Synaptic-like axo-axonal transmission from striatal cholinergic interneurons onto dopaminergic fibers
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Abstract
Transmission from striatal cholinergic interneurons (CINs) controls dopamine release through nicotinic acetylcholine receptors (nAChRs) on dopaminergic axons. Anatomical studies suggest that cholinergic terminals signal predominantly through non-synaptic volume transmission. However, the influence of cholinergic transmission on electrical signaling in axons remains unclear. We examined axo-axonal transmission from CINs onto dopaminergic axons using perforated-patch recordings, which revealed rapid spontaneous EPSPs with properties characteristic of fast synapses. Pharmacology showed that axonal EPSPs (axEPSPs) were mediated primarily by high-affinity α6-containing receptors. Remarkably, axEPSPs triggered spontaneous action potentials, suggesting that these axons perform integration to convert synaptic input into spiking, a function associated with somatodendritic compartments. We investigated the cross-species validity of cholinergic axo-axonal transmission by recording dopaminergic axons in macaque putamen and found similar axEPSPs. Thus, we reveal that synaptic-like neurotransmission underlies cholinergic signaling onto dopaminergic axons, supporting the idea that striatal dopamine release can occur independently of somatic firing to provide distinct signaling.
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Direct recordings from DA axon terminals in the striatum determined that Ach release from CINs onto dopamine axons primarily activates nAchRs and can locally induce action potentials.
“Heroic electrophysiological experiments that intracellularly recorded directly from DA axon terminals in the striatum unambiguously determined that synaptic release of Ach from CINs onto dopamine axons primarily activates nAchRs and is even capable of locally inducing APs.62”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [62]
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- Authors
- Kramer, P. F., Brill-Weil, S. G., Cummins, A. C., Zhang, R., Camacho-Hernandez, G. A., Newman, A. H., Eldridge, M. A. G., Averbeck, B. B., & Khaliq, Z. M.
- Affiliations
- National Institutes of Health (US)
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- Khaliq, Zayd M.
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- 2949-2960.e4
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- 0896-6273 (ISSN-L)
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- PMC9509469
- OpenAlex
- W4289780969
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- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Newcastle University ePrints (Newcastle Univesity) (cc-by-nc-nd)
- Funders
- National Institutes of Health
- National Institute of Mental Health (ZIAMH002928)
- National Institute on Drug Abuse (ZIADA000610)
- National Institute of Neurological Disorders and Stroke (NS003135, ZIANS003135)
- 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 › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- striatal cholinergic interneurons, dopaminergic axons, nicotinic acetylcholine receptors, spontaneous action potentials, striatal dopamine release, putamen, macaque
- MeSH terms
- Axons, Cholinergic Fibers, Corpus Striatum, Dopamine, Interneurons, Synaptic Transmission, Receptors, Nicotinic, Cholinergic Agents
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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