Impulsivity as a mediating mechanism between early-life adversity and addiction: Theoretical comment on Lovic et al. (2011)

Behavioral Neuroscience

Volumn 125, Issue 4, 2011, Pages 681-686

  Hosking, Jay ^a   Winstanley, Catharine A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Addiction; Dopamine; Early life adversity; Impulsivity; Perseveration

Indexed keywords

AMPHETAMINE; DOPAMINE;

ANATOMICAL VARIATION; BEHAVIOR; BRAIN FUNCTION; DOPAMINERGIC SYSTEM; DRUG DEPENDENCE; DRUG EXPOSURE; ELECTROENCEPHALOGRAM; HUMAN; IMPULSIVENESS; LIFE EVENT; LIMBIC SYSTEM; NONHUMAN; NOTE; NUCLEUS ACCUMBENS; ORBITAL CORTEX; PERSEVERATION; SOCIAL ISOLATION;

ANIMALS; CHOICE BEHAVIOR; FEMALE; IMPULSIVE BEHAVIOR; MALE; MATERNAL DEPRIVATION; SOCIAL ISOLATION;

EID: 79960945333     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0024612     Document Type: Note

References (75)

1. Bechara A., Dolan S., Denburg N., Hindes A., Anderson S.W., Nathan P.E. Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers. Neuropsychologia 2001, 39:376-389.
2. Bolla K.I., Eldreth D.A., London E.D., Kiehl K.A., Mouratidis M., Contoreggi C., Ernst M. Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task. Neuroimage 2003, 19:1085-1094.
3. Buckholtz, J. W., Treadway, M. T., Cowan, M. J., Woodward, N. D., Li, R., Ansari, M. S., Zald, D. H. (2010a, November). Adverse childhood experience is associated with alterations in corticolimbic D2/D3 dopamine receptor availability in humans. Paper presented at the annual meeting of Society for Neuroscience, San Diego, CA.
4. Buckholtz J.W., Treadway M.T., Cowan R.L., Woodward N.D., Li R., Ansari M.S., Zald D.H. Dopaminergic network differences in human impulsivity. Science 2010, 329:532.
5. Burton C.L., Chatterjee D., Chatterjee-Chakraborty M., Lovic V., Grella S.L., Steiner M., Fleming A.S. Prenatal restraint stress and motherless rearing disrupts expression of plasticity markers and stress-induced corticosterone release in adult female Sprague-Dawley rats. Brain Research 2007, 1158:28-38.
6. Burton C.L., Lovic V., Fleming A.S. Early adversity alters attention and locomotion in adult Sprague-Dawley rats. Behavioral Neuroscience 2006, 120:665-675.
7. 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.
8. Chudasama Y., Passetti F., Rhodes S.E., Lopian D., Desai A., Robbins T.W. Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: Differential effects on selectivity, impulsivity and compulsivity. Behavioural Brain Research 2003, 146:105-119.
9. Chugani H.T., Behen M.E., Muzik O., Juhasz C., Nagy F., Chugani D.C. Local brain functional activity following early deprivation: A study of postinstitutionalized Romanian orphans. Neuroimage 2001, 14:1290-1301.
10. Cole B.J., Robbins T.W. Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: Implications for theories of selective attention and arousal. Behavioural Brain Research 1989, 33:165-179.
11. Congdon E., Lesch K.P., Canli T. Analysis of DRD4 and DAT polymorphisms and behavioral inhibition in healthy adults: Implications for impulsivity. American Journal of Medicine Genetics B: Neuropsychiatric Genetics 2008, 147B:27-32. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics.
12. Dalley J.W., Fryer T.D., Brichard L., Robinson E.S., Theobald D.E., Laane K., Robbins T.W. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 2007, 315:1267-1270.
13. Dias R., Robbins T.W., Roberts A.C. Primate analogue of the Wisconsin Card Sorting Test: Effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behavioral Neuroscience 1996, 110:872-886.
14. Enoch M.A. The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology (Berl) 2011, 214:17-31.
15. Ersche K.D., Roiser J.P., Robbins T.W., Sahakian B.J. Chronic cocaine but not chronic amphetamine use is associated with perseverative responding in humans. Psychopharmacology (Berl) 2008, 197:421-431.
16. Faraone S.V., Biederman J. Neurobiology of attention-deficit hyperactivity disorder. Biological Psychiatry 1998, 44:951-958.
17. Fellows L.K., Farah M.J. Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. Cerebral Cortex 2005, 15:58-63.
18. Floresco S.B., St Onge J.R., Ghods-Sharifi S., Winstanley C.A. Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making. Cognitive, Affective, & Behavioral Neuroscience 2008, 8:375-389.
19. Franklin T.R., Acton P.D., Maldjian J.A., Gray J.D., Croft J.R., Dackis C.A., Childress A.R. Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients. Biological Psychiatry 2002, 51:134-142.
20. Gonzalez A., Lovic V., Ward G.R., Wainwright P.E., Fleming A.S. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats. Developmental Psychobiology 2001, 38:11-32.
21. Gooding D.C., Burroughs S., Boutros N.N. Attentional deficits in cocaine-dependent patients: Converging behavioral and electrophysiological evidence. Psychiatry Research 2008, 160:145-154.
22. Harrison A.A., Everitt B.J., Robbins T.W. Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: Interactions with dopaminergic mechanisms. Psychopharmacology (Berl) 1997, 133:329-342.
23. Hatzinger M., Brand S., Perren S., von Wyl A., von Klitzing K., Holsboer-Trachsler E. Hypothalamic-pituitary-adrenocortical (HPA) activity in kindergarten children: Importance of gender and associations with behavioral/emotional difficulties. Journal of Psychiatric Research 2007, 41:861-870.
24. Jentsch J.D., Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: Implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 1999, 146:373-390.
25. Jentsch J.D., Taylor J.R. Impaired inhibition of conditioned responses produced by subchronic administration of phencyclidine to rats. Neuropsychopharmacology 2001, 24:66-74.
26. Kjome K.L., Lane S.D., Schmitz J.M., Green C., Ma L., Prasla I., Moeller F.G. Relationship between impulsivity and decision making in cocaine dependence. Psychiatry Research 2010, 178:299-304.
27. Koob G.F., Nestler E.J. The neurobiology of drug addiction. Journal of Neuropsychiatry and Clinical Neurosciences 1997, 9:482-497.
28. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35:217-238.
29. Limosin F., Loze J.Y., Dubertret C., Gouya L., Ades J., Rouillon F., Gorwood P. Impulsiveness as the intermediate link between the dopamine receptor D2 gene and alcohol dependence. Psychiatric Genetics 2003, 13:127-129.
30. Lomanowska A.M., Lovic V., Rankine M.J., Mooney S.J., Robinson T.E., Kraemer G.W. Inadequate early social experience increases the incentive salience of reward-related cues in adulthood. Behavioural Brain Research 2011, 220:91-99.
31. Lovic V., Fleming A.S. Artificially-reared female rats show reduced prepulse inhibition and deficits in the attentional set shifting task-reversal of effects with maternal-like licking stimulation. Behavioural Brain Research 2004, 148:209-219.
32. Lovic V., Fleming A.S., Fletcher P.J. Early life tactile stimulation changes adult rat responsiveness to amphetamine. Pharmacology, Biochemistry and Behavior 2006, 84:497-503.
33. Lovic V., Gonzalez A., Fleming A.S. Maternally separated rats show deficits in maternal care in adulthood. Developmental Psychobiology 2001, 39:19-33.
34. Lovic V., Keen D., Fletcher P.J., Fleming A.S. Early-life maternal separation and social isolation produce an increase in impulsive action but not impulsive choice. Behavioral Neuroscience 2011, 125:481-491.
35. Lovic V., Saunders B.T., Yager L.M., Robinson T.E. Rats prone to attribute incentive salience to reward cues are also prone to impulsive action. Behavioural Brain Research 2011, doi: 10.1016/j.bbr.2011.04.006.
36. McAlonan K., Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behavioural Brain Research 2003, 146:97-103.
37. Mendez I.A., Simon N.W., Hart N., Mitchell M.R., Nation J.R., Wellman P.J., Setlow B. Self-administered cocaine causes long-lasting increases in impulsive choice in a delay discounting task. Behavioral Neuroscience 2010, 124:470-477.
38. Michel G.F., Tyler A.N. Critical period: A history of the transition from questions of when, to what, to how. Developmental Psychobiology 2005, 46:156-162.
39. Mobini S., Body S., Ho M.Y., Bradshaw C.M., Szabadi E., Deakin J.F., Anderson I.M. Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology (Berl) 2002, 160:290-298.
40. Moeller F.G., Dougherty D.M., Barratt E.S., Oderinde V., Mathias C.W., Harper R.A., Swann A.C. Increased impulsivity in cocaine dependent subjects independent of antisocial personality disorder and aggression. Drug and Alcohol Dependence 2002, 68:105-111.
41. Moeller F.G., Dougherty D.M., Barratt E.S., Schmitz J.M., Swann A.C., Grabowski J. The impact of impulsivity on cocaine use and retention in treatment. Journal of Substance Abuse Treatment 2001, 21:193-198.
42. Molander A.C., Mar A., Norbury A., Steventon S., Moreno M., Caprioli D., Dalley J.W. High impulsivity predicting vulnerability to cocaine addiction in rats: Some relationship with novelty preference but not novelty reactivity, anxiety or stress. Psychopharmacology (Berl) 2011, 215:721-731.
43. Nader M.A., Morgan D., Gage H.D., Nader S.H., Calhoun T.L., Buchheimer N., Mach R.H. PET imaging of dopamine D2 receptors during chronic cocaine self-administration in monkeys. Nature Neuroscience 2006, 9:1050-1056.
44. Nestler E.J. Molecular basis of long-term plasticity underlying addiction. Nature Reviews Neuroscience 2001, 2:119-128.
45. Nurco D.N., Kinlock T.W., O'Grady K.E., Hanlon T.E. Early family adversity as a precursor to narcotic addiction. Drug and Alcohol Dependence 1996, 43:103-113.
46. Patkar A.A., Murray H.W., Mannelli P., Gottheil E., Weinstein S.P., Vergare M.J. Pre-treatment measures of impulsivity, aggression and sensation seeking are associated with treatment outcome for African-American cocaine-dependent patients. Journal of Addictive Diseases 2004, 23:109-122.
47. Perry J.L., Larson E.B., German J.P., Madden G.J., Carroll M.E. Impulsivity (delay discounting) as a predictor of acquisition of IV cocaine self-administration in female rats. Psychopharmacology (Berl) 2005, 178:193-201.
48. Petry N.M. Delay discounting of money and alcohol in actively using alcoholics, currently abstinent alcoholics, and controls. Psychopharmacology (Berl) 2001, 154:243-250.
49. Ragozzino M.E. The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Annals of the New York Academy of Sciences 2007, 1121:355-375.
50. Rauscher F.H., Shaw G.L., Ky K.N. Music and spatial task-performance. Nature 1993, 365:611-612.
51. Robbins T.W. The 5-choice serial reaction time task: Behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 2002, 163:362-380.
52. Rudebeck P.H., Walton M.E., Smyth A.N., Bannerman D.M., Rushworth M.F. Separate neural pathways process different decision costs. Nature Neuroscience 2006, 9:1161-1168.
53. Salgado J.V., Malloy-Diniz L.F., Campos V.R., Abrantes S.S., Fuentes D., Bechara A., Correa H. Neuropsychological assessment of impulsive behavior in abstinent alcohol-dependent subjects. Revista Brasileira Psiquiatria 2009, 31:4-9.
54. Schmidt M.E., Rich M., Rifas-Shiman S.L., Oken E., Taveras E.M. Television viewing in infancy and child cognition at 3 years of age in a US cohort. Pediatrics 2009, 123:e370-e375.
55. Schoenbaum G., Saddoris M.P., Stalnaker T.A. Reconciling the roles of orbitofrontal cortex in reversal learning and the encoding of outcome expectancies. Annals of the New York Academy of Sciences 2007, 1121:320-335.
56. Shaham Y., Shalev U., Lu L., De Wit H., Stewart J. The reinstatement model of drug relapse: History, methodology and major findings. Psychopharmacology (Berl) 2003, 168:3-20.
57. Tanabe J., Tregellas J.R., Dalwani M., Thompson L., Owens E., Crowley T., Banich M. Medial orbitofrontal cortex gray matter is reduced in abstinent substance-dependent individuals. Biological Psychiatry 2009, 65:160-164.
58. Tarter R.E., Kirisci L., Habeych M., Reynolds M., Vanyukov M. Neurobehavior disinhibition in childhood predisposes boys to substance use disorder by young adulthood: Direct and mediated etiologic pathways. Drug and Alcohol Dependence 2004, 73:121-132.
59. Tarter R.E., Kirisci L., Mezzich A., Cornelius J.R., Pajer K., Vanyukov M., Clark D. Neurobehavioral disinhibition in childhood predicts early age at onset of substance use disorder. American Journal of Psychiatry 2003, 160:1078-1085.
60. Thomas M.S.C., Johnson M.H. New advances in understanding sensitive periods in brain development. Current Directions in Psychological Science 2008, 17:1-5.
61. Turner R.J., Lloyd D.A. Cumulative adversity and drug dependence in young adults: Racial/ethnic contrasts. Addiction 2003, 98:305-315.
62. Volkow N.D., Fowler J.S. Addiction, a disease of compulsion and drive: Involvement of the orbitofrontal cortex. Cerebral Cortex 2000, 10:318-325.
63. Volkow N.D., Fowler J.S., Wang G.J. The addicted human brain viewed in the light of imaging studies: Brain circuits and treatment strategies. Neuropharmacology, 47 Suppl 2004, 1:3-13.
64. Volkow N.D., Hitzemann R., Wang G.J., Fowler J.S., Burr G., Pascani K., Wolf A.P. Decreased brain metabolism in neurologically intact healthy alcoholics. American Journal of Psychiatry 1992, 149:1016-1022.
65. Volkow N.D., Wang G.J., Hitzemann R., Fowler J.S., Overall J.E., Burr G., Wolf A.P. Recovery of brain glucose metabolism in detoxified alcoholics. American Journal of Psychiatry 1994, 151:178-183.
66. Wallace D.L., Han M.H., Graham D.L., Green T.A., Vialou V., Iniguez S.D., Nestler E.J. CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nature Neuroscience 2009, 12:200-209.
67. Widom C.S., Weiler B.L., Cottler L.B. Childhood victimization and drug abuse: A comparison of prospective and retrospective findings. Journal of Consulting and Clinical Psychology 1999, 67:867-880.
68. Winstanley C.A. The orbitofrontal cortex, impulsivity, and addiction: Probing orbitofrontal dysfunction at the neural, neurochemical, and molecular level. Annals of the New York Academy of Sciences 2007, 1121:639-655.
69. Winstanley C.A., Bachtell R.K., Theobald D.E., Laali S., Green T.A., Kumar A., Nestler E.J. Increased impulsivity during withdrawal from cocaine self-administration: Role for DeltaFosB in the orbitofrontal cortex. Cerebral Cortex 2009, 19:435-444.
70. Winstanley C.A., Olausson P., Taylor J.R., Jentsch J.D. Insight into the relationship between impulsivity and substance abuse from studies using animal models. Alcoholism, Clinical and Experimental Research 2010, 34:1306-1318.
71. Winstanley C.A., Theobald D.E., Cardinal R.N., Robbins T.W. Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. Journal of Neuroscience 2004, 24:4718-4722.
72. Wyvell C.L., Berridge K.C. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: Enhancement of reward "wanting" without enhanced "liking" or response reinforcement. Journal of Neuroscience 2000, 20:8122-8130.
73. Zeeb F.D., Floresco S.B., Winstanley C.A. Contributions of the orbitofrontal cortex to impulsive choice: Interactions with basal levels of impulsivity, dopamine signalling, and reward-related cues. Psychopharmacology (Berl) 2010, 211:87-98.
74. Zeeb F.D., Robbins T.W., Winstanley C.A. Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 2009, 34:2329-2343.
75. Zimmerman F.J., Christakis D.A., Meltzoff A.N. Associations between media viewing and language development in children under age 2 years. Journal of Pediatrics 2007, 151:364-368.