Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas

Mansvelder, Huibert D; Keath, J.Russel; McGehee, Daniel S

doi:10.1016/s0896-6273(02)00625-6

Cited by 701Nicotinic Acetylcholine Receptors StudyNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas

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Mansvelder, Huibert D, Keath, J.Russel, McGehee, Daniel S·2002·Neuron

DOI 10.1016/s0896-6273(02)00625-6

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Abstract

A single nicotine exposure increases dopamine levels in the mesolimbic reward system for hours, but nicotine concentrations experienced by smokers desensitize nAChRs on dopamine neurons in seconds to minutes. Here, we show that persistent modulation of both GABAergic and glutamatergic synaptic transmission by nicotine can contribute to the sustained increase in dopamine neuron excitability. Nicotine enhances GABAergic transmission transiently, which is followed by a persistent depression of these inhibitory inputs due to nAChR desensitization. Simultaneously, nicotine enhances glutamatergic transmission through nAChRs that desensitize less than those on GABA neurons. The net effect is a shift toward excitation of the dopamine reward system. These results suggest that spatial and temporal differences in nicotinic receptor activity on both excitatory and inhibitory neurons in reward areas coordinate to reinforce nicotine self-administration.

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Nicotine can desensitize β2* nAChRs on GABAergic inputs to DA neurons, shifting from mixed excitation and inhibition to more unmixed stimulation of nAChRs on presynaptic glutamatergic terminals.
“In addition, nicotine can desensitize β2 Ã nAChRs on GABAergic inputs to DA neurons, resulting in a shift from mixed excitation and inhibition of DA neurons by nicotine, to a more unmixed stimulation of nAChRs on presynaptic glutamatergic terminals (Mansvelder et al. 2002;Wooltorton et al. 2003).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Mansvelder et al. 2002
At lower nicotine concentrations (250 nM), β2* nAChRs also desensitize rapidly.
“However, at lower nicotine concentrations, which may be more similar to those observed at steady state in a smoker's brain (250 nM), β2* nAChRs also desensitize rapidly (Mansvelder et al., 2002; Mansvelder and McGehee, 2000).”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Mansvelder et al., 2002
Chronic nicotine exposure would greatly increase response to environmental stimuli that increase DA neuron burst firing, and greatly decrease DA responses under conditions when these neurons were firing tonically.
“Since sustained nicotine exposure shifts the balance toward glutamate-mediated excitation of DA neurons (Mansvelder et al., 2002; Wooltorton et al., 2003) the combination of increased drive on the cell bodies in the VTA and increased filtering in the striatum/nucleus accumbens suggests that chronic nicotine exposure would greatly increase response to environmental stimuli that increase DA neuron”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Mansvelder et al., 2002
Presynaptic effects of lower concentrations of nicotine blocked by α7* selective agents persist in the continued presence of nicotine in rat and mouse brain slices, whereas presynaptic effects blocked by β2* selective agents desensitize during continued nicotine application.
“More recent studies have shown that presynaptic effects of lower concentrations of nicotine that are blocked by nicotinic agents that are thought to be selective for α7* nAChRs persist in the continued presence of nicotine in rat (Mansvelder et al., 2002) and mouse (Wooltorton et al., 2003) brain slices, whereas presynaptic effects that are blocked with agents thought to be selective for β2* nAChR”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Mansvelder et al., 2002
Low level nicotine concentrations experienced by smokers over long periods preferentially desensitize α4β2 nAChRs on GABAergic terminals and not α7 nAChRs on glutamatergic terminals in the VTA, shifting presynaptic effects of nicotine from mixed inhibition and excitation of DA neurons toward the glutamatergic response.
“The low level nicotine concentrations experienced by smokers over long periods are suggested to preferentially desensitize α4β2 nAChRs on GABAergic terminals and not α7 nAChRs on glutamatergic terminals in the VTA, thus shifting the presynaptic effects of nicotine from a mixed inhibition and excitation of DA neurons, toward the glutamatergic response to nicotine (Mansvelder et al., 2002; Mansvel”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Mansvelder et al., 2002

The temporal sequence of activation of β2* nAChRs on DA neurons in the VTA, followed by their desensitization, results in a shift from a brief, direct drive of DA neuronal firing toward presynaptic, α7-mediated activation of glutamate release onto DA neurons.
“the temporal sequence of activation of β2* nAChRs on DA neurons in the VTA, followed by their desensitization, appears to result in a shift from a brief, direct drive of DA neuronal firing toward presynaptic, α7-mediated activation of glutamate release onto DA neurons (Mansvelder et al., 2002; Wooltorton et al., 2003).”
From It is not “either/or”: Activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood (2008) · cites this paper as Mansvelder et al., 2002
Nicotinic modulation of neurotransmitter release is often subtype-specific and this specificity can vary across brain areas.
“Nicotinic modulation of neurotransmitter release is often subtype-specific and this specificity can vary across brain areas, with distinct nAChRs coupling to release of glutamate (α7) vs. GABA (α4β2*) (Mansvelder et al., 2002) or DA (α4/α6β2*) vs. ACh (α3β4*) (Grady et al., 2001) in the VTA, while β2* nAChRs can modulate the release of glutamate from thalamo-cortical projections (Parikh et al., 20”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Mansvelder et al., 2002
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 Mansvelder et al., 2002
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 Mansvelder et al., 2002
α4β2* nAChRs can be rapidly and persistently desensitized in the presence of nicotine, whereas α7 nAChRs can maintain their activity.
“α4β2* nAChRs can be rapidly and persistently desensitized in the presence of nicotine, whereas α7 nAChRs can maintain their activity (Mansvelder et al., 2002)”
From Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states (2015) · cites this paper as Mansvelder et al., 2002

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Authors: Mansvelder, H. D., Keath, J. R., & McGehee, D. S.
Affiliations: University of Chicago (US)
Corresponding author: McGehee, Daniel S
ORCID: Mansvelder, Huibert D
McGehee, Daniel S
Venue: Neuron
Publisher: Elsevier BV
Published: 2002-03
Volume: 33
Issue: 6
Pages: 905-919
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/s0896-6273(02)00625-6
OpenAlex: W2157815289
Cited by: 701
References: 71
Citations by year: 2026: 11 · 2025: 11 · 2024: 10 · 2023: 10 · 2022: 18 · 2021: 16 · 2020: 25 · 2019: 17 · 2018: 30 · 2017: 20 · 2016: 22 · 2015: 39 · 2014: 28 · 2013: 30 · 2012: 41
FWCI: 12.66
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 4156 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
VU Research Portal (publishedVersion, other-oa)
Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek
National Institute on Drug Abuse (DA07255, T32DA007255)
National Institute of Neurological Disorders and Stroke (R01NS035090, NS-35090)
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
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: nicotine, nicotinic acetylcholine receptors, receptor desensitization, dopaminergic neurons, mesolimbic reward system, GABAergic neurotransmission, glutamatergic neurotransmission, neuronal excitability, synaptic depression, nicotine self-administration
MeSH terms: Acetylcholinesterase, Action Potentials, Adolescent, Animals, Atropine, Cholinesterase Inhibitors, Dopamine, Electrophysiology, gamma-Aminobutyric Acid, Ganglionic Stimulants, Humans, Insecticides, Synaptic Transmission, Neurons, Nicotine, Organothiophosphorus Compounds, Quinoxalines, Receptors, Nicotinic, Reward, Smoking, Rats, Sprague-Dawley, Ventral Tegmental Area, Patch-Clamp Techniques, Cholinergic Antagonists, Excitatory Amino Acid Antagonists, Glutamic Acid, Muscarinic Antagonists, Mice, Rats, In Vitro Techniques

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Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas

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