Cortical ChAT+ neurons co-transmit acetylcholine and GABA in a target- and brain-region-specific manner
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Abstract
Abstract The cerebral cortex contains neurons that express choline acetyltransferase (ChAT) and are a potential local source of acetylcholine. However, the neurotransmitters released by cortical ChAT + neurons and their synaptic connectivity are unknown. We show that the nearly all cortical ChAT + neurons are specialized VIP + interneurons that release GABA strongly onto other inhibitory interneurons and acetylcholine sparsely onto layer 1 interneurons and other VIP + /ChAT + interneurons. This differential transmission of ACh and GABA based on the postsynaptic target neuron is reflected in VIP + /ChAT + interneuron pre-synaptic terminals, as quantitative molecular analysis shows that only a subset of these are specialized to release acetylcholine. In addition, we identify a separate, sparse population of non-VIP ChAT + neurons in the medial prefrontal cortex with a distinct developmental origin that robustly release acetylcholine in layer 1. These results demonstrate both cortex-region heterogeneity in cortical ChAT + interneurons and target-specific co-release of acetylcholine and GABA.
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Ach is the primary transmitter when the postsynaptic neuron is a layer 1 interneuron or another VIP/Chat+ neuron and the receptors are nAchRs.
“Ach is the primary transmitter when the postsynaptic neuron is a layer 1 interneuron or another VIP/Chat+ neuron and the postsynaptic receptors are nAchRs.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
The regional differences in VIP/ChAT+ transmission may arise from a distinct population of VIP-negative cholinergic interneurons in mPFC.
“However, these differences may be due to the existence of a unique population of VIPÀ CINs in this region.97”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
Optogenetic excitation of VIP/ChAT+ neurons in motor and visual cortex revealed GABAergic output primarily to other interneuron subtypes, with a bias toward Sst+ cortical interneurons.
“Optogenetic excitation of VIP/Chat+ neurons in the motor and visual cortex revealed GABAergic output primarily to other interneuron subtypes, with a bias toward the Sst+ cortical interneurons.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
Cholinergic EPSCs from VIP/ChAT+ neurons were sparse but primarily detected in layer 1 interneurons and other VIP cells.
“Cholinergic EPSCs were sparse, but primarily detected in layer 1 interneurons and other VIP cells.97”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
The net effect of VIP/Chat+ activity on the cortical microcircuit is disinhibition of excitatory pyramidal neurons by engaging multiple cell types across the cortical column.
“The net effect of VIP/Chat+ activity on the cortical microcircuit is disinhibition of excitatory pyramidal neurons by engaging multiple cell types across the cortical column.97,98”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
GABA is the primary transmitter when the postsynaptic neuron is a Sst+, PV+, or 5HT3aR+ interneuron.
“But GABA is the primary transmitter when the postsynaptic neuron is a Sst+, PV+, or 5HT3aR+ interneuron.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
In mouse and rat medial prefrontal cortex, cholinergic transmission from VIP/ChAT+ neurons onto layer 1 interneurons occurs with higher probability and evokes larger postsynaptic responses.
“as cholinergic output from VIP/ChAT+ neurons to layer 1 interneurons in the mouse and rat medial prefrontal cortex occurs at a higher probability and produces a larger postsynaptic response.97,98”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
GABA and Ach coreleased in cortex may act in parallel on different targets to achieve a common function, such as placing cortex in a more excitable and pro-plasticity state.
“GABA and Ach coreleased in the cortex may act in parallel on different targets to achieve a single common function, such as placing the cortex in a more excitable and pro-plasticity state by simultaneously inhibiting Sst+ interneurons with GABA while using Ach release to excite disinhibitory interneurons and activate muscarinic receptors on pyramidal cells.90,97,98,140,141”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [97]
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- Authors
- Granger, A. J., Wang, W., Robertson, K., El-Rifai, M., Zanello, A. F., Bistrong, K., Saunders, A., Chow, B. W., Nuñez, V., Turrero García, M., Harwell, C. C., Gu, C., & Sabatini, B. L.
- Affiliations
- Howard Hughes Medical Institute (US)
- Harvard University (US)
- Department of Neurobiology, Harvard Medical School, Boston, United States
- Corresponding author
- Sabatini, Bernardo L
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2020-07-02
- Volume
- 9
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC7360370
- OpenAlex
- W3038435474
- Cited by
- 124
- References
- 70
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 56 · 2023: 16 · 2022: 17 · 2021: 15 · 2020: 4
- FWCI
- 5.96
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Neurological Disorders and Stroke (R37 NS046579, K99 NS102429, P30Ns072030)
- Jane Coffin Childs Memorial Fund for Medical Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- choline acetyltransferase, acetylcholine, VIP interneurons, cortical interneurons, layer 1 interneurons, medial prefrontal cortex, synaptic connectivity, cholinergic interneurons, mouse cortex
- MeSH terms
- Acetylcholine, Animals, Brain, Cerebral Cortex, Choline O-Acetyltransferase, gamma-Aminobutyric Acid, Heterozygote, Interneurons, Neurons, Prefrontal Cortex, Presynaptic Terminals, Mice
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