Nucleus accumbens shell and core dopamine: differential role in behavior and addiction

Di Chiara, Gaetano

doi:10.1016/s0166-4328(02)00286-3

Cited by 1,000Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesSubstance Abuse Treatment and Outcomes

Nucleus accumbens shell and core dopamine: differential role in behavior and addiction

Di Chiara, Gaetano·2002·Behavioural Brain Research

DOI 10.1016/s0166-4328(02)00286-3

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Abstract

Drug addiction can be conceptualized as a disturbance of behavior motivated by drug-conditioned incentives. This abnormality has been explained by Incentive-Sensitization and Allostatic-Counteradaptive theories as the result of non-associative mechanisms acting at the stage of the expression of incentive motivation and responding for drug reinforcement. Each one of these theories, however, does not account per se for two basic properties of the motivational disturbance of drug addiction: (1). focussing on drug- at the expenses of non-drug-incentives; (2). virtual irreversibility. To account for the above aspects we have proposed an associative learning hypothesis. According to this hypothesis the basic disturbance of drug addiction takes place at the stage of acquisition of motivation and in particular of Pavlovian incentive learning. Drugs share with non-drug rewards the property of stimulating dopamine (DA) transmission in the nucleus accumbens shell but this effect does not undergo habituation upon repeated drug exposure, as instead is the case of non-drug rewards. Repetitive, non-decremental stimulation of DA transmission by drugs in the nucleus accumbens septi (NAc) shell abnormally strengthens stimulus-drug associations. Thus, stimuli contingent upon drug reward acquire powerful incentive properties after a relatively limited number of predictive associations with the drug and become particularly resistant to extinction. Non-contingent occurrence of drug-conditioned incentive cues or contexts strongly facilitates and eventually reinstates drug self-administration. Repeated drug exposure also induces a process of sensitization of drug-induced stimulation of DA transmission in the NAc core. The precise significance of this adaptive change for the mechanism of drug addiction is unclear given the complexity and uncertainties surrounding the role of NAc core DA in responding but might be more directly related to instrumental performance.

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The approach module comprises subcortical and cortical structures that are major sites of dopamine action, primarily striatum and medial/orbital prefrontal cortices.
“This neural system comprises subcortical and cortical structures that are major sites of dopamine action, and include primarily the striatum (caudate nucleus, putamen and nucleus accumbens) (e.g., Di Chiara, 2002; Di Chiara and Bassareo, 2007; McClure et al., 2004; Schultz et al., 1998; Wise, 2004) and the medial and orbital prefrontal cortices (Jensen et al., 2003; Kringelbach, 2005).”
From A systematic review of fMRI reward paradigms used in studies of adolescents vs. adults: The impact of task design and implications for understanding neurodevelopment (2013) · cites this paper as Di Chiara, 2002
The NAc is regarded as the reward circuitry's center and is strongly implicated in substance use and craving.
“The primary subcortical brain target is the nucleus accumbens (NAc) which is considered the center of the reward circuitry and heavily implicated in substance use and craving [18–22].”
From Transcranial magnetic stimulation, deep brain stimulation, and other forms of neuromodulation for substance use disorders: Review of modalities and implications for treatment (2020) · cites this paper as [18]
Many studies found that the accumbens core and shell are involved in different functions.
“To date, much of the functional analysis of the nucleus accumbens has focused on the differences between the accumbens core and shell, and many studies found that the core and shell are involved in different functions (Di Chiara, 2002; Kelley, 2004; Everitt and Robbins, 2005).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Di Chiara, 2002
Many studies since Ikemoto and Panksepp (1999) provide rich data indicating differential functions between the medial portion of the nucleus accumbens shell and the core in appetitive tasks.
“Since our review (Ikemoto and Panksepp, 1999), many studies have been conducted providing rich data indicating differential functions between the medial portion of the nucleus accumbens shell and the core in appetitive tasks (see Di Chiara, 2002; Kelley, 2004; Everitt and Robbins, 2005).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Di Chiara, 2002
Behavioral data indicate otherwise.
“Indeed, behavioral data indicate otherwise (Di Chiara, 2002; Kelley, 2004; Everitt and Robbins, 2005, Yin and Knowlton, 2006).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Di Chiara, 2002

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Dopamine, learning and motivation.
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Cognition and Learning
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The tempted brain eats: Pleasure and desire circuits in obesity and eating disorders
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Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens
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Cue-induced activation of the striatum and medial prefrontal cortex is associated with subsequent relapse in abstinent alcoholics
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Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior
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Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards
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Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell
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Infralimbic Prefrontal Cortex Is Responsible for Inhibiting Cocaine Seeking in Extinguished Rats
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Reward system and addiction: what dopamine does and doesn’t do
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Dopamine: 50 years in perspective
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The Addiction-Stroop test: Theoretical considerations and procedural recommendations.
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Internet gaming addiction: current perspectives
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Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds
Aragona, B. J., Liu, Y., Yu, Y. J., Curtis, J. T., Detwiler, J. M., Insel, T. R., & Wang, Z. (2006) · Nature Neuroscience · doi:10.1038/nn1613 · Cited by 473 · see citing works
Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine
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Internet and Gaming Addiction: A Systematic Literature Review of Neuroimaging Studies
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REVIEW: Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked?
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Annual Research Review: All mothers are not created equal: neural and psychobiological perspectives on mothering and the importance of individual differences
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Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse
Salamone, J. D., Correa, M., Mingote, S., & Weber, S. M. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.035063 · Cited by 433 · see citing works
Stress and the dopaminergic reward system
Baik, J. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00532-4 · Cited by 446 · see citing works
The neurocircuitry of addiction: an overview
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Neurobiology of craving, conditioned reward and relapse
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Episodic memory in normal aging and Alzheimer disease: Insights from imaging and behavioral studies
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Rewarding properties of social interactions in adolescent and adult male and female rats: Impact of social versus isolate housing of subjects and partners
Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004) · Developmental Psychobiology · doi:10.1002/dev.20025 · Cited by 389 · see citing works
The limbic lobe and its output channels: implications for emotional functions and adaptive behavior
Heimer, L., & Van Hoesen, G. W. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.006 · Cited by 366 · see citing works
The nucleus accumbens as part of a basal ganglia action selection circuit
Nicola, S. M. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0510-4 · Cited by 360 · see citing works
Nicotine-induced upregulation of nicotinic receptors: Underlying mechanisms and relevance to nicotine addiction
Govind, A. P., Vezina, P., & Green, W. N. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.06.011 · Cited by 338 · see citing works
The mesoaccumbens dopamine in coping with stress
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The role of the striatum in aversive learning and aversive prediction errors
Delgado, M. R., Li, J., Schiller, D., & Phelps, E. A. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2008.0161 · Cited by 328 · see citing works
Neuroscience of Addiction: Relevance to Prevention and Treatment
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Identifying the neural circuitry of alcohol craving and relapse vulnerability
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Constitutive Activity of the Serotonin2C Receptor InhibitsIn VivoDopamine Release in the Rat Striatum and Nucleus Accumbens
Deurwaerdère, P. D., Navailles, S., Berg, K. A., Clarke, W. P., & Spampinato, U. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0112-04.2004 · Cited by 309 · see citing works
A New Anatomical Framework for Neuropsychiatric Disorders and Drug Abuse
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Serotonin and psychostimulant addiction: Focus on 5-HT1A-receptors
Müller, C. P., Carey, R. J., Huston, J. P., & Silva, M. A. D. S. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.01.001 · Cited by 302 · see citing works
The role of mesolimbic dopamine in the development and maintenance of ethanol reinforcement
Gonzales, R. A., Job, M. O., & Doyon, W. M. (2004) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2004.06.002 · Cited by 297 · see citing works
Considering the Definition of Addiction
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Neural and Behavioral Plasticity Associated with the Transition from Controlled to Escalated Cocaine Use
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Mice with Chronically Elevated Dopamine Exhibit Enhanced Motivation, but not Learning, for a Food Reward
Cagniard, B., Balsam, P. D., Brunner, D., & Zhuang, X. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300966 · Cited by 282 · see citing works
Nucleus accumbens and impulsivity
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Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration
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The Dopamine Hypothesis of Drug Addiction: Hypodopaminergic State
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Excessive cocaine use results from decreased phasic dopamine signaling in the striatum
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Acetylcholine–Dopamine Interactions in the Pathophysiology and Treatment of CNS Disorders
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Dopamine Neurons Control Striatal Cholinergic Neurons via Regionally Heterogeneous Dopamine and Glutamate Signaling
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Anandamide administration alone and after inhibition of fatty acid amide hydrolase (FAAH) increases dopamine levels in the nucleus accumbens shell in rats
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Association of Low Striatal Dopamine D 2 Receptor Availability With Nicotine Dependence Similar to That Seen With Other Drugs of Abuse
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The subthalamic nucleus exerts opposite control on cocaine and 'natural' rewards
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Neural and psychological mechanisms underlying appetitive learning: links to drug addiction
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Rapid dopamine signaling in the nucleus accumbens during contingent and noncontingent cocaine administration
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Persistent Disruption of an Established Morphine Conditioned Place Preference
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Dopamine-Regulated MicroRNA MiR-181a Controls GluA2 Surface Expression in Hippocampal Neurons
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Noradrenergic transmission in the extended amygdala: role in increased drug-seeking and relapse during protracted drug abstinence
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A dopaminergic switch for fear to safety transitions
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Dopamine signaling in the nucleus accumbens of animals self-administering drugs of abuse
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Ventral Striatal Neurons Encode the Value of the Chosen Action in Rats Deciding between Differently Delayed or Sized Rewards
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Respiratory depression and brain hypoxia induced by opioid drugs: Morphine, oxycodone, heroin, and fentanyl
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Decoding molecular and cellular heterogeneity of mouse nucleus accumbens
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Alcohol Dependence, Withdrawal, and Relapse
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Self-citation
Dopamine and drug addiction: the nucleus accumbens shell connection
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Authors: Di Chiara, G.
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 2002-12
Volume: 137
Issue: 1-2
Pages: 75-114
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/s0166-4328(02)00286-3
OpenAlex: W1980890656
Cited by: 996
References: 300
Citations by year: 2026: 17 · 2025: 28 · 2024: 30 · 2023: 24 · 2022: 33 · 2021: 30 · 2020: 30 · 2019: 40 · 2018: 40 · 2017: 39 · 2016: 45 · 2015: 56 · 2014: 49 · 2013: 54 · 2012: 54
FWCI: 3.92
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Health Sciences › Medicine › Epidemiology › Substance Abuse Treatment and Outcomes
Keywords: nucleus accumbens shell, nucleus accumbens core, dopamine, drug addiction, incentive sensitization, self-administration, reinstatement, extinction, habituation
MeSH terms: Animals, Appetitive Behavior, Brain Mapping, Conditioning, Classical, Dopamine, Humans, Motivation, Neural Pathways, Synaptic Transmission, Nucleus Accumbens, Behavior, Addictive, Prefrontal Cortex, Substance-Related Disorders, Rats

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Nucleus accumbens shell and core dopamine: differential role in behavior and addiction

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