risinger R, Rainey C, Cho JK, Salmeron BJ, Stein EA (2000) Cocaine administration decreases functional connectivity in human primary visual and motor cortex as detected by functional MRI. Magn Reson Med 43:45-51. (Pubitemid 30027111)
49. Makris N, Meyer JW, Bates JF, Yeterian EH, Kennedy DN, Caviness VS (1999) MRI-Based topographic parcellation of human cerebral white matter and nuclei II. Rationale and applications with systematics of cerebral connectivity. Neuroimage 9:18-45.
50. Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2007) Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37:579-588. (Pubitemid 47444255)
51. Mattay VS, Tessitore A, Callicott JH, Bertolino A, Goldberg TE, Chase TN, Hyde TM, Weinberger DR (2002) Dopaminergic modulation of cortical function in patients with Parkinson's disease. Ann Neurol 51:156-164. (Pubitemid 34111437)
52. McKiernan KA, Kaufman JN, Kucera-Thompson J, Binder JR (2003) A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. J Cogn Neurosci 15:394-408. (Pubitemid 36438949)
53. Montague PR, Hyman SE, Cohen JD (2004) Computational roles for dopamine in behavioural control. Nature 431:760-767. (Pubitemid 39434064)
54. Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anticorrelated networks introduced? Neuroimage 44:893-905.
55. Nagano-Saito A, Leyton M, Monchi O, Goldberg YK, He Y, Dagher A (2008) Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. J Neurosci 28:3697-3706.
56. Neychev VK, Fan X, Mitev VI, Hess EJ, Jinnah HA (2008) The basal ganglia and cerebellum interact in the expression of dystonic movement. Brain 131:2499-2509.
57. Nicola SM, Woodward Hopf F, Hjelmstad GO (2004) Contrast enhancement: a physiological effect of striatal dopamine? Cell Tissue Res 318:93-106.
58. Olanow W, Schapira AH, Rascol O (2000) Continuous dopamine-receptor stimulation in early Parkinson's disease. Trends Neurosci 23:S117-126.
59. Palmer SJ, Eigenraam L, Hoque T, McCaig RG, Troiano A, McKeown MJ (2009) Levodopa-sensitive, dynamic changes in effective connectivity during simultaneous movements in Parkinson's disease. Neuroscience 158:693-704.
60. Polli FE, Barton JJ, Cain MS, Thakkar KN, Rauch SL, Manoach DS (2005) Rostral and dorsal anterior cingulate cortex make dissociable contributions during antisaccade error commission. Proc Natl Acad Sci U S A 102:15700-15705. (Pubitemid 41528119)
61. Postuma RB, Dagher A (2006) Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. Cereb Cortex 16:1508-1521. (Pubitemid 44526974)
62. Robbins TW (2005) Chemistry of the mind: neurochemical modulation of prefrontal cortical function. J Comp Neurol 493:140-146. (Pubitemid 41636196)
63. Rolls ET, Thorpe SJ, Boytim M, Szabo I, Perrett DI (1984) Responses of striatal neurons in the behaving monkey. 3. Effects of iontophoretically applied dopamine on normal responsiveness. Neuroscience 12:1201-1212.
64. Rowe JB, Hughes L, Ghosh BC, Eckstein D, Williams-Gray CH, Fallon S, Barker RA, Owen AM (2008) Parkinson's disease and dopaminergic therapy-differential effects on movement, reward and cognition. Brain 131:2094-2105.
65. Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI atlas of the human cerebellum. San Diego: Academic.
66. Shehzad Z, Kelly AM, Reiss PT, Gee DG, Gotimer K, Lee SH, Margulies DS, Roy AK, Biswal BB, Petkova E, Castellanos FX, Milham MP (2009) The resting brain: unconstrained yet reliable. Cereb Cortex, in press.
67. Shulman GL, Fiez JA, Corbetta M, Buckner RL, Miezin FM, Raichle ME, Petersen SE (1997) Common blood flow changes across visual tasks. 2. Decreases in cerebral cortex. J Cogn Neurosci 9:648-663.
68. Skudlarski P, Jaqannathan K, Calhoun VD, Hampson M, Skudlarska BA, Pearlson G (2008) Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. Neuroimage 43:554-561.
69. Sorg C, Riedl V, Mühlau M, Calhoun VD, Eichele T, Läer L, Drzezga A, Förstl H, Kurz A, Zimmer C, Wohlschläger AM (2007) Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A 104:18760-18765. (Pubitemid 350210770)
70. Stark DE, Margulies DS, Shehzad ZE, Reiss P, Kelly AM, Uddin LQ, Gee DG, Roy AK, Banich MT, Castellanos FX, Milham MP (2008) Regional variation in interhemispheric coordination of intrinsic hemodynamic fluctuations. J Neurosci 28:13754-13764.
71. Tomasi D, Ernst T, Caparelli EC, Chang L (2006) Common deactivation patterns during working memory and visual attention tasks: an intrasubject fMRI study at 4 Tesla. Hum Brain Mapp 27:694-705. (Pubitemid 44182457)
72. Tripp G, Wickens JR (2008) Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD. J Child Psychol Psychiatry 49:691-704.
73. Vaughan JT, Adriany G, Garwood M, Yacoub E, Duong T, DelaBarre L, Andersen P, Ugurbil K (2002) Detunable transverse electromagnetic (TEM) volume coil for high-field NMR. Magn Reson Med 47:990-1000.
74. Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006) Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:3517-3531. (Pubitemid 44837893)
75. Weissman DH, Roberts KC, Visscher KM, Woldorff MG (2006) The neural bases of momentary lapses in attention. Nat Neurosci 9:971-978. (Pubitemid 43980513)
76. Yu H, Sternad D, Corcos DM, Vaillancourt DE (2007) Role of hyperactive cerebellum and motor cortex in Parkinson's disease. Neuroimage 35:222-233. (Pubitemid 46240941)
77. Zaitsev M, Hennig J, Speck O (2003) Automated onlnie EPI distortion correction for fMRI applications. In: Proceedings of the 11th annual meeting of the International Society for Magnetic Resonance in Medicine, July 10-16, 2003, Toronto, ON, Canada, 1042 [abstr].
78. Zhou Y, Liang M, Tian L, Wang K, Hao Y, Liu H, Liu Z, Jiang T (2007) Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophr Res 97:194-205. (Pubitemid 350088382)