Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction.
- Authors
- Belin, David; Jonkman, Sietse; Dickinson, Anthony; Robbins, Trevor W; Everitt, Barry J
- Year
- 2009
- Journal
- Behavioural brain research
- PMID
- 18950658
- DOI
- 10.1016/j.bbr.2008.09.027
In this review we discuss the evidence that drug addiction, defined as a maladaptive compulsive habit, results from the progressive subversion by addictive drugs of striatum-dependent operant and Pavlovian learning mechanisms that are usually involved in the control over behaviour by stimuli associated with natural reinforcement. Although mainly organized through segregated parallel cortico-striato-pallido-thalamo-cortical loops involved in motor or emotional functions, the basal ganglia, and especially the striatum, are key mediators of the modulation of behavioural responses, under the control of both action-outcome and stimulus-response mechanisms, by incentive motivational processes and Pavlovian associations. Here we suggest that protracted exposure to addictive drugs recruits serial and dopamine-dependent, striato-nigro-striatal ascending spirals from the nucleus accumbens to more dorsal regions of the striatum that underlie a shift from action-outcome to stimulus-response mechanisms in the control over drug seeking. When this progressive ventral to dorsal striatum shift is combined with drug-associated Pavlovian influences from limbic structures such as the amygdala and the orbitofrontal cortex, drug seeking behaviour becomes established as an incentive habit. This instantiation of implicit sub-cortical processing of drug-associated stimuli and instrumental responding might be a key mechanism underlying the development of compulsive drug seeking and the high vulnerability to relapse which are hallmarks of drug addiction.
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In this knowledge base
| Title | Year | PMID |
|---|---|---|
| Alcohol and basal ganglia circuitry: Animal models. | 2017 | 28341206 |
| The genetic epidemiology of substance use disorder: A review. | 2017 | 28938182 |
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| Maturation of silent synapses in amygdala-accumbens projection contributes to incubation of cocaine craving. | Lee BR et al. | β | 2013 | β |
| Rapid dopamine dynamics in the accumbens core and shell: learning and action. | Saddoris MP et al. | β | 2013 | β |
| Recent developments in animal models of drug relapse. | Marchant NJ et al. | β | 2013 | β |
| Targeting cocaine versus heroin memories: divergent roles within ventromedial prefrontal cortex. | Peters J et al. | β | 2013 | β |
| The amygdala: securing pleasure and avoiding pain. | Fernando AB et al. | β | 2013 | β |
| The contributions of value-based decision-making and attentional bias to alcohol-seeking following devaluation. | Rose AK et al. | β | 2013 | β |
| The effects of N-methyl D-aspartate and B-adrenergic receptor antagonists on the reconsolidation of reward memory: a meta-analysis. | Das RK et al. | β | 2013 | β |
| The Impact of Caffeine on the Behavioral Effects of Ethanol Related to Abuse and Addiction: A Review of Animal Studies. | LΓ³pez-Cruz L et al. | β | 2013 | β |
| Unbalanced neuronal circuits in addiction. | Volkow ND et al. | β | 2013 | β |
| Updating appetitive memory during reconsolidation window: critical role of cue-directed behavior and amygdala central nucleus. | Olshavsky ME et al. | β | 2013 | β |
| Using optogenetics to study habits. | Smith KS et al. | β | 2013 | β |
| ΞΌ-Opioid receptors within subregions of the striatum mediate pair bond formation through parallel yet distinct reward mechanisms. | Resendez SL et al. | β | 2013 | β |
| Abnormal brain structure implicated in stimulant drug addiction. | Ersche KD et al. | β | 2012 | β |
| Active and passive MDMA ('ecstasy') intake induces differential transcriptional changes in the mouse brain. | FernΓ ndez-Castillo N et al. | β | 2012 | β |
| Adenosine A(2A)-cannabinoid CB(1) receptor interaction: an integrative mechanism in striatal glutamatergic neurotransmission. | Tebano MT et al. | β | 2012 | β |
| Alcohol-related effects on automaticity due to experimentally manipulated conditioning. | Gladwin TE et al. | β | 2012 | β |
| Alpha7-nicotinic receptors modulate nicotine-induced reinforcement and extracellular dopamine outflow in the mesolimbic system in mice. | Besson M et al. | β | 2012 | β |
| Association of time-dependent changes in mu opioid receptor mRNA, but not BDNF, TrkB, or MeCP2 mRNA and protein expression in the rat nucleus accumbens with incubation of heroin craving. | Theberge FR et al. | β | 2012 | β |
| Automaticity and multiple memory systems. | Ashby FG et al. | β | 2012 | β |
| Changes in nucleus accumbens and neostriatal c-Fos and DARPP-32 immunoreactivity during different stages of food-reinforced instrumental training. | Segovia KN et al. | β | 2012 | β |
| Decomposing effects of dopaminergic medication in Parkinson's disease on probabilistic action selection--learning or performance? | Smittenaar P et al. | β | 2012 | β |
| Distinct neurochemical adaptations within the nucleus accumbens produced by a history of self-administered vs non-contingently administered intravenous methamphetamine. | Lominac KD et al. | β | 2012 | β |
| Dopamine and glutamate release in the dorsolateral caudate putamen following withdrawal from cocaine self-administration in rats. | Gabriele A et al. | β | 2012 | β |
| Double dissociation of the dorsomedial and dorsolateral striatal control over the acquisition and performance of cocaine seeking. | Murray JE et al. | β | 2012 | β |
| Effect of fenfluramine on reinstatement of food seeking in female and male rats: implications for the predictive validity of the reinstatement model. | Pickens CL et al. | β | 2012 | β |
| Enhanced dorsolateral striatal activity in drug use: the role of outcome in stimulus-response associations. | Schneck N et al. | β | 2012 | β |
| Ethanol-mediated facilitation of AMPA receptor function in the dorsomedial striatum: implications for alcohol drinking behavior. | Wang J et al. | β | 2012 | β |
| Ethanol seeking by Long Evans rats is not always a goal-directed behavior. | Mangieri RA et al. | β | 2012 | β |
| Food and drug reward: overlapping circuits in human obesity and addiction. | Volkow ND et al. | β | 2012 | β |
| Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. | Corbit LH et al. | β | 2012 | β |
| Integrating neurotransmission in striatal medium spiny neurons. | Girault JA | β | 2012 | β |
| Integrating synaptic plasticity and striatal circuit function in addiction. | Grueter BA et al. | β | 2012 | β |
| Intrastriatal shifts mediate the transition from drug-seeking actions to habits. | Belin-Rauscent A et al. | β | 2012 | β |
| Linking ADHD, impulsivity, and drug abuse: a neuropsychological perspective. | Urcelay GP et al. | β | 2012 | β |
| Neonatal exposure to antiepileptic drugs disrupts striatal synaptic development. | Forcelli PA et al. | β | 2012 | β |
| Quinpirole elicits differential in vivo changes in the pre- and postsynaptic distributions of dopamine Dβ receptors in mouse striatum: relation to cannabinoid-1 (CBβ) receptor targeting. | Lane DA et al. | β | 2012 | β |
| Responses to novelty and vulnerability to cocaine addiction: contribution of a multi-symptomatic animal model. | Belin D et al. | β | 2012 | β |
| Sex differences in the neural mechanisms mediating addiction: a new synthesis and hypothesis. | Becker JB et al. | β | 2012 | β |
| Sex hormone activity in alcohol addiction: integrating organizational and activational effects. | Lenz B et al. | β | 2012 | β |
| Signaling in striatal neurons: the phosphoproteins of reward, addiction, and dyskinesia. | Girault JA | β | 2012 | β |
| Striatal dopamine release codes uncertainty in pathological gambling. | Linnet J et al. | β | 2012 | β |
| The detrimental effects of emotional process dysregulation on decision-making in substance dependence. | Murphy A et al. | β | 2012 | β |
| The mesoaccumbens dopamine in coping with stress. | Cabib S et al. | β | 2012 | β |
| The mysterious motivational functions of mesolimbic dopamine. | Salamone JD et al. | β | 2012 | β |
| The persistence of maladaptive memory: addiction, drug memories and anti-relapse treatments. | Milton AL et al. | β | 2012 | β |
| Thorndike's Law 2.0: Dopamine and the Regulation of Thrift. | Beeler JA | β | 2012 | β |
| A comparison of economic demand and conditioned-cued reinstatement of methamphetamine-seeking or food-seeking in rats. | Galuska CM et al. | β | 2011 | β |
| Cocaine-induced plasticity in the nucleus accumbens is cell specific and develops without prolonged withdrawal. | Dobi A et al. | β | 2011 | β |
| Cortical and striatal contributions to automaticity in information-integration categorization. | Waldschmidt JG et al. | β | 2011 | β |
| Disrupting effect of drug-induced reward on spatial but not cue-guided learning: implication of the striatal protein kinase A/cAMP response element-binding protein pathway. | Baudonnat M et al. | β | 2011 | β |
| Does extinction of responses to cigarette cues occur during smoking cessation? | O'Connell KA et al. | β | 2011 | β |
| Dopamine signaling in dorsal versus ventral striatum: the dynamic role of cholinergic interneurons. | Threlfell S et al. | β | 2011 | β |
| Dorsal striatum mediation of cocaine-seeking after withdrawal from short or long daily access cocaine self-administration in rats. | Pacchioni AM et al. | β | 2011 | β |
| Effects of systemic or nucleus accumbens-directed dopamine D1 receptor antagonism on sucrose seeking in rats. | Grimm JW et al. | β | 2011 | β |
| Ethanol-induced effects on the dopamine and serotonin systems in adult Wistar rats are dependent on early-life experiences. | Oreland S et al. | β | 2011 | β |
| Ethanol-mediated long-lasting adaptations of the NR2B-containing NMDA receptors in the dorsomedial striatum. | Wang J et al. | β | 2011 | β |
| Human category learning 2.0. | Ashby FG et al. | β | 2011 | β |
| Identifying neurobiological phenotypes associated with alcohol use disorder severity. | Claus ED et al. | β | 2011 | β |
| Metabolic and hedonic drives in the neural control of appetite: who is the boss? | Berthoud HR | β | 2011 | β |
| Molecular substrates of action control in cortico-striatal circuits. | Shiflett MW et al. | β | 2011 | β |
| Neural mechanisms of operant conditioning and learning-induced behavioral plasticity in Aplysia. | Nargeot R et al. | β | 2011 | β |
| Neurobiology of the incubation of drug craving. | Pickens CL et al. | β | 2011 | β |
| Opiate versus psychostimulant addiction: the differences do matter. | Badiani A et al. | β | 2011 | β |
| Speed/accuracy trade-off between the habitual and the goal-directed processes. | Keramati M et al. | β | 2011 | β |
| Stress decreases the ability to resist smoking and potentiates smoking intensity and reward. | McKee SA et al. | β | 2011 | β |
| Striatal Dopamine and the Interface between Motivation and Cognition. | Aarts E et al. | β | 2011 | β |
| The Basal Ganglia as a Substrate for the Multiple Actions of Amphetamines. | Natarajan R et al. | β | 2011 | β |
| The role of impulsivity in the aetiology of drug dependence: reward sensitivity versus automaticity. | Hogarth L | β | 2011 | β |
| Unraveling the differential functions and regulation of striatal neuron sub-populations in motor control, reward, and motivational processes. | Ena S et al. | β | 2011 | β |
| What have positron emission tomography and 'Zippy' told us about the neuropharmacology of drug addiction? | Cumming P et al. | β | 2011 | β |
| What neurophysiological recordings tell us about cognitive and behavioral functions of the human subthalamic nucleus. | Marceglia S et al. | β | 2011 | β |
| Appetite and reward. | Fulton S | β | 2010 | β |
| Behavioral evidence for the significance of serotoninergic (5-HT) receptors in cocaine addiction. | Filip M et al. | β | 2010 | β |
| Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. | Ikemoto S | β | 2010 | β |
| Comparative neuroscience of stimulant-induced memory dysfunction: role for neurogenesis in the adult hippocampus. | Canales JJ | β | 2010 | β |
| Compulsive use of dopaminergic drug therapy in Parkinson's disease: reward and anti-reward. | Evans AH et al. | β | 2010 | β |
| Cortical and basal ganglia contributions to habit learning and automaticity. | Ashby FG et al. | β | 2010 | β |
| Discrimination between cocaine-associated context and cue in a modified conditioned place preference paradigm: role of the nNOS gene in cue conditioning. | Itzhak Y et al. | β | 2010 | β |
| Dopamine, reward, and frontostriatal circuitry in impulse control disorders in Parkinson's disease: insights from functional imaging. | Ray N et al. | β | 2010 | β |
| Effects of disconnection of amygdala dopamine and nucleus accumbens N-methyl-d-aspartate receptors on ethanol-seeking behavior in mice. | Gremel CM et al. | β | 2010 | β |
| Genome-wide gene expression analysis identifies K-ras as a regulator of alcohol intake. | Repunte-Canonigo V et al. | β | 2010 | β |
| Heterogeneity of reward mechanisms. | Lajtha A et al. | β | 2010 | β |
| Individual differences in prefrontal cortex function and the transition from drug use to drug dependence. | George O et al. | β | 2010 | β |
| Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. | Pan WX et al. | β | 2010 | β |
| Insight into the relationship between impulsivity and substance abuse from studies using animal models. | Winstanley CA et al. | β | 2010 | β |
| Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. | Merz CJ et al. | β | 2010 | β |
| Is there an inhibitory-response-control system in the rat? Evidence from anatomical and pharmacological studies of behavioral inhibition. | Eagle DM et al. | β | 2010 | β |
| Long-lasting adaptations of the NR2B-containing NMDA receptors in the dorsomedial striatum play a crucial role in alcohol consumption and relapse. | Wang J et al. | β | 2010 | β |
| MeCP2 and drug addiction. | Feng J et al. | β | 2010 | β |
| Neural mechanisms of reproduction in females as a predisposing factor for drug addiction. | Hedges VL et al. | β | 2010 | β |
| Neurotransmission in Parkinson's disease: beyond dopamine. | Barone P | β | 2010 | β |
| Pavlovian to instrumental transfer: a neurobehavioural perspective. | Holmes NM et al. | β | 2010 | β |
| Progressive ratio responding in an obese mouse model: Effects of fenfluramine. | Finger BC et al. | β | 2010 | β |
| Regional differences in the action of antipsychotic drugs: implications for cognitive effects in schizophrenic patients. | Beninger RJ et al. | β | 2010 | β |
| Reward sensitivity: issues of measurement, and achieving consilience between human and animal phenotypes. | Stephens DN et al. | β | 2010 | β |
| Risky decisions and their consequences: neural processing by boys with Antisocial Substance Disorder. | Crowley TJ et al. | β | 2010 | β |
| Sensory and motor aspects of addiction. | Yalachkov Y et al. | β | 2010 | β |
| Shift from goal-directed to habitual cocaine seeking after prolonged experience in rats. | Zapata A et al. | β | 2010 | β |
| Special issue in honor of professor Armen Galoyan. Preface. | Lajtha A | β | 2010 | β |
| Striatal volume predicts level of video game skill acquisition. | Erickson KI et al. | β | 2010 | β |
| The associative basis of cue-elicited drug taking in humans. | Hogarth L et al. | β | 2010 | β |
| The Potent Effect of Environmental Context on Relapse to Alcohol-Seeking After Extinction. | Janak PH et al. | β | 2010 | β |
| The role of the nucleus accumbens core in impulsive choice, timing, and reward processing. | Galtress T et al. | β | 2010 | β |
| Toward a neurobiology of delusions. | Corlett PR et al. | β | 2010 | β |
| Translating the neuroscience of alcoholism into clinical treatments: from blocking the buzz to curing the blues. | Heilig M et al. | β | 2010 | β |
| What is the Degree of Segregation between Striatonigral and Striatopallidal Projections? | Bertran-Gonzalez J et al. | β | 2010 | β |
| Anxiety, cognition, and habit: a multiple memory systems perspective. | Packard MG | β | 2009 | β |
| Cocaine self-administration alters the relative effectiveness of multiple memory systems during extinction. | Gabriele A et al. | β | 2009 | β |
| Corticostriatal Interactions during Learning, Memory Processing, and Decision Making. | Pennartz CM et al. | β | 2009 | β |
| Differential effects of chronic ethanol consumption and withdrawal on homer/glutamate receptor expression in subregions of the accumbens and amygdala of P rats. | Obara I et al. | β | 2009 | β |
| Endogenous BDNF in the dorsolateral striatum gates alcohol drinking. | Jeanblanc J et al. | β | 2009 | β |
| Inhibition of CREB activity in the dorsal portion of the striatum potentiates behavioral responses to drugs of abuse. | Fasano S et al. | β | 2009 | β |
| Molecular profiling of striatonigral and striatopallidal medium spiny neurons past, present, and future. | Lobo MK | β | 2009 | β |
| Role of dopamine D(1)-family receptors in dorsolateral striatum in context-induced reinstatement of heroin seeking in rats. | Bossert JM et al. | β | 2009 | β |
| Stable encoding of task structure coexists with flexible coding of task events in sensorimotor striatum. | Kubota Y et al. | β | 2009 | β |
| Transient role of the rat prelimbic cortex in goal-directed behaviour. | Tran-Tu-Yen DA et al. | β | 2009 | β |
| Viral vector approaches to modify gene expression in the brain. | Papale A et al. | β | 2009 | β |