Hostname: page-component-6b989bf9dc-vmcqm Total loading time: 0 Render date: 2024-04-14T01:40:14.979Z Has data issue: false hasContentIssue false

Dopamine D2/3 receptor availability and human cognitive impulsivity: a high-resolution positron emission tomography imaging study with [11C]raclopride

Published online by Cambridge University Press:  24 June 2013

Jong-Hoon Kim*
Affiliation:
Department of Psychiatry, Gil Medical Center, Gachon University, Namdong-Gu, Incheon, Korea
Young-Don Son
Affiliation:
Neuroscience Research Institute, Gachon University, Namdong-Gu, Incheon, Korea
Hang-Keun Kim
Affiliation:
Neuroscience Research Institute, Gachon University, Namdong-Gu, Incheon, Korea
Sang-Yoon Lee
Affiliation:
Neuroscience Research Institute, Gachon University, Namdong-Gu, Incheon, Korea
Young-Bo Kim
Affiliation:
Neuroscience Research Institute, Gachon University, Namdong-Gu, Incheon, Korea Department of Neurosurgery, Gil Medical Center, Gachon University, Namdong-Gu, Incheon, Korea
Zang-Hee Cho
Affiliation:
Neuroscience Research Institute, Gachon University, Namdong-Gu, Incheon, Korea
*
Jong-Hoon Kim, Department of Psychiatry, Gil Medical Center, Gachon University, Namdong-gu, Incheon, South Korea. Tel: +82 32 460 8505; Fax: +82 32 472 8813; E-mail: jhnp@chol.com

Abstract

Objective

Human impulsivity is a complex multidimensional construct encompassing cognitive, emotional, and behavioural aspects. Previous animal studies have suggested that striatal dopamine receptors play a critical role in impulsivity. In this study, we investigated the relationship between self-reported impulsiveness and dopamine D2/3 receptor availability in striatal subdivisions in healthy subjects using high-resolution positron emission tomography (PET) with [11C]raclopride.

Methods

Twenty-one participants completed 3-T magnetic resonance imaging and high-resolution PET scans with [11C]raclopride. The trait of impulsiveness was measured using the Barratt Impulsiveness Scale (BIS-11). Partial correlation analysis was performed between BIS-11 scores and D2/3 receptor availability in striatal subregions, controlling for the confounding effects of temperament characteristics that are conceptually or empirically related to dopamine, which were measured by the Temperament and Character Inventory.

Results

The analysis revealed that the non-planning (p = 0.004) and attentional (p = 0.007) impulsiveness subscale scores on the BIS-11 had significant positive correlations with D2/3 receptor availability in the pre-commissural dorsal caudate. There was a tendency towards positive correlation between non-planning impulsiveness score and D2/3 receptor availability in the post-commissural caudate.

Conclusion

These results suggest that cognitive subtrait of impulsivity is associated with D2/3 receptor availability in the associative striatum that plays a critical role in cognitive processes involving attention to detail, judgement of alternative outcomes, and inhibitory control.

Type
Original Articles
Copyright
Copyright © Scandinavian College of Neuropsychopharmacology 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Evenden, JL. Varieties of impulsivity. Psychopharmacology 1999;146:348361.Google Scholar
2.Lee, B, London, ED, Poldrack, RAet al. Striatal dopamine d2/d3 receptor availability is reduced in methamphetamine dependence and is linked to impulsivity. J Neurosci 2009;29:1473414740.Google Scholar
3.Chamorro, J, Bernardi, S, Potenza, MNet al. Impulsivity in the general population: a national study. J Psychiatr Res 2012;46:9941001.CrossRefGoogle ScholarPubMed
4.Buckholtz, JW, Treadway, MT, Cowan, RLet al. Dopaminergic network differences in human impulsivity. Science 2010;329:532.Google Scholar
5.Volkow, ND, Wang, GJ, Fowler, JS, Tomasi, D, Telang, F. Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci USA 2011;108:1503715042.Google Scholar
6.Tomasi, D, Volkow, ND. Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 2012;71:443450.CrossRefGoogle ScholarPubMed
7.Zuckerman, M, Kuhlman, DM. Personality and risk-taking: common biosocial factors. J Pers 2000;68:9991029.Google Scholar
8.Dalley, JW, Fryer, TD, Brichard, Let al. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 2007;315:12671270.CrossRefGoogle ScholarPubMed
9.van Gaalen, MM, van Koten, R, Schoffelmeer, AN, Vanderschuren, LJ. Critical involvement of dopaminergic neurotransmission in impulsive decision making. Biol Psychiatry 2006;60:6673.Google Scholar
10.Patton, JH, Stanford, MS, Barratt, ES. Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol 1995;51:768774.Google Scholar
11.Reeves, SJ, Polling, C, Stokes, PRet al. Limbic striatal dopamine D2/3 receptor availability is associated with non-planning impulsivity in healthy adults after exclusion of potential dissimulators. Psychiatry Res 2012;202:6064.Google Scholar
12.Oswald, LM, Wong, DF, Zhou, Yet al. Impulsivity and chronic stress are associated with amphetamine-induced striatal dopamine release. Neuroimage 2007;36:153166.Google Scholar
13.Bernow, N, Yakushev, I, Landvogt, Cet al. Dopamine D2/D3 receptor availability and venturesomeness. Psychiatry Res 2011;193:8084.Google Scholar
14.Suhara, T, Yasuno, F, Sudo, Yet al. Dopamine D2 receptors in the insular cortex and the personality trait of novelty seeking. Neuroimage 2001;13:891895.Google Scholar
15.Zald, DH, Cowan, RL, Riccardi, Pet al. Midbrain dopamine receptor availability is inversely associated with novelty-seeking traits in humans. J Neurosci 2008;28:1437214378.Google Scholar
16.Gjedde, A, Kumakura, Y, Cumming, P, Linnet, J, Møller, A. Inverted-U-shaped correlation between dopamine receptor availability in striatum and sensation seeking. Proc Natl Acad Sci USA 2010;107:38703875.Google Scholar
17.Mawlawi, O, Martinez, D, Slifstein, Met al. Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D(2)receptor parameter measurements in ventral striatum. J Cereb Blood Flow Metab 2001;21:10341057.Google Scholar
18.Martinez, D, Slifstein, M, Broft, Aet al. Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: amphetamine-induced dopamine release in the functional subdivisions of the striatum. J Cereb Blood Flow Metab 2003;23:285300.Google Scholar
19.Cloninger, CR, Svrakic, DM, Przybeck, TR. A psychobiological model of temperament and character. Arch Gen Psychiatry 1993;50:975990.Google Scholar
20.Yasuno, F, Suhara, T, Sudo, Yet al. Relation among dopamine D(2) receptor binding, obesity and personality in normal human subjects. Neurosci Lett 2001;300:5961.Google Scholar
21.Kim, JH, Son, YD, Kim, HKet al. Association of harm avoidance with dopamine D2/3 receptor availability in striatal subdivisions: a high resolution PET study. Biol Psychol 2011;87:164167.Google Scholar
22.First, MB, Spitzer, RL, Gibbon, M, Williams, JBW. Structured Clinical Interview for DSM-IV Axis I Disorders Research Version (SCID-I). New York: New York State Psychiatric Institute Biometrics Research, 1996.Google Scholar
23.Fei, X, Mock, BH, DeGrado, TRet al. An improved synthesis of PET dopamine D2 receptors radioligand [11C]raclopride. Synth Commun 2004;34:18971907.Google Scholar
24.Hong, IK, Chung, ST, Kim, HKet al. Ultra fast symmetry and SIMD-based projection-back projection (SSP) algorithm for 3-D PET image reconstruction. IEEE Trans Med Imaging 2007;26:789803.Google Scholar
25.Logan, J, Fowler, JS, Volkow, NDet al. Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab 1996;16:834840.Google Scholar
26.Joshi, A, Fessler, JA, Koeppe, RA. Improving PET receptor binding estimates from Logan plots using principal component analysis. J Cereb Blood Flow Metab 2008;28:852865.CrossRefGoogle ScholarPubMed
27.Haber, SN, McFarland, NR. The concept of the ventral striatum in nonhuman primates. Ann N Y Acad Sci 1999;877:3348.CrossRefGoogle ScholarPubMed
28.Dickman, SJ, Meyer, DE. Impulsivity and speed-accuracy tradeoffs in information processing. J Pers Soc Psychol 1988;54:274290.Google Scholar
29.Stanford, MS, Mathias, CW, Dougherty, DMet al. Fifty years of the Barratt Impulsiveness Scale: an update and review. Pers Individ Dif 2009;47:385395.Google Scholar
30.Barratt, ES. Impulsiveness and aggression. In: Monahan J, Steadman HJ, eds. Violence and mental disorder. Chicago: University of Chicago Press, 1994:6179.Google Scholar
31.Whitney, P, Jameson, T, Hinson, JM. Impulsiveness and executive control of working memory. Pers Individ Dif 2004;37:417428.Google Scholar
32.Garavan, H, Ross, TJ, Murphy, K, Roche, RA, Stein, EA. Dissociable executive functions in the dynamic control of behavior: inhibition, error detection, and correction. Neuroimage 2002;17:18201829.CrossRefGoogle ScholarPubMed
33.Abi-Dargham, A. Evidence from brain imaging studies for dopaminergic alterations in schizophrenia. In: Kapur S, Lecrubier Y, eds. Dopamine in the pathophysiology and treatment of schizophrenia: new findings. London: Martin Dunitz, 2003:1548.Google Scholar
34.Kegeles, LS, Abi-Dargham, A, Frankle, WGet al. Increased synaptic dopamine function in associative regions of the striatum in schizophrenia. Arch Gen Psychiatry 2010;67:231239.Google Scholar
35.Martinez, D, Orlowska, D, Narendran, Ret al. Dopamine type 2/3 receptor availability in the striatum and social status in human volunteers. Biol Psychiatry 2010;67:275278.Google Scholar
36.Dagher, A, Robbins, TW. Personality, addiction, dopamine: insights from Parkinson's disease. Neuron 2009;61:502510.Google Scholar
37.Weintraub, D. Dopamine and impulse control disorders in Parkinson's disease. Ann Neurol 2008;64(Suppl. 2):S93S100.Google Scholar
38.Dalley, JW, Mar, AC, Economidou, D, Robbins, TW. Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacol Biochem Behav 2008;90:250260.Google Scholar
39.Varrone, A, Sjöholm, N, Eriksson, Let al. Advancement in PET quantification using 3D-OP-OSEM point spread function reconstruction with the HRRT. Eur J Nucl Med Mol Imaging 2009;36:16391650.Google Scholar
40.Leroy, C, Comtat, C, Trébossen, Ret al. Assessment of 11C-PE2I binding to the neuronal dopamine transporter in humans with the high-spatial-resolution PET scanner HRRT. J Nucl Med 2007;48:538546.Google Scholar
41.Uchida, H, Chow, TW, Mamo, DCet al. Effects of aging on 5-HT(2A) R binding: a HRRT PET study with and without partial volume corrections. Int J Geriatr Psychiatry 2011;26:13001308.Google Scholar