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Glutamatergic Contributions to Nicotinic Acetylcholine Receptor Agonist-Evoked Cholinergic Transients in the Prefrontal Cortex
Open accessAbstract
Because modulation of cortical cholinergic neurotransmission has been hypothesized to represent a necessary mechanism mediating the beneficial cognitive effects of nicotine and nicotinic acetylcholine receptor (nAChR) subtype-selective agonists, we used choline-sensitive microelectrodes for the real-time measurement of ACh release in vivo, to characterize cholinergic transients evoked by nicotine and the α4β2*-selective nAChR partial agonist 2-methyl-3-(2-(S)-pyrrolindinylmethoxy)pyridine dihydrochloride (ABT-089), a clinically effective cognition enhancer. In terms of cholinergic signal amplitudes, ABT-089 was significantly more potent than nicotine in evoking ACh cholinergic transients. Moreover, cholinergic signals evoked by ABT-089 were characterized by faster signal rise time and decay rate. The nAChR antagonist mecamylamine attenuated the cholinergic signals evoked by either compound. Cholinergic signals evoked by ABT-089 were more efficaciously attenuated by the relatively β2*-selective nAChR antagonist dihydro-β-erythroidine. The α7 antagonist methyllycaconitine did not affect choline signal amplitudes but partly attenuated the relatively slow decay rate of nicotine-evoked cholinergic signals. Furthermore, the AMPA receptor antagonist DNQX as well as the NMDA receptor antagonist APV more potently attenuated cholinergic signals evoked by ABT-089. Using glutamate-sensitive microelectrodes to measure glutamatergic transients, ABT-089 was more potent than nicotine in evoking glutamate release. Glutamatergic signals were highly sensitive to tetrodotoxin-induced blockade of voltage-regulated sodium channels. Together, the present evidence indicates that compared with nicotine, ABT-089 evokes more potent and sharper cholinergic transients in prefrontal cortex. Glutamatergic mechanisms necessarily mediate the cholinergic effects of nAChR agonists in the prefrontal cortex.
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“rapid acetylcholine transients in the mPFC are correlated with attention to brief cues”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Parikh et al. 2008
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“mice lacking the β2, but not the α7, subunit show impaired performance in an attentional task (Parikh et al. 2007(Parikh et al. , 2008)).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Parikh et al. 2008
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“nicotine can stimulate the firing of both POMC neurons that signal satiety, and neuropeptide Y (NPY) neurons that stimulate food seeking (Parikh et al. 2007(Parikh et al. , 2008)).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Parikh et al. 2008
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“in a slice preparation, the effects of nicotine on firing of POMC neurons persist longer than firing of NPY neurons (Parikh et al. 2007(Parikh et al. , 2008))”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Parikh et al. 2008
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Cites
Fitting curves to data using nonlinear regression: a practical and nonmathematical review
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Self-citationPrefrontal Acetylcholine Release Controls Cue Detection on Multiple Timescales
Parikh, V., Kozak, R., Martinez, V., & Sarter, M. (2007) · Neuron · doi:10.1016/j.neuron.2007.08.025 · Cited by 623
Self-citationMore attention must be paid: The neurobiology of attentional effort
Sarter, M., Gehring, W. J., & Kozak, R. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2005.11.002 · Cited by 552
Self-citationHasselmo, M. E., & McGaughy, J. (2004) · Progress in Brain Research · doi:10.1016/s0079-6123(03)45015-2 · Cited by 525
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“Because of evidence indicating that cortical ACh release mediates attentional performance (McGaughy et al., 1996; Gill et al., 2000; Dalley et al., 2004; Apparsundaram et al., 2005; Sarter et al., 2005, 2006; Kozak et al., 2006; Parikh et al., 2007), the enhancement of attentional functions and capacities by nAChR ago…”
BackgroundSelf-citationCholine transporters, cholinergic transmission and cognition
Sarter, M. F., & Parikh, V. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1588 · Cited by 400
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Research works printed but not linked: 1
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Harris, K. D., & Thiele, A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3084 · Cited by 915
Modes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733
Self-citationSofouglu, M., Herman, A. I., Robinson, C. D., & Waters, A. J. (2014) · Lincoln (University of Nebraska) · Cited by 417
Thiele, A., & Bellgrove, M. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.008 · Cited by 350
Phasic acetylcholine release and the volume transmission hypothesis: time to move on
Sarter, M. F., Parikh, V., & Howe, W. M. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2635 · Cited by 340
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Metadata
- Authors
- Parikh, V., Man, K., Decker, M. W., & Sarter, M.
- Affiliations
- University of Michigan (US)
- Abbott (United States) (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2008-04-02
- Volume
- 28
- Issue
- 14
- Pages
- 3769-3780
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6671097
- OpenAlex
- W2039986616
- Cited by
- 127
- References
- 71
- Citations by year
- 2025: 3 · 2024: 4 · 2023: 2 · 2022: 1 · 2021: 5 · 2020: 6 · 2019: 4 · 2018: 3 · 2017: 7 · 2016: 11 · 2015: 5 · 2014: 14 · 2013: 13 · 2012: 11
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Abbott Laboratories
- National Institute of Mental Health (R01MH080332, MH 080332)
- 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
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Smoking Behavior and Cessation
- Keywords
- nicotinic acetylcholine receptors, nicotine, prefrontal cortex, glutamate release, choline release, alpha4beta2 nAChR, alpha7 nAChR, mecamylamine, dihydro-beta-erythroidine, methyllycaconitine, AMPA receptors, NMDA receptor, cognitive enhancement
- MeSH terms
- Acetylcholine, Analysis of Variance, Animals, Choline, Dihydro-beta-Erythroidine, Dose-Response Relationship, Drug, Electrochemistry, Evoked Potentials, Male, Mecamylamine, Neostigmine, Nicotine, Pyridines, Pyrrolidines, Quinoxalines, Tetrodotoxin, Valine, Prefrontal Cortex, Excitatory Amino Acid Antagonists, Glutamic Acid, Nicotinic Agonists, Nicotinic Antagonists, Sodium Channel Blockers, Rats, In Vitro Techniques
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