Simultaneous release of glutamate and acetylcholine from single magnocellular “cholinergic” basal forebrain neurons
Open accessAbstract
Basal forebrain (BF) neurons provide the principal cholinergic drive to the hippocampus and cortex. Their degeneration is associated with the cognitive defects of Alzheimer's disease. Immunohistochemical studies suggest that some of these neurons contain glutamate, so might also release it. To test this, we made microisland cultures of single BF neurons from 12- to 14-d-old rats. Over 1-8 weeks in culture, neuronal processes made autaptic connections onto the neuron. In 34 of 36 cells tested, a somatically generated action potential was followed by a short-latency EPSC that was blocked by 1 mM kynurenic acid, showing that they released glutamate. To test whether the same neuron also released acetylcholine, we placed a voltage-clamped rat myoball expressing nicotinic receptors in contact with a neurite. In six of six neurons tested, the glutamatergic EPSC was accompanied by a nicotinic (hexamethonium-sensitive) myoball current. Stimulation of the M2-muscarinic presynaptic receptors (characterized using tripitramine and pirenzepine) produced a parallel inhibition of autaptic glutamatergic and myoball nicotinic responses; metabotropic glutamate receptor stimulation produced similar but less consistent and weaker effects. Atropine enhanced the glutamatergic EPSCs during repetitive stimulation by 25 +/- 6%; the anti-cholinesterase neostigmine reduced the train EPSCs by 37 +/- 6%. Hence, synaptically released acetylcholine exerted a negative-feedback inhibition of coreleased glutamate. We conclude that most cholinergic basal forebrain neurons are capable of releasing glutamate as a cotransmitter and that the release of both transmitters is subject to simultaneous feedback inhibition by synaptically released acetylcholine. This has implications for BF neuron function and for the use of cholinesterase inhibitors in Alzheimer's disease.
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Many cholinergic neurons also contain vGluT1/2/3 coexpressed with Ach synthesis, packaging, and release machinery in the striatum, basal forebrain, and medial habenula.
“However, many of these neurons also contain the vesicular glutamate transporters (vGluT1/2/3) that are coexpressed with molecular machinery for Ach synthesis, vesicular packaging, and release in multiple brain regions, including the striatum, basal forebrain, and medial habenula (mHb).22,56,57”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [57]
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Neurons, Receptors, and Channels
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Preparation and maintenance of single-cell micro-island cultures of basal forebrain neurons
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Memantine ameliorates scopolamine-induced amnesia in chicks trained on taste-avoidance learning
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- Authors
- Allen, T. G. J., Abogadie, F. C., & Brown, D. A.
- Affiliations
- University College London (GB)
- ORCID
- Brown, David A.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-02-01
- Volume
- 26
- Issue
- 5
- Pages
- 1588-1595
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6675485
- OpenAlex
- W2063583191
- Cited by
- 79
- References
- 58
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 5 · 2020: 4 · 2019: 2 · 2018: 3 · 2017: 3 · 2016: 5 · 2015: 5 · 2014: 4 · 2013: 5 · 2012: 5
- FWCI
- 2.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- basal forebrain neurons, glutamate release, acetylcholine release, co-transmission, cholinergic neurons, kynurenic acid, nicotinic acetylcholine receptors, M2 muscarinic receptor, metabotropic glutamate receptors, negative feedback inhibition, cholinesterase inhibitors, Alzheimer's disease
- MeSH terms
- Acetylcholine, Action Potentials, Animals, Cells, Cultured, Neural Inhibition, Neurons, Synapses, Prosencephalon, Rats, Sprague-Dawley, Receptors, Glutamate, Receptors, Presynaptic, Patch-Clamp Techniques, Glutamic Acid, Receptor, Muscarinic M2, Rats
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