Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction
Open accessAbstract
Tobacco use is a major health problem that is estimated to cause 4 million deaths a year worldwide. Nicotine is the main addictive component of tobacco. It acts as an agonist to activate and desensitize nicotinic acetylcholine receptors (nAChRs). A component of nicotine's addictive power is attributable to actions on the mesolimbic dopaminergic system, which serves a fundamental role in the acquisition of behaviors that are inappropriately reinforced by addictive drugs. Here we show that nicotine, in the same concentration and time ranges as obtained from tobacco, has three main actions that regulate the activity of midbrain dopamine (DA) neurons. Nicotine first activates and then desensitizes nAChRs on the DA neurons. This process directly excites the DA neurons for a short period of time before the nAChRs desensitize. Nicotine also enhances glutamatergic excitation and decreases GABAergic inhibition onto DA neurons. These events increase the probability for synaptic plasticity, such as long-term potentiation. The short-lived direct excitation of the DA neurons coupled with the enhanced glutamatergic afferent activity provides the presynaptic and postsynaptic coincidence necessary to initiate synaptic potentiation. In total, these synaptic events lead to a relatively long-lasting heightened activity of midbrain DA neurons. Consistent with other summarized studies, this work indicates that the synaptic changes normally associated with learning and memory can be influenced and commandeered during the nicotine addiction process.
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Nicotinic receptors on GABAergic neurons appear to be quickly desensitized and to stay desensitized for prolonged periods.
“However, nicotinic receptors on GABAergic neurons appear to be quickly desensitized and to stay desensitized for prolonged periods (Mansvelder et al., 2002; Pidoplichko et al., 2004).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Pidoplichko et al., 2004
The action of nicotine on glutamatergic transmission appears to persist and does not readily desensitize.
“The action of nicotine on glutamatergic transmission appears to persist and does not readily desensitize (Mansvelder and McGehee, 2000; Mansvelder et al., 2002; Pidoplichko et al., 2004).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Pidoplichko et al., 2004
These nicotinic receptors appear to be desensitized within a few seconds after exposure to high, reward-mediating concentrations of nicotine.
“However, these receptors appear to be desensitized within a few seconds after exposure to high, reward-mediating concentrations of nicotine (Pidoplichko et al., 1997; 2004; Wooltorton et al., 2003).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Pidoplichko et al., 2004
Rats self-administer nicotine continuously over minutes or hours, and a single systemic injection of nicotine increases and maintains extracellular dopamine levels in the nucleus accumbens for over an hour.
“The brief excitatory capacity that nicotine has on dopaminergic neurons does not readily explain the finding that rats self-administer nicotine continuously over minutes or hours and that a single systemic injection of nicotine increases and maintains extracellular dopamine levels in the nucleus accumbens for over an hour (Imperato et al., 1986; Pidoplichko et al., 2004).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Pidoplichko et al., 2004
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“The PPT/LDT cholinergic afferents boost glutamate afferent transmission via presynaptic nAChRs (Pidoplichko et al. 2004, Schilstrom et al. 2000) and provide some excitatory drive to GABA projection neurons and interneurons, mainly via β2containing (β2*) nAChRs (Mansvelder et al. 2002, Pidoplichko…”
BackgroundInfluentialSelf-citationNeuronal nicotinic acetylcholine receptor structure and function and response to nicotine
Dani, J. A. (2015) · International Review of Neurobiology · doi:10.1016/bs.irn.2015.07.001 · Cited by 309 · see citing works
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Nicotine: from molecular mechanisms to behaviour
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Regulation of synaptic transmission and plasticity by neuronal nicotinic acetylcholine receptors
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“For example, increased glutamate transmission onto VTA DA neurons is an important component of the action of nicotine that mediates enhanced firing activity and synaptic plasticity in DA neurons (4,6,7,45,46).”
BackgroundSelf-citationNicotinic modulation of synaptic transmission and plasticity in cortico-limbic circuits
Mansvelder, H. D., Mertz, M., & Role, L. W. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2009.01.007 · Cited by 126 · see citing works
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A psychobiological framework of the substrates that mediate nicotine use during adolescence
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Cholinergic modulation of dopamine pathways through nicotinic acetylcholine receptors
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Age dependent nicotinic influences over dopamine neuron synaptic plasticity
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Self-citationAddiction‐related neuroadaptations following chronic nicotine exposure
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Mesolimbic Dopamine and Habenulo-Interpeduncular Pathways in Nicotine Withdrawal
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- Authors
- Pidoplichko, V. I., Noguchi, J., Areola, O. O., Liang, Y., Peterson, J., Zhang, T., & Dani, J. A.
- Affiliations
- Baylor College of Medicine (US)
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2004-01
- Volume
- 11
- Issue
- 1
- Pages
- 60-69
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- PMC
- PMC321315
- OpenAlex
- W2047098919
- Cited by
- 196
- References
- 96
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 5 · 2020: 3 · 2019: 5 · 2018: 7 · 2017: 3 · 2016: 6 · 2015: 8 · 2014: 8 · 2013: 11 · 2012: 11
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse (DA-12661, DA09411, R01DA009411, P01DA012661)
- National Institute of Neurological Disorders and Stroke (NS 21229, R37NS021229, R01NS021229)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- nicotine dependence, nicotinic acetylcholine receptors, ventral tegmental area, midbrain dopaminergic neurons, mesolimbic dopamine system, receptor desensitization, glutamatergic excitation, GABAergic inhibition, synaptic plasticity, long-term potentiation, coincidence detection, tobacco use
- MeSH terms
- Acetylcholine, Afferent Pathways, Animals, Cholinergic Fibers, Dopamine, Electrophysiology, Extracellular Space, gamma-Aminobutyric Acid, Immunohistochemistry, Synaptic Transmission, Neuronal Plasticity, Nicotine, Nucleus Accumbens, Receptors, Nicotinic, Time Factors, Rats, Sprague-Dawley, Microdialysis, Ventral Tegmental Area, Glutamic Acid, Substance-Related Disorders, Rats
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