Neural systems of reinforcement for drug addiction: from actions to habits to compulsion (original) (raw)
Haber, S.N., Fudge, J.L. & McFarland, N.R. Striatonigral pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci.20, 2369–2382 (2000). ArticleCASPubMedPubMed Central Google Scholar
Dickinson, A. & Balleine, B. Motivational control of goal-directed action. Anim. Learn. Behav.22, 1–18 (1994). Article Google Scholar
White, N.M. & McDonald, R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem.77, 125–184 (2002). ArticlePubMed Google Scholar
O'Brien, C.P. & McLellan, A.T. Myths about the treatment of addiction. Lancet347, 237–240 (1996). ArticleCASPubMed Google Scholar
Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci.23, 473–500 (2000). ArticleCASPubMed Google Scholar
Fiorillo, C.D., Tobler, P.N. & Schultz, W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science299, 1898–1902 (2003). ArticleCASPubMed Google Scholar
Robbins, T.W. & Everitt, B.J. Functions of dopamine in the dorsal and ventral striatum. Seminars in the Neurosciences4, 119–128 (1992). Article Google Scholar
Ito, R., Dalley, J.W., Howes, S.R., Robbins, T.W. & Everitt, B.J. Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behavior in rats. J. Neurosci.20, 7489–7495 (2000). ArticleCASPubMedPubMed Central Google Scholar
Parkinson, J.A., Olmstead, M.C., Burns, L.H., Robbins, T.W. & Everitt, B.J. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive Pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J. Neurosci.19, 2401–2411 (1999). ArticleCASPubMedPubMed Central Google Scholar
Di Ciano, P., Cardinal, R.N., Cowell, R.A., Little, S.J. & Everitt, B.J. Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of Pavlovian approach behavior. J. Neurosci.21, 9471–9477 (2001). ArticleCASPubMedPubMed Central Google Scholar
Dalley, J.W. et al. Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc. Natl. Acad. Sci. USA102, 6189–6194 (2005). ArticleCASPubMedPubMed Central Google Scholar
Hall, J., Parkinson, J.A., Connor, T.M., Dickinson, A. & Everitt, B.J. Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur. J. Neurosci.13, 1984–1992 (2001). ArticleCASPubMed Google Scholar
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. J. Neurosci.20, 8122–8130 (2000). ArticleCASPubMedPubMed Central Google Scholar
Robinson, T.E. & Berridge, K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev.18, 247–291 (1993). ArticleCASPubMed Google Scholar
Kearns, D.N. & Weiss, S.J. Sign-tracking (autoshaping) in rats: A comparison of cocaine and food as unconditioned stimuli. Learn. Behav.32, 463–476 (2004). ArticlePubMed Google Scholar
Grimm, J.W., Kruzich, P.J. & See, R.E. Contingent access to stimuli associated with cocaine self- administration is required for reinstatement of drug-seeking behavior. Psychobiology28, 383–386 (2000). CAS Google Scholar
Di Ciano, P. & Everitt, B.J. Differential control over drug-seeking behavior by drug-associated conditioned reinforcers and discriminative stimuli predictive of drug availability. Behav. Neurosci.117, 952–960 (2003). ArticlePubMed Google Scholar
Cardinal, R.N. & Everitt, B.J. Neural and psychological mechanisms underlying appetitive learning: links to drug addiction. Curr. Opin. Neurobiol.14, 156–162 (2004). ArticleCASPubMed Google Scholar
Everitt, B.J., Dickinson, A. & Robbins, T.W. The neuropsychological basis of addictive behaviour. Brain Res. Brain Res. Rev.36, 129–138 (2001). ArticleCASPubMed Google Scholar
Cardinal, R.N., Robbins, T.W. & Everitt, B.J. The effects of d-amphetamine, chlordiazepoxide, alpha- flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats. Psychopharmacology (Berl.)152, 362–375 (2000). ArticleCAS Google Scholar
Taylor, J.R. & Robbins, T.W. Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology (Berl.)84, 405–412 (1984). ArticleCAS Google Scholar
Di Ciano, P. & Everitt, B.J. Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin or sucrose: implications for the persistence of addictive behaviour. Neuropharmacology47 (Suppl.) 202–213 (2004). ArticleCASPubMed Google Scholar
Everitt, B.J. & Robbins, T.W. Second-order schedules of drug reinforcement in rats and monkeys: measurement of reinforcing efficacy and drug-seeking behaviour. Psychopharmacology (Berl.)153, 17–30 (2000). ArticleCAS Google Scholar
Groenewegen, H.J., Wright, C.I. & Beijer, A.V.J. The nucleus accumbens: Gateway for limbic structures to reach the motor system? Prog. Brain Res.107, 485–511 (1996). ArticleCASPubMed Google Scholar
Ikemoto, S., Qin, M. & Liu, Z.H. The functional divide for primary reinforcement of D-amphetamine lies between the medial and lateral ventral striatum: Is the division of the accumbens core, shell, and olfactory tubercle valid? J. Neurosci.25, 5061–5065 (2005). ArticleCASPubMedPubMed Central Google Scholar
Fenu, S., Bassareo, V. & Di Chiara, G. A role for dopamine D1 receptors of the nucleus accumbens shell in conditioned taste aversion learning. J. Neurosci.21, 6897–6904 (2001). ArticleCASPubMedPubMed Central Google Scholar
Yin, H.H., Ostlund, S.B., Knowlton, B.J. & Balleine, B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci.22, 513–523 (2005). ArticlePubMed Google Scholar
Ostlund, S.B. & Balleine, B.W. Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J. Neurosci.25, 7763–7770 (2005). ArticleCASPubMedPubMed Central Google Scholar
Yin, H.H., Knowlton, B.J. & Balleine, B.W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci.19, 181–189 (2004). ArticlePubMed Google Scholar
Wolffgramm, J. & Heyne, A. From controlled drug intake to loss of control - the irreversible development of drug-addiction in the rat. Behav. Brain Res.70, 77–94 (1995). ArticleCASPubMed Google Scholar
Deroche-Gamonet, V., Belin, D. & Piazza, P.V. Evidence for addiction-like behavior in the rat. Science305, 1014–1017 (2004). ArticleCASPubMed Google Scholar
Vanderschuren, L.J. & Everitt, B.J. Drug seeking becomes compulsive after prolonged cocaine self-administration. Science305, 1017–1019 (2004). ArticleCASPubMed Google Scholar
Ito, R., Dalley, J.W., Robbins, T.W. & Everitt, B.J. Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J. Neurosci.22, 6247–6253 (2002). ArticleCASPubMedPubMed Central Google Scholar
Jakes, I. Theoretical Approaches to Obsessive-Compulsive Disorder (Cambridge Univ. Press, Cambridge, 1996). Book Google Scholar
Barrett, J.E., Katz, J.L. & Glowa, J.R. Effects of D-amphetamine on responding of squirrel-monkeys maintained under 2nd-order schedules of food presentation, electric-shock presentation or stimulus-shock termination. J. Pharmacol. Exp. Ther.218, 692–700 (1981). CASPubMed Google Scholar
Dickinson, A., Nicholas, D.J. & Adams, C.D. The effect of instrumental training contingency on susceptibility to reinforcer devaluation. Q. J. Exp. Psychol.35B, 35–51 (1983). Article Google Scholar
Faure, A., Haberland, U., Conde, F. & El Massioui, N. Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation. J. Neurosci.25, 2771–2780 (2005). ArticleCASPubMedPubMed Central Google Scholar
Dickinson, A., Wood, N. & Smith, J.W. Alcohol seeking by rats: Action or habit? Q. J. Exp. Psychol. B55, 331–348 (2002). ArticlePubMed Google Scholar
Miles, F.J., Everitt, B.J. & Dickinson, A. Oral cocaine seeking by rats: action or habit? Behav. Neurosci.117, 927–938 (2003). ArticlePubMed Google Scholar
Di Ciano, P. & Everitt, B.J. Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J. Neurosci.24, 7167–7173 (2004). ArticleCASPubMedPubMed Central Google Scholar
Vanderschuren, L.M.J., Di Ciano, P. & Everitt, B.J. Involvement of the dorsal striatum in cue-controlled cocaine seeking. J. Neurosci.25, 8665–8770 (2005). ArticleCASPubMedPubMed Central Google Scholar
Goldstein, R.Z. & Volkow, N.D. Drug addiction and its underlying neurobiological basis: Neuroimaging evidence for the involvement of the frontal cortex. Am. J. Psychiatry159, 1642–1652 (2002). ArticlePubMedPubMed Central Google Scholar
Letchworth, S.R., Nader, M.A., Smith, H.R., Friedman, D.P. & Porrino, L.J. Progression of changes in dopamine transporter binding site density as a result of cocaine self-administration in rhesus monkeys. J. Neurosci.21, 2799–2807 (2001). ArticleCASPubMedPubMed Central Google Scholar
Porrino, L.J., Lyons, D., Smith, H.R., Daunais, J.B. & Nader, M.A. Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J. Neurosci.24, 3554–3562 (2004). ArticleCASPubMedPubMed Central Google Scholar
Nader, M.A. et al. Effects of cocaine self-administration on striatal dopamine systems in rhesus monkeys: Initial and chronic exposure. Neuropsychopharmacology27, 35–46 (2002). ArticleCASPubMed Google Scholar
O'Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science304, 452–454 (2004). ArticleCASPubMed Google Scholar
Whitelaw, R.B., Markou, A., Robbins, T.W. & Everitt, B.J. Excitotoxic lesions of the basolateral amygdala impair the acquisition of cocaine-seeking behaviour under a second-order schedule of reinforcement. Psychopharmacology (Berl.)127, 213–224 (1996). ArticleCAS Google Scholar
Alderson, H.L., Robbins, T.W. & Everitt, B.J. The effects of excitotoxic lesions of the basolateral amygdala on the acquisition of heroin-seeking behaviour in rats. Psychopharmacology (Berl.)153, 111–119 (2000). ArticleCAS Google Scholar
Hutcheson, D.M., Parkinson, J.A., Robbins, T.W. & Everitt, B.J. The effects of nucleus accumbens core and shell lesions on intravenous heroin self-administration and the acquisition of drug-seeking behaviour under a second-order schedule of heroin reinforcement. Psychopharmacology (Berl.)153, 464–472 (2001). ArticleCAS Google Scholar
Ito, R., Robbins, T.W. & Everitt, B.J. Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat. Neurosci.7, 389–397 (2004). ArticleCASPubMed Google Scholar
Winstanley, C.A., Theobald, D.E.H., Cardinal, R.N. & Robbins, T.W. Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice. J. Neurosci.24, 4718–4722 (2004). ArticleCASPubMedPubMed Central Google Scholar
Cardinal, R.N. & Cheung, T.H. Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat. BMC Neurosci.6, 9 (2005). ArticlePubMedPubMed CentralCAS Google Scholar
Hutcheson, D.M. & Everitt, B.J. The effects of selective orbitofrontal cortex lesions on the acquisition and performance of cue-controlled cocaine seeking in rats. Ann. NY Acad. Sci.1003, 410–411 (2003). ArticlePubMed Google Scholar
Pears, A., Parkinson, J.A., Hopewell, L., Everitt, B.J. & Roberts, A.C. Lesions of the orbitofrontal but not medial prefrontal cortex disrupt conditioned reinforcement in primates. J. Neurosci.23, 11189–11201 (2003). ArticleCASPubMedPubMed Central Google Scholar
Schoenbaum, G., Setlow, B., Saddoris, M.P. & Gallagher, M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron39, 855–867 (2003). ArticleCASPubMed Google Scholar
Kalivas, P.W. & McFarland, K. Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl.)168, 44–56 (2003). ArticleCAS Google Scholar
Shaham, Y., Shalev, U., Lu, L., de Wit, H. & Stewart, J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl.)168, 3–20 (2003). ArticleCAS Google Scholar
Meil, W.M. & See, R.E. Lesions of the basolateral amygdala abolish the ability of drug associated cues to reinstate responding during withdrawal from self-administered cocaine. Behav. Brain Res.87, 139–148 (1997). ArticleCASPubMed Google Scholar
Fuchs, R.A., Evans, K.A., Parker, M.P. & See, R.E. Differential involvement of orbitofrontal cortex subregions in conditioned cue-induced and cocaine-primed reinstatement of cocaine seeking in rats. J. Neurosci.24, 6600–6610 (2004). ArticleCASPubMedPubMed Central Google Scholar
McFarland, K. & Kalivas, P.W. The circuitry mediating cocaine-induced reinstatement of drug seeking behavior. J. Neurosci.21, 8655–8663 (2001). ArticleCASPubMedPubMed Central Google Scholar
McFarland, K., Lapish, C.C. & Kalivas, P.W. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug seeking behavior. J. Neurosci.23, 3531–3537 (2003). ArticleCASPubMedPubMed Central Google Scholar
See, R.E., Kruzich, P.J. & Grimm, J.W. Dopamine, but not glutamate, receptor blockade in the basolateral amygdala attenuates conditioned reward in a rat model of relapse to cocaine-seeking behavior. Psychopharmacology (Berl.)154, 301–310 (2001). ArticleCAS Google Scholar
Fuchs, R.A. et al. The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology30, 296–309 (2005). ArticleCASPubMed Google Scholar
Vorel, S.R., Liu, X., Hayes, R.J., Spector, J.A. & Gardner, E.L. Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science292, 1175–1178 (2001). ArticleCASPubMed Google Scholar
Selden, N.R.W., Everitt, B.J., Jarrard, L.E. & Robbins, T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience42, 335–350 (1991). ArticleCASPubMed Google Scholar
Pennartz, C.M.A., Groenewegan, H.J. & Lopas da Silva, F.H. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog. Neurobiol.42, 719–761 (1994). ArticleCASPubMed Google Scholar
Goto, Y. & Grace, A.A. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat. Neurosci.8, 805–812 (2005). ArticleCASPubMed Google Scholar
Grace, A.A., Floresco, S.B., West, A.R. & Goto, Y. Dissociation of tonic and phasic dopamine neuron activity by afferent pathway activation: Relationship to patterns of dopamine release. Int. J. Neuropsychopharmacol.7, S15–S15 (2004). ArticleCAS Google Scholar
O'Donnell, P. Dopamine gating of forebrain neural ensembles. Eur. J. Neurosci.17, 429–435 (2003). ArticlePubMed Google Scholar
Floresco, S.B., Blaha, C.D., Yang, C.R. & Phillips, A.G. Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: cellular mechanisms of input selection. J. Neurosci.21, 2851–2860 (2001). ArticleCASPubMedPubMed Central Google Scholar
Caine, S.B., Humby, T., Robbins, T.W. & Everitt, B.J. Behavioral effects of psychomotor stimulants in rats with dorsal or ventral subiculum lesions: Locomotion, cocaine self- administration, and prepulse inhibition of startle. Behav. Neurosci.115, 880–894 (2001). ArticleCASPubMed Google Scholar
Burns, L.H., Robbins, T.W. & Everitt, B.J. Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions of D-amphetamine. Behav. Brain Res.55, 167–183 (1993). ArticleCASPubMed Google Scholar
Weissenborn, R., Robbins, T.W. & Everitt, B.J. Effects of medial prefrontal or anterior cingulate cortex lesions on responding for cocaine under fixed-ratio and second-order schedules of reinforcement in rats. Psychopharmacology (Berl.)134, 242–257 (1997). ArticleCAS Google Scholar
Dalley, J.W., Cardinal, R.N. & Robbins, T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci. Biobehav. Rev.28, 771–784 (2004). ArticleCASPubMed Google Scholar
Rogers, R.D. & Robbins, T.W. Investigating the neurocognitive deficits associated with chronic drug misuse. Curr. Opin. Neurobiol.11, 250–257 (2001). ArticleCASPubMed Google Scholar
Bolla, K.I. et al. Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task. Neuroimage19, 1085–1094 (2003). ArticleCASPubMed Google Scholar
Hester, R. & Garavan, H. Executive dysfunction in cocaine addiction: evidence for discordant frontal, cingulate, and cerebellar activity. J. Neurosci.24, 11017–11022 (2004). ArticleCASPubMedPubMed Central Google Scholar
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. Neuropharmacology47, 3–13 (2004). ArticleCASPubMed Google Scholar
Crombag, H.S., Gorny, G., Li, Y.L., Kolb, B. & Robinson, T.E. Opposite effects of amphetamine self-administration experience on dendritic spines in the medial and orbital prefrontal cortex. Cereb. Cortex15, 341–348 (2005). ArticlePubMed Google Scholar
Killcross, S. & Coutureau, E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex13, 400–408 (2003). ArticlePubMed Google Scholar
Corbit, L.H. & Balleine, B.W. The role of prelimbic cortex in instrumental conditioning. Behav. Brain Res.146, 145–157 (2003). ArticlePubMed Google Scholar
Taylor, J.R. & Horger, B.A. Enhanced responding for conditioned reward produced by intra-accumbens amphetamine is potentiated after cocaine sensitization. Psychopharmacology (Berl.)142, 31–40 (1999). ArticleCAS Google Scholar
Vezina, P. Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci. Biobehav. Rev.27, 827–839 (2004). ArticleCASPubMed Google Scholar
Koob, G.F. & Le Moal, M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology24, 97–129 (2001). ArticleCASPubMed Google Scholar
Koob, G.F. et al. Neurobiological mechanisms in the transition from drug use to drug dependence. Neurosci. Biobehav. Rev.27, 739–749 (2004). ArticleCASPubMed Google Scholar
The Frontal Lobes and Neuropsychiatric Illness (Salloway, S.P., Malloy, P.E. & Duffy, J.D., eds.) (American Psychiatric Press, Washington, D.C., 2001).
Altman, J. et al. The biological, social and clinical bases of drug addiction: Commentary and debate. Psychopharmacology (Berl.)125, 285–345 (1996). ArticleCAS Google Scholar
Stewart, J., de Wit, H. & Eikelboom, R. The role of unconditioned and conditioned drug effects in the self administration of opiates and stimulants. Psychol. Rev.91, 251–268 (1984). ArticleCASPubMed Google Scholar
Di Chiara, G. A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J. Psychopharmacol.12, 54–67 (1998). ArticleCASPubMed Google Scholar
Kadohisa, M., Rolls, E.T. & Verhagen, J.V. Orbitofrontal cortex: Neuronal representation of oral temperature and capsaicin in addition to taste and texture. Neuroscience127, 207–221 (2004). ArticleCASPubMed Google Scholar
Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A. & Dolan, R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci.7, 189–195 (2004). ArticleCASPubMed Google Scholar
Stewart, J. & de Wit, H. in Methods of Assessing the Reinforcing Properties of Abused Drugs (ed. Bozarth, M.A.) 211–227 (Springer-Verlag, New York, 1987). Book Google Scholar
Lu, L., Grimm, J.W., Hope, B.T. & Shaham, Y. Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology47, 214–226 (2004). ArticleCASPubMed Google Scholar