Morphology and physiology of cortical neurons in layer I
Open accessAbstract
The electrophysiological and morphological properties of layer I neurons were studied in visual cortex slices from 7- to 19-d-old rats using whole-cell recording and biocytin labeling. A heterogeneous population of small, nonpyramidal neurons was found. Approximately one third of the cells we recorded were neurogliaform cells; another third were multipolar neurons with axons descending out of layer I. The remaining cells were heterogeneous and were not classified. In slices from 7- to 10-d-old animals only, we identified Cajal-Retzius cells. Neurogliaform neurons had a very dense local axonal field, which was largely contained within layer I. Cells with descending axons had a relatively sparse local axonal arbor and projected at least to layer II and sometimes deeper. Spiking in neurogliaform neurons was followed by an afterdepolarizing potential, whereas spiking in cells with descending axons was followed by a slow after-hyperpolarizing potential (AHP). In addition, neurogliaform cells exhibited less spike broadening and a larger fast AHP after single spikes than did cells with descending axons. Generally, cells in layer I received synaptic inputs characterized as either GABA- or glutamate-mediated, suggesting the presence of excitatory and inhibitory inputs. With their output largely limited to layer I, neurogliaform cells could synapse with other layer I neurons, the most distal dendritic branches of pyramidal cells, or the dendrites of layer II/III interneurons, which invade layer I. Cells with descending axons could contact a wide variety of cortical cells throughout their vertical projection.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Elongated neurogliaform cells resemble typical spherical neurogliaform cells in having a dense axonal arbor surrounding a short multipolar dendritic tree, and in having similar intrinsic and functional properties, including frequent late spiking, apparent lack of spike frequency adaptation at threshold, and mediation of GABAB responses in connected postsynaptic targets.
“Sometimes called “elongated neurogliaform cells” (Jiang et al., 2015; Jiang et al., 2013) this subtype of NGFC resembles typical “spherical” NGFCs not only in having a very dense axonal arbor surrounding a short multipolar dendritic tree, but in having seemingly similar intrinsic and functional properties, including a frequent late spiking firing pattern, an apparent lack of spike frequency adapta”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Hestrin and Armstrong, 1996
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredIn layer 1, a large proportion of interneurons with neurogliaform-type morphology have a horizontal axonal arbor that extends for longer horizontal distances than classical neurogliaform cells, perhaps spanning several columns and largely remaining within the same layer.
“In L1, a large proportion of INs with neurogliaform-type morphology have been reported to have an horizontal axonal arbor that extends for longer horizontal distances than classical NGFCs, perhaps spanning several columns and largely remaining within the same layer (Hestrin and Armstrong, 1996; Jiang et al., 2015; Jiang et al., 2013; Kubota et al., 2011b; Zhou and Hablitz, 1996).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Hestrin and Armstrong, 1996
The Neurogliaform cells section (page unavailable) reports that 8 of 26 recorded layer I cells had dense axonal arbors almost entirely confined to that layer, with projection fields extending 200–300 μm anteroposteriorly. It does not compare their horizontal reach with classical neurogliaform cells or say that they may span several columns. (LLM, conf=0.86)
Experimental — accuracy not yet measuredNeurogliaform morphology is often associated with a late-spiking firing pattern, characterized by a slow ramp depolarization preceding firing and non-adapting spike trains near threshold.
“The neurogliaform morphology has often been associated with a late-spiking (LS) firing pattern, characterized by a slow ramp depolarization preceding firing and non-adapting spike trains near threshold (Hestrin and Armstrong, 1996; Kawaguchi, 1995; Kubota et al., 2011a; Olah et al., 2009; Tamas et al., 2003).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Hestrin and Armstrong, 1996
The Neurogliaform cells section (page unavailable) reports a prior finding of delayed spiking in neurogliaform cells, but says the authors did not observe late spiking in their layer I cells. It also reports less frequency adaptation than in cells with descending axons, not non-adapting trains near threshold: threshold stimulation elicited single spikes, and stronger stimulation produced trains with some adaptation. The slow depolarization described in this paper occurred after spikes, not as a ramp preceding firing. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Ogawa, M., Miyata, T., Nakajimat, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., & Mikoshibat, K. (1995) · Neuron · doi:10.1016/0896-6273(95)90329-1 · Cited by 889 · cited 1× · see citing works
“Recent findings suggest that they are important developmentally (Ogawa et al., 1995); however, their fate in the adult cortex has not been resolved.”
Background
Flagged first, then by citations
Research works printed but not linked: 2
- DeFelipe J, Jones EG (1988) Cajal on the cerebral cortex: an annotated translation of the complete writings. Oxford: Oxford UP.
- Ramon y Cajal S (1911) Histologie du System Nerveux de l'Homme et des Vertebrates. (Translated into English by N Swanson and LW Swanson as Histology of the Nervous System of Man and Vertebrates.) Oxford: Oxford UP, 1995.
Cited by
Sorted by citations
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
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 · see citing works
Adult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · see citing works
Reconstruction and Simulation of Neocortical Microcircuitry
Markram, H., Muller, E., Ramaswamy, S., Reimann, M. W., Abdellah, M., Sanchez, C. A., Ailamaki, A., Alonso-Nanclares, L., Antille, N., Arsever, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.029 · Cited by 1,705 · see citing works
GABAergic cell subtypes and their synaptic connections in rat frontal cortex
Kawaguchi, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.476 · Cited by 1,416 · see citing works
Interneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · see citing works
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 · see citing works
A disinhibitory microcircuit for associative fear learning in the auditory cortex
Letzkus, J. J., Wolff, S. B. E., Meyer, E. M. M., Tovote, P., Courtin, J., Herry, C., & Lüthi, A. (2011) · Nature · doi:10.1038/nature10674 · Cited by 840 · see citing works
Differences in Synaptic GABAA Receptor Number Underlie Variation in GABA Mini Amplitude
Nusser, Z., Cull-Candy, S., & Farrant, M. (1997) · Neuron · doi:10.1016/s0896-6273(00)80382-7 · Cited by 449 · see citing works
Identified sources and targets of slow inhibition in the neocortex
Tamás, G., Simon, A. L., & Szabadics, J. (2003) · Science · doi:10.1126/science.1082053 · Cited by 359 · see citing works
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
Price, C. J., Cauli, B., Kovacs, E. R., Kulik, A., Lambolez, B., Shigemoto, R., & Capogna, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1135-05.2005 · Cited by 255 · see citing works
Classification of NPY-Expressing Neocortical Interneurons
Karagiannis, A., Gallopin, T., Dávid, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E. M. C., Staiger, J. F., & Cauli, B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0058-09.2009 · Cited by 256 · see citing works
Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., Hirai, Y., Morishima, M., & Kawaguchi, Y. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq252 · Cited by 235 · see citing works
Thalamic control of layer 1 circuits in prefrontal cortex
Cruikshank, S. J., Ahmed, O. J., Stevens, T. R., Patrick, S. L., Gonzalez, A. N., Elmaleh, M., & Connors, B. W. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3231-12.2012 · Cited by 212 · see citing works
Four Unique Interneuron Populations Reside in Neocortical Layer 1
Schuman, B., Machold, R. P., Hashikawa, Y., Fuzik, J., Fishell, G. J., & Rudy, B. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.1613-18.2018 · Cited by 184 · see citing works
“…with short dendrites and a wider dense axonal arbor, which differs from NGFCs in other layers by often extending horizontally across several columns, as described previously (Hestrin and Armstrong, 1996; Zhou and Hablitz, 1996b; Kubota et al., 2011; Jiang et al., 2013, 2015; Tremblay et al., 2016).”
BackgroundResultInfluentialNeuronal circuits in barrel cortex for whisker sensory perception
Staiger, J. F., & Petersen, C. C. H. (2021) · Physiological Reviews · doi:10.1152/physrev.00019.2019 · Cited by 165 · see citing works
Synaptic interactions of late-spiking neocortical neurons in layer 1
Chu, Z., Galarreta, M., & Hestrin, S. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00096.2003 · Cited by 172 · see citing works
Self-citationGap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex
Simon, A., Oláh, S., Molnár, G., Szabadics, J., & Tamás, G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1431-05.2005 · Cited by 163 · see citing works
Neocortical Layer 1: an elegant solution to top-down and bottom-up integration
Schuman, B., Dellal, S., Prönneke, A., Machold, R., & Rudy, B. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100520-012117 · Cited by 148 · see citing works
Vucurovic, K., Gallopin, T., Ferezou, I., Rancillac, A., Chameau, P., van Hooft, J. A., Geoffroy, H., Monyer, H., Rossier, J., & Vitalis, T. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp310 · Cited by 139 · see citing works
Wozny, C., & Williams, S. R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq257 · Cited by 129 · see citing works
Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex
Oláh, S. (2007) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.004.2007 · Cited by 118 · see citing works
Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons
Christophe, E., Roebuck, A., Staiger, J. F., Lavery, D. J., Charpak, S., & Audinat, E. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1318 · Cited by 130 · see citing works
GABAA,slow: causes and consequences
Capogna, M., & Pearce, R. A. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2010.10.005 · Cited by 129 · see citing works
Connectivity of GABAergic Calretinin-immunoreactive Neurons in Rat Primary Visual Cortex
Gonchar, Y. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.7.683 · Cited by 117 · see citing works
Fuentealba, P., Klausberger, T., Karayannis, T., Suen, W. Y., Huck, J., Tomioka, R., Rockland, K., Capogna, M., Studer, M., Morales, M., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4199-09.2010 · Cited by 113 · see citing works
Zsiros, V., & Maccaferri, G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2810-05.2005 · Cited by 88 · see citing works
A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus
Ceranik, K., Bender, R., Geiger, J. R. P., Monyer, H., Jonas, P., Frotscher, M., & Lübke, J. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05380.1997 · Cited by 83 · see citing works
Time-dependent, layer-specific modulation of sensory responses mediated by neocortical layer 1
Shlosberg, D., Amitai, Y., & Azouz, R. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00520.2006 · Cited by 34 · see citing works
Digital PCR to Determine the number of Transcripts from Single Neurons after Patch-Clamp Recording
Faragó, N., Kocsis, Á. K., Lovas, S., Molnár, G., Boldog, E., Rózsa, M., Szemenyei, V., Vámos, E., Nagy, L. I., Tamás, G., et al. (2013) · BioTechniques · doi:10.2144/000114029 · Cited by 26 · see citing works
- Authors
- Hestrin, S., & Armstrong, W. E.
- Affiliations
- University of Tennessee Health Science Center (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1996-09-01
- Volume
- 16
- Issue
- 17
- Pages
- 5290-5300
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6578880
- OpenAlex
- W2116491807
- Cited by
- 194
- References
- 2
- Citations by year
- 2025: 3 · 2024: 6 · 2023: 4 · 2022: 2 · 2021: 5 · 2020: 9 · 2019: 1 · 2018: 12 · 2017: 8 · 2016: 9 · 2015: 11 · 2014: 9 · 2013: 7 · 2012: 9
- FWCI
- 2.84
- 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 Eye Institute (EY09120, R01EY009120)
- National Institute of Neurological Disorders and Stroke (R56NS023941, NS 23941, R01NS023941)
- 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 › Visual perception and processing mechanisms
- Keywords
- visual cortex, neurogliaform cells, Cajal-Retzius cells, descending axons, spike broadening, GABAergic synapses, glutamatergic synapses, synaptic input, neuronal morphology, axonal arbors, interneurons, pyramidal neurons, cortical development
- MeSH terms
- Animals, Axons, Neural Inhibition, Neuroglia, Neurons, Synapses, Visual Cortex, Rats, Wistar, Patch-Clamp Techniques, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
