Relationship between impulsivity, prefrontal anticipatory activation, and striatal dopamine release during rewarded task performance

Psychiatry Research - Neuroimaging

Volumn 223, Issue 3, 2014, Pages 244-252

  Weiland, Barbara J ^a,b   Heitzeg, Mary M ^b   Zald, David ^c   Cummiford, Chelsea ^b   Love, Tiffany ^b   Zucker, Robert A ^b   Zubieta, Jon Kar ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Dopamine; FMRI; MPFC; NAcc; PET; Reward

Indexed keywords

DOPAMINE; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; RACLOPRIDE C 11;

ADULT; ANGULAR GYRUS; ANTICIPATION; ARTICLE; BOLD SIGNAL; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; EMOTION; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMPULSIVENESS; LEARNING; MAMMILLARY BODY; NEO PERSONALITY INVENTORY REVISED; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEUS ACCUMBENS; PERSONALITY TEST; PET SCANNER; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECEPTOR BINDING; REWARD; TASK PERFORMANCE;

DOPAMINE; FMRI; MPFC; NACC; PET; REWARD;

ADULT; ANTICIPATION, PSYCHOLOGICAL; CARBON RADIOISOTOPES; CORPUS STRIATUM; DOPAMINE; DOPAMINE ANTAGONISTS; FEMALE; HUMANS; IMPULSIVE BEHAVIOR; INCOME; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; NEOSTRIATUM; NUCLEUS ACCUMBENS; POSITRON-EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; RACLOPRIDE; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; REWARD; TASK PERFORMANCE AND ANALYSIS;

EID: 84905217243     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2014.05.015     Document Type: Article

References (88)

1. Andersen S.L., Teicher M.H. Sex differences in dopamine receptors and their relevance to ADHD. Neuroscience & Biobehavioral Reviews 2000, 24:137-141.
2. Barratt E.S., Stanford M.S., Dowdy L., Liebman M.J., Kent T.A. Impulsive and premeditated aggression: a factor analysis of self-reported acts. Psychiatry Research 1999, 86:163-173.
3. Bechara A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nature Neuroscience 2005, 8:1458-1463.
4. Becker J.B. Direct effect of 17 beta-estradiol on striatum: sex differences in dopamine release. Synapse 1990, 5:157-164.
5. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacology, Biochemistry and Behavior 1999, 64:803-812.
6. Bjork J.M., Smith A.R., Hommer D.W. Striatal sensitivity to reward deliveries and omissions in substance dependent patients. Neuroimage 2008, 42:1609-1621.
7. Breier A., Su T.-P., Saunders R., Carson R.E., Kolachana B.S., de Bartolomeis A., Weinberger D.R., Weisenfeld N., Malhotra A.K., Eckelman W.C., Pickar D. Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: Evidence from a novel positron emission tomography method. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:2569-2574.
8. Brett, M., Anton, J.-L., Valabregue, R., Poline, J.B., 2002. Region of interest analysis using an SPM toolbox, In: Proceedings of the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.
9. Buckholtz J.W., Treadway M.T., Cowan R.L., Woodward N.D., Benning S.D., Li R., Ansari M.S., Baldwin R.M., Schwartzman A.N., Shelby E.S., Smith C.E., Cole D., Kessler R.M., Zald D.H. Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits. Nature Neuroscience 2010, 13:419-421.
10. Buckholtz J.W., Treadway M.T., Cowan R.L., Woodward N.D., Li R., Ansari M.S., Baldwin R.M., Schwartzman A.N., Shelby E.S., Smith C.E., Kessler R.M., Zald D.H. Dopaminergic network differences in human impulsivity. Science 2010, 329:532.
11. Cardinal R.N., Pennicott D.R., Sugathapala C.L., Robbins T.W., Everitt B.J. Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 2001, 292:2499-2501.
12. Carr D.B., Sesack S.R. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. The Journal of Neuroscience 2000, 20:3864-3873.
13. Carson R.E. Precision and accuracy considerations of physiological quantitation in PET. Journal of Cerebral Blood Flow & Metabolism 1991, 11:A45-A50.
14. Carson R.E., Breier A., de Bartolomeis A., Saunders R.C., Su T.P., Schmall B., Der M.G., Pickar D., Eckelman W.C. Quantification of amphetamine-induced changes in [11c] raclopride binding with continuous infusion. Journal of Cerebral Blood Flow & Metabolism 1997, 17:437-447.
15. Castellani B., Rugle L. A comparison of pathological gamblers to alcoholics and cocaine misusers on impulsivity, sensation seeking, and craving. Substance Use & Misuse 1995, 30:275-289.
16. Christie M.J., James L.B., Beart P.M. An excitant amino acid projection from the medial prefrontal cortex to the anterior part of nucleus accumbens in the rat. Journal of Neurochemistry 1985, 45:477-482.
17. Congdon E., Canli T. The endophenotype of impulsivity: reaching consilience through behavioral, genetic, and neuroimaging approaches. Behavioral and Cognitive Neuroscience Reviews 2005, 4:262-281.
18. Cooper J.C., Knutson B. Valence and salience contribute to nucleus accumbens activation. NeuroImage 2008, 39:538-547.
19. Costa P., McRae R. Normal personality assessment in clinical practice: the NEO Personality Inventory. Psychological Assessment 1992, 4:5-13.
20. Costa P.T., McCrae R. The NEO Personality Inventory Manual 1985, Psychological Assessment Resources, Odessa, FL.
21. Crews F.T., Boettiger C.A. Impulsivity, frontal lobes and risk for addiction. Pharmacology, Biochemistry and Behavior 2009, 93:237-247.
22. Cyders M.A., Smith G.T. Emotion-based dispositions to rash action: positive and negative urgency. Psychological Bullein 2008, 134:807-828.
23. Dellu F., Piazza P.V., Mayo W., Le Moal M., Simon H. Novelty-seeking in rats--biobehavioral characteristics and possible relationship with the sensation-seeking trait in man. Neuropsychobiology 1996, 34:136-145.
24. Deutch A.Y., Roth R.H. The determinants of stress-induced activation of the prefrontal cortical dopamine system. Progress in Brain Research 1991, 367-403. Elsevier, Amsterdam, (Chapter 19). H.B.M. Uylings, C.G. C.G. van Eden, J.P.C. de Bruin, M.A. Corner, M.G.P. Feenstra (Eds.).
25. Dick D.M., Smith G., Olausson P., Mitchell S.H., Leeman R.F., O'Malley S.S., Sher K. Understanding the construct of impulsivity and its relationship to alcohol use disorders. Addiction Biology 2010, 15:217-226.
26. Fessler J., Lee S., Olafsson V., Shi H., Noll D. Toeplitz-based iterative image reconstruction for MRI with correction for magnetic field inhomogeneity. IEEE Transactions on Signal Processing 2005, 53:3393-3402.
27. Fischer S., Anderson K.G., Smith G.T. Coping with distress by eating or drinking: role of trait urgency and expectancies. Psychology of Addictive Behaviors 2004, 18:269-274.
28. Fitzgerald H.E., Sullivan L.A., Ham H.P., Zucker R.A., Bruckel S., Schneider A.M., Noll R.B. Predictors of behavior problems in three-year-old sons of alcoholics: early evidence for the onset of risk. Child Development 1993, 64:110-123.
29. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintun M.A., Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance in Medicine 1995, 33:636-647.
30. Friston K., Holmes A., Worsley K., Pline J., Frith C., Frackowiak R. Statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapping 1995, 2:189-210.
31. Glascher J., Adolphs R., Damasio H., Bechara A., Rudrauf D., Calamia M., Paul L.K., Tranel D. Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:14681-14686.
32. Glover G.H., Law C.S. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magnetic Resonance Medicine 2001, 46:515-522.
33. Herman J.P., Guillonneau D., Dantzer R., Scatton B., Semerdjian-Rouquier L., Le Moal M. Differential effects of inescapable footshocks and of stimuli previously paired with inescapable footshocks on dopamine turnover in cortical and limbic areas of the rat. Life Sciences 1982, 30:2207-2214.
34. Howard M.A., Cowell P.E., Boucher J., Broks P., Mayes A., Farrant A., Roberts N. Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport 2000, 11:2931-2935.
35. Innis R.B., Cunningham V.J., Delforge J., Fujita M., Gjedde A., Gunn R.N., Holden J., Houle S., Huang S.-C., Ichise M., Iida H., Ito H., Kimura Y., Koeppe R.A., Knudsen G.M., Knuuti J., Lammertsma A.A., Laruelle M., Logan J., Maguire R.P., Mintun M.A., Morris E.D., Parsey R., Price J.C., Slifstein M., Sossi V., Suhara T., Votaw J.R., Wong D.F., Carson R.E. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. Journal of Cerebral Blood Flow & Metabolism 2007, 27:1533-1539.
36. 123I]IBZM binding to the D2 receptor in nonhuman primates. Synapse 1992, 10:177-184.
37. Johnson B.A. Opportunities, challenges, and successes in the development of medicines for the treatment of addiction. Addiction Medicine: Science and Practice 2010, 1525-1537. Springer Science+Business Media, New York. B.A. Johnson (Ed.).
38. Kaiser A.J., Milich R., Lynam D.R., Charnigo R.J. Negative urgency, distress tolerance, and substance abuse among college students. Addictive Behaviors 2012, 37:1075-1083.
39. Knutson B., Adams C.M., Fong G.W., Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience 2001, 21:RC159.
40. Knutson B., Fong G.W., Adams C.M., Varner J.L., Hommer D. Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 2001, 12:3683-3687.
41. Knutson B., Westdorp A., Kaiser E., Hommer D. FMRI visualization of brain activity during a monetary incentive delay task. Neuroimage 2000, 12:20-27.
42. Kohno, M., Morales, A.M., Ghahremani. D.G., Hellemann, G., London, E.D., 2014. Risky decision making, prefrontal cortex, and mesocorticolimbic functional connectivity in methamphetamine dependence. JAMA Psychiatry, (Published online May 21, 2014). http://dx.doi.org/10.1001/jamapsychiatry.2014.399.
43. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 2001, 24:97-129.
44. Laruelle M. Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. Journal of Cerebral Blood Flow and Metabolism 2000, 20:423-451.
45. Le Moal M., Simon H. Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiological Reviews 1991, 71:155-234.
46. Louilot A., Le Moal M., Simon H. Opposite influences of dopaminergic pathways to the prefrontal cortex or the septum on the dopaminergic transmission in the nucleus accumbens. an in vivo voltammetric study. Neuroscience 1989, 29:45-56.
47. Love T.M., Enoch M.-A., Hodgkinson C.A., Peciña M., Mickey B., Koeppe R.A., Stohler C.S., Goldman D., Zubieta J.-K. Oxytocin gene polymorphisms influence human dopaminergic function in a sex-dependent manner. Biological Psychiatry 2012, 72:198-206.
48. Mawlawi O., Martinez D., Slifstein M., Broft A., Chatterjee R., Hwang D.-R., Huang Y., Simpson N., Ngo K., Van Heertum R., Laruelle M. Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D2 receptor parameter measurements in ventral striatum. Journal of Cerebral Blood Flow and Metabolism 2001, 21:1034-1057.
49. Michalczuk R., Bowden-Jones H., Verdejo-Garcia A., Clark L. Impulsivity and cognitive distortions in pathological gamblers attending the UK National Problem Gambling Clinic: a preliminary report. Psychological Medicine 2011, 41:2625-2635.
50. Minoshima S., Koeppe R.A., Mintun M.A., Berger K.L., Taylor S.F., Frey K.A., Kuhl D.E. Automated detection of the intercommissural line for stereotactic localization of functional brain images. Journal of Nuclear Medicine 1993, 34:322-329.
51. Montague P.R., Berns G.S. Neural economics and the biological substrates of valuation. Neuron 2002, 36:265-284.
52. Munro C.A., McCaul M.E., Wong D.F., Oswald L.M., Zhou Y., Brasic J., Kuwabara H., Kumar A., Alexander M., Ye W., Wand G.S. Sex differences in striatal dopamine release in healthy adults. Biological Psychiatry 2006, 59:966-974.
53. Nordstrom A.L., Olsson H., Halldin C. A PET study of D2 dopamine receptor density at different phases of the menstrual cycle. Psychiatry Research 1998, 83:1-6.
54. 11C]raclopride binding at high D2 receptor occupancy. A PET study in haloperidol-treated patients. Psychiatry Research 1996, 67:163-171.
55. O'Reilly R.C. The what and how of prefrontal cortical organization. Trends in Neurosciences 2010, 33:355-361.
56. Olsen C.M., Duvauchelle C.L. Intra-prefrontal cortex injections of SCH 23390 influence nucleus accumbens dopamine levels 24h post-infusion. Brain Research 2001, 922:80-86.
57. Oswald L.M., Wong D.F., Zhou Y., Kumar A., Brasic J., Alexander M., Ye W., Kuwabara H., Hilton J., Wand G.S. Impulsivity and chronic stress are associated with amphetamine-induced striatal dopamine release. NeuroImage 2007, 36:153-166.
58. 11C]raclopride and a single dynamic scan approach. NeuroImage 2002, 16:1015-1027.
59. Phan K.L., Taylor S.F., Welsh R.C., Ho S.-H., Britton J.C., Liberzon I. Neural correlates of individual ratings of emotional salience: a trial-related fMRI study. NeuroImage 2004, 21:768-780.
60. Phillips A.G., Vacca G., Ahn S. A top-down perspective on dopamine, motivation and memory. Pharmacology, Biochemistry and Behavior 2008, 90:236-249.
61. Preacher K.J., Hayes A.F. SPSS and SAS procedures for estimating indirect effects in simple mediation models. Behavior Research Methods, Instruments, & Computers 2004, 36:717-731.
62. 18F]fallypride in striatal and extrastriatal regions: a PET study. The American Journal of Psychiatry 2006, 163:1639-1641.
63. Ridderinkhof K.R., van den Wildenberg W.P.M., Segalowitz S.J., Carter C.S. Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain and Cognition 2004, 56:129-140.
64. Robinson T.E., Berridge K.C. Addiction. Annual Review of Psychology 2003, 54:25-53.
65. Rogers R.D., Ramnani N., Mackay C., Wilson J.L., Jezzard P., Carter C.S., Smith S.M. Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition. Biological Psychiatry 2004, 55:594-602.
66. Schott B.H., Minuzzi L., Krebs R.M., Elmenhorst D., Lang M., Winz O.H., Seidenbecher C.I., Coenen H.H., Heinze H.-J., Zilles K., Duzel E., Bauer A. Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. The Journal of Neuroscience 2008, 28:14311-14319.
67. Schultz W. Predictive reward signal of dopamine neurons. Journal of Neurophysiology 1998, 80:1-27.
68. Scott D.J., Heitzeg M.M., Koeppe R.A., Stohler C.S., Zubieta J.K. Variations in the human pain stress experience mediated by ventral and dorsal basal ganglia dopamine activity. The Journal of Neuroscience 2006, 26:10789-10795.
69. Scott D.J., Stohler C.S., Egnatuk C.M., Wang H., Koeppe R.A., Zubieta J.K. Individual differences in reward responding explain placebo-induced expectations and effects. Neuron 2007, 55:325-336.
70. Seeman P., Wilson A., Gmeiner P., Kapur S. Dopamine D2 and D3 receptors in human putamen, caudate nucleus, and globus pallidus. Synapse 2006, 60:205-211.
71. Smith G.T., Fischer S., Cyders M.A., Annus A.M., Spillane N.S., McCarthy D.M. On the validity and utility of discriminating among impulsivity-like traits. Assessment 2007, 14:155-170.
72. Sutton B.P., Noll D.C., Fessler J.A. Fast, iterative image reconstruction for MRI in the presence of field inhomogeneities. IEEE Transactions on Medical Imaging 2003, 22:178-188.
73. Thompson T.L., Moss R.L. in vivo stimulated dopamine release in the nucleus accumbens: Modulation by the prefrontal cortex. Brain Research 1995, 686:93-98.
74. 11C]raclopride. Biological Psychiatry 2010, 68:689-696.
75. Urban N.L., Slifstein M., Meda S., Xu X., Ayoub R., Medina O., Pearlson G., Krystal J., Abi-Dargham A. Imaging human reward processing with positron emission tomography and functional magnetic resonance imaging. Psychopharmacology 2012, 221:67-77.
76. Urcelay G.P., Dalley J.W. Linking ADHD, impulsivity, and drug abuse: a neuropsychological perspective. Current Topics in Behavioral Neurosciences 2011, 173. Springer, Verlag, Berlin. M.A. Geyer, B.A. Ellenbroek, C.A. Marsden (Eds.).
77. Verdejo-García A., Lawrence A.J., Clark L. Impulsivity as a vulnerability marker for substance-use disorders: review of findings from high-risk research, problem gamblers and genetic association studies. Neuroscience & Biobehavioral Reviews 2008, 32:777-810.
78. Volkow N.D., Fowler J.S., Wang G.J., Baler R., Telang F. Imaging dopamine's role in drug abuse and addiction. Neuropharmacology 2009, 56:3-8.
79. Volkow N.D., Fowler J.S., Wang G.J., Swanson J.M., Telang F. Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Archives of Neurology 2007, 64:1575-1579.
80. Walker Q.D., Ray R., Kuhn C.M. Sex differences in neurochemical effects of dopaminergic drugs in rat striatum. Neuropsychopharmacology 2005, 31:1193-1202.
81. Walker Q.D., Rooney M.B., Wightman R.M., Kuhn C.M. Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience 1999, 95:1061-1070.
82. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology 1988, 54:1063-1070.
83. Weiland B.J., Welsh R.C., Yau W.Y., Zucker R.A., Zubieta J.K., Heitzeg M.M. Accumbens functional connectivity during reward mediates sensation-seeking and alcohol use in high-risk youth. Drug and Alcohol Dependence 2013, 128:130-139.
84. Whiteside S.P., Lynam D.R. The Five Factor Model and impulsivity: using a structural model of personality to understand impulsivity. Personality and Individual Differences 2001, 30:669-689.
85. Wise R.A. Brain reward circuitry: insights from unsensed incentives. Neuron 2002, 36:229-240.
86. Worsley K.J., Marrett S., Neelin P., Vandal A.C., Friston K.J., Evans A.C. A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping 1996, 4:58-73.
87. Zald D.H., Boileau I., El-Dearedy W., Gunn R., McGlone F., Dichter G.S., Dagher A. Dopamine transmission in the human striatum during monetary reward tasks. Journal of Neuroscience 2004, 24:4105-4112.
88. Zucker R.A., Heitzeg M.M., Nigg J.T. Parsing the undercontrol/disinhibition pathway to substance use disorders: a multilevel developmental problem. Child Development Perspectives 2011, 5:248-255.