Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas
Open accessAbstract
Although many psychopharmacological factors contribute to nicotine addiction, midbrain dopaminergic systems have received much attention because of their roles in reinforcement and associative learning. It is generally thought that the mesocorticolimbic dopaminergic system is important for the acquisition of behaviors that are reinforced by the salient drives of the environment or by the inappropriate stimuli of addictive drugs. Nicotine, as obtained from tobacco, can activate nicotinic acetylcholine receptors (nAChRs) and excite midbrain neurons of the mesocorticolimbic system. Using midbrain slices from rats, wild-type mice, and genetically engineered mice, we have found differences in the nAChR currents from the ventral tegmental area (VTA) and the substantia nigra compacta (SNc). Nicotinic AChRs containing the alpha7 subunit (alpha7* nAChRs) have a low expression density. Electrophysiological analysis of nAChR currents, autoradiography of [125I]-alpha-bungarotoxin binding, and in situ hybridization revealed that alpha7* nAChRs are more highly expressed in the VTA than the SNc. In contrast, beta2* nAChRs are move evenly distributed at a higher density in both the VTA and SNc. At the concentration of nicotine obtained by tobacco smokers, the slow components of current (mainly mediated by beta2* nAChRs) become essentially desensitized. However, the minority alpha7* component of the current in the VTA/SNc is not significantly desensitized by nicotine in the range < or =100 nm. These results suggest that nicotine, as obtained from tobacco, can have multiple effects on the midbrain areas by differentially influencing dopamine neurons of the VTA and SNc and differentially desensitizing alpha7* and non-alpha7 nAChRs.
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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 Wooltorton et al., 2003
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Experimental — accuracy not yet measuredSteady states of nicotine that would be achieved in the bloodstream of a regular smoker can desensitize midbrain nAChRs with a time course of recovery that requires several minutes.
“In addition, electrophysiological studies show that steady states of nicotine that would be achieved in the bloodstream of a regular smoker can desensitize midbrain nAChRs with a time course of recovery that requires several minutes (Pidoplichko et al., 1997; 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 Wooltorton et al., 2003
The section on nicotine concentrations obtained from tobacco reports that smoker-relevant concentrations (20–80 nM) desensitized the slower nAChR current in VTA neurons. The discussion says recovery can be slow and variable, but our copy does not establish that recovery from this desensitization requires several minutes; it also notes that some receptor subtypes remain functional at these concentrations. Page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe 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 Wooltorton et al., 2003
The Results (Figure 6; page unavailable) show desensitization of a slow nicotinic current in VTA dopamine neurons. The discussion (page unavailable) says β2-containing receptors become desensitized while α7-containing receptors remain functional, including on glutamatergic afferents that enhance excitation of dopamine neurons. It does not establish the claimed temporal shift from an initial, direct β2-mediated drive of dopamine-neuron firing to presynaptic glutamate release. (LLM, conf=0.83)
Experimental — accuracy not yet measuredNicotine 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 Wooltorton et al. 2003
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 Wooltorton et al., 2003
At even lower nicotine concentrations (20-80 nM), robust β2* desensitization is observed without any α7 desensitization.
“Furthermore, when even lower nicotine concentrations (20-80 nM) were examined in an attempt to model the low levels experienced by chronic smokers over long time periods, robust β2* desensitization was observed without any α7 desensitization (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 Wooltorton et al., 2003
Presynaptic effects of nicotinic acetylcholine receptors contribute to synaptic plasticity in the VTA, hippocampus, and prefrontal cortex.
“Presynaptic effects of nAChRs contribute to synaptic plasticity in the VTA (Mansvelder and McGehee, 2000; Wooltorton et al., 2003), hippocampus (Ge and Dani, 2005; Ji et al., 2001; Radcliffe and Dani, 1998), and prefrontal cortex (Couey et al., 2007).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Wooltorton et al., 2003
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 Wooltorton et al., 2003
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“The dense striatal acetylcholine esterase rapidly hydrolyzes the released ACh, preventing the appearance of long-lasting ACh signals that would strongly desensitize the high-affinity subtypes of nAChRs (Dani et al. 2000, Grady et al. 1994, Wooltorton et al. 2003).”
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- Authors
- Wooltorton, J. R. A., Pidoplichko, V. I., Broide, R. S., & Dani, J. A.
- Affiliations
- Baylor College of Medicine (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-04-15
- Volume
- 23
- Issue
- 8
- Pages
- 3176-3185
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6742341
- OpenAlex
- W2122921281
- Cited by
- 363
- References
- 105
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2023: 7 · 2022: 10 · 2021: 4 · 2020: 9 · 2019: 6 · 2018: 13 · 2017: 10 · 2016: 10 · 2015: 17 · 2014: 23 · 2013: 23 · 2012: 18
- FWCI
- 8.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- National Institute on Drug Abuse (DA 04077, DA-12661, DA09411, R01DA009411, F32DA005947, P01DA012661, DA05947)
- 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
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- nicotinic acetylcholine receptors, receptor desensitization, alpha7 nicotinic acetylcholine receptor, ventral tegmental area, substantia nigra pars compacta, midbrain dopaminergic neurons, nicotine dependence, mesocorticolimbic system, alpha-bungarotoxin binding
- MeSH terms
- Animals, Dopamine, Mesencephalon, Mice, Inbred C57BL, Mice, Mutant Strains, Neurons, Nicotine, Receptors, Nicotinic, Substantia Nigra, Rats, Sprague-Dawley, Ventral Tegmental Area, Mice, Knockout, Patch-Clamp Techniques, Nicotinic Antagonists, Mice, Rats, alpha7 Nicotinic Acetylcholine Receptor, In Vitro Techniques
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