FMRI of cocaine self-administration in macaques reveals functional inhibition of basal ganglia

Neuropsychopharmacology

Volumn 36, Issue 6, 2011, Pages 1187-1198

  Mandeville, Joseph B ^a,b   Choi, Ji Kyung ^a,b   Jarraya, Bechir ^a,b,c   Rosen, Bruce R ^a,b   Jenkins, Bruce G ^a,b   Vanduffel, Wim ^a,b,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c INSERM   (France)

^d KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

CBV; cocaine; fMRI; monkey; NHP; self administration

Indexed keywords

COCAINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BASAL GANGLION; BRAIN BLOOD VOLUME; BRAIN REGION; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE METABOLISM; HUMAN; MACACA; MAGNET; MOTOR CORTEX; NONHUMAN; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIMATE; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; REINFORCEMENT; SENSORY STIMULATION; TASK PERFORMANCE;

ANIMALS; BASAL GANGLIA; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; COCAINE; COCAINE-RELATED DISORDERS; CONTRAST MEDIA; DOPAMINE UPTAKE INHIBITORS; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MOTOR CORTEX; NEURAL INHIBITION; PREFRONTAL CORTEX; SELF ADMINISTRATION;

EID: 79954615467     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2011.1     Document Type: Article

References (91)

1. Bartlett SE, Enquist J, Hopf FW, Lee JH, Gladher F, Kharazia V et al (2005). Dopamine responsiveness is regulated by targeted sorting of D2 receptors. Proc Natl Acad Sci USA 102: 11521-11526. (Pubitemid 41153852)
2. Beveridge TJ, Smith HR, Nader MA, Porrino LJ (2009). Abstinence from chronic cocaine self-administration alters striatal dopa-mine systems in rhesus monkeys. Neuropsychopharmacology 34: 1162-1171.
3. Black KJ, Gado MH, Perlmutter JS (1997). PET measurement of dopamine D2 receptor-mediated changes in striatopallidal function. J Neurosci 17: 3168-3177. (Pubitemid 27175829)
4. Boeuf J, Trigo JM, Moreau PH, Lecourtier L, Vogel E, Cassel JC et al (2009). Attenuated behavioural responses to acute and chronic cocaine in GASP-1-deficient mice. Eur J Neurosci 30: 860-868.
5. Booze R, Lehner A, Wallace D, Welch M, Mactutus C (1997). Dose-response cocaine pharmacokinetics and metabolite profile following intravenous administration and arterial sampling in unanesthetized, freely moving male rats. Neurotoxicol Teratol 19: 7-15. (Pubitemid 27146399)
6. Bradberry CW (2000). Acute and chronic dopamine dynamics in a nonhuman primate model of recreational cocaine use. J Neurosci 20: 7109-7115.
7. Bradberry CW (2007). Cocaine sensitization and dopamine mediation of cue effects in rodents, monkeys, and humans: areas of agreement, disagreement, and implications for addiction. Psychopharmacology (Berl) 191: 705-717. (Pubitemid 46355892)
8. Bradberry CW, Rubino SR (2006). Dopaminergic responses to self-administered cocaine in Rhesus monkeys do not sensitize following high cumulative intake. Eur J Neurosci 23: 2773-2778. (Pubitemid 43801469)
9. Breiter H, Gollub RL, Weisskoff RM, Kennedy D, Makris N, Berke J et al (1997). Acute effects of cocaine on human brain activity and emotion. Neuron 19: 591-611. (Pubitemid 27430747)
10. 3H]Nisoxetine binding sites in the cat brain: an autoradio-graphic study. Neuroscience 69: 259-270.
11. Chen YC, Choi JK, Andersen SL, Rosen BR, Jenkins BG (2005). Mapping dopamine D2/D3 receptor function using pharmacological magnetic resonance imaging. Psychopharmacology (Berl) 180: 705-715. (Pubitemid 41317866)
12. Chen YI, Brownell AL, Galpern W, Isacson O, Bogdanov M, Beal MF et al (1999). Detection of dopaminergic cell loss and neural transplantation using pharmacological MRI, PET and behavioral assessment. Neuroreport 10: 2881-2886. (Pubitemid 29507746)
13. Chen YI, Choi JK, Xu H, Ren J, Andersen SL, Jenkins BG (2010). Pharmacologic neuroimaging of the ontogeny of dopamine receptor function. Dev Neurosci 32: 125-138.
14. Chen YI, Mandeville JB, Nguyen TV, Talele A, Cavagna F, Jenkins BG (2001). Improved mapping of pharmacologically induced neuronal activation using the IRON technique with superparamagnetic iron blood pool agents. J Magn Reson Imaging 14: 517-524. (Pubitemid 33029537)
15. Choi JK, Chen YI, Hamel E, Jenkins BG (2006). Brain hemo-dynamic changes mediated by dopamine receptors: role of the cerebral microvasculature in dopamine-mediated neurovascular coupling. NeuroImage 30: 700-712.
16. Choi JK, Deng H, Vanduffel W, Mandeville JB (2009). fMRI of cocaine self-administration in non-human primates. Paper Presented at the International Society of Magnetic Resonance Medicine, Honolulu, HI
17. Dumartin B, Caille I, Gonon F, Bloch B (1998). Internalization of D1 dopamine receptor in striatal neurons in vivo as evidence of activation by dopamine agonists. J Neurosci 18: 1650-1661. (Pubitemid 28103073)
18. Evans SM, Cone EJ, Henningfield JE (1996). Arterial and venous cocaine plasma concentrations in humans: relationship to route of administration, cardiovascular effects and subjective effects. J Pharmacol Exp Ther 279: 1345-1356. (Pubitemid 27166783)
19. Febo M, Segarra AC, Nair G, Schmidt K, Duong TQ, Ferris CF (2005). The neural consequences of repeated cocaine exposure revealed by functional MRI in awake rats. Neuropsychopharmacology 30: 936-943. (Pubitemid 40570909)
20. Ferry AT, Ongur D, An X, Price JL (2000). Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol 425: 447-470. (Pubitemid 30659209)
21. Flory GS, Woods JH (2003). The ascending limb of the cocaine dose-response curve for reinforcing effect in rhesus monkeys. Psychopharmacology (Berl) 166: 91-94. (Pubitemid 36286725)
22. Fowler JS, Volkow ND, Wolf AP, Dewey SL, Schlyer DJ, MacGregor RR et al (1989). Mapping cocaine binding sites in human and baboon brain in vivo. Synapse 4: 371-377. (Pubitemid 20044793)
23. Gatley SJ, Volkow ND, Wang GJ, Fowler JS, Logan J, Ding YS et al (2005). PET imaging in clinical drug abuse research. Curr Pharm Des 11: 3203-3219. (Pubitemid 41300772)
24. 2+ regulates amphetamine-induced dopamine efflux and currents mediated by the human dopamine transporter. Mol Pharmacol 66: 137-143. (Pubitemid 38822096)
25. Goldman-Rakic PS, Bergson C, Krimer LS, Lidow MS, Williams SM, Wiliams GV (1999). Chapter V: the primate mesocortical dopamine system. In: Bloom FE, Bjorklund A, Hokfelt T (eds). Handbook of Chemical Neuroanatomy. Amsterdam: Elsevier. pp 403-428.
26. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J et al (2002). Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47: 1202-1210. (Pubitemid 34587412)
27. Haber SN, Calzavara R (2009). The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78: 69-74.
28. Hall H, Sedvall G, Magnusson O, Kopp J, Halldin C, Farde L (1994). Distribution of D1- and D2-dopamine receptors, and dopamine and its metabolites in the human brain. Neuropsychopharmacology 11: 245-256. (Pubitemid 24372813)
29. Howell LL, Hoffman JM, Votaw JR, Landrum AM, Wilcox KM, Lindsey KP (2002). Cocaine-induced brain activation determined by positron emission tomography neuroimaging in conscious rhesus monkeys. Psychopharmacology (Berl) 159: 154-160. (Pubitemid 34146558)
30. Howell LL, Votaw JR, Goodman MM, Lindsey KP (2010). Cortical activation during cocaine use and extinction in rhesus monkeys. Psychopharmacology (Berl) 208: 191-199.
31. 11C]AFM. J Cereb Blood Flow Metab 22: 1377-1398. (Pubitemid 35285095)
32. 3H-SCH 23390 to dopamine D-1 receptors. Correlation to other D-1 and D-2 measures and effect of selective lesions. J Neural Transm 68: 171-189. (Pubitemid 17008058)
33. Jakovcevic D, Harder DR (2007). Role of astrocytes in matching blood flow to neuronal activity. Curr Top Dev Biol 79: 75-97.
34. Jarraya B, Arsenault J, Van Kerkoerle T, Ekstrom L, Mandeville JB, Marota JJA et al (2007). Predictive reward value related fMRI activations in macaque. Paper Presented at the Society for Neuroscience, San Diego, CA
35. Jenkins BG, Sanchez-Pernaute R, Brownell AL, Chen YC, Isacson O (2004). Mapping dopamine function in primates using pharmacologic magnetic resonance imaging. J Neurosci 24: 9553-9560. (Pubitemid 39441509)
36. Kalivas PW, Stewart J (1991). Dopamine transmission in the initiation and expression of drug- and stress-induced sensitiza-tion of motor activity. Brain Res Brain Res Rev 16: 223-244.
37. Kirkland Henry P, Davis M, Howell LL (2009). Effects of cocaine self-administration history under limited and extended access conditions on in vivo striatal dopamine neurochemistry and acoustic startle in rhesus monkeys. Psychopharmacology (Berl) 205: 237-247.
38. Kufahl P, Li Z, Risinger R, Rainey C, Piacentine L, Wu G et al (2008). Expectation modulates human brain responses to acute cocaine: a functional magnetic resonance imaging study. Biol Psychiatry 63: 222-230. (Pubitemid 350299317)
39. Kufahl PR, Li Z, Risinger RC, Rainey CJ, Wu G, Bloom AS et al (2005). Neural responses to acute cocaine administration in the human brain detected by fMRI. NeuroImage 28: 904-914. (Pubitemid 41713625)
40. Leite FP, Tsao D, Vanduffel W, Fize D, Sasaki Y, Wald LL et al (2002). Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. NeuroImage 16: 283-294. (Pubitemid 34852447)
41. Lewis JW, Van Essen DC (2000). Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol 428: 79-111.
42. London ED, Cascella NG, Wong DF, Phillips RL, Dannals RF, Links JM et al (1990). Cocaine-induced reduction of glucose utilization in human brain. Arch Gen Psychiatry 47: 567-574.
43. Lu H, Xi ZX, Gitajn L, Rea W, Yang Y, Stein EA (2007). Cocaine-induced brain activation detected by dynamic manganese-enhanced magnetic resonance imaging (MEMRI). Proc Natl Acad Sci USA 104: 2489-2494. (Pubitemid 46391423)
44. Lyons D, Friedman DP, Nader MA, Porrino LJ (1996). Cocaine alters cerebral metabolism within the ventral striatum and limbic cortex of monkeys. J Neurosci 16: 1230-1238. (Pubitemid 26140879)
45. Madras BK, Fahey MA, Canfield DR, Spealman RD (1988). D1 and D2 dopamine receptors in caudate-putamen of nonhuman primates (Macaca fascicularis). J Neurochem 51: 934-943.
46. Mandeville JB, Ekstrom L, Marota JJA, Jenkins BG, Vanduffel W (2005). Contrast-enhanced fMRI of cocaine action in awake non-human primate. Paper Presented at the International Society of Magnetic Resonance Medicine, Miami, FL.
47. Mandeville JB, Jenkins BG, Chen YC, Choi JK, Kim YR, Belen D et al (2004). Exogenous contrast agent improves sensitivity of gradient-echo functional magnetic resonance imaging at 9.4 T. Magn Reson Med 52: 1272-1281. (Pubitemid 39612815)
48. Mandeville JB, Jenkins BG, Kosofsky BE, Moskowitz MA, Rosen BR, Marota JJA (2001). Regional sensitivity and coupling of BOLD and CBV changes during stimulation of rat brain. Magn Reson Med 45: 443-447. (Pubitemid 32173271)
49. Mandeville JB, Marota JJA, Kosofsky BE, Keltner JR, Weissleder R, Rosen BR et al (1998). Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn Reson Med 39: 615-624. (Pubitemid 28150996)
50. Marota JJA, Mandeville JB, Weisskoff RM, Moskowitz MA, Rosen BR, Kosofsky BE (2000). Cocaine activation discriminates dopamergic projections by temporal response: an fMRI study in rat. NeuroImage 11: 13-23. (Pubitemid 30090152)
51. Martinez D, Narendran R, Foltin RW, Slifstein M, Hwang DR, Broft A et al (2007). Amphetamine-induced dopamine release: markedly blunted in cocaine dependence and predictive of the choice to self-administer cocaine. Am J Psychiatry 164: 622-629. (Pubitemid 46650194)
52. 11C]WIN-35,428. J Neurosci 18: 8417-8422. (Pubitemid 28465016)
53. McLaren DG, Kosmatka KJ, Oakes TR, Kroenke CD, Kohama SG, Matochik JA et al (2009). A population-average MRI-based atlas collection of the rhesus macaque. NeuroImage 45: 52-59.
54. Moore RJ, Vinsant SL, Nader MA, Porrino LJ, Friedman DP (1998a). Effect of cocaine self-administration on dopamine D2 receptors in rhesus monkeys. Synapse 30: 88-96. (Pubitemid 28361187)
55. Moore RJ, Vinsant SL, Nader MA, Porrino LJ, Friedman DP (1998b). Effect of cocaine self-administration on striatal dopamine D1 receptors in rhesus monkeys. Synapse 28: 1-9. (Pubitemid 128770597)
56. Nader MA, Daunais JB, Moore T, Nader SH, Moore RJ, Smith HR et al (2002). Effects of cocaine self-administration on striatal dopamine systems in rhesus monkeys: initial and chronic exposure. Neuropsychopharmacology 27: 35-46. (Pubitemid 34626741)
57. Nader MA, Morgan D, Gage HD, Nader SH, Calhoun TL, Buchheimer N et al (2006). PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nat Neurosci 9: 1050-1056. (Pubitemid 44264918)
58. Narendran R, Martinez D (2008). Cocaine abuse and sensitization of striatal dopamine transmission: a critical review of the preclinical and clinical imaging literature. Synapse 62: 851-869.
59. Nguyen TV, Brownell AL, Iris Chen YC, Livni E, Coyle JT, Rosen BR et al (2000). Detection of the effects of dopamine receptor supersensitivity using pharmacological MRI and correlations with PET. Synapse 36: 57-65. (Pubitemid 30134125)
60. Nikulina EM, Kapralova NS (1992). Role of dopamine receptors in the regulation of aggression in mice; relationship to genotype. Neurosci Behav Physiol 22: 364-369.
61. Pfeuffer J, Shmuel A, Keliris GA, Steudel T, Merkle H, Logothetis NK (2007). Functional MR imaging in the awake monkey: effects of motion on dynamic off-resonance and processing strategies. Magn Reson Imaging 25: 869-882. (Pubitemid 47081373)
62. Piggott MA, Marshall EF, Thomas N, Lloyd S, Court JA, Jaros E et al (1999). Dopaminergic activities in the human striatum: rostrocaudal gradients of uptake sites and of D1 and D2 but not of D3 receptor binding or dopamine. Neuroscience 90: 433-445. (Pubitemid 29161394)
63. Porrino LJ (1993). Functional consequences of acute cocaine treatment depend on route of administration. Psychopharmacology 112: 343-351. (Pubitemid 23278299)
64. Puglisi-Allegra S, Cabib S (1988). Pharmacological evidence for a role of D2 dopamine receptors in the defensive behavior of the mouse. Behav Neural Biol 50: 98-111.
65. Richfield EK, Young AB, Penney JB (1989). Comparative distributions of dopamine D-1 and D-2 receptors in the cerebral cortex of rats, cats, and monkeys. J Comp Neurol 286: 409-426. (Pubitemid 19223569)
66. Risinger RC, Salmeron BJ, Ross TJ, Amen SL, Sanfilipo M, Hoffmann RG et al (2005). Neural correlates of high and craving during cocaine self-administration using BOLD fMRI. NeuroImage 26: 1097-1108. (Pubitemid 40806488)
67. Ritz MC, Cone EJ, Kuhar MJ (1990). Cocaine inhibition of ligand binding at dopamine, norepinephrine and serotonin transporters: a structure-activity study. Life Sci 46: 635-645. (Pubitemid 20056887)
68. Rogers KJ, Nahorski SR (1973). Depression of cerebral metabolism by stimulant doses of cocaine. Brain Res 57: 255-258.
69. Saleem KS, Logothetis NK (2006). A Combined MRI and Histology Atlas of the Rhesus Monkey Brain. Academic Press: London, UK.
70. Sanchez-Pernaute R, Jenkins BG, Choi JK, Iris Chen YC, Isacson O (2007). In vivo evidence of D3 dopamine receptor sensitization in parkinsonian primates and rodents with L-DOPA-induced dyskinesias. Neurobiol Dis 27: 220-227. (Pubitemid 47088981)
71. Schmidt KF, Febo M, Shen Q, Luo F, Sicard KM, Ferris CF et al (2006). Hemodynamic and metabolic changes induced by cocaine in anesthetized rat observed with multimodal functional MRI. Psychopharmacology (Berl) 185: 479-486.
72. Schwarz AJ, Zocchi A, Reese T, Gozzi A, Garzotti M, Varnier G et al (2004). Concurrent pharmacological MRI and in situ microdialysis of cocaine reveal a complex relationship between the central hemodynamic response and local dopamine concentration. NeuroImage 23: 296-304. (Pubitemid 39119460)
73. 18F] FMeNER-D2. Psychopharmacology (Berl) 188: 119-127. (Pubitemid 44268248)
74. Sharkey J, McBean DE, Kelly PAT (1991). Acute cocaine administration: effects on local cerebral blood flow and metabolic demand in the rat. Brain Res 548: 310-314.
75. Stein EA, Fuller SA (1993). Cocaine's time action profile on regional cerebral blood flow in the rat. Brain Res 626: 117-126. (Pubitemid 23306819)
76. Sweidan S, Edinger H, Siegel A (1990). The role of D1 and D2 receptors in dopamine agonist-induced modulation of affective defense behavior in the cat. Pharmacol Biochem Behav 36: 491-499. (Pubitemid 20223013)
77. Thanos PK, Michaelides M, Benveniste H, Wang GJ, Volkow ND (2008). The effects of cocaine on regional brain glucose metabolism is attenuated in dopamine transporter knockout mice. Synapse 62: 319-324. (Pubitemid 351451799)
78. Thompson D, Martini L, Whistler JL (2010). Altered ratio of D1 and D2 dopamine receptors in mouse striatum is associated with behavioral sensitization to cocaine. PLoS One 5: e11038.
79. Tsukada H, Nishiyama S, Kakiuchi T, Ohba H, Sato K, Harada N (2001). Ketamine alters the availability of striatal dopamine transporter as measured by [(11)C]betacFT and [(11)C]betacIT-FE in the monkey brain. Synapse 42: 273-280. (Pubitemid 33027301)
80. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001). An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8: 443-459. (Pubitemid 32847795)
81. Vanduffel W, Fize D, Mandeville JB, Nelissen K, Van Hecke P, Rosen BR et al (2001). Visual motion processing investigated using contrast-enhanced fMRI in awake behaving monkeys. Neuron 32: 565-577. (Pubitemid 33145192)
82. Vanduffel W, Fize D, Peuskens H, Denys K, Sunaert S, Todd JT et al (2002). Extracting 3D from motion: differences in human and monkey intraparietal cortex. Science 298: 413-415. (Pubitemid 35176349)
83. Volkow ND, Fowler JS, Wang G-J, Hitzemann R, Logan J, Schlyer DJ et al (1993). Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14: 169-177. (Pubitemid 23157765)
84. Volkow ND, Fowler JS, Wolf AP, Schlyer D, Shiue C-Y, Alpert R et al (1990). Effects of chronic cocaine abuse on postsynaptic dopamine receptors. Am J Psychiatry 147: 719-724. (Pubitemid 20188509)
85. Volkow ND, Wang G-J, Fowler JS, Logan J, Gatley SJ, Hitzemann R et al (1997). Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 386: 830-833. (Pubitemid 27181256)
86. Ward AS, Haney M, Fischman MW, Foltin RW (1997). Binge cocaine self-administration in humans: intravenous cocaine. Psychopharmacology (Berl) 132: 375-381. (Pubitemid 27373479)
87. Weed MR, Woolverton WL, Paul IA (1998). Dopamine D1 and D2 receptor selectivities of phenyl-benzazepines in rhesus monkey striata. Eur J Pharmacol 361: 129-142. (Pubitemid 28522167)
88. Weerts EM, Fantegrossi WE, Goodwin AK (2007). The value of nonhuman primates in drug abuse research. Exp Clin Psychopharmacol 15: 309-327. (Pubitemid 47445259)
89. Worsley KJ, Liao CH, Aston J, Petre V, Duncan GH, Morales F et al (2002). A general statistical analysis for fMRI data. NeuroImage 15: 1-15. (Pubitemid 34852200)
90. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4: 58-73. (Pubitemid 26195721)
91. Zocchi A, Conti G, Orzi F (2001). Differential effects of cocaine on local cerebral glucose utilization in the mouse and in the rat. Neurosci Lett 306: 177-180. (Pubitemid 32530828)