The DOI matches its Crossref record; 62 of the 62 references it cites were found in a registry or an index.
Hippocampal CA1 interneurons: an in vivo intracellular labeling study
Open accessAbstract
Fast spiking interneurons in the CA1 area of the dorsal hippocampus were recorded from and filled with biocytin in anesthetized rats. The full extent of their dendrites and axonal arborizations as well as their calcium binding protein content were examined. Based on the spatial extent of axon collaterals, local circuit cells (basket and O- LM neurons) and long-range cells (bistratified, trilaminar, and backprojection neurons) could be distinguished. Basket cells were immunoreactive for parvalbumin and their axon collaterals were confined to the pyramidal layer. A single basket cell contacted more than 1500 pyramidal neurons and 60 other parvalbumin-positive interneurons. Commissural stimulation directly discharged basket cells, followed by an early and late IPSPs, indicating interneuronal inhibition of basket cells. The dendrites of another local circuit neuron (O-LM) were confined to stratum oriens and it had a small but high-density axonal terminal field in stratum lacunosum-moleculare. The fastest firing cell of all interneurons was a calbindin-immunoreactive bistratified neuron with axonal targets in stratum oriens and radiatum. Two neurons with their cell bodies in the alveus innervated the CA3 region (backprojection cells), in addition to rich axon collaterals in the CA1 region. The trilaminar interneuron had axon collaterals in strata radiatum, oriens and pyramidale with its dendrites confined to stratum oriens. Commissural stimulation evoked an early EPSP-IPSP-late depolarizing potential sequence in this cell. All interneurons formed symmetric synapses with their targets at the electron microscopic level. These findings indicate that interneurons with distinct axonal targets have differential functions in shaping the physiological patterns of the CA1 network.
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In the citing paper
“In addition, PV-INs connect to many principal neurons [74,75,87,88].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [88]
In the citing paper
“PVBCs predominantly display mostly aspiny, pyramidal-shaped, or bitufted dendritic trees spanning from the alveus to s.l.m., positioning them to receive input from all excitatory afferent projections innervating the hippocampal CA1 region (FIGURE 2C) (135, 768, 1014).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1014]
In the citing paper
“O-LMs are named for their striking anatomy with soma and dendrites restricted to s.o. and the alveus while the axon ascends with minimal branching through s.p. and s.r. to densely collateralize within s.l.m. (FIGURE 3C) (352, 719, 721, 768, 1014).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1014]
In the citing paper
“After emerging from the soma or a proximal dendrite, ~7% of an O-LM axon remains in s.o. while greater than 90% is targeted to s.l.m. (1014).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1014]
In the citing paper
“Individual O-LMs are estimated to contact around 1,450 pyramidal cells with an average of 10 synapses per connection (102, 1014).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [1014]
Citations
Cites
Llinás, R. R. (1988) · Science · doi:10.1126/science.3059497 · Cited by 2,285
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180
Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat
Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00047.1995 · Cited by 1,527
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
Self-citationBaude, A., Nusser, Z., Roberts, J. D. B., Mulvihill, E., Jeffrey Mcllhinney, R. A., & Somogyi, P. (1993) · Neuron · doi:10.1016/0896-6273(93)90086-7 · Cited by 927
Neuronal Networks of the Hippocampus
Traub, R. D., & Miles, R. (1991) · doi:10.1017/cbo9780511895401 · Cited by 802
The hippocampal CA3 network: An in vivo intracellular labeling study
Li, X. ‐., Somogyi, P., Ylinen, A., & Buzsáki, G. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903390204 · Cited by 751
Self-citationParvalbumin in Most γ-Aminobutyric Acid-Containing Neurons of the Rat Cerebral Cortex
Celio, M. R. (1986) · Science · doi:10.1126/science.3945815 · Cited by 740
Sloviter, R. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902800203 · Cited by 686
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
Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin
Kawaguchi, Y., Katsumaru, H., Kosaka, T., Heizmann, C. W., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90921-8 · Cited by 485
Anatomic organization and physiology of the limbic cortex
Lopes, F. H. D. S., Witter, M. P., Boeijinga, P. H., & Lohman, A. H. M. (1990) · Physiological Reviews · doi:10.1152/physrev.1990.70.2.453 · Cited by 471
Soltész, I., & Deschênes, M. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.97 · Cited by 410
Sloviter, R. S., & Nilaver, G. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902560105 · Cited by 390
Lacaille, J., Mueller, A., Kunkel, D., & Schwartzkroin, P. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01979.1987 · Cited by 388
Hippocampal pyramidal cells excite inhibitory neurons through a single release site
Gulyás, A. I., Miles, R., Sik, A., Tóth, K., Tamamaki, N., & Freund, T. F. (1993) · Nature · doi:10.1038/366683a0 · Cited by 384
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
Self-citationSerotonergic control of the hippocampus via local inhibitory interneurons.
Freund, T. F., Gulyás, A. I., Acsády, L., Görcs, T. J., & Tóth, K. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.21.8501 · Cited by 363
Physiological and morphological identification of a nonpyramidal hippocampal cell type
Schwartzkroin, P. A., & Mathers, L. H. (1978) · Brain Research · doi:10.1016/0006-8993(78)90991-5 · Cited by 330
A branching dendritic model of a rodent CA3 pyramidal neurone.
Traub, R. D., Jefferys, J. G. R., Miles, R., Whittington, M. A., & Tóth, K. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020420 · Cited by 322
Thompson, S. M., & Gähwiler, B. H. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.3.501 · Cited by 319
McBain, C., DiChiara, T., & Kauer, J. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-07-04433.1994 · Cited by 303
Excitatory Synaptic Responses Mediated by GABA A Receptors in the Hippocampus
Michelson, H. B., & Wong, R. K. S. (1991) · Science · doi:10.1126/science.1654594 · Cited by 279
Andersen, P. N., Eccles, J. C., & Løyning, Y. (1963) · Nature · doi:10.1038/198540a0 · Cited by 273
Somogyi, P., Nunzi, M. G., Gorio, A., & Smith, A. D. (1983) · Brain Research · doi:10.1016/0006-8993(83)91076-4 · Cited by 273
Lacaille, J., & Schwartzkroin, P. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-04-01400.1988 · Cited by 272
Lacaille, J., & Schwartzkroin, P. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-04-01411.1988 · Cited by 270
Tóth, K., & Freund, T. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90357-8 · Cited by 257
Otis, T. S., De Koninck, Y., & Mody, I. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.16.7698 · Cited by 257
Gulyás, A. I., Miettinen, R. A., Jacobowitz, D. M., & Freund, T. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90334-x · Cited by 247
Direct afferent excitation and long-term potentiation of hippocampal interneurons.
Buzsáki, G., & Eidelberg, E. (1982) · Journal of Neurophysiology · doi:10.1152/jn.1982.48.3.597 · Cited by 246
Scharfman, H. E., Kunkel, D. D., & Schwartzkroin, P. A. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90100-i · Cited by 238
Gulyás, A. I., Mlles, R., Hájos, N., & Freund, T. F. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00240.x · Cited by 226
McBain, C. J., & Dingledine, R. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019560 · Cited by 221
Kosaka, T., Wu, J., & Benoit, R. (1988) · Experimental Brain Research · doi:10.1007/bf00247498 · Cited by 218
Miettinen, R. A., Gulyás, A. I., Baimbridge, K. G., Jacobowitz, D. M., & Freund, T. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90335-y · Cited by 210
Two calcium-binding proteins mark many chick sensory neurons
ROGERS, J. H. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90434-x · Cited by 191
Alonso, A., & Köhler, C. (1982) · Neuroscience Letters · doi:10.1016/0304-3940(82)90021-0 · Cited by 182 · cited 1×
“Recent works suggest, however, that there are several groups of hippocampal inhibitory cells with different circuit, physiological and biochemical properties, and hypothesized functions (Struble et al., 1978; Alonso and Kohler, 1982; Somogyi et al., 1983, 1984; Misgeld and Frotscher, 1986; Ribak et al., 1986; Michelso…”
BackgroundGulyás, A. I., Tóth, K., Dános, P., & Freund, T. F. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903120305 · Cited by 175
Intrinsic membrane potential oscillations in hippocampal neurons in vitro
Leung, L.-W. S., & Yim, C. Y. (1991) · Brain Research · doi:10.1016/0006-8993(91)90834-i · Cited by 172
Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions.
Faber, D. S., Young, W., Legendre, P., & Korn, H. (1992) · Science · doi:10.1126/science.1279813 · Cited by 168
Lacaille, J., & Williams, S. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90431-3 · Cited by 160
Tamamaki, N., Abe, K., & Nojyo, Y. (1988) · Brain Research · doi:10.1016/0006-8993(88)90030-3 · Cited by 156
Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurones.
Sah, P., Hestrin, S., & Nicoll, R. A. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018310 · Cited by 156
Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus
Schwartzkroin, P. A., & Kunkel, D. D. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902320206 · Cited by 156
Li, X.-G., Somogyi, P., Tepper, J. M., & Buzs�ki, G. (1992) · Experimental Brain Research · doi:10.1007/bf00230934 · Cited by 149
Neuronal networks of the hippocampus
(1992) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(92)90749-g · Cited by 147
Interneurons and inhibition in the dentate gyrus of the rat in vivo
Buckmaster, P. S., & Schwartzkroin, P. A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00774.1995 · Cited by 141
Postsynaptic-gabaergic inhibition of non-pyramidal neurons in the guinea-pig hippocampus
Misgeld, U., & Frotscher, M. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90015-1 · Cited by 140
Attila Gabor, S. I. K., Tamamaki, N., & Freund, T. F. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00239.x · Cited by 134
Self-citationUltrastructure of stratum lacunosum moleculare interneurons of hippocampal CA1 region
Kunkel, D. D., Lacaille, J., & Schwartzkroin, P. A. (1988) · Synapse · doi:10.1002/syn.890020405 · Cited by 133
A GABAergic inhibitory component within the hippocampal commissural pathway
Ribak, C., Seress, L., Peterson, G., Seroogy, K. B., Jh, F., & Schmued, L. C. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-12-03492.1986 · Cited by 126
Lacaille, J. C. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.5.1441 · Cited by 112
Tamamaki, N., & Nojyo, Y. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902910403 · Cited by 102
Fraser, D., & MacVicar, B. A. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-09-02812.1991 · Cited by 102
Kawaguchi, Y., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90700-1 · Cited by 99
Anatomical evidence for interlamellar inhibition in the fascia dentata
Struble, R. G., Desmond, N. L., & Levy, W. B. (1978) · Brain Research · doi:10.1016/0006-8993(78)91113-7 · Cited by 88
Fast-spiking non-pyramidal cells in the hippocampal CA3 region, dentate gyrus and subiculum of rats
Kawaguchi, Y., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90518-x · Cited by 77
Hippocampal inhibitory neuron activity in the elevated potassium model of epilepsy
McBain, C. J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.2.2853 · Cited by 76
Crossing fiber arrays in the rat hippocampus as demonstrated by three‐dimensional reconstruction
Tamamaki, N., & Nojyo, Y. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903030309 · Cited by 58
Hippocampal inhibitory neuron activity in the elevated potassium model of epilepsy
McBain, C. J. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.72.6.2853 · Cited by 52
Nicoll, R. A. (1994) · Nature · doi:10.1038/368808a0 · Cited by 13
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Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,478
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Metadata
- Authors
- Sik, A., Penttonen, M., Ylinen, A., & Buzsaki, G.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1995-10-01
- Volume
- 15
- Issue
- 10
- Pages
- 6651-6665
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6577981
- OpenAlex
- W1568625389
- Cited by
- 669
- References
- 62
- Citations by year
- 2026: 3 · 2025: 18 · 2024: 10 · 2023: 12 · 2022: 15 · 2021: 11 · 2020: 26 · 2019: 26 · 2018: 23 · 2017: 27 · 2016: 29 · 2015: 18 · 2014: 27 · 2013: 14 · 2012: 23
- FWCI
- 12.66
- 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
- U.S. Public Health Service (34994)
- 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, fast-spiking interneurons, basket cells, parvalbumin, calbindin, axon collaterals, dendritic branching, inhibitory postsynaptic potentials, local circuit neurons, synaptic ultrastructure
- MeSH terms
- Animals, Axons, Electrophysiology, Hippocampus, Interneurons, Intracellular Membranes, Lysine, Microscopy, Electron, Nerve Tissue Proteins, Parvalbumins, Rats, Sprague-Dawley, Rats, Calbindins, S100 Calcium Binding Protein G
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