The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Open accessAbstract
In the cerebral cortex, diverse types of neurons form intricate circuits and cooperate in time for the processing and storage of information. Recent advances reveal a spatiotemporal division of labor in cortical circuits, as exemplified in the CA1 hippocampal area. In particular, distinct GABAergic (gamma-aminobutyric acid-releasing) cell types subdivide the surface of pyramidal cells and act in discrete time windows, either on the same or on different subcellular compartments. They also interact with glutamatergic pyramidal cell inputs in a domain-specific manner and support synaptic temporal dynamics, network oscillations, selection of cell assemblies, and the implementation of brain states. The spatiotemporal specializations in cortical circuits reveal that cellular diversity and temporal dynamics coemerged during evolution, providing a basis for cognitive behavior.
Overview
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
Verification
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In the hippocampal CA1 region, Somogyi and his colleagues have been successful at implementing an interneuron classification that starts with morphological features, i.e. somatic location and dendritic and axonal innervation fields”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Klausberger and Somogyi, 2008
Experimental — accuracy not yet measuredIn the citing paper
“Over 20 different types of inhibitory neuron have been described in the neocortex and hippocampus with that level of resolution”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Klausberger and Somogyi, 2008
In the citing paper
“The sharp resonance in the theta-range detected in individual RCs and its potential spread through gap junctions to a rosehip network could phase-selectively interact with long range inputs similarly to mechanisms suggested for example in oscillation dependent memory consolidation30,46.”
From Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type (2018) · cites this paper as [46]
In the citing paper
“The spectacular diversity of GABAergic neurons enables an elaborate division of labour in deploying a rich repertoire of inhibitory control mechanisms to shape highly nuanced spatiotemporal dynamics of cortical circuit computation6,7.”
From The diversity of GABAergic neurons and neural communication elements (2019) · cites this paper as [6]
In the citing paper
“Indeed, it is now recognized that anatomical specialization among cortical interneuron subtypes allows for a division of labor that affords inhibitory networks exquisite spatiotemporal control over principal cell activity, rather than providing generalized inhibition (586, 1036).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [586]
In the citing paper
“The diversity of interneuron subtypes leads to sophisticated control of synaptic integration along the somatodendritic axis of PCs, as they differentially target distinct subcompartments (see sect. VIID) (586).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [586]
In the citing paper
“Moreover, the observations that specific interneuron subtypes are necessary for the generation of coherent cortical and hippocampal oscillations (333, 1200) and that interneuron subtypes fire at specific phases of the oscillatory cycle (586) suggest that synchronization among interneurons is critical for cortical circuit function (151).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [586]
In the citing paper
“In rodents, hippocampal theta is a 5–10 Hz oscillation in the local field potential (LFP) and neuronal firing probabilities (Soltesz and Deschênes, 1993; Lee et al., 1994; Ylinen et al., 1995; Klausberger and Somogyi, 2008; Varga et al., 2012, 2014), occurring during locomotion and in REM sleep (Buzsáki, 2002).”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Klausberger and Somogyi, 2008
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Invariant visual representation by single neurons in the human brain
Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C., & Fried, I. (2005) · Nature · doi:10.1038/nature03687 · Cited by 1,988
Reverse replay of behavioural sequences in hippocampal place cells during the awake state
Foster, D. J., & Wilson, M. A. (2006) · Nature · doi:10.1038/nature04587 · Cited by 1,727
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
Self-citationKatona, I., Sperlágh, B., Sı́k, A., Käfalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04544.1999 · Cited by 1,218
Forward and reverse hippocampal place-cell sequences during ripples
Diba, K., & Buzsáki, G. (2007) · Nature Neuroscience · doi:10.1038/nn1961 · Cited by 1,205
Ylinen, A., Bragin, A., Nadasdy, Z., Jando, G., Szabo, I., Sik, A., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00030.1995 · Cited by 1,092
On the Origin of Interictal Activity in Human Temporal Lobe Epilepsy in Vitro
Cohen, I., Navarro, V., Clémenceau, S., Baulac, M., & Miles, R. (2002) · Science · doi:10.1126/science.1076510 · Cited by 1,001
Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat
Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A., & Buzsáki, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00274.1999 · Cited by 966
Differences between somatic and dendritic inhibition in the hippocampus
Miles, R., Tóth, K., Gulyás, A. I., Hájos, N., & Freund, T. F. (1996) · Neuron · doi:10.1016/s0896-6273(00)80101-4 · Cited by 942
Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits
Szabadics, J., Varga, C., Molnár, G., Oláh, S., Barzó, P., & Tamás, G. (2006) · Science · doi:10.1126/science.1121325 · Cited by 598
Hefft, S., & Jonas, P. (2005) · Nature Neuroscience · doi:10.1038/nn1542 · Cited by 583
Fuchs, E. C., Zivkovic, A. R., Cunningham, M. O., Middleton, S., LeBeau, F. E. N., Bannerman, D. M., Rozov, A., Whittington, M. A., Traub, R. D., Rawlins, J. N. P., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.031 · Cited by 532
Molecular taxonomy of major neuronal classes in the adult mouse forebrain
Sugino, K., Hempel, C. M., Miller, M. N., Hattox, A. M., Shapiro, P., Wu, C., Huang, Z. J., & Nelson, S. B. (2006) · Nature Neuroscience · doi:10.1038/nn1618 · Cited by 521
Gulyás, A. I., Hájos, N., & Freund, T. F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03397.1996 · Cited by 512
Klausberger, T., Marton, L. F., O'Neill, J., Huck, J. H. J., Dalezios, Y., Fuentealba, P., Suen, W. Y., Papp, E., Kaneko, T., Watanabe, M., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3269-05.2005 · Cited by 469
Self-citationBehavioural report of single neuron stimulation in somatosensory cortex
Houweling, A. R., & Brecht, M. (2007) · Nature · doi:10.1038/nature06447 · Cited by 458
Routing of spike series by dynamic circuits in the hippocampus
Pouille, F., & Scanziani, M. (2004) · Nature · doi:10.1038/nature02615 · Cited by 434
Soltész, I., & Deschênes, M. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.97 · Cited by 410
Klausberger, T., Márton, L. F., Baude, A., Roberts, J. D. B., Magill, P. J., & Somogyi, P. (2004) · Nature Neuroscience · doi:10.1038/nn1159 · Cited by 393
Self-citationYlinen, A., Soltész, I., Bragin, A., Penttonen, M., Attila Gabor, S. I. K., & Buzsáki, G. (1995) · Hippocampus · doi:10.1002/hipo.450050110 · Cited by 381
Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus
Jinno, S., Klausberger, T., Marton, L. F., Dalezios, Y., Roberts, J. D. B., Fuentealba, P., Bushong, E. A., Henze, D., Buzsáki, G., & Somogyi, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1847-07.2007 · Cited by 369
Self-citationIdentified 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
Hájos, N., Pálhalmi, J., Mann, E. O., Németh, B., Paulsen, O., & Freund, T. F. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2113-04.2004 · Cited by 321
Acsády, L., Görcs, T. J., & Freund, T. F. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00609-5 · Cited by 310
Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo
Penttonen, M., Kamondi, A., Acsády, L., & Buzsáki, G. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00096.x · Cited by 306
Cell Type-Specific Tuning of Hippocampal Interneuron Firing during Gamma Oscillations In Vivo
Tukker, J. J., Fuentealba, P., Hartwich, K., Somogyi, P., & Klausberger, T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1685-07.2007 · Cited by 304
Self-citationTóth, K., Borhegyi, Z., & Freund, T. F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03712.1993 · Cited by 301
Lien, C., & Jónás, P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02058.2003 · Cited by 285
Somogyi, P., Nunzi, M. G., Gorio, A., & Smith, A. D. (1983) · Brain Research · doi:10.1016/0006-8993(83)91076-4 · Cited by 273
Self-citationHippocampal place cell assemblies are speed-controlled oscillators
Geisler, C. E., Robbe, D., Zugaro, M., Sirota, A., & Buzsáki, G. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610121104 · Cited by 273
Pawelzik, H., Hughes, D. I., & Thomson, A. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10118 · Cited by 262
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
Fuentealba, P., Begum, R., Capogna, M., Jinno, S., Márton, L. F., Csicsvari, J., Thomson, A., Somogyi, P., & Klausberger, T. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.034 · Cited by 255
Self-citationGloveli, T., Dugladze, T., Saha, S., Monyer, H., Heinemann, U., Traub, R. D., Whittington, M. A., & Buhl, E. H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.073007 · Cited by 238
Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells
Glickfeld, L. L., & Scanziani, M. (2006) · Nature Neuroscience · doi:10.1038/nn1688 · Cited by 222
Demonstration of long‐range GABAergic connections distributed throughout the mouse neocortex
Tomioka, R., Okamoto, K., Furuta, T., Fujiyama, F., Iwasato, T., Yanagawa, Y., Obata, K., Kaneko, T., & Tamamaki, N. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03989.x · Cited by 218
Lund, J. S., & Lewis, D. A. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903280209 · Cited by 208
Phase Segregation of Medial Septal GABAergic Neurons during Hippocampal Theta Activity
Borhegyi, Z., Varga, V., Szilágyi, N., Fabó, D., & Freund, T. F. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1413-04.2004 · Cited by 207
Inhibitory CA1-CA3-Hilar Region Feedback in the Hippocampus
Attila Gabor, S. I. K., Ylinen, A., Penttonen, M., & Buzsáki, G. (1994) · Science · doi:10.1126/science.8085161 · Cited by 203
Ali, A. B., & Thomson, A. M. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.185bu.x · Cited by 202
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
Szabadics, J., Tamás, G., & Soltesz, I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707204104 · Cited by 170
Epileptogenic Actions of GABA and Fast Oscillations in the Developing Hippocampus
Khalilov, I., Quyen, M. L. V., GOZLAN, H., & Ben‐Ari, Y. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.026 · Cited by 160
Kocsis, B., Varga, V., Dahan, L., & Attila Gabor, S. I. K. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508360103 · Cited by 158
Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat
Cenquizca, L. A., & Swanson, L. W. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20985 · Cited by 157
Stanić, D., Brumovsky, P. R., Fetissov, S. O., Shuster, S. J., Herzog, H., & Hökfelt, T. G. M. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21046 · Cited by 137
Hájos, N., & Mody, I. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08427.1997 · Cited by 131
Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus
Jarsky, T., Mady, R., Kennedy, B., & Spruston, N. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21564 · Cited by 129
Maurer, A. P., Cowen, S. L., Burke, S. N., Barnes, C. A., & McNaughton, B. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2882-06.2006 · Cited by 129
Cell type–specific gating of perisomatic inhibition by cholecystokinin
Földy, C., Lee, S. Y., Szabadics, J., Neu, A. D., & Soltész, I. (2007) · Nature Neuroscience · doi:10.1038/nn1952 · Cited by 121
Marshall, L., Henze, D. A., Hirase, H., Leinekugel, X., Dragoi, G., & Buzsáki, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-j0001.2002 · Cited by 118
Spatial selectivity and theta phase precession in CA1 interneurons
Ego‐Stengel, V., & Wilson, M. A. (2006) · Hippocampus · doi:10.1002/hipo.20253 · Cited by 113
Lawrence, J. J., Statland, J. M., Grinspan, Z. M., & McBain, C. J. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.100875 · Cited by 109
Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses
Biró, Á. A., Holderith, N. B., & Nusser, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3688-04.2005 · Cited by 102
Discrete Place Fields of Hippocampal Formation Interneurons
Wilent, W. B., & Nitz, D. A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.01200.2006 · Cited by 82
Traub, R. D., Pais, I., Bibbig, A., LeBeau, F. E. N., Buhl, E. H., Garner, H., Monyer, H., & Whittington, M. A. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00069.2005 · Cited by 82
Silberberg, G., Wu, C., & Markram, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.060962 · Cited by 77
Recognition Memory Correlates of Hippocampal Theta Cells
Wiebe, S. P., & Staubli, U. V. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-03955.2001 · Cited by 74
Papp, E., Hájos, N., Acsády, L., & Freund, T. F. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00455-2 · Cited by 56
Regional specificity of chandelier neuron axon terminal alterations in schizophrenia
Konopaske, G. T., Sweet, R. A., Wu, Q., Sampson, A. R., & Lewis, D. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.070 · Cited by 50
Ganter, P., Szűcs, P., Paulsen, O., & Somogyi, P. (2004) · Hippocampus · doi:10.1002/hipo.10170 · Cited by 47
Self-citationInterneurons targeting similar layers receive synaptic inputs with similar kinetics
Cossart, R., Petanjek, Z., Dumitriu, D., Hirsch, J. C., Ben‐Ari, Y., Esclapez, M., & Bernard, C. (2006) · Hippocampus · doi:10.1002/hipo.20169 · Cited by 42
Tamás, G., Szabadics, J., Lörincz, A., & Somogyi, P. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03719.x · Cited by 40
Self-citationHardie, J. B., & Pearce, R. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0547-06.2006 · Cited by 40
Research works printed but not linked: 4
- 10.1016/0014-4886(76)90055-8 · DOI · Paper page
- J. Szabadics, G. Tamas, I. Soltesz, Proc. Natl. Acad. Sci. U.S.A.102, 14831 (2007).
- 10.1126/science.1114037 · DOI
- We thank the colleagues whose work laid the foundations for this review but could not be cited because of space restrictions. We also thank M. Capogna N. Hajos I. Katona and Z. Nusser for commenting on an earlier manuscript.
Cited by
Sorted by citations
The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes
Buzsáki, G., Anastassiou, C. A., & Koch, C. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3241 · Cited by 4,225
Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq
Zeisel, A., Muñoz-Manchado, A. B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. (2015) · Science · doi:10.1126/science.aaa1934 · Cited by 3,124
Mechanisms of Gamma Oscillations
Buzsáki, G., & Wang, X.-J. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150444 · Cited by 2,796
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
“, somatic location and dendritic and axonal innervation fields (Klausberger and Somogyi, 2008; Somogyi and Klausberger, 2005).”
A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828
Metadata
- Authors
- Klausberger, T., & Somogyi, P.
- Affiliations
- University of Oxford (GB)
- MRC Anatomical Neuropharmacology Unit, Oxford University, Oxford OX1 3TH, UK.
- Corresponding author
- Klausberger, Thomas
- ORCID
- Klausberger, Thomas
- Venue
- Science
- Published
- 2008-07-04
- Volume
- 321
- Issue
- 5885
- Pages
- 53-57
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4487503
- OpenAlex
- W2008027377
- Cited by
- 2,050
- References
- 64
- Citations by year
- 2026: 64 · 2025: 110 · 2024: 86 · 2023: 99 · 2022: 116 · 2021: 114 · 2020: 120 · 2019: 126 · 2018: 129 · 2017: 129 · 2016: 127 · 2015: 133 · 2014: 143 · 2013: 131 · 2012: 116
- FWCI
- 8.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- hippocampal CA1, neuronal heterogeneity, GABAergic interneurons, pyramidal neurons, network oscillations, brain states, cortical circuits
- MeSH terms
- Animals, Axons, Cognition, Dendrites, Biological Evolution, gamma-Aminobutyric Acid, Hippocampus, Humans, Interneurons, Nerve Net, Neural Pathways, Neurons, Synapses, Pyramidal Cells
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
