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Special Issue

A review of positron emission tomography studies exploring the dopaminergic system in substance use with a focus on tobacco as a co-variate

, MSc, , PhD & , MD, PhD, MCFP
Pages 197-214 | Received 15 Jun 2016, Accepted 31 Oct 2016, Published online: 30 Nov 2016

References

  • Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 1998;28:309–369.
  • Volkow ND, Fowler JS, Wang GJ, Baler R, Telang F. Imaging dopamine’s role in drug abuse and addiction. Neuropharmacology, 2009;56:3–8.
  • Morris ED, Lucas MV, Cosgrove KP. How to study smoking and drinking with PET, positron emission tomography - recent developments in instrumentation, research and clinical oncological practice, S. Misciagna, Editor. 2013, InTech, doi:10.5772/57414.
  • Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN, Holden J, et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab 2007;27:1533–1539.
  • Laruelle M. Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J Cereb Blood Flow Metab 2000;20:423–451.
  • Breier A, Su TP, Saunders R, Carson RE, Kolachana BS, de Bartolomeis A, Weinberger DR, et al. Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proc Natl Acad Sci USA 1997;94:2569–2574.
  • Kalman D, Morissette SB, George TP. Co-morbidity of smoking in patients with psychiatric and substance use disorders. Am J Addict 2005;14:106–123.
  • Scott DJ, Domino EF, Heitzeg MM, Koeppe RA,Ni L, Guthrie S, Zubieta JK. Smoking modulation of mu-opioid and dopamine D2 receptor-mediated neurotransmission in humans. Neuropsychopharmacology 2007;32:450–457.
  • Brody AL, Mandelkern MA, Olmstead RE, Allen-Martinez Z, Scheibal D, Abrams AL, Costello MR, et al. Ventral striatal dopamine release in response to smoking a regular vs a denicotinized cigarette. Neuropsychopharmacology 2009;34:282–289.
  • Montgomery AJ, Lingford-Hughes AR, Egerton A, Nutt DJ, Grasby PM. The effect of nicotine on striatal dopamine release in man: a [11C]raclopride PET study. Synapse 2007;61:637–645.
  • Takahashi H, Fujimura Y, Hayashi M, Takano H, Kato M, Okubo Y, Kanno I, et al. Enhanced dopamine release by nicotine in cigarette smokers: a double-blind, randomized, placebo-controlled pilot study. Int J Neuropsychopharmacol 2008;11:413–417.
  • Domino EF, Ni L, Domino JS, Yang W, Evans C, Guthrie S, Wang H, et al. Denicotinized versus average nicotine tobacco cigarette smoking differentially releases striatal dopamine. Nicotine Tob Res 2013;15:11–21.
  • Domino EF, Evans CL, Ni L, Guthrie SK, Koeppe RA, Zubieta JK. Tobacco smoking produces greater striatal dopamine release in G-allele carriers with mu opioid receptor A118G polymorphism. Prog Neuropsychopharmacol Biol Psychiatry 2012;38:236–240.
  • Brody AL, Mandelkern MA, Olmstead RE, Scheibal D, Hahn E, Shiraga S, Zamora-Paja E, et al. Gene variants of brain dopamine pathways and smoking-induced dopamine release in the ventral caudate/nucleus accumbens. Arch Gen Psychiatry 2006;63:808–816.
  • Di Chiara G, Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 1988;85:5274–5278.
  • Imperato A, Mulas A, Di Chiara G. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol 1986;132:337–338.
  • Morris ED, Kim SJ, Sullivan JM, Wang S, Normandin MD, Constantinescu CC, Cosgrove KP. Creating dynamic images of short-lived dopamine fluctuations with lp-ntPET: dopamine movies of cigarette smoking. J Vis Exp 2013.
  • Cosgrove KP, Wang S, Kim SJ, McGovern E, Nabulsi N, Gao H, Labaree D, et al. Sex differences in the brain’s dopamine signature of cigarette smoking. J Neurosci 2014;34:16851–1685.
  • Shotbolt P, Tziortzi AC, Searle GE, Colasanti A, van der Aart J, Abanades S, Plisson C, et al. Within-subject comparison of [(11)C]-(+)-PHNO and [(11)C]raclopride sensitivity to acute amphetamine challenge in healthy humans. J Cereb Blood Flow Metab 2012;32:127–136.
  • Narendran R, Slifstein M, Guillin O, Hwang Y, Hwang DR, Scher E, Reeder S, et al. Dopamine (D2/3) receptor agonist positron emission tomography radiotracer [11C]-(+)-PHNO is a D3 receptor preferring agonist in vivo. Synapse 2006;60:485–495.
  • Le Foll B, Wilson AA, Graff A, Boileau I, Di Ciano P. Recent methods for measuring dopamine D3 receptor occupancy in vivo: importance for drug development. Front Pharmacol 2014;5:161.
  • Tziortzi AC, Searle GE, Tzimopoulou S, Salinas C, Beaver JD, Jenkinson M, Laruelle M, et al. Imaging dopamine receptors in humans with [11C]-(+)-PHNO: dissection of D3 signal and anatomy. Neuroimage 2011;54:264–77.
  • Le Foll B, Guranda M, Wilson AA, Houle S, Rusjan PM, Wing VC, Zawertailo L, et al. Elevation of dopamine induced by cigarette smoking: Novel insights from a [(11)C]-(+)-PHNO PET study in humans. Neuropsychopharmacology 2014;39:415–424.
  • Smith KS, Tindell AJ, Aldridge JW, Berridge KC. Ventral pallidum roles in reward and motivation. Behav Brain Res 2009;196:155–167.
  • Le Foll B, Goldberg SR, Sokoloff P. The dopamine D3 receptor and drug dependence: effects on reward or beyond? Neuropharmacology 2005;49:525–541.
  • Vandehey NT, Moirano JM, Converse AK, Holden JE, Mukherjee J, Murali D, Nickles RJ, et al. High-affinity dopamine D2/D3 PET radioligands 18F-fallypride and 11C-FLB457: a comparison of kinetics in extrastriatal regions using a multiple-injection protocol. J Cereb Blood Flow Metab 2010;30:994–1007.
  • Wing VC, Payer DE, Houle S, George TP, Boileau I. Measuring cigarette smoking-induced cortical dopamine release: A [11C]FLB-457 PET study. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2015;40:1417–1427.
  • Yasuno F, Ota M, Ando K, Ando T, Maeda J, Ichimiya T, Takano A, et al. Role of ventral striatal dopamine D1 receptor in cigarette craving. Biol Psychiatry 2007;61:1252–1259.
  • Busto UE, Redden L, Mayberg H, Kapur S, Houle S, Zawertailo LA. Dopaminergic activity in depressed smokers: a positron emission tomography study. Synapse (New York, NY) 2009;63:681–689.
  • Fehr C, Yakushev I, Hohmann N, Buchholz H-G, Landvogt C, Deckers H, Eberhardt A, et al. Association of low striatal dopamine d2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. Am J Psychiatry 2008;165:507–514.
  • Brown, A.K., M.A. Mandelkern, J. Farahi, C. Robertson, D.G. Ghahremani, B. Sumerel, N. Moallem, and E.D. London, Sex differences in striatal dopamine D2/D3 receptor availability in smokers and non-smokers. Int J Neuropsychopharmacol, 2012. 15:989–994.
  • Bloomfield MAP, Pepper F, Egerton A, Demjaha A, Tomasi G, Mouchlianitis E, Maximen L, et al. Dopamine function in cigarette smokers: an [18F]-DOPA PET study. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2014;39:2397–2404.
  • Leroy C, Karila L, Martinot J-L, Lukasiewicz M, Duchesnay E, Comtat C, Dolle F, et al. Striatal and extrastriatal dopamine transporter in cannabis and tobacco addiction: a high-resolution PET study. Addict Biol 2012;17:981–990.
  • Brody AL, London ED, Olmstead RE, Allen-Martinez Z, Shulenberger S, Costello MR, Abrams AL, et al. Smoking-induced change in intrasynaptic dopamine concentration: effect of treatment for Tobacco Dependence. Psychiatry Res 2010;183:218–224.
  • Yoder KK, Kareken DA, Seyoum RA, O’Connor J, Wang SC, Zheng QH, Mock B, Morris ED. Dopamine D(2) receptor availability is associated with subjective responses to alcohol. Alcohol Clin Exp Res 2005;29:965–970.
  • Yoder KK, Constantinescu CC, Kareken DA, Normandin MD, Cheng TE, O’Connor SJ, Morris ED. Heterogeneous effects of alcohol on dopamine release in the striatum: a PET study. Alcohol Clin Exp Res 2007;31:965–973.
  • Oberlin BG, Dzemidzic M, Tran SM, Soeurt CM, Albrecht DS, Yoder KK, Kareken DA. Beer flavor provokes striatal dopamine release in male drinkers: mediation by family history of alcoholism. Neuropsychopharmacology 2013;38:1617–1624.
  • Oberlin BG, Dzemidzic M, Tran SM, Soeurt CM, O’Connor SJ, Yoder KK, Kareken DA. Beer self-administration provokes lateralized nucleus accumbens dopamine release in male heavy drinkers. Psychopharmacology (Berl) 2015;232:861–870.
  • Setiawan E, Pihl RO, Dagher A, Schlagintweit H, Casey KF, Benkelfat C, Leyton M. Differential Striatal Dopamine Responses Following Oral Alcohol in Individuals at Varying Risk for Dependence. Alcohol Clin Exp Res 2013.
  • Urban NB, Kegeles LS, Slifstein M, Xu X, Martinez D, Sakr E, Castillo F, et al. Sex differences in striatal dopamine release in young adults after oral alcohol challenge: a positron emission tomography imaging study with [(1)(1)C]raclopride. Biol Psychiatry 2010;68:689–696.
  • Yoder KK, Morris ED, Constantinescu CC, Cheng TE, Normandin MD, O’Connor SJ, Kareken DA. When what you see isn’t what you get: alcohol cues, alcohol administration, prediction error, and human striatal dopamine. Alcohol Clin Exp Res 2009;33:139–149.
  • Yoder KK, Albrecht DS, Dzemidzic M, Normandin MD, Federici LM, Graves T, Herring CM, et al. Differences in IV alcohol-induced dopamine release in the ventral striatum of social drinkers and nontreatment-seeking alcoholics. Drug Alcohol Depend 2016;160:163–169.
  • Ramchandani VA, Umhau J, Pavon FJ, Ruiz-Velasco V, Margas W, Sun H, Damadzic R, et al. A genetic determinant of the striatal dopamine response to alcohol in men. Mol Psychiatry 2011;16:809–817.
  • Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Jayne M, Ma Y, et al. Profound decreases in dopamine release in striatum in detoxified alcoholics: possible orbitofrontal involvement. J Neurosci 2007;27:12700–12706.
  • Martinez D, Gil R, Slifstein M, Hwang DR, Huang Y, Perez A, Kegeles L, et al. Alcohol dependence is associated with blunted dopamine transmission in the ventral striatum. Biol Psychiatry 2005;58:779–786.
  • Erritzoe D, Tziortzi A, Bargiela D, Colasanti A, Searle GE, Gunn RN, Beaver JD, et al. In Vivo Imaging of Cerebral Dopamine D3 receptors in Alcoholism. Neuropsychopharmacology 2014.
  • Rominger A, Cumming P, Xiong G, Koller G, Boning G, Wulff M, Zwergal A, et al. [18F]Fallypride PET measurement of striatal and extrastriatal dopamine D 2/3 receptor availability in recently abstinent alcoholics. Addict Biol 2012;17:490–503.
  • Narendran R, Mason NS, Paris J, Himes ML, Douaihy AB, Frankle WG. Decreased prefrontal cortical dopamine transmission in alcoholism. Am J Psychiatry 2014;171:881–888.
  • Deserno L, Beck A, Huys QJM, Lorenz RC, Buchert R, Buchholz H-G, Plotkin M, et al. Chronic alcohol intake abolishes the relationship between dopamine synthesis capacity and learning signals in the ventral striatum. Eur J Neurosci, 2015;41:477–486.
  • Heinz A, Siessmeier T, Wrase J, Buchholz HG, Grunder G, Kumakura Y, Cumming P, et al. Correlation of alcohol craving with striatal dopamine synthesis capacity and D2/3 receptor availability: a combined [18F]DOPA and [18F]DMFP PET study in detoxified alcoholic patients. Am J Psychiatry 2005;162:1515–1520.
  • Albrecht DS, Kareken DA, Yoder KK. Effects of smoking on D(2)/D(3) striatal receptor availability in alcoholics and social drinkers. Brain Imaging Behav 2013;7:326–334.
  • Oswald LM, Wong DF, McCaul M, Zhou Y, Kuwabara H, Choi L, Brasic J, Wand GS. Relationships among ventral striatal dopamine release, cortisol secretion, and subjective responses to amphetamine. Neuropsychopharmacology 2005;30:821–832.
  • Munro CA, McCaul ME, Wong DF, Oswald LM, Zhou Y, Brasic J, Kuwabara H, et al. Sex differences in striatal dopamine release in healthy adults. Biol Psychiatry 2006;59:966–974.
  • Casey KF, Benkelfat C, Cherkasova MV, Baker GB, Dagher A, Leyton M. Reduced dopamine response to amphetamine in subjects at ultra-high risk for addiction. Biol Psychiatry 2014;76:23–30.
  • Volkow ND, Wang G-J, Ma Y, Fowler JS, Wong C, Ding Y-S, Hitzemann R, et al. Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J Neurosci Off J Soc Neurosci 2005;25:3932–3939.
  • Martinez D, Narendran R, Foltin RW, Slifstein M, Hwang D-R, Broft A, Huang Y, et al. Amphetamine-induced dopamine release: markedly blunted in cocaine dependence and predictive of the choice to self-administer cocaine. Am J Psychiatry 2007;164:622–629.
  • Wang GJ, Smith L, Volkow ND, Telang F, Logan J, Tomasi D, Wong CT, et al. Decreased dopamine activity predicts relapse in methamphetamine abusers. Mol Psychiatry 2012;17:918–925.
  • Volkow ND, Tomasi D, Wang GJ, Logan J, Alexoff DL, Jayne M, Fowler JS, et al. Stimulant-induced dopamine increases are markedly blunted in active cocaine abusers. Mol Psychiatry 2014;19:1037–1043.
  • Volkow ND, Wang G-J, Telang F, Fowler JS, Logan J, Childress A-R, Jayne M, et al. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci Off J Soc Neurosci 2006;26:6583–6588.
  • Wong DF, Kuwabara H, Schretlen DJ, Bonson KR, Zhou Y, Nandi A, Brasic JR, et al. Increased occupancy of dopamine receptors in human striatum during cue-elicited cocaine craving. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2006;31:2716–2727.
  • Johanson C-E, Frey KA, Lundahl LH, Keenan P, Lockhart N, Roll J, Galloway GP, et al. Cognitive function and nigrostriatal markers in abstinent methamphetamine abusers. Psychopharmacology 2006;185:327–338.
  • McCann UD, Kuwabara H, Kumar A, Palermo M, Abbey R, Brasic J, Ye W, et al. Persistent cognitive and dopamine transporter deficits in abstinent methamphetamine users. Synapse (New York, NY) 2008;62:91–100.
  • Boileau I, Rusjan P, Houle S, Wilkins D, Tong J, Selby P, Guttman M, et al. Increased vesicular monoamine transporter binding during early abstinence in human methamphetamine users: Is VMAT2 a stable dopamine neuron biomarker? J Neurosci Off J Soc Neurosci 2008;28:9850–9856.
  • Boileau I, McCluskey T, Tong J, Furukawa Y, Houle S, Kish SJ. Rapid recovery of vesicular dopamine levels in methamphetamine users in early abstinence. Neuropsychopharmacology 2016;41:1179–1187.
  • Narendran R, Lopresti BJ, Martinez D, Mason NS, Himes M, May MA, Daley DC, et al. In vivo evidence for low striatal vesicular monoamine transporter 2 (VMAT2) availability in cocaine abusers. Am J Psychiatry 2012;169:55–63.
  • Martinez D, Slifstein M, Narendran R, Foltin RW, Broft A, Hwang D-R, Perez A, et al. Dopamine D1 receptors in cocaine dependence measured with PET and the choice to self-administer cocaine. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol 2009;34:1774–1782.
  • Martinez D, Greene K, Broft A, Kumar D, Liu F, Narendran R, Slifstein M, et al. Lower level of endogenous dopamine in patients with cocaine dependence: findings from PET imaging of D(2)/D(3) receptors following acute dopamine depletion. Am J Psychiatry 2009;166:1170–1177.
  • Lee B, London ED, Poldrack RA, Farahi J, Nacca A, Monterosso JR, Mumford JA, et al. Striatal dopamine d2/d3 receptor availability is reduced in methamphetamine dependence and is linked to impulsivity. J Neurosci Off J Soc Neurosci 2009; 29:14734–14740.
  • Boileau I, Payer D, Houle S, Behzadi A, Rusjan PM, Tong J, Wilkins D, et al. Higher binding of the dopamine D3 receptor-preferring ligand [11C]-(+)-propyl-hexahydro-naphtho-oxazin in methamphetamine polydrug users: a positron emission tomography study. J Neurosci 2012;32:1353–1359.
  • Payer DE, Behzadi A, Kish SJ, Houle S, Wilson AA, Rusjan PM, Tong J, et al. Heightened D(3) dopamine receptor levels in cocaine dependence and contributions to the addiction behavioral phenotype: a positron emission tomography study with [(11)C]-(+)-PHNO. Neuropsychopharmacology 2014;39:311–318.
  • Matuskey D, Gallezot JD, Pittman B, Williams W, Wanyiri J, Gaiser E, Lee DE, et al. Dopamine D(3) receptor alterations in cocaine-dependent humans imaged with [(1)(1)C](+)PHNO. Drug Alcohol Depend 2014;139:100–105.
  • Daglish MR, Williams TM, Wilson SJ, Taylor LG, Eap CB, Augsburger M, Giroud C, et al. Brain dopamine response in human opioid addiction. Br J Psychiatry 2008;193:65–72.
  • Watson BJ, Taylor LG, Reid AG, Wilson SJ, Stokes PR, Brooks DJ, Myers JF, et al. Investigating expectation and reward in human opioid addiction with [(11) C]raclopride PET. Addict Biol 2014;19:1032–1040.
  • Martinez D, Saccone PA, Liu F, Slifstein M, Orlowska D, Grassetti A, Cook S, et al. Deficits in dopamine D(2) receptors and presynaptic dopamine in heroin dependence: commonalities and differences with other types of addiction. Biol Psychiatry 2012;71:192–198.
  • Shi J, Zhao LY, Copersino ML, Fang YX, Chen Y, Tian J, Deng Y, et al. PET imaging of dopamine transporter and drug craving during methadone maintenance treatment and after prolonged abstinence in heroin users. Eur J Pharmacol 2008;579:160–166.
  • Stokes PRA, Mehta MA, Curran HV, Breen G, Grasby PM. Can recreational doses of THC produce significant dopamine release in the human striatum? NeuroImage 2009;48:186–190.
  • Bossong MG, van Berckel BN, Boellaard R, Zuurman L, Schuit RC, Windhorst AD, van Gerven JM, et al. Delta 9-tetrahydrocannabinol induces dopamine release in the human striatum. Neuropsychopharmacology 2009;34:759–766.
  • Bossong MG, Mehta MA, van Berckel BN, Howes OD, Kahn RS, Stokes PR. Further human evidence for striatal dopamine release induced by administration of 9-tetrahydrocannabinol (THC): selectivity to limbic striatum. Psychopharmacology (Berl) 2015; 232:2723–2729.
  • Kuepper R, Ceccarini J, Lataster J, van Os J, van Kroonenburgh M, van Gerven JM, Marcelis M, et al. Delta-9-tetrahydrocannabinol-induced dopamine release as a function of psychosis risk: 18F-fallypride positron emission tomography study. PLoS One 2013;8:e70378.
  • Albrecht DS, Skosnik PD, Vollmer JM, Brumbaugh MS, Perry KM, Mock BH, Zheng QH, et al. Striatal D(2)/D(3) receptor availability is inversely correlated with cannabis consumption in chronic marijuana users. Drug Alcohol Depend 2013;128:52–57.
  • Sevy S, Smith GS, Ma Y, Dhawan V, Chaly T, Kingsley PB, Kumra S, et al. Cerebral glucose metabolism and D2/D3 receptor availability in young adults with cannabis dependence measured with positron emission tomography. Psychopharmacology (Berl) 2008;197:549–556.
  • Stokes PR, Egerton A, Watson B, Reid A, Lappin J, Howes OD, Nutt DJ, Lingford-Hughes AR. History of cannabis use is not associated with alterations in striatal dopamine D2/D3 receptor availability. J Psychopharmacol 2012;26:144–149.
  • Urban NB, Slifstein M, Thompson JL, Xu X, Girgis RR, Raheja S, Haney M, Abi-Dargham A. Dopamine release in chronic cannabis users: a [11c]raclopride positron emission tomography study. Biol Psychiatry 2012;71:677–683.
  • Volkow ND, Wang GJ, Telang F, Fowler JS, Alexoff D, Logan J, Jayne M, et al. Decreased dopamine brain reactivity in marijuana abusers is associated with negative emotionality and addiction severity. Proc Natl Acad Sci USA 2014;111:E3149–E3156.
  • Bloomfield MA, Morgan CJ, Egerton A, Kapur S, Curran HV, Howes OD. Dopaminergic function in cannabis users and its relationship to cannabis-induced psychotic symptoms. Biol Psychiatry 2014;75:470–478.
  • Bloomfield MA, Morgan CJ, Kapur S, Curran HV, Howes OD. The link between dopamine function and apathy in cannabis users: an [18F]-DOPA PET imaging study. Psychopharmacology (Berl) 2014;231:2251–2259.
  • Madras BK. Dopamine challenge reveals neuroadaptive changes in marijuana abusers. Proc Natl Acad Sci USA 2014;111:11915–11916.
  • Ghazzaoui R, Abi-Dargham A. Imaging dopamine transmission parameters in cannabis dependence. Prog Neuropsychopharmacol Biol Psychiatry 2014;52:28–32.
  • Sevy S, Smith GS, Ma Y, Dhawan V, Chaly T, Kingsley PB, Kumra S, et al. Cerebral glucose metabolism and D2/D3 receptor availability in young adults with cannabis dependence measured with positron emission tomography. Psychopharmacology 2008;197:549–556.
  • Nutt DJ, Lingford-Hughes A, Erritzoe D, Stokes PR. The dopamine theory of addiction: 40 years of highs and lows. Nat Rev Neurosci 2015;16:305–312.
  • Leggio GM, Camillieri G, Platania CB, Castorina A, Marrazzo G, Torrisi SA, Nona CN, et al. Dopamine D3 receptor is necessary for ethanol consumption: an approach with buspirone. Neuropsychopharmacology 2014;39:2017–228.
  • Le Foll B, Diaz J, Sokoloff P. Increased dopamine D3 receptor expression accompanying behavioral sensitization to nicotine in rats. Synapse 2003;47:176–183.
  • Le Foll B, Diaz J, Sokoloff P. A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning. Neuroreport 2005;16:175–178.
  • Heidbreder CA, Newman AH. Current perspectives on selective dopamine D(3) receptor antagonists as pharmacotherapeutics for addictions and related disorders. Ann NY Acad Sci 2010;1187:4–34.

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