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Laminar Specificity of Functional Input to Distinct Types of Inhibitory Cortical Neurons
Open accessAbstract
Despite the presence of numerous inhibitory cell types, laminar excitatory input has only been characterized for limited identified types, and it is unknown whether there are differences between cell types in their laminar sources of inhibitory input. In the present study, we characterized sources of local input to nine distinct types of layer 2/3 inhibitory neurons in living slices of mouse somatosensory cortex. Whole-cell recordings from identified cell types, facilitated by use of transgenic mice expressing green fluorescent protein in limited inhibitory neuron populations, were combined with laser scanning photostimulation. We found that each inhibitory cell type received distinct excitatory and inhibitory laminar input patterns. Excitatory inputs could be grouped into three categories. All inhibitory cell types received strong excitation from layer 2/3, and for calretinin (CR)-positive Martinotti cells and burst-spiking interneurons, this was their dominant source of excitatory input. Three other cell types, including fast-spiking basket cells, CR-negative Martinotti cells, and bipolar interneurons, also received strong excitatory input from layer 4. The remaining four inhibitory cell types, including chandelier cells, neurogliaform cells, irregular spiking basket cells, and regular spiking presumptive basket cells, received strong excitatory input from layer 5A and not layer 4. Laminar sources of inhibitory input varied between cell types and could not be predicted from the sources of excitatory input. Thus, there are cell-type specific differences in laminar sources of both excitation and inhibition, and complementary input patterns from layer 4 versus layer 5A suggest cell type differences in their relationships to lemniscal versus paralemniscal pathways.
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“some reports have found different excitatory input sources and in vivo responses between PV FS basket and chandelier INs”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Xu and Callaway, 2009
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“L2/3 bipolar INs have been shown to receive inputs from several layers, which was less common for most other cell types studied (Xu and Callaway, 2009).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Xu and Callaway, 2009
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“Although so far only minor electrophysiological or morphological differences between CR+ and CR- Sst INs have been identified, distinct excitatory input patterns have been found (Xu and Callaway, 2009; Xu et al., 2006).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Xu and Callaway, 2009
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Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
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Two networks of electrically coupled inhibitory neurons in neocortex
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Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells
Silberberg, G., & Markram, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.012 · Cited by 768
Excitatory cortical neurons form fine-scale functional networks
Yoshimura, Y., Dantzker, J. L. M., & Callaway, E. M. (2005) · Nature · doi:10.1038/nature03252 · Cited by 601
Self-citationChattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., & Huang, Z. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1851-04.2004 · Cited by 596
Pyramidal cell communication within local networks in layer 2/3 of rat neocortex.
Holmgren, C., Harkany, T., Svennenfors, B., & Zilberter, Y. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.044784 · Cited by 573
Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex
Cruikshank, S. J., Lewis, T. J., & Connors, B. W. (2007) · Nature Neuroscience · doi:10.1038/nn1861 · Cited by 558
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Sorted by citations
GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033
Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons
Rudy, B., Fishell, G., Lee, S., & Hjerling‐Leffler, J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20853 · Cited by 1,420
Principles of connectivity among morphologically defined cell types in adult neocortex
Jiang, X., Shen, S., Cadwell, C. R., Berens, P., Sinz, F., Ecker, A. S., Patel, S., & Tolias, A. S. (2015) · Science · doi:10.1126/science.aac9462 · Cited by 908
Parallel processing strategies of the primate visual system
Nassi, J. J., & Callaway, E. M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2619 · Cited by 802
Self-citationBroadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex
Kerlin, A. M., Andermann, M. L., Berezovskii, V. K., & Reid, R. C. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.002 · Cited by 613
Metadata
- Authors
- Xu, X., & Callaway, E. M.
- Affiliations
- Salk Institute for Biological Studies (US)
- Corresponding author
- Callaway, Edward M.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-01-07
- Volume
- 29
- Issue
- 1
- Pages
- 70-85
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2656387
- OpenAlex
- W2124626486
- Cited by
- 218
- References
- 37
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 7 · 2023: 11 · 2022: 10 · 2021: 4 · 2020: 14 · 2019: 8 · 2018: 6 · 2017: 13 · 2016: 22 · 2015: 17 · 2014: 21 · 2013: 17 · 2012: 17
- FWCI
- 8.18
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH063912, R01MH063912)
- National Institute on Drug Abuse (R00DA023700, K99DA023700)
- National Eye Institute (EY-010742, R01EY010742)
- 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
- inhibitory interneurons, laminar specificity, somatosensory cortex, layer 2/3, layer 4, Martinotti cells, basket cells, chandelier cells, neurogliaform cells, calretinin, excitatory synaptic input, inhibitory synaptic input, lemniscal pathway
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Animals, Newborn, Dendrites, Electric Stimulation, Mice, Transgenic, Nerve Net, Neural Inhibition, Neurons, Photic Stimulation, Proteins, RNA, Messenger, Somatosensory Cortex, Somatostatin, Models, Statistical, Patch-Clamp Techniques, Statistics, Nonparametric, Excitatory Postsynaptic Potentials, Green Fluorescent Proteins, Mice, S100 Calcium Binding Protein G, Calbindin 2, In Vitro Techniques
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