The DOI matches its Crossref record; 33 of the 33 references it cites were found in a registry or an index.
Routing of spike series by dynamic circuits in the hippocampus
Abstract
Recurrent inhibitory loops are simple neuronal circuits found in the central nervous system, yet little is known about the physiological rules governing their activity. Here we use simultaneous somatic and dendritic recordings in rat hippocampal slices to show that during a series of action potentials in pyramidal cells recurrent inhibition rapidly shifts from their soma to the apical dendrites. Two distinct inhibitory circuits are sequentially recruited to produce this shift: one, time-locked with submillisecond precision to the onset of the action potential series, transiently inhibits the somatic and perisomatic regions of pyramidal cells; the other, activated in proportion to the rate of action potentials in the series, durably inhibits the distal apical dendrites. These two operating modes result from the synergy between pre- and postsynaptic properties of excitatory synapses onto recurrent inhibitory neurons with distinct projection patterns. Thus, the onset of a series of action potentials and the rate of action potentials in the series are selectively captured and transformed into different spatial patterns of recurrent inhibition.
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In the citing paper
“excitatory inputs onto Sst INs, apparently regardless of subtypes, are strongly facilitating”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Pouille and Scanziani, 2004
In the citing paper
“Indeed, the restriction of horizontally oriented O-LM soma and spiny dendrites within s.o. and the alveus dictates that the dominant source of excitatory recruitment is from CA1 pyramidal cell collaterals while the preferential axonal targeting to s.l.m. then distributes inhibition back to the distal apical dendritic tufts of CA1 pyramidal cells to gate excitatory input from the entorhinal cortex”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [923]
In the citing paper
“Trains of action potentials from CA1 pyramidal cells drive excitation onto two populations of interneurons termed “onset transient” and “late persistent” interneurons (923).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [923]
In the citing paper
“Pouille and Scanziani (923) provided the first demonstration that recurrent inhibition onto CA1 pyramidal cells occurs via a dynamic rerouting of inhibitory drive that commences via perisomatic inhibitory input followed by a delayed primarily dendritic inhibition.”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [923]
Citations
Cites
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,478
Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems
Dayan, P., & Abbott, L. F. (2001) · Cited by 3,153
Spikes: Exploring the Neural Code
Rieke, F. M., Warland, D., van Steveninck, R. R. D. R., & Bialek, W. (1996) · Medical Entomology and Zoology · Cited by 2,844
Phase relationship between hippocampal place units and the EEG theta rhythm
O'Keefe, J. M., & Recce, M. L. (1993) · Hippocampus · doi:10.1002/hipo.450030307 · Cited by 2,643
Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Pouille, F., & Scanziani, M. (2001) · Science · doi:10.1126/science.1060342 · Cited by 1,097
Self-citationMegı́as, M., Emri, Z., Freund, T. F., & Gulyás, A. I. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00496-6 · Cited by 950
Somogyi, P., Tamás, G., Luján, R., & Buhl, E. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00061-1 · Cited by 876
Activity-Dependent Action Potential Invasion and Calcium Influx into Hippocampal CA1 Dendrites
Spruston, N., Schiller, Y., Stuart, G. J., & Sakmann, B. J. (1995) · Science · doi:10.1126/science.7716524 · Cited by 839
Stuart, G. J., Dodt, H., & Sakmann, B. J. (1993) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00374949 · Cited by 800
Two dynamically distinct inhibitory networks in layer 4 of the neocortex
Beierlein, M., Gibson, J. R., & Connors, B. W. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00283.2003 · Cited by 591
Feed‐forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro
Alger, B. E., & Nicoll, R. A. (1982) · The Journal of Physiology · doi:10.1113/jphysiol.1982.sp014255 · Cited by 528
ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: I. SEQUENTIAL INVASION AND SYNAPTIC ORGANIZATION
Kandel, E. R., Spencer, W. A., & Brinley, F. J. (1961) · Journal of Neurophysiology · doi:10.1152/jn.1961.24.3.225 · Cited by 482
Gulyás, A. I., Megı́as, M., Emri, Z., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-22-10082.1999 · Cited by 476
Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse
Geiger, J. R. P., Lübke, J., Roth, A., Frotscher, M., & Jonas, P. (1997) · Neuron · doi:10.1016/s0896-6273(00)80339-6 · Cited by 407
Shigemoto, R., Kulik, A., Roberts, J. D. B., Ohishi, H., Nusser, Z., Kaneko, T., & Somogyi, P. (1996) · Nature · doi:10.1038/381523a0 · Cited by 400
Spruston, N., Jaffe, D. B., Williams, S. H., & Johnston, D. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.2.781 · Cited by 362
Physiological evidence for two distinct GABAA responses in rat hippocampus
Pearce, R. A. (1993) · Neuron · doi:10.1016/0896-6273(93)90310-n · Cited by 307
Electrophysiology of Hippocampal Neurons
Schwartzkroin, P. A., & Mueller, A. L. (1987) · Cerebral cortex · doi:10.1007/978-1-4615-6616-8_8 · Cited by 299
Andersen, P. N., Eccles, J. C., & Løyning, Y. (1963) · Nature · doi:10.1038/198540a0 · Cited by 273
Differential Mechanisms of Transmission at Three Types of Mossy Fiber Synapse
Toth, K., Suares, G., Lawrence, J. J., Philips-Tansey, E., & McBain, C. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-22-08279.2000 · Cited by 262
EPSP Amplification and the Precision of Spike Timing in Hippocampal Neurons
Fricker, D., & Miles, R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00133-1 · Cited by 254
Ali, A. B., & Thomson, A. M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.185bu.x · Cited by 202
Maccaferri, G., & McBain, C. J. (1995) · Neuron · doi:10.1016/0896-6273(95)90071-3 · Cited by 182
The Mechanism of the Nervous System
Hill, A. V. (1929) · Nature · doi:10.1038/123009a0 · Cited by 182
Ali, A. B., Deuchars, J., Pawelzik, H., & Thomson, A. M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.201bu.x · Cited by 181
Target cell-specific modulation of transmitter release at terminals from a single axon
Scanziani, M., Gähwiler, B. H., & Charpak, S. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.12004 · Cited by 167
Self-citationThe basis of sensation : the action of the sense organs
Adrian, E. D. (1964) · Hafner eBooks · Cited by 166
Interactions between Distinct GABAA Circuits in Hippocampus
Banks, M. I., White, J. A., & Pearce, R. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)80907-1 · Cited by 134
Losonczy, A., Zhang, L., Shigemoto, R., Somogyi, P., & Nusser, Z. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.020024 · Cited by 133
Benzamide-Type AMPA Receptor Modulators Form Two Subfamilies with Distinct Modes of Action
Arai, A., Xia, Y., Rogers, G. A., LYNCH, G. S., & Kessler, M. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.040360 · Cited by 113
Conductance changes and inhibitory actions of hippocampal recurrent IPSPs
Dingledine, R. J., & Langmoen, I. A. (1980) · Brain Research · doi:10.1016/0006-8993(80)91068-9 · Cited by 102
Hampson, R. E., Byrd, D. R., Konstantopoulos, J. K., Bunn, T., & Deadwyler, S. A. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:3 · Cited by 82
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Millisecond-timescale, genetically targeted optical control of neural activity
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., & Deisseroth, K. A. (2005) · Nature Neuroscience · doi:10.1038/nn1525 · Cited by 5,015
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050
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
Pyramidal neurons: dendritic structure and synaptic integration
Spruston, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2286 · Cited by 1,688
Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., & Scanziani, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3446 · Cited by 1,353
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Metadata
- Authors
- Pouille, F., & Scanziani, M.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Scanziani, Massimo
- ORCID
- Scanziani, Massimo
- Venue
- Nature
- Published
- 2004-05-30
- Volume
- 429
- Issue
- 6993
- Pages
- 717-723
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2047403459
- Cited by
- 434
- References
- 33
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 13 · 2023: 24 · 2022: 20 · 2021: 28 · 2020: 14 · 2019: 24 · 2018: 22 · 2017: 12 · 2016: 12 · 2015: 17 · 2014: 23 · 2013: 17 · 2012: 25
- FWCI
- 8.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Foundation for the National Institutes of Health
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- 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
- recurrent inhibition, hippocampus, pyramidal neurons, dendritic inhibition, inhibitory interneurons, excitatory synapses, synaptic plasticity, rat hippocampal slices
- MeSH terms
- Action Potentials, Animals, Dendrites, Electrophysiology, Hippocampus, Interneurons, Rats, Wistar, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques
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