Multiple clusters of release sites formed by individual thalamic afferents onto cortical interneurons ensure reliable transmission
Open accessAbstract
Thalamic afferents supply the cortex with sensory information by contacting both excitatory neurons and inhibitory interneurons. Interestingly, thalamic contacts with interneurons constitute such a powerful synapse that even one afferent can fire interneurons, thereby driving feedforward inhibition. However, the spatial representation of this potent synapse on interneuron dendrites is poorly understood. Using Ca imaging and electron microscopy we show that an individual thalamic afferent forms multiple contacts with the interneuronal proximal dendritic arbor, preferentially near branch points. More contacts are correlated with larger amplitude synaptic responses. Each contact, consisting of a single bouton, can release up to seven vesicles simultaneously, resulting in graded and reliable Ca transients. Computational modeling indicates that the release of multiple vesicles at each contact minimally reduces the efficiency of the thalamic afferent in exciting the interneuron. This strategy preserves the spatial representation of thalamocortical inputs across the dendritic arbor over a wide range of release conditions.
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These thalamocortical connections onto PV cells are provided by high quantal amplitude with calcium-permeable AMPA receptors and multiple clustered release sites.
“provided by high quantal amplitude with calcium permeable AMPA receptors (Hull et al., 2009) and multiple synaptic contacts forming clusters of neurotransmitter release sites (Bagnall et al., 2011).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Bagnall et al., 2011
Output synapses of FS cells rely exclusively on P/Q-type Ca2+ channels, which have faster kinetics and mediate nanodomain coupling between Ca2+ influx and neurotransmitter release.
“Output synapses rely exclusively on P/Q-type Ca2+ channels14–17, which have faster kinetics18 and mediate nanodomain coupling between Ca2+ influx and neurotransmitter release15,19.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as [14]
The Results passage on postsynaptic Ca hotspots concerns calcium signals in FS-cell dendrites after thalamic input, not the channels at FS-cell output synapses. The Discussion passage on multivesicular release likewise does not identify P/Q-type channels, compare their kinetics, or describe nanodomain coupling. Searches for those terms found no passage addressing the attributed claim. (LLM, conf=0.75)
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- Authors
- Bagnall, M. W., Hull, C., Bushong, E. A., Ellisman, M. H., & Scanziani, M.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of California San Diego (US)
- Corresponding author
- Bagnall, Martha W.
- Scanziani, Massimo
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-07
- Volume
- 71
- Issue
- 1
- Pages
- 180-194
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3271052
- OpenAlex
- W2040879146
- Cited by
- 80
- References
- 76
- Citations by year
- 2025: 4 · 2023: 8 · 2022: 6 · 2021: 7 · 2020: 4 · 2019: 5 · 2018: 4 · 2017: 7 · 2016: 4 · 2015: 5 · 2014: 10 · 2013: 9 · 2012: 6
- FWCI
- 3.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 747 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Gatsby Charitable Foundation
- National Institutes of Health (MH070058)
- Howard Hughes Medical Institute
- National Center for Research Resources (5P41RR004050)
- 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 › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- thalamic afferents, cortical interneurons, thalamocortical synapses, dendritic branching, synaptic vesicle release, feedforward inhibition, calcium transients, synaptic reliability
- MeSH terms
- Animals, Calcium, Computer Simulation, Dendrites, Electric Stimulation, Interneurons, Mice, Inbred ICR, Microscopy, Electron, Neural Pathways, Synaptic Transmission, Neurons, Afferent, Thalamus, Excitatory Postsynaptic Potentials, Mice, Molecular Imaging
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