Cholinergic Modulation of Locomotion and Striatal Dopamine Release Is Mediated by 6 4* Nicotinic Acetylcholine Receptors

Drenan, R. M.; Grady, S. R.; Steele, A. D.; McKinney, S.; Patzlaff, N. E.; McIntosh, J. M.; Marks, M. J.; Miwa, J. M.; Lester, H. A.

doi:10.1523/jneurosci.2056-10.2010

Cited by 128Nicotinic Acetylcholine Receptors StudyNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Cholinergic Modulation of Locomotion and Striatal Dopamine Release Is Mediated by 6 4* Nicotinic Acetylcholine Receptors

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Drenan, R. M., Grady, S. R., Steele, A. D., McKinney, S., Patzlaff, N. E., McIntosh, J. M., Marks, M. J., Miwa, J. M. +1 more·2010·Journal of Neuroscience

DOI 10.1523/jneurosci.2056-10.2010PMC PMC3390922

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Abstract

Dopamine (DA) release in striatum is governed by firing rates of midbrain DA neurons, striatal cholinergic tone, and nicotinic ACh receptors (nAChRs) on DA presynaptic terminals. DA neurons selectively express alpha6* nAChRs, which show high ACh and nicotine sensitivity. To help identify nAChR subtypes that control DA transmission, we studied transgenic mice expressing hypersensitive alpha6(L9'S)* receptors. alpha6(L9'S) mice are hyperactive, travel greater distance, exhibit increased ambulatory behaviors such as walking, turning, and rearing, and show decreased pausing, hanging, drinking, and grooming. These effects were mediated by alpha6alpha4* pentamers, as alpha6(L9'S) mice lacking alpha4 subunits displayed essentially normal behavior. In alpha6(L9'S) mice, receptor numbers are normal, but loss of alpha4 subunits leads to fewer and less sensitive alpha6* receptors. Gain-of-function nicotine-stimulated DA release from striatal synaptosomes requires alpha4 subunits, implicating alpha6alpha4beta2* nAChRs in alpha6(L9'S) mouse behaviors. In brain slices, we applied electrochemical measurements to study control of DA release by alpha6(L9'S) nAChRs. Burst stimulation of DA fibers elicited increased DA release relative to single action potentials selectively in alpha6(L9'S), but not WT or alpha4KO/alpha6(L9'S), mice. Thus, increased nAChR activity, like decreased activity, leads to enhanced extracellular DA release during phasic firing. Bursts may directly enhance DA release from alpha6(L9'S) presynaptic terminals, as there was no difference in striatal DA receptor numbers or DA transporter levels or function in vitro. These results implicate alpha6alpha4beta2* nAChRs in cholinergic control of DA transmission, and strongly suggest that these receptors are candidate drug targets for disorders involving the DA system.

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Expression of a hypersensitive α6 subunit in a BAC transgenic mouse line potentiates nicotine-induced burst firing in DA neurons and potentiates nicotine place preference at low doses.
“Similarly, expression of a hypersensitive α6 subunit in a bacterial artificial chromosome (BAC) transgenic mouse line potentiates nicotine-induced burst firing in DA neurons, and potentiates nicotine place preference at low doses of nicotine (Drenan et al. 2008a(Drenan et al. , 2010)).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Drenan et al. 2010
The Results (α6α4* nAChR-mediated locomotion and behavioral analysis; page unavailable) identify the hypersensitive α6L9′S BAC mouse line. The Results (Burst firing selectively increases DA release in α6L9′S dorsal striatum; page unavailable) report that nicotine increases DA-neuron firing, but only suggest that it may increase burst firing. Our copy does not report nicotine place preference at low doses; its low-dose behavioral finding concerns locomotor activation. (LLM, conf=0.85)
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Authors: Drenan, R. M., Grady, S. R., Steele, A. D., McKinney, S., Patzlaff, N. E., McIntosh, J. M., Marks, M. J., Miwa, J. M., & Lester, H. A.
Affiliations: California Institute of Technology (US)
University of Colorado Boulder (US)
University of Utah (US)
Corresponding author: Lester, H. A.
ORCID: Drenan, R. M.
Steele, A. D.
McIntosh, J. M.
Marks, M. J.
Miwa, J. M.
Lester, H. A.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2010-07-21
Volume: 30
Issue: 29
Pages: 9877-9889
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.2056-10.2010
PMC: PMC3390922
OpenAlex: W2010309382
Cited by: 127
References: 61
Citations by year: 2026: 2 · 2025: 4 · 2024: 4 · 2023: 1 · 2022: 4 · 2021: 1 · 2020: 10 · 2019: 8 · 2018: 9 · 2017: 7 · 2016: 2 · 2015: 8 · 2014: 19 · 2013: 14 · 2012: 13
FWCI: 6.39
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by-nc-sa)
Funders: Ellison Medical Foundation
Gordon and Betty Moore Foundation
Tobacco-Related Disease Research Program
California Institute of Technology
National Institutes of Health (5t32ns007251-22, AG033954, MH53631, GM 48677)
National Institute on Aging (R01AG033954, AG033954)
National Institute of Mental Health (MH53631, R01MH053631, R29MH053631)
National Institute on Drug Abuse (DA-19375, U19DA019375, DA 015663, DA 03194, DA17279, R01DA017279, P30DA015663, F32DA021492, R01DA003194, R01DA012242, DA12242, DA021492)
National Institute of General Medical Sciences (P01GM048677, GM48677)
National Institute of Neurological Disorders and Stroke (T32 NS-007251, NS007251)
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: nicotinic acetylcholine receptors, alpha4 subunit, striatal dopamine release, locomotion, burst firing, presynaptic terminals, dopaminergic neurons
MeSH terms: Animals, Corpus Striatum, Dopamine, Ganglionic Stimulants, Hyperkinesis, Locomotion, Mice, Inbred C57BL, Mice, Transgenic, Mutation, Nicotine, Receptors, Dopamine, Receptors, Nicotinic, Synaptosomes, Mice, Knockout, Dopamine Plasma Membrane Transport Proteins, Mice

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Cholinergic Modulation of Locomotion and Striatal Dopamine Release Is Mediated by 6 4* Nicotinic Acetylcholine Receptors

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