Acetylcholine release in the mesocorticolimbic dopamine system during cocaine seeking: conditioned and unconditioned contributions to reward and motivation

You, Zhi-Bing; Wang, Bin; Zitzman, Dawnya; Wise, Roy A.

doi:10.1523/jneurosci.0694-08.2008

Cited by 71Neurotransmitter Receptor Influence on BehaviorNicotinic Acetylcholine Receptors StudyNeuroscience and Neuropharmacology Research

Acetylcholine release in the mesocorticolimbic dopamine system during cocaine seeking: conditioned and unconditioned contributions to reward and motivation

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You, Zhi-Bing, Wang, Bin, Zitzman, Dawnya, Wise, Roy A.·2008·The Journal of Neuroscience

DOI 10.1523/jneurosci.0694-08.2008PMC PMC2562350

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Abstract

Microdialysis was used to assess the contribution to cocaine seeking of cholinergic input to the mesocorticolimbic dopamine system in ventral tegmental area (VTA). VTA acetylcholine (ACh) was elevated in animals lever pressing for intravenous cocaine and in cocaine-experienced and cocaine-naive animals passively receiving similar "yoked" injections. In cocaine-trained animals, the elevations comprised an initial (first hour) peak to approximately 160% of baseline and a subsequent plateau of 140% of baseline for the rest of the cocaine intake period. In cocaine-naive animals, yoked cocaine injections raised ACh levels to the 140% plateau but did not cause the initial 160% peak. In cocaine-trained animals that received unexpected saline (extinction conditions) rather than the expected cocaine, the initial peak was seen but the subsequent plateau was absent. VTA ACh levels played a causal role and were not just a correlate of cocaine seeking. Blocking muscarinic input to the VTA increased cocaine intake; the increase in intake offset the decrease in cholinergic input, resulting in the same VTA dopamine levels as were seen in the absence of the ACh antagonists. Increased VTA ACh levels (resulting from 10 microM VTA neostigmine infusion) increased VTA dopamine levels and reinstated cocaine seeking in cocaine-trained animals that had undergone extinction; these effects were strongly attenuated by local infusion of a muscarinic antagonist and weakly attenuated by a nicotinic antagonist. These findings identify two cholinergic responses to cocaine self-administration, an unconditioned response to cocaine itself and a conditioned response triggered by cocaine-predictive cues, and confirm that these cholinergic responses contribute to the control of cocaine seeking.

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Extracellular acetylcholine levels are increased in the VTA during drug self-administration.
“Extracellular ACh levels are increased in the VTA during drug self-administration (You et al., 2008), that could result from an increase in ACh release from PPTg and LDTg afferents (Futami et al., 1995; Omelchenko and Sesack, 2006).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as You et al., 2008

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Attenuation of Cocaine's Reinforcing and Discriminative Stimulus Effects via Muscarinic M1 Acetylcholine Receptor Stimulation
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“Intra-VTA infusions of muscarinic antagonists opposed cocaine self-administration and blunted its effect on extracellular VTA dopamine (You et al., 2008).”
Background
A Switch in the Neuromodulatory Effects of Dopamine in the Oval Bed Nucleus of the Stria Terminalis Associated with Cocaine Self-Administration in Rats
Krawczyk, M., Sharma, R., Mason, X. L., deBacker, J., Jones, A. A., & Dumont, É. C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0377-11.2011 · Cited by 46 · see citing works
“…and voluntary intake of drugs of abuse in animals has different neurological consequences than passive intake of the same substances or intake of natural rewards, such as sucrose (Dumont et al., 2005; Martin et al., 2006; Chen et al., 2008; You et al., 2008; Caillé et al., 2009; Kalant, 2010).”
Ventral tegmental area cholinergic mechanisms mediate behavioral responses in the forced swim test
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“Very recent data indicate that ACh fluctuations within the VTA underlie cocaine-seeking behavior (You et al, 2008), providing further evidence that cholinergic inputs within the VTA are part of important segments of the reward circuitry.”
Reciprocal Inhibitory Interactions Between the Reward-Related Effects of Leptin and Cocaine
You, Z., Wang, B., Liu, Q., Wu, Y., Otvos, L. J., & Wise, R. A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.230 · Cited by 39 · see citing works
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Lesions of Cholinergic Pedunculopontine Tegmental Nucleus Neurons Fail to Affect Cocaine or Heroin Self-Administration or Conditioned Place Preference in Rats
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Influential
Effect of the use-dependent, nicotinic receptor antagonist BTMPS in the forced swim test and elevated plus maze after cocaine discontinuation in rats
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Background
Cholinergic Receptor Blockade in the VTA Attenuates Cue-Induced Cocaine-Seeking and Reverses the Anxiogenic Effects of Forced Abstinence
Nunes, E. J., Bitner, L. E., Hughley, S. M., Small, K. M., Walton, S. N., Rupprecht, L. E., & Addy, N. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.06.028 · Cited by 23 · see citing works
“It has also been reported that intra-VTA infusions of muscarinic and nicotinic receptor antagonists, respectively, attenuated the ability of increased VTA cholinergic tone by neostigmine to induce reinstatement of cocaine seeking in rats following extinction training (You et al., 2008).”
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Muscarinic type 2 receptors in the lateral dorsal tegmental area modulate cocaine and food seeking behavior in rats
Shabani, S., Foster, R., Gubner, N. R., Phillips, T. J., & Mark, G. P. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.07.028 · Cited by 21 · see citing works
“Increased acetylcholine (ACh) levels in the VTA in response to cocaine (You et al., 2008) affect both NAc DA levels and reward seeking behaviors, and these effects appear to involve both muscarinic (Forster et al.”
Dopamine Neurons in the Ventral Tegmental Area: Drug-induced Synaptic Plasticity and Its Role in Relapse to Drug-seeking Behavior
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BackgroundInfluential
Cholinergic and dopaminergic‐mediated motivated behavior in healthy states and in substance use and mood disorders
Nunes, E. J., Kebede, N., Bağdaş, D., & Addy, N. (2022) · Journal of the Experimental Analysis of Behavior · doi:10.1002/jeab.747 · Cited by 18 · see citing works
Heroin Self-Administration Experience Establishes Control of Ventral Tegmental Glutamate Release by Stress and Environmental Stimuli
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“Despite the presence of the same heroin-predictive cues when heroin is actually earned, VTA glutamate was not elevated and dopamine was elevated to a little more than 200% of baseline, about half the elevation in VTA dopamine that is seen when cocaine is earned (You et al, 2008).”
Background
The stereotypy‐inducing and OCD‐like effects of chronic ‘binge’ cocaine are modulated by distinct subtypes of nicotinic acetylcholine receptors
Metaxas, A., Keyworth, H., Yoo, J.-H., Chen, Y., Kitchen, I., & Bailey, A. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.02023.x · Cited by 18 · see citing works
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Regulation of cocaine-induced reinstatement by group II metabotropic glutamate receptors in the ventral tegmental area
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“In addition, stimulation of the VTA is sufficient to induce reinstatement related to various drugs (Stewart 1984; Vorel et al. 2001; Harris et al. 2005; Wang et al. 2007; You et al. 2008).”
Background
Bidirectional Modulation of Cocaine Expectancy by Phasic Glutamate Fluctuations in the Nucleus Accumbens
Suto, N., Elmer, G. I., Wang, B., You, Z., & Wise, R. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0503-13.2013 · Cited by 16 · see citing works
“A glutamatergic projection from the VTA has also recently been characterized (Yamaguchi et al., 2011), and the ventral tegmental area is known to receive cocaine-predictive glutamatergic (You et al., 2007) and cholinergic (You et al., 2008) input.”
Varenicline effects on cocaine self administration and reinstatement behavior
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“…given the different actions of the drugs at nicotinic receptors, and the relative importance of the receptors in mediating the reinforcing properties of the drugs (Picciotto et al., 1998; Picciotto and Corrigall, 2002; Davis and de Fiebre, 2006; Steensland et al., 2007; You et al., 2008).”
BackgroundInfluential
Acetylcholine from the mesopontine tegmental nuclei differentially affects methamphetamine induced locomotor activity and neurotransmitter levels in the mesolimbic pathway
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“Neostigmine was removed for the DA analysis since it is only necessary to prevent the breakdown of ACh and may artificially inflate DA levels [29].”
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Separating analgesia from reward within the ventral tegmental area
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Anhydroecgonine Methyl Ester (AEME), a Product of Cocaine Pyrolysis, Impairs Spatial Working Memory and Induces Striatal Oxidative Stress in Rats
Gomes, E. F., Lipaus, I. F. S., Martins, C. W., Araújo, A. M., Mendonça, J. B., Pelição, F. S., Lebarch, E. C., Rodrigues, L. C. D. M., & Nakamura-Palacios, E. M. (2017) · Neurotoxicity Research · doi:10.1007/s12640-017-9813-y · Cited by 15 · see citing works
“Extracellular levels of ACh are increased in the VTA during the self-administration of drugs, such as cocaine (Williams and Adinoff 2008; You et al. 2008).”
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Biperiden (an M1 antagonist) reduces memory consolidation of cocaine-conditioned place preference
Zacarias, M. S., Ramos, A. C., Alves, D. R., & Galduróz, J. C. F. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.01.073 · Cited by 14 · see citing works
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“However, the available literature demonstrates that ACh levels in the VTA increase during cocaine self-administration (You et al., 2008), and cocaine facilitates LDT stimulation-induced DA release”
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Increased latencies to initiate cocaine self-administration following laterodorsal tegmental nucleus lesions
Steidl, S., Cardiff, K. M., & Wise, R. A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.02.049 · Cited by 12 · see citing works
“Alternatively, it may be necessary to lesion both LDTg and PPTg in order to effectively deprive the VTA of all cholinergic input, in order alter cocaine selfadministration as is seen following local VTA pharmacological manipulations [8].”
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Association of CHRNA5 Gene Variants with Crack Cocaine Addiction
Aroche, A. P., Rovaris, D. L., Grevet, E. H., Stolf, A. R., Sanvicente‐Vieira, B., Kessler, F. H. P., DIEMEN, L. V., Grassi‐Oliveira, R., Bau, C. H. D., & Schuch, J. B. (2020) · NeuroMolecular Medicine · doi:10.1007/s12017-020-08596-1 · Cited by 12 · see citing works
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“Intra-VTA infusions of scopolamine or atropine, both mACh receptor antagonists, block consumption of food reward [9–11], cause compensatory increases in cocaine intake [12] and reduce break points in rats pressing a lever for food under a progressive ratio schedule of reinforcement, suggesting reductions in reward [9].”
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Extracellular dopamine, acetylcholine, and activation of dopamine D1 and D2 receptors after selective breeding for cocaine self-administration in rats
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BackgroundInfluential
Effects ofBrugmansia arboreaExtract and Its Secondary Metabolites on Morphine Tolerance and Dependence in Mice
Mattioli, L., Bracci, A., Titomanlio, F., Perfumi, M. C., & Feo, V. D. (2012) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2012/741925 · Cited by 9 · see citing works
“Moreover it was demonstrated that VTA ACh levels played a causal role on drug seeking and reward, and these effects were strongly attenuated by local infusion of a muscarinic antagonist, like atropine [21, 22].”
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Cocaine + nicotine mixture enhances induction and expression of behavioral sensitization in rats
Barbosa-Méndez, S., & Salazar‐Juárez, A. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.024 · Cited by 8 · see citing works
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“expression of CBs was accompanied by escalated extracellular acetylcholine (ACh) levels in the VTA.(55) Therefore, CBs were possibly induced by METH-CPP via ACh release.”
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Biperiden reverses the increase in 50-kHz ultrasonic vocalizations but not the increase in locomotor activity induced by cocaine
Vaz, T. C. S. S., Sanchez, W. N., Palombo, P., Cruz, F. C., Galduróz, J. C. F., Schwarting, R. K. W., Andreatini, R., Cunha, C. D., & Pochapski, J. A. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114841 · Cited by 5 · see citing works
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Authors: You, Z.-B., Wang, B., Zitzman, D., & Wise, R. A.
Affiliations: National Institutes of Health (US)
ORCID: Wise, Roy A.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2008-09-03
Volume: 28
Issue: 36
Pages: 9021-9029
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.0694-08.2008
PMC: PMC2562350
OpenAlex: W2039959923
Cited by: 71
References: 67
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 2 · 2022: 5 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 3 · 2017: 8 · 2016: 2 · 2015: 4 · 2014: 5 · 2013: 3 · 2012: 9
FWCI: 3.32
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 181 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Health and Human Services
National Institutes of Health (Z99 DA999999)
National Institute on Drug Abuse
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: acetylcholine, cocaine seeking, mesocorticolimbic dopamine system, ventral tegmental area, cocaine self-administration, conditioned response, unconditioned response, extinction, reinstatement, muscarinic receptors, nicotinic acetylcholine receptors, neostigmine, reward, motivation, predictive cues
MeSH terms: Acetylcholine, Analysis of Variance, Animals, Atropine, Behavior, Animal, Cocaine, Conditioning, Psychological, Dopamine, Extinction, Psychological, Male, Mecamylamine, Motivation, Reward, Self Administration, Substantia Nigra, Microdialysis, Ventral Tegmental Area, Cholinergic Antagonists, Cocaine-Related Disorders, Rats, Long-Evans, Rats

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Acetylcholine release in the mesocorticolimbic dopamine system during cocaine seeking: conditioned and unconditioned contributions to reward and motivation

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