Unbalanced neuronal circuits in addiction

Current Opinion in Neurobiology

Volumn 23, Issue 4, 2013, Pages 639-648

  Volkow, Nora D ^a   Wang, Gen Jack ^b   Tomasi, Dardo ^b   Baler, Ruben D ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADDICTION; AMYGDALOID NUCLEUS; BRAIN MAPPING; BRAIN REGION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; EPITHALAMUS; HABITUATION; HUMAN; INSULA; LIMBIC SYSTEM; MESOLIMBIC DOPAMINERGIC SYSTEM; MESOSTRIATOCORTICAL SYSTEM; NERVOUS SYSTEM; NEUROPATHOLOGY; NEUROTRANSMISSION; PRIORITY JOURNAL; REVIEW; SUBTHALAMIC NUCLEUS; THALAMUS;

EID: 84881026905     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.01.002     Document Type: Review

References (101)

1. Bechara A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 2005, 8:1458-1463.
2. Blum K., Gardner E., Oscar-Berman M., Gold M. 'Liking' and 'wanting' linked to Reward Deficiency Syndrome (RDS): hypothesizing differential responsivity in brain reward circuitry. Curr Pharm Des 2012, 18:113-118.
3. Berridge K.C. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 2007, 191:391-431.
4. Koob G.F., Stinus L., Le Moal M., Bloom F.E. Opponent process theory of motivation: neurobiological evidence from studies of opiate dependence. Neurosci Biobehav Rev 1989, 13:135-140.
5. Redish A.D., Jensen S., Johnson A. A unified framework for addiction: vulnerabilities in the decision process. Behav Brain Sci 2008, 31:415-437. discussion 437-487.
6. Belin D., Jonkman S., Dickinson A., Robbins T.W., Everitt B.J. Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav Brain Res 2009, 199:89-102.
7. Kalivas P.W., Volkow N.D. The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 2005, 162:1403-1413.
8. Moussawi K., Kalivas P.W. Group II metabotropic glutamate receptors (mGlu2/3) in drug addiction. Eur J Pharmacol 2010, 639:115-122.
9. Sesack S.R., Grace A.A. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 2010, 35:27-47.
10. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005, 8:1481-1489.
11. Choi J.S., Shin Y.C., Jung W.H., Jang J.H., Kang D.H., Choi C.H., Choi S.W., Lee J.Y., Hwang J.Y., Kwon J.S. Altered brain activity during reward anticipation in pathological gambling and obsessive-compulsive disorder. PLoS One 2012, 7:e45938.
12. Filbey F.M., Myers U.S., Dewitt S. Reward circuit function in high BMI individuals with compulsive overeating: Similarities with addiction. Neuroimage 2012, 63:1800-1806.
13. Goldstein R.Z., Volkow N.D. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 2012, 12:652-669.
14. Barnes T.D., Kubota Y., Hu D., Jin D.Z., Graybiel A.M. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 2005, 437:1158-1161.
15. Graybiel A.M. Habits, rituals, and the evaluative brain. Annu Rev Neurosci 2008, 31:359-387.
16. Graybiel A.M. The basal ganglia and chunking of action repertoires. Neurobiol Learn Mem 1998, 70:119-136.
17. Girault J.A. Integrating neurotransmission in striatal medium spiny neurons. Adv Exp Med Biol 2012, 970:407-429.
18. Shiflett M.W., Balleine B.W. Molecular substrates of action control in cortico-striatal circuits. Prog Neurobiol 2011, 95:1-13.
19. Rodriguez Parkitna J., Engblom D. Addictive drugs and plasticity of glutamatergic synapses on dopaminergic neurons: what have we learned from genetic mouse models?. Front Mol Neurosci 2012, 5:89.
20. Morales M., Pickel V.M. Insights to drug addiction derived from ultrastructural views of the mesocorticolimbic system. Ann N Y Acad Sci 2012, 1248:71-88.
21. Surmeier D.J., Ding J., Day M., Wang Z., Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 2007, 30:228-235.
22. Berglind W.J., Case J.M., Parker M.P., Fuchs R.A., See R.E. Dopamine D1 or D2 receptor antagonism within the basolateral amygdala differentially alters the acquisition of cocaine-cue associations necessary for cue-induced reinstatement of cocaine-seeking. Neuroscience 2006, 137:699-706.
23. Luo Z., Volkow N.D., Heintz N., Pan Y., Du C. Acute cocaine induces fast activation of D1 receptor and progressive deactivation of D2 receptor striatal neurons: in vivo optical microprobe [Ca2+]i imaging. J Neurosci 2011, 31:13180-13190.
24. Eagle D.M., Wong J.C., Allan M.E., Mar A.C., Theobald D.E., Robbins T.W. Contrasting roles for dopamine D1 and D2 receptor subtypes in the dorsomedial striatum but not the nucleus accumbens core during behavioral inhibition in the stop-signal task in rats. J Neurosci 2011, 31:7349-7356.
25. Parker J.G., Zweifel L.S., Clark J.J., Evans S.B., Phillips P.E., Palmiter R.D. Absence of NMDA receptors in dopamine neurons attenuates dopamine release but not conditioned approach during Pavlovian conditioning. Proc Natl Acad Sci U S A 2010, 107:13491-13496.
26. Thompson D., Martini L., Whistler J.L. Altered ratio of D1 and D2 dopamine receptors in mouse striatum is associated with behavioral sensitization to cocaine. PLoS One 2010, 5:e11038.
27. Volkow N.D., Fowler J.S., Wolf A.P., Schlyer D., Shiue C.Y., Alpert R., Dewey S.L., Logan J., Bendriem B., Christman D., et al. Effects of chronic cocaine abuse on postsynaptic dopamine receptors. Am J Psychiatry 1990, 147:719-724.
28. Feil J., Sheppard D., Fitzgerald P.B., Yucel M., Lubman D.I., Bradshaw J.L. Addiction, compulsive drug seeking, and the role of frontostriatal mechanisms in regulating inhibitory control. Neurosci Biobehav Rev 2010, 35:248-275.
29. Muhammad A., Carroll C., Kolb B. Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 2012, 216:103-109.
30. Eluvathingal T.J., Chugani H.T., Behen M.E., Juhasz C., Muzik O., Maqbool M., Chugani D.C., Makki M. Abnormal brain connectivity in children after early severe socioemotional deprivation: a diffusion tensor imaging study. Pediatrics 2006, 117:2093-2100.
31. Laplante D.P., Brunet A., Schmitz N., Ciampi A., King S. Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry 2008, 47:1063-1072.
32. Bennett D.S., Bendersky M., Lewis M. Children's cognitive ability from 4 to 9 years old as a function of prenatal cocaine exposure, environmental risk, and maternal verbal intelligence. Dev Psychol 2008, 44:919-928.
33. Rosenberg S.D., Lu W., Mueser K.T., Jankowski M.K., Cournos F. Correlates of adverse childhood events among adults with schizophrenia spectrum disorders. Psychiatr Serv 2007, 58:245-253.
34. Stinson F.S., Ruan W.J., Pickering R., Grant B.F. Cannabis use disorders in the USA: prevalence, correlates and co-morbidity. Psychol Med 2006, 36:1447-1460.
35. Tomasi D, Volkow N: Functional connectivity of substantia nigra and ventral tegmental area: maturation during adolescence and effects of ADHD. Cereb Cortex 2013, in press.
36. Ungless M.A., Singh V., Crowder T.L., Yaka R., Ron D., Bonci A. Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron 2003, 39:401-407.
37. Wise R.A., Morales M. A ventral tegmental CRF-glutamate-dopamine interaction in addiction. Brain Res 2010, 1314:38-43.
38. Wang H.L., Morales M. Corticotropin-releasing factor binding protein within the ventral tegmental area is expressed in a subset of dopaminergic neurons. J Comp Neurol 2008, 509:302-318.
39. Ousdal O.T., Reckless G.E., Server A., Andreassen O.A., Jensen J. Effect of relevance on amygdala activation and association with the ventral striatum. Neuroimage 2012, 62:95-101.
40. Koob G.F., Le Moal M. Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat Neurosci 2005, 8:1442-1444.
41. Pickens C.L., Airavaara M., Theberge F., Fanous S., Hope B.T., Shaham Y. Neurobiology of the incubation of drug craving. Trends Neurosci 2011, 34:411-420.
42. Stevenson C.W., Gratton A. Basolateral amygdala modulation of the nucleus accumbens dopamine response to stress: role of the medial prefrontal cortex. Eur J Neurosci 2003, 17:1287-1295.
43. Xi Z.X., Li X., Li J., Peng X.Q., Song R., Gaal J., Gardner E.L. Blockade of dopamine D(3) receptors in the nucleus accumbens and central amygdala inhibits incubation of cocaine craving in rats. Addict Biol 2012.
44. Langevin J.P. The amygdala as a target for behavior surgery. Surg Neurol Int 2012, 3:S40-S46.
45. Paulus M.P., Tapert S.F., Schulteis G. The role of interoception and alliesthesia in addiction. Pharmacol Biochem Behav 2009, 94:1-7.
46. Bonson K.R., Grant S.J., Contoreggi C.S., Links J.M., Metcalfe J., Weyl H.L., Kurian V., Ernst M., London E.D. Neural systems and cue-induced cocaine craving. Neuropsychopharmacology 2002, 26:376-386.
47. Pelchat M.L., Johnson A., Chan R., Valdez J., Ragland J.D. Images of desire: food-craving activation during fMRI. Neuroimage 2004, 23:1486-1493.
48. Wang Z., Faith M., Patterson F., Tang K., Kerrin K., Wileyto E.P., Detre J.A., Lerman C. Neural substrates of abstinence-induced cigarette cravings in chronic smokers. J Neurosci 2007, 27:14035-14040.
49. Verdejo-Garcia A., Clark L., Dunn B.D. The role of interoception in addiction: a critical review. Neurosci Biobehav Rev 2012, 36:1857-1869.
50. Naqvi N.H., Rudrauf D., Damasio H., Bechara A. Damage to the insula disrupts addiction to cigarette smoking. Science 2007, 315:531-534.
51. Kang O.S., Chang D.S., Jahng G.H., Kim S.Y., Kim H., Kim J.W., Chung S.Y., Yang S.I., Park H.J., Lee H., et al. Individual differences in smoking-related cue reactivity in smokers: an eye-tracking and fMRI study. Prog Neuropsychopharmacol Biol Psychiatry 2012, 38:285-293.
52. Goudriaan A.E., de Ruiter M.B., van den Brink W., Oosterlaan J., Veltman D.J. Brain activation patterns associated with cue reactivity and craving in abstinent problem gamblers, heavy smokers and healthy controls: an fMRI study. Addict Biol 2010, 15:491-503.
53. Padula C.B., Simmons A.N., Matthews S.C., Robinson S.K., Tapert S.F., Schuckit M.A., Paulus M.P. Alcohol attenuates activation in the bilateral anterior insula during an emotional processing task: a pilot study. Alcohol Alcohol 2011, 46:547-552.
54. Gardini S., Venneri A. Reduced grey matter in the posterior insula as a structural vulnerability or diathesis to addiction. Brain Res Bull 2012, 87:205-211.
55. Goldstein R.Z., Craig A.D., Bechara A., Garavan H., Childress A.R., Paulus M.P., Volkow N.D. The neurocircuitry of impaired insight in drug addiction. Trends Cogn Sci 2009, 13:372-380.
56. Naqvi N.H., Bechara A. The hidden island of addiction: the insula. Trends Neurosci 2009, 32:56-67.
57. Janes A.C., Pizzagalli D.A., Richardt S., de B.F.B., Chuzi S., Pachas G., Culhane M.A., Holmes A.J., Fava M., Evins A.E., et al. Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biol Psychiatry 2010, 67:722-729.
58. Tomasi D., Volkow N.D. Association between functional connectivity hubs and brain networks. Cereb Cortex 2011, 21:2003-2013.
59. Tomasi D., Volkow N.D., Wang R., Carrillo J.H., Maloney T., Alia-Klein N., Woicik P.A., Telang F., Goldstein R.Z. Disrupted functional connectivity with dopaminergic midbrain in cocaine abusers. PLoS One 2010, 5:e10815.
60. Volkow N.D., Kim S., Wang G.J., Alexoff D., Logan J., Muench L., Shea C., Telang F., Fowler J.S., Wong C., et al. Acute alcohol intoxication decreases glucose metabolism but increases acetate uptake in the human brain. Neuroimage 2013, 64:277-283.
61. Moeller S.J., Tomasi D., Woicik P.A., Maloney T., Alia-Klein N., Honorio J., Telang F., Wang G.J., Wang R., Sinha R., et al. Enhanced midbrain response at 6-month follow-up in cocaine addiction, association with reduced drug-related choice. Addict Biol 2012, 17:1013-1025.
62. Temel Y., Blokland A., Steinbusch H.W., Visser-Vandewalle V. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol 2005, 76:393-413.
63. Zaghloul K.A., Weidemann C.T., Lega B.C., Jaggi J.L., Baltuch G.H., Kahana M.J. Neuronal activity in the human subthalamic nucleus encodes decision conflict during action selection. J Neurosci 2012, 32:2453-2460.
64. Whitmer D., White C. Evidence of human subthalamic nucleus involvement in decision making. J Neurosci 2012, 32:8753-8755.
65. Weiland B.J., Nigg J.T., Welsh R.C., Yau W.Y., Zubieta J.K., Zucker R.A., Heitzeg M.M. Resiliency in adolescents at high risk for substance abuse: flexible adaptation via subthalamic nucleus and linkage to drinking and drug use in early adulthood. Alcohol Clin Exp Res 2012, 36:1355-1364.
66. van Wouwe N.C., Ridderinkhof K.R., van den Wildenberg W.P., Band G.P., Abisogun A., Elias W.J., Frysinger R., Wylie S.A. Deep brain stimulation of the subthalamic nucleus improves reward-based decision-learning in Parkinson's disease. Front Hum Neurosci 2011, 5:30.
67. Chabardes S., Polosan M., Krack P., Bastin J., Krainik A., David O., Bougerol T., Benabid A.L. Deep brain stimulation for obsessive-compulsive disorder: subthalamic nucleus target. World Neurosurg 2013, in press.
68. Rouaud T., Lardeux S., Panayotis N., Paleressompoulle D., Cador M., Baunez C. Reducing the desire for cocaine with subthalamic nucleus deep brain stimulation. Proc Natl Acad Sci U S A 2010, 107:1196-1200.
69. Matsumoto M., Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 2007, 447:1111-1115.
70. Matsumoto M., Hikosaka O. Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 2009, 12:77-84.
71. Zhang F., Zhou W., Liu H., Zhu H., Tang S., Lai M., Yang G. Increased c-Fos expression in the medial part of the lateral habenula during cue-evoked heroin-seeking in rats. Neurosci Lett 2005, 386:133-137.
72. Brown R.M., Short J.L., Lawrence A.J. Identification of brain nuclei implicated in cocaine-primed reinstatement of conditioned place preference: a behaviour dissociable from sensitization. PLoS One 2011, 5:e15889.
73. Baldwin P.R., Alanis R., Salas R. The role of the habenula in nicotine addiction. J Addict Res Ther 2011, S1.
74. Volkow N.D., Wang G.J., Ma Y., Fowler J.S., Zhu W., Maynard L., Telang F., Vaska P., Ding Y.S., Wong C., et al. Expectation enhances the regional brain metabolic and the reinforcing effects of stimulants in cocaine abusers. J Neurosci 2003, 23:11461-11468.
75. Anderson C.M., Maas L.C., Frederick B., Bendor J.T., Spencer T.J., Livni E., Lukas S.E., Fischman A.J., Madras B.K., Renshaw P.F., et al. Cerebellar vermis involvement in cocaine-related behaviors. Neuropsychopharmacology 2006, 31:1318-1326.
76. Janu L., Rackova S., Horacek J. Regional cerebellar metabolism (18FDG PET) predicts the clinical outcome of the short-term inpatient treatment of alcohol addiction. Neuro Endocrinol Lett 2012, 33.
77. Kalivas P.W., McFarland K. Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl) 2003, 168:44-56.
78. Ikai Y., Takada M., Mizuno N. Single neurons in the ventral tegmental area that project to both the cerebral and cerebellar cortical areas by way of axon collaterals. Neuroscience 1994, 61:925-934.
79. Zeki S., Romaya J. The brain reaction to viewing faces of opposite- and same-sex romantic partners. PLoS One 2010, 5:e15802.
80. Di Chiara G. Drug addiction as dopamine-dependent associative learning F disorder. Eur J Pharmacol 1999, 375:13-30.
81. Volkow N.D., Wang G.J., Fowler J.S., Logan J., Gatley S.J., Hitzemann R., Chen A.D., Dewey S.L., Pappas N. Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature 1997, 386:830-833.
82. Goldstein R.Z., Volkow N.D. Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 2002, 159:1642-1652.
83. Volkow N.D., Wang G.J., Tomasi D., Baler R.D. Obesity and addiction: neurobiological overlaps. Obes Rev 2013, 14:2-18.
84. Volkow N.D., Fowler J.S., Wang G.J., Hitzemann R., Logan J., Schlyer D.J., Dewey S.L., Wolf A.P. Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 1993, 14:169-177.
85. Volkow N.D., Chang L., Wang G.J., Fowler J.S., Ding Y.S., Sedler M., Logan J., Franceschi D., Gatley J., Hitzemann R., et al. Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am J Psychiatry 2001, 158:2015-2021.
86. Volkow N.D., Wang G.J., Telang F., Fowler J.S., Logan J., Jayne M., Ma Y., Pradhan K., Wong C. Profound decreases in dopamine release in striatum in detoxified alcoholics: possible orbitofrontal involvement. J Neurosci 2007, 27:12700-12706.
87. Chang L., Chronicle E.P. Functional imaging studies in cannabis users. Neuroscientist 2007, 13:422-432.
88. Volkow N., Hitzemann R., Wang G.J., Fowler J., Wolf A., Dewey S., Handlesman L. Long-term frontal brain metabolic changes in cocaine abusers. Synapse 1992, 11:184-190.
89. Goldstein R.Z., Woicik P.A., Maloney T., Tomasi D., Alia-Klein N., Shan J., Honorio J., Samaras D., Wang R., Telang F., et al. Oral methylphenidate normalizes cingulate activity in cocaine addiction during a salient cognitive task. Proc Natl Acad Sci U S A 2010, 107:16667-16672.
90. Volkow N.D., Fowler J.S. Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex 2000, 10:318-325.
91. Yuan K., Qin W., Wang G., Zeng F., Zhao L., Yang X., Liu P., Liu J., Sun J., von Deneen K.M., et al. Microstructure abnormalities in adolescents with internet addiction disorder. PLoS One 2012, 6:e20708.
92. St Onge J.R., Abhari H., Floresco S.B. Dissociable contributions by prefrontal D1 and D2 receptors to risk-based decision making. J Neurosci 2011, 31:8625-8633.
93. Volkow N., Fowler J. Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex 2000, 10:318-325.
94. Volkow N.D., Wang G.J., Begleiter H., Porjesz B., Fowler J.S., Telang F., Wong C., Ma Y., Logan J., Goldstein R., et al. High levels of dopamine D2 receptors in unaffected members of alcoholic families: possible protective factors. Arch Gen Psychiatry 2006, 63:999-1008.
95. Ersche K.D., Jones P.S., Williams G.B., Turton A.J., Robbins T.W., Bullmore E.T. Abnormal brain structure implicated in stimulant drug addiction. Science 2012, 335:601-604.
96. Parvaz M.A., Maloney T., Moeller S.J., Woicik P.A., Alia-Klein N., Telang F., Wang G.J., Squires N.K., Volkow N.D., Goldstein R.Z. Sensitivity to monetary reward is most severely compromised in recently abstaining cocaine addicted individuals: a cross-sectional ERP study. Psychiatry Res 2012, 203:75-82.
97. Goldstein R.Z., Volkow N.D. Oral methylphenidate normalizes cingulate activity and decreases impulsivity in cocaine addiction during an emotionally salient cognitive task. Neuropsychopharmacology 2011, 36:366-367.
98. Luigjes J., van den Brink W., Feenstra M., van den Munckhof P., Schuurman P.R., Schippers R., Mazaheri A., De Vries T.J., Denys D. Deep brain stimulation in addiction: a review of potential brain targets. Mol Psychiatry 2011, 17:572-583.
99. Marsch L.A., Dallery J. Advances in the psychosocial treatment of addiction: the role of technology in the delivery of evidence-based psychosocial treatment. Psychiatr Clin North Am 2012, 35:481-493.
100. Eisenberger N.I., Cole S.W. Social neuroscience and health: neurophysiological mechanisms linking social ties with physical health. Nat Neurosci 2012, 15:669-674.
101. Bromberg-Martin E.S., Matsumoto M., Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.