Midbrain muscarinic receptor mechanisms underlying regulation of mesoaccumbens and nigrostriatal dopaminergic transmission in the rat

Miller, Anthony D.; Blaha, Charles D.

doi:10.1111/j.1460-9568.2005.04017.x

Cited by 94Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNicotinic Acetylcholine Receptors Study

Midbrain muscarinic receptor mechanisms underlying regulation of mesoaccumbens and nigrostriatal dopaminergic transmission in the rat

Miller, Anthony D., Blaha, Charles D.·2005·European Journal of Neuroscience

DOI 10.1111/j.1460-9568.2005.04017.x

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Abstract

Laterodorsal (LDT) and pedunculopontine (PPT) tegmental nuclei in the mesopontine project cholinergic inputs to the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc), respectively, to directly and indirectly influence the activity of dopamine neuronal cells via actions on muscarinic and nicotinic receptors. The present study investigated the role of midbrain muscarinic receptors in the functional modulation of VTA and SNc dopamine cell activity as reflected by alterations in, respectively, nucleus accumbens (NAc) and striataldopamine efflux. In vivo chronoamperometry was used to measure changes in basal dopamine efflux via stearate–graphite paste electrodes implanted unilaterally in the NAc or striatum of urethane‐anaesthetized rats, following blockade or activation of, respectively, VTA or SNc muscarinic receptors. Intra‐VTA or ‐SNc infusion of the muscarinic antagonist scopolamine (200 µg/µL) reduced, respectively, NAc and striatal dopamine efflux while infusion of the muscarinic and nicotinic agonist carbachol (0.5 µg/µL) or the prototypical muscarinic agonist muscarine (0.5 µg/µL) increased NAc and striatal dopamine efflux. Transient decreases in dopamine efflux preceded these increases selectively in the striatum, suggesting a reduction in excitatory or increase in inhibitory drive to the SNc by preferential activation of M3 muscarinic receptors on GABA interneurons and glutamatergic inputs. This was confirmed by showing that selective blockade of M3 receptors with p‐F‐HHSiD (0.5 µg/µL) increased striatal, but not NAc, dopamine efflux. Together, these findings suggest that midbrain muscarinic receptors, probably M5 subtypes on VTA and SNc dopamine neurons, contribute to the tonic excitatory regulation of forebrain basal dopamine transmission whereas presynaptic M3 receptors serve to counter excessive excitation of nigral dopamine cell activity.

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Both muscarinic and nicotinic ACh receptors are present on VTA dopamine neurons, as well as on cholinergic and glutamatergic terminals regulating different aspects of dopamine release in output sites such as the striatum and NAc.
“Both muscarinic and nicotinic ACh receptors are present on VTA dopamine neurons, as well as on cholinergic and glutamatergic terminals regulating different aspects of dopamine release in output sites, such as the striatum and NAc [160–162].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [160]
Stimulation of nicotinic receptors and M5-type muscarinic receptors increases the tonic excitability of dopamine neurons.
“Stimulation of nAChR and M5-type mAChRs increases the tonic excitability of these DA neurons (Corrigall et al., 2002; Miller and Blaha, 2005; Yeomans and Baptista, 1997).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Miller and Blaha, 2005

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Muscarine Reduces Calcium-Dependent Electrical Activity in Substantia Nigra Dopaminergic Neurons
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Nicotinic and muscarinic receptor-evoked depolarizations recorded from a novel cortical brain slice preparation
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Hagihara (1999) · doi:10.1002/(sici)1096-9861(19990726)410:2

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Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
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Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area
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Molecular Targets for Treating Cognitive Dysfunction in Schizophrenia
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Genetical genomic determinants of alcohol consumption in rats and humans
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Segregated cholinergic transmission modulates dopamine neurons integrated in distinct functional circuits
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Multiple roles for nicotine in Parkinson's disease
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SK channels control the firing pattern of midbrain dopaminergic neurons <i>in vivo</i>
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M‐type channels selectively control bursting in rat dopaminergic neurons
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Changes in the neuronal activity in the pedunculopontine nucleus in chronic MPTP-treated primates: an in situ hybridization study of cytochrome oxidase subunit I, choline acetyl transferase and substance P mRNA expression
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Operant responding for optogenetic excitation of LDTg inputs to the VTA requires D1 and D2 dopamine receptor activation in the NAcc
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Structural Modifications to Tetrahydropyridine-3-carboxylate Esters en Route to the Discovery of M5-Preferring Muscarinic Receptor Orthosteric Antagonists
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Novel pharmacotherapeutic targets for the management of drug addiction
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Roles of pedunculopontine tegmental cholinergic receptors in brain stimulation reward in the rat
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Postnatal development of neurotransmitter systems and their relevance to extinction of conditioned fear
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Subcortical Connections of the Basal Ganglia
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Lobeline, a potential pharmacotherapy for drug addiction, binds to μ opioid receptors and diminishes the effects of opioid receptor agonists
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Age-related changes in nicotine response of cholinergic and non-cholinergic laterodorsal tegmental neurons: Implications for the heightened adolescent susceptibility to nicotine addiction
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Midbrain acetylcholine and glutamate receptors modulate accumbal dopamine release
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Muscarinic receptor blockade in the ventral tegmental area attenuates cocaine enhancement of laterodorsal tegmentum stimulation‐evoked accumbens dopamine efflux in the mouse
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Targeting the Actions of Muscarinic Receptors on Dopamine Systems: New Strategies for Treating Neuropsychiatric Disorders
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Variation in the gene coding for the M5 Muscarinic receptor (CHRM5) influences cigarette dose but is not associated with dependence to drugs of addiction: evidence from a prospective population based cohort study of young adults
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Cholinergic tone in ventral tegmental area: Functional organization and behavioral implications
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Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks
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“Both muscarinic and nicotinic ACh receptors are present on VTA dopamine neurons, as well as on cholinergic and glutamatergic terminals regulating different aspects of dopamine release in output sites, such as the striatum and NAc [160 – 162].”
Effect of muscarinic receptor agonists xanomeline and sabcomeline on acetylcholine and dopamine efflux in the rat brain; comparison with effects of 4-[3-(4-butylpiperidin-1-yl)-propyl]-7-fluoro-4H-benzo[1,4]oxazin-3-one (AC260584) and N-desmethylclozapine
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A food-associated CS activates c-Fos in VTA DA neurons and elicits conditioned approach
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Muscarinic type 2 receptors in the lateral dorsal tegmental area modulate cocaine and food seeking behavior in rats
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Differential corticosteroid receptor regulation of mesoaccumbens dopamine efflux during the peak and nadir of the circadian rhythm: A molecular equilibrium in the midbrain?
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Cholinergic and dopaminergic‐mediated motivated behavior in healthy states and in substance use and mood disorders
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Glucocorticoid Programing of the Mesopontine Cholinergic System
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Muscarinic receptors in energy homeostasis: Physiology and pharmacology
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Acetylcholine from the mesopontine tegmental nuclei differentially affects methamphetamine induced locomotor activity and neurotransmitter levels in the mesolimbic pathway
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Modulation of Muscarinic Signalling in the Central Nervous System by Steroid Hormones and Neurosteroids
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GABAA receptors in GtoPdb v.2021.3
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Blockade of muscarinic acetylcholine receptors in the ventral tegmental area blocks the acquisition of reward-related learning
Galaj, E., Nisanov, R., & Ranaldi, R. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.04.037 · Cited by 12 · see citing works
Motor activity-induced dopamine release in the substantia nigra is regulated by muscarinic receptors
Andersson, D. R., Björnsson, E., Bergquist, F., & Nissbrandt, H. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.11.011 · Cited by 11 · see citing works
Neurochemistry of Parkinson's disease
Rao, J. (2007) · Handbook of clinical neurology · doi:10.1016/s0072-9752(07)83007-7 · Cited by 11 · see citing works
Plasticity in the Brainstem: Prenatal and Postnatal Experience Can Alter Laterodorsal Tegmental (LDT) Structure and Function
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Blockade of M1 muscarinic acetylcholine receptors modulates the methamphetamine-induced psychomotor stimulant effect
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Rêve et schizophrénie : Un même support neurobiologique ?
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Feeding and systemic d-amphetamine increase extracellular acetylcholine in the medial thalamus: A possible reward enabling function
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Nicotine Disrupts Top-Down Habenular Control Over Cholinergic Inputs to the Ventral Tegmental Area to Increase Motivational Valence of Food Rewards
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Nicotinic and muscarinic acetylcholine receptor antagonism dose-dependently decreases sign- but not goal-tracking behavior in male rats
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GABAA receptors in GtoPdb v.2023.1
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Intra-ventral tegmental area microinjections of urotensin II modulate the effects of cocaine
Mueller, L. E., Kausch, M. A., Markovic, T., MacLaren, D. A. A., Dietz, D., Park, J., & Clark, S. D. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.036 · Cited by 2 · see citing works
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Conditional and non-conditional reward- related responses to alcohol - nicotinic mechanisms
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Nigrostriatal dopamine release modulated by mesopontine muscarinic receptors
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Authors: Miller, A. D., & Blaha, C. D.
Affiliations: Macquarie University (AU)
University of Memphis (US)
Corresponding author: Blaha, Charles D.
ORCID: Miller, Anthony D.
Blaha, Charles D.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2005-04
Volume: 21
Issue: 7
Pages: 1837-1846
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/j.1460-9568.2005.04017.x
OpenAlex: W1978171390
Cited by: 93
References: 92
Citations by year: 2026: 1 · 2025: 2 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 5 · 2018: 1 · 2017: 4 · 2016: 2 · 2015: 3 · 2014: 4 · 2013: 5 · 2012: 2
FWCI: 3.13
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 27 d)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
Keywords: M3 muscarinic receptor, M5 muscarinic receptor, ventral tegmental area, substantia nigra pars compacta, scopolamine, carbachol, muscarine, GABAergic interneurons, nicotinic acetylcholine receptors
MeSH terms: Animals, Carbachol, Dopamine, Drug Interactions, Electrochemistry, Electrodes, Male, Synaptic Transmission, Nucleus Accumbens, Piperidines, Receptors, Muscarinic, Scopolamine, Substantia Nigra, Rats, Wistar, Ventral Tegmental Area, Cholinergic Agonists, Muscarinic Antagonists, Rats

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Midbrain muscarinic receptor mechanisms underlying regulation of mesoaccumbens and nigrostriatal dopaminergic transmission in the rat

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