Human dopamine receptor D2/D3 availability predicts amygdala reactivity to unpleasant stimuli

Human Brain Mapping

Volumn 31, Issue 5, 2010, Pages 716-726

  Kobiella, Andrea ^a,b   Vollstädt Klein, Sabine ^a   Bühler, Mira ^a   Graf, Caroline ^a   Buchholz, Hans Georg ^c   Bernow, Nina ^c   Yakushev, Igor Y ^c   Landvogt, Christian ^c   Schreckenberger, Mathias ^c   Gründer, Gerhard ^d   Bartenstein, Peter ^e   Fehr, Christoph ^c   Smolka, Michael N ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d RWTH AACHEN UNIVERSITY   (Germany)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

18F fallypride; Amygdala; Emotion processing; fMRI; PET; Prefrontal cortex

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; FALLYPRIDE F 18; RADIOPHARMACEUTICAL AGENT; UNCLASSIFIED DRUG;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DOPAMINERGIC TRANSMISSION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE; OXYGEN BLOOD LEVEL; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SMOKING; STIMULUS RESPONSE; TOBACCO DEPENDENCE; VISUAL STIMULATION;

ADULT; AMYGDALA; BENZAMIDES; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; EMOTIONS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PHOTIC STIMULATION; POSITRON-EMISSION TOMOGRAPHY; PYRROLIDINES; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; SMOKING; TOBACCO USE DISORDER; VISUAL PERCEPTION;

EID: 77951586964     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.20900     Document Type: Article

References (67)

1. Buchsbaum MS, Christian BT, Lehrer DS, Narayanan TK, Shi B, Mantil J, Kemether E, Oakes TR, Mukherjee J (2006): D2/D3 dopamine receptor binding with [F-18]fallypride in thalamus and cortex of patients with schizophrenia. Schizophr Res 85:232-244. (Pubitemid 43947535)
2. Christian BT, Lehrer DS, Shi B, Narayanan TK, Strohmeyer PS, Buchsbaum MS, Mantil JC (2006): Measuring dopamine neuro-modulation in the thalamus: Using [F-18]fallypride PET to study dopamine release during a spatial attention task. Neuro-image 31:139-152. (Pubitemid 43728994)
3. Christian BT, Vandehey NT, Fox AS, Murali D, Oakes TR, Converse AK, Nickles RJ, Shelton SE, Davidson RJ, Kalin NH (2009): The distribution of D2/D3 receptor binding in the adolescent rhesus monkey using small animal PET imaging. Neuro-image 44:1334-1344.
4. Dagher A, Bleicher C, Aston JA, Gunn RN, Clarke PB, Cumming P (2001): Reduced dopamine D1 receptor binding in the ventral striatum of cigarette smokers. Synapse 42:48-53. (Pubitemid 32786423)
5. Delaveau P, Salgado-Pineda P, Micallef-Roll J, Blin O (2007): Amygdala activation modulated by levodopa during emotional recognition processing in healthy volunteers: A double-blind, placebo-controlled study. J Clin Psychopharmacol 27:692-697. (Pubitemid 351343694)
6. Denys D, van der WN, Janssen J, De Geus F, Westenberg HG (2004): Low level of dopaminergic D2 receptor binding in obsessive-compulsive disorder. Biol Psychiatry 55:1041-1045. (Pubitemid 38581920)
7. D'haenen HA, Bossuyt A (1994): Dopamine D2 receptors in depression measured with single photon emission computed tomography. Biol Psychiatry 35:128-132.
8. Enoch MA, Xu K, Ferro E, Harris CR, Goldman D (2003): Genetic origins of anxiety in women: A role for a functional catechol-O-methyltransferase polymorphism. Psychiatr Genet 13:33-41. (Pubitemid 36293143)
9. Etkin A, Wager TD (2007): Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476-1488. (Pubitemid 350069724)
10. Fehr C, Yakushev I, Hohmann N, Buchholz HG, Landvogt C, Deckers H, Eberhardt A, Klager M, Smolka MN, Scheurich A, Dielentheis T, Schmidt LG, Rosch F, Bartenstein P, Grunder G, Schreckenberger M (2008): Association of low striatal dopamine d2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. Am J Psychiatry 165:507-514. (Pubitemid 351694294)
11. Floresco SB, Tse MT (2007): Dopaminergic regulation of inhibitory and excitatory transmission in the basolateral amygdala-prefrontal cortical pathway. J Neurosci 27:2045-2057. (Pubitemid 46310314)
12. Fowler JS, Volkow ND, Wang GJ, Pappas N, Logan J, MacGregor R, Alexoff D, Shea C, Schlyer D, Wolf AP, Warner D, Zezulkova I, Cilento R (1996a): Inhibition of monoamine oxidase B in the brains of smokers. Nature 379:733-736. (Pubitemid 26061736)
13. Fowler JS, Volkow ND, Wang GJ, Pappas N, Logan J, Shea C, Alexoff D, MacGregor RR, Schlyer DJ, Zezulkova I, Wolf AP (1996b): Brain monoamine oxidase A inhibition in cigarette smokers. Proc Natl Acad Sci USA 93:14065-14069. (Pubitemid 26424246)
14. Gaspar P, Bloch B, Le Moine C (1995): D1 and D2 receptor gene expression in the rat frontal cortex: Cellular localization in different classes of efferent neurons. Eur J Neurosci 7:1050-1063.
15. Gilbert DG, Sugai C, Zuo Y, Eau CN, McClernon FJ, Rabinovich NE, Markus T, Asgaard G, Radtke R (2004): Effects of nicotine on brain responses to emotional pictures. Nicotine Tob Res 6:985-996. (Pubitemid 40124755)
16. Gilbert DL, Christian BT, Gelfand MJ, Shi B, Mantil J, Sallee FR (2006): Altered mesolimbocortical and thalamic dopamine in Tourette syndrome. Neurology 67:1695-1697. (Pubitemid 44747951)
17. Gilman JM, Hommer DW (2008): Modulation of brain response to emotional images by alcohol cues in alcohol-dependent patients. Addict Biol 13:423-434.
18. Ginovart N, Wilson AA, Houle S, Kapur S (2004): Amphetamine pretreatment induces a change in both D2-receptor density and apparent affinity: A [11C]raclopride positron emission tomography study in cats. Biol Psychiatry 55:1188-1194. (Pubitemid 38739453)
19. Gogos JA, Morgan M, Luine V, Santha M, Ogawa S, Pfaff D, Karayiorgou M (1998): Catechol-O-methyltransferase-deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior. Proc Natl Acad Sci USA 95:9991-9996. (Pubitemid 28415282)
20. Gunn RN, Lammertsma AA, Hume SP, Cunningham VJ (1997): Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. Neuroimage 6:279-287.
21. Hall H, Kohler C, Gawell L, Farde L, Sedvall G (1988): Raclopride, a new selective ligand for the dopamine-d2 receptors. Prog Neuropsychopharmacol Biol Psychiatry 12:559-568.
22. Hariri AR, Mattay VS, Tessitore A, Fera F, Smith WG, Weinberger DR (2002): Dextroamphetamine modulates the response of the human amygdala. Neuropsychopharmacology 27:1036-1040. (Pubitemid 35447640)
23. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO (1991): The Fagerstrom test for nicotine dependence: A revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86:1119-1127.
24. Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, Hermann D, Klein S, Grusser SM, Flor H, Schumann G, Mann K, Buchel C (2005a): Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 8:20-21. (Pubitemid 41236725)
25. Heinz A, Siessmeier T, Wrase J, Buchholz HG, Grunder G, Kumakura Y, Cumming P, Schreckenberger M, Smolka MN, Rosch F, Mann K, Bartenstein P (2005b): Correlation of alcohol craving with striatal dopamine synthesis capacity and D-2/3 receptor availability: A combined [18F]DOPA and [18F]DMFP PET study in detoxified alcoholic patients. Am J Psychiatry 162:1515-1520. (Pubitemid 41105567)
26. Hirvonen J, Karlsson H, Kajander J, Markkula J, Rasi-Hakala H, Nagren K, Salminen JK, Hietala J (2008): Striatal dopamine D-2 receptors in medication-naive patients with major depressive disorder as assessed with [C-11]raclopride PET. Psychopharmacology 197:581-590.
27. Iizuka Y, Sei Y, Weinberger DR, Straub RE (2007): Evidence that the BLOC-1 protein dysbindin modulates dopamine D2 receptor internalization and signaling but not D1 internalization. J Neurosci 27:12390-12395. (Pubitemid 350085456)
28. Inglis FM, Moghaddam B (1999): Dopaminergic innervation of the amygdala is highly responsive to stress. J Neurochem 72:1088-1094.
29. Khan ZU, Gutierrez A, Martin R, Penafiel A, Rivera A, De La CA (1998): Differential regional and cellular distribution of dopamine D2-like receptors: An immunocytochemical study of subtype-specific antibodies in rat and human brain. J Comp Neurol 402:353-371.
30. Kienast T, Hariri AR, Schlagenhauf F, Wrase J, Sterzer P, Buchholz HG, Smolka MN, Grunder G, Cumming P, Kumakura Y, Bartenstein P, Dolan RJ, Heinz A (2008a): Dopamine in amygdala gates limbic processing of aversive stimuli in humans. Nat Neurosci 11:1381-1382.
31. Kienast T, Siessmeier T, Wrase J, Braus DF, Smolka MN, Buchholz HG, Rapp M, Schreckenberger M, Rosch F, Cumming P, Gruender G, Mann K, Bartenstein P, Heinz A (2008b): Ratio of dopamine synthesis capacity to D2 receptor availability in ventral striatum correlates with central processing of affective stimuli. Eur J Nucl Med Mol Imaging 35:1147-1158.
32. Kung HF, Pan S, Kung MP, Billings J, Kasliwal R, Reilley J, Alavi A (1989): In vitro and in vivo evaluation of [123I]IBZM: A potential CNS D-2 dopamine receptor imaging agent. J Nucl Med 30:88-92.
33. Laje RP, Berman JA, Glassman AH (2001): Depression and nicotine: Preclinical and clinical evidence for common mechanisms. Curr Psychiatry Rep 3:470-474.
34. Lang PJ, Bradley MM, Cuthbert BN (2008): The International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual. Technical Report A-8. Gainesville, FL: University of Florida.
35. Leppanen JM (2006): Emotional information processing in mood disorders: A review of behavioral and neuroimaging findings. Curr Opin Psychiatry 19:34-39.
36. Llamas A, Avendano C, Reinoso-Suarez F (1977): Amygdaloid projections to prefrontal and motor cortex. Science 195:794-796. (Pubitemid 8055732)
37. Mcdonald AJ, Mascagni F, Guo L (1996): Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71:55-75. (Pubitemid 26042870)
38. Mukherjee J, Yang ZY, Das MK, Brown T (1995): Fluorinated benzamide neuroleptics. 3. Development of (S)-N-[(1-allyl-2-pyrrolidinyl)methyl]-5-(3-[F- 18] fluoropropyl)-2,3-dimethoxybenzamide as an improved dopamine D-2 receptor tracer. Nucl Med Biol 22:283-296.
39. Mukherjee J, Yang ZY, Brown T, Lew R, Wernick M, Ouyang X, Yasillo N, Chen CT, Mintzer R, Cooper M (1999): Preliminary assessment of extrastriatal dopamine D-2 receptor binding in the rodent and nonhuman primate brains using the high affinity radioligand, 18F-fallypride. Nucl Med Biol 26:519-527. (Pubitemid 29378486)
40. Mukherjee J, Christian BT, Dunigan KA, Shi B, Narayanan TK, Satter M, Mantil J (2002): Brain imaging of 18F-fallypride in normal volunteers: Blood analysis, distribution, test-retest studies, and preliminary assessment of sensitivity to aging effects on dopamine D-2/D-3 receptors. Synapse 46:170-188. (Pubitemid 35155170)
41. Nader MA, Morgan D, Gage HD, Nader SH, Calhoun TL, Buchheimer N, Ehrenkaufer R, Mach RH (2006): PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nat Neurosci 9:1050-1056. (Pubitemid 44264918)
42. Parsey RV, Oquendo MA, Zea-Ponce Y, Rodenhiser J, Kegeles LS, Pratap M, Cooper TB, Van Heertum R, Mann JJ, Laruelle M (2001): Dopamine D-2 receptor availability and amphetamine-induced dopamine release in unipolar depression. Biol Psychiatry 50:313-322. (Pubitemid 32816943)
43. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, Egan MF, Mattay VS, Hariri AR, Weinberger DR (2005): 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: A genetic susceptibility mechanism for depression. Nat Neurosci 8:828-834. (Pubitemid 43085851)
44. Picciotto MR (1998): Common aspects of the action of nicotine and other drugs of abuse. Drug Alcohol Depend 51:165-172.
45. Price JL (2003): Comparative aspects of amygdala connectivity. Ann N Y Acad Sci 985:50-58.
46. Riccardi P, Li R, Ansari MS, Zald D, Park S, Dawant B, Anderson S, Doop M, Woodward N, Schoenberg E, Schmidt D, Baldwin R, Kessler R (2006): Amphetamine-induced displacement of [18F] fallypride in striatum and extrastriatal regions in humans. Neuropsychopharmacology 31:1016-1026.
47. Riccardi P, Baldwin R, Salomon R, Anderson S, Ansari MS, Li R, Dawant B, Bauernfeind A, Schmidt D, Kessler R (2008): Estimation of baseline dopamine D2 receptor occupancy in striatum and extrastriatal regions in humans with positron emission tomography with [18F] fallypride. Biol Psychiatry 63:241-244. (Pubitemid 350299319)
48. Salgado-Pineda P, Delaveau P, Blin O, Nieoullon A (2005): Dopaminergic contribution to the regulation of emotional perception. Clin Neuropharmacol 28:228-237. (Pubitemid 41579621)
49. Schneier FR, Liebowitz MR, Abi-Dargham A, Zea-Ponce Y, Lin SH, Laruelle M (2000): Low dopamine D(2) receptor binding potential in social phobia. Am J Psychiatry 157:457-459. (Pubitemid 30145936)
50. Schneier FR, Martinez D, Abi-Dargham A, Zea-Ponce Y, Simpson HB, Liebowitz MR, Laruelle M (2008): Striatal dopamine D(2) receptor availability in OCD with and without comorbid social anxiety disorder: Preliminary findings. Depress Anxiety 25:1-7. (Pubitemid 351213919)
51. Siessmeier T, Zhou Y, Buchholz HG, Landvogt C, Vernaleken I, Piel M, Schirrmacher R, Rosch F, Schreckenberger M, Wong DF, Cumming P, Grunder G, Bartenstein P (2005): Parametric mapping of binding in human brain of D2 receptor ligands of different affinities. J Nucl Med 46:964-972. (Pubitemid 43733511)
52. Siessmeier T, Kienast T, Wrase J, Larsen JL, Braus DF, Smolka MN, Buchholz HG, Schreckenberger M, Rosch F, Cumming P, Mann K, Bartenstein P, Heinz A (2006): Net influx of plasma 6-[18F]fluoro-L-DOPA (FDOPA) to the ventral striatum correlates with prefrontal processing of affective stimuli. Eur J Neurosci 24:305-313. (Pubitemid 44050688)
53. Slifstein M, Laruelle M (2000): Effects of statistical noise on graphic analysis of PET neuroreceptor studies. J Nucl Med 41:2083-2088. (Pubitemid 32038700)
54. Smolka MN, Schumann G, Wrase J, Grusser SM, Flor H, Mann K, Braus DF, Goldman D, Buchel C, Heinz A (2005): Catechol-Omethyltransferase val158met genotype affects processing of emotional stimuli in the amygdala and prefrontal cortex. J Neurosci 25:836-842. (Pubitemid 40170998)
55. Smolka MN, Buhler M, Schumann G, Klein S, Hu XZ, Moayer M, Zimmer A, Wrase J, Flor H, Mann K, Braus DF, Goldman D, Heinz A (2007): Gene-gene effects on central processing of aversive stimuli. Mol Psychiatry 12:307-317. (Pubitemid 46328512)
56. Stark D, Piel M, Hubner H, Gmeiner P, Grunder G, Rosch F (2007): In vitro affinities of various halogenated benzamide derivatives as potential radioligands for non-invasive quantification of D(2)-like dopamine receptors. Bioorg Med Chem 15:6819-6829.
57. Takahashi H, Yahata N, Koeda M, Takano A, Asai K, Suhara T, Okubo Y (2005): Effects of dopaminergic and serotonergic manipulation on emotional processing: A pharmacological fMRI study. Neuroimage 27:991-1001. (Pubitemid 41317266)
58. Taylor SF, Phan KL, Decker LR, Liberzon I (2003): Subjective rating of emotionally salient stimuli modulates neural activity. Neuroimage 18:650-659.
59. Tessitore A, Hariri AR, Fera F, Smith WG, Chase TN, Hyde TM, Weinberger DR, Mattay VS (2002): Dopamine modulates the response of the human amygdala: A study in Parkinson's disease. J Neurosci 22:9099-9103. (Pubitemid 35379080)
60. Volkow ND, Wang GJ, Fowler JS, Logan J, Hitzemann R, Ding YS, Pappas N, Shea C, Piscani K (1996): Decreases in dopamine receptors but not in dopamine transporters in alcoholics. Alcohol Clin Exp Res 20:1594-1598. (Pubitemid 26428110)
61. Volkow ND, Wang GJ, Begleiter H, Porjesz B, Fowler JS, Telang F, Wong C, Ma Y, Logan J, Goldstein R, Alexoff D, Thanos PK (2006): High levels of dopamine D2 receptors in unaffected members of alcoholic families: Possible protective factors. Arch Gen Psychiatry 63:999-1008. (Pubitemid 44330458)
62. Wang GJ, Volkow ND, Fowler JS, Logan J, Abumrad NN, Hitzemann RJ, Pappas NS, Pascani K (1997): Dopamine D2 receptor availability in opiate-dependent subjects before and after naloxone-precipitated withdrawal. Neuropsychopharmacology 16:174-182. (Pubitemid 27086432)
63. Werhahn KJ, Landvogt C, Klimpe S, Buchholz HG, Yakushev I, Siessmeier T, Muller-Forell W, Piel M, Rosch F, Glaser M, Schreckenberger M, Bartenstein P (2006): Decreased dopamine D2/D3-receptor binding in temporal lobe epilepsy: An [18F]fallypride PET study. Epilepsia 47:1392-1396. (Pubitemid 44200421)
64. Wicker B, Keysers C, Plailly J, Royet JP, Gallese V, Rizzolatti G (2003): Both of us disgusted in My insula: The common neural basis of seeing and feeling disgust. Neuron 40:655-664. (Pubitemid 37494712)
65. Wienhard K, Eriksson L, Grootoonk S, Casey M, Pietrzyk U, Heiss WD (1992): Performance evaluation of the positron scanner ECAT EXACT. J Comput Assist Tomogr 16:804-813.
66. Wittchen HU, Lachner G, Wunderlich U, Pfister H (1998): Test-retest reliability of the computerized DSM-IV version of the Munich-Composite International Diagnostic Interview (M-CIDI). Soc Psychiatry Psychiatr Epidemiol 33:568-578. (Pubitemid 28477089)
67. Zubieta JK, Heitzeg MM, Smith YR, Bueller JA, Xu K, Xu Y, Koeppe RA, Stohler CS, Goldman D (2003): COMT val158met genotype affects mu-opioid neurotransmitter responses to a pain stressor. Science 299:1240-1243.