Precisely Timed Nicotinic Activation Drives SST Inhibition in Neocortical Circuits
Open accessAbstract
Sleep, waking, locomotion, and attention are associated with cell-type-specific changes in neocortical activity. The effect of brain state on circuit output requires understanding of how neuromodulators influence specific neuronal classes and their synapses, with normal patterns of neuromodulator release from endogenous sources. We investigated the state-dependent modulation of a ubiquitous feedforward inhibitory motif in mouse sensory cortex, local pyramidal (Pyr) inputs onto somatostatin (SST)-expressing interneurons. Paired whole-cell recordings in acute brain slices and in vivo showed that Pyr-to-SST synapses are remarkably weak, with failure rates approaching 80%. Pharmacological screening revealed that cholinergic agonists uniquely enhance synaptic efficacy. Brief, optogenetically gated acetylcholine release dramatically enhanced Pyr-to-SST input, via nicotinic receptors and presynaptic PKA signaling. Importantly, endogenous acetylcholine release preferentially activated nicotinic, not muscarinic, receptors, thus differentiating drug effects from endogenous neurotransmission. Brain state- and synapse-specific unmasking of synapses may be a powerful way to functionally rewire cortical circuits dependent on behavioral demands.
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Cholinergic receptors are expressed by inhibitory and excitatory cortical neurons and on the terminals of thalamocortical neurons.
“Cholinergic receptors are expressed by inhibitory and excitatory cortical neurons119,124,158–164, as well as on the terminals of thalamocortical neurons165–169.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [164]
SST+ interneurons receive strong GABAergic input from VIP+ interneurons.
“In turn, SST+ interneurons receive strong GABAergic input from VIP+ interneurons and themselves exhibit mAChR-mediated depolarization, and connections from pyramidal neurons to SST+ interneurons are selectively enhanced by activation of presynaptic nAChRs164.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [164]
SST+ interneurons exhibit mAChR-mediated depolarization.
“In turn, SST+ interneurons receive strong GABAergic input from VIP+ interneurons and themselves exhibit mAChR-mediated depolarization, and connections from pyramidal neurons to SST+ interneurons are selectively enhanced by activation of presynaptic nAChRs164.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [164]
Connections from pyramidal neurons to SST+ interneurons are selectively enhanced by activation of presynaptic nAChRs.
“In turn, SST+ interneurons receive strong GABAergic input from VIP+ interneurons and themselves exhibit mAChR-mediated depolarization, and connections from pyramidal neurons to SST+ interneurons are selectively enhanced by activation of presynaptic nAChRs164.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [164]
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Correction: Cell type-specific long-range connections of basal forebrain circuit
Do, J. P. H., Xu, M., Lee, S., Chang, W.-C., Zhang, S., Chung, S., Yung, T. J., Fan, J. L., Miyamichi, K., Luo, L., et al. (2016) · eLife · doi:10.7554/elife.22475 · Cited by 27 · see citing works
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Research works printed but not linked: 2
- Alitto HJ, and Dan Y (2013). Cell-type-specific modulation of neocortical activity by basal forebrain input. Front Syst Neurosci 6, 79. 23316142 PMC3540901
- Chen N, Sugihara H, and Sur M (2015b). An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity. Nat Neurosci 18, 892– 902. 25915477 PMC4446146
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- Authors
- Urban-Ciecko, J., Jouhanneau, J.-S., Myal, S. E., Poulet, J. F. A., & Barth, A. L.
- Affiliations
- Center for the Neural Basis of Cognition (US)
- Max Delbrück Center (DE)
- Corresponding author
- Barth, Alison L.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2018-02
- Volume
- 97
- Issue
- 3
- Pages
- 611-625.e5
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6588401
- OpenAlex
- W2787738769
- Cited by
- 93
- References
- 92
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 11 · 2023: 8 · 2022: 7 · 2021: 12 · 2020: 14 · 2019: 17 · 2018: 10
- FWCI
- 6.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Funders
- McKnight Foundation
- NIH (R01NS088958)
- National Science Centre, Poland (2015/18/E/NZ4/00721)
- European Research Council (ERC-2015-CoG-682422)
- DFG (DFG-FOR-2143-Interneuron)
- Berlin Institute of Health
- European Union (FP7)
- 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 › Neural dynamics and brain function
- Keywords
- nicotinic acetylcholine receptors, somatostatin interneurons, pyramidal neurons, cholinergic modulation, acetylcholine release, feedforward inhibition, sensory cortex, muscarinic receptors, cortical circuits
- MeSH terms
- Acetylcholine, Animals, Carbachol, Female, Interneurons, Male, Mice, Inbred C57BL, Neural Inhibition, Receptors, Nicotinic, Somatostatin, Signal Transduction, Cyclic AMP-Dependent Protein Kinases, Pyramidal Cells, Cholinergic Agonists, Neocortex, Excitatory Postsynaptic Potentials, Basal Forebrain
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