AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/3 of rat neocortex
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A novel, local inhibitory circuit in layer 2/3 of rat somatosensory cortex is described that connects pyramidal cells reciprocally with GABAergic vasoactive intestinal polypeptide-immunoreactive bipolar interneurons. In paired whole-cell recordings, the glutamatergic unitary responses (EPSPs or EPSCs) in bipolar cells evoked by repetitive (10 Hz) stimulation of a pyramidal cell show strong frequency-dependent depression. Unitary IPSPs evoked in pyramidal cells by repetitive stimulation of bipolar cells, on average, maintained their amplitude. This suggests that the excitatory synapses on bipolar cells act as a low-pass filter in the reciprocal pyramid-to-bipolar circuit. The EPSCs in bipolar cells are mediated predominantly by AMPA receptor (AMPAR) channels. AMPARs desensitize rapidly and recover slowly from desensitization evoked by a brief pulse of glutamate. In slices, reduction of AMPAR desensitization by cyclothiazide (50-100 microm) or conditioning steady-state desensitization induced by application of extracellular AMPA (50 nm) or glutamate (50 microm) strongly reduced synaptic depression. It is concluded that in the local circuits between pyramidal and bipolar cells the desensitization of AMPARs in bipolar cells contributes to low-pass feedback inhibition of layer 2/3 pyramidal neurons by bipolar cells.
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Excitatory inputs to VIP cells are depressing, as is the case for inputs to most interneurons.
“Excitatory inputs to VIP cells are depressing, as is the case for the inputs from most INs (Porter et al., 1998; Rozov et al., 2001).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Rozov et al., 2001
The Identification of bipolar interneurons section reports frequency-dependent depression of excitatory EPSPs in VIP-immunoreactive bipolar interneurons, supporting the claim about inputs to VIP cells. The passages do not establish that inputs to most interneurons are depressing; the Anatomical and functional signature section instead notes facilitating input to bitufted interneurons. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn situ hybridization and RT-PCR coupled with electrophysiological approaches revealed the presence of both inwardly rectifying, GluA2-lacking Ca2+-permeable (CP) AMPARs and GluA2-containing CI-AMPARs on inhibitory interneurons throughout the cortex and hippocampal formation.
“In situ hybridization and RT-PCR coupled with electrophysiological approaches subsequently revealed the presence of both inwardly rectifying, GluA2-lacking Ca2+-permeable (CP) AMPARs and GluA2-containing CI-AMPARs on inhibitory interneurons throughout the cortex and hippocampal formation (11, 51, 107, 388, 539, 769, 960).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [960]
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- Authors
- Rozov, A., Jerecic, J., Sakmann, B., & Burnashev, N.
- Affiliations
- Max Planck Society (DE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-10-15
- Volume
- 21
- Issue
- 20
- Pages
- 8062-8071
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6763867
- OpenAlex
- W2135917845
- Cited by
- 103
- References
- 33
- Citations by year
- 2024: 2 · 2023: 4 · 2021: 2 · 2020: 2 · 2019: 1 · 2018: 1 · 2017: 4 · 2016: 8 · 2015: 4 · 2014: 3 · 2013: 4 · 2012: 4
- FWCI
- 2.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam) (submittedVersion)
- Discovery Research Portal (University of Dundee) (submittedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- VU Research Portal (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Keywords
- AMPA receptor desensitization, synaptic depression, vasoactive intestinal peptide, pyramidal neurons, reciprocal inhibition, product inhibition, low-pass filtering, somatosensory cortex, layer 2/3, cyclothiazide, glutamate, inhibitory interneurons
- MeSH terms
- Animals, Axons, Benzothiadiazines, Dendrites, Electric Stimulation, Feedback, gamma-Aminobutyric Acid, Interneurons, Ion Channels, Lysine, Membrane Potentials, Synaptic Transmission, Somatosensory Cortex, Synapses, Rats, Wistar, Receptors, Glutamate, Pyramidal Cells, Receptors, AMPA, Patch-Clamp Techniques, Neocortex, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques
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