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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
PV-INs connect to many principal neurons.
“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]
PVBCs predominantly display mostly aspiny, pyramidal-shaped, or bitufted dendritic trees spanning from the alveus to stratum lacunosum moleculare, positioning them to receive input from all excitatory afferent projections innervating the hippocampal CA1 region.
“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]
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.
“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]
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.
“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]
Individual O-LMs are estimated to contact around 1,450 pyramidal cells with an average of 10 synapses per connection.
“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]
Cites
Llinás, R. R. (1988) · Science · doi:10.1126/science.3059497 · Cited by 2,285 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Neuronal Networks of the Hippocampus
Traub, R. D., & Miles, R. (1991) · doi:10.1017/cbo9780511895401 · Cited by 802 · see citing works
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 · see citing works
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 · see citing works
Sloviter, R. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902800203 · Cited by 686 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Soltész, I., & Deschênes, M. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.97 · Cited by 410 · see citing works
Sloviter, R. S., & Nilaver, G. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902560105 · Cited by 392 · see citing works
Lacaille, J., Mueller, A., Kunkel, D., & Schwartzkroin, P. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-07-01979.1987 · Cited by 388 · see citing works
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 · see citing works
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 383 · see citing works
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 360 · see citing works
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 · see citing works
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 · see citing works
Thompson, S. M., & Gähwiler, B. H. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.3.501 · Cited by 319 · see citing works
McBain, C., DiChiara, T., & Kauer, J. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-07-04433.1994 · Cited by 303 · see citing works
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 · see citing works
Andersen, P. N., Eccles, J. C., & Løyning, Y. (1963) · Nature · doi:10.1038/198540a0 · Cited by 277 · see citing works
Somogyi, P., Nunzi, M. G., Gorio, A., & Smith, A. D. (1983) · Brain Research · doi:10.1016/0006-8993(83)91076-4 · Cited by 273 · see citing works
Lacaille, J., & Schwartzkroin, P. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-04-01400.1988 · Cited by 272 · see citing works
Lacaille, J., & Schwartzkroin, P. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-04-01411.1988 · Cited by 270 · see citing works
Tóth, K., & Freund, T. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90357-8 · Cited by 260 · see citing works
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 · see citing works
Gulyás, A. I., Miettinen, R. A., Jacobowitz, D. M., & Freund, T. F. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90334-x · Cited by 252 · see citing works
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 · see citing works
Scharfman, H. E., Kunkel, D. D., & Schwartzkroin, P. A. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90100-i · Cited by 239 · see citing works
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 · see citing works
McBain, C. J., & Dingledine, R. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019560 · Cited by 221 · see citing works
Kosaka, T., Wu, J., & Benoit, R. (1988) · Experimental Brain Research · doi:10.1007/bf00247498 · Cited by 218 · see citing works
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 215 · see citing works
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 · see citing works
Alonso, A., & Köhler, C. (1982) · Neuroscience Letters · doi:10.1016/0304-3940(82)90021-0 · Cited by 182 · see citing works
Gulyás, A. I., Tóth, K., Dános, P., & Freund, T. F. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903120305 · Cited by 180 · see citing works
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 · see citing works
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 · see citing works
Lacaille, J., & Williams, S. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90431-3 · Cited by 160 · see citing works
Tamamaki, N., Abe, K., & Nojyo, Y. (1988) · Brain Research · doi:10.1016/0006-8993(88)90030-3 · Cited by 156 · see citing works
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 · see citing works
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 · see citing works
Li, X.-G., Somogyi, P., Tepper, J. M., & Buzs�ki, G. (1992) · Experimental Brain Research · doi:10.1007/bf00230934 · Cited by 149 · see citing works
Neuronal networks of the hippocampus
(1992) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(92)90749-g · Cited by 147 · see citing works
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 · see citing works
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 · see citing works
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 135 · see citing works
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 · see citing works
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 · see citing works
Lacaille, J. C. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.5.1441 · Cited by 112 · see citing works
Tamamaki, N., & Nojyo, Y. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902910403 · Cited by 103 · see citing works
Fraser, D., & MacVicar, B. A. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-09-02812.1991 · Cited by 102 · see citing works
Kawaguchi, Y., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90700-1 · Cited by 99 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Nicoll, R. A. (1994) · Nature · doi:10.1038/368808a0 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Synchronization in complex networks
Arenas, A., Díaz-Guilera, A., Kurths, J., Moreno, Y., & Zhou, C. (2008) · Physics Reports · doi:10.1016/j.physrep.2008.09.002 · Cited by 3,713 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
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 · see citing works
Bassett, D. S., & Bullmore, E. (2006) · The Neuroscientist · doi:10.1177/1073858406293182 · Cited by 2,600 · see citing works
Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks
Bartos, M., Vida, I., & Jonas, P. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2044 · Cited by 2,070 · see citing works
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition
Wang, X.-J. (2010) · Physiological Reviews · doi:10.1152/physrev.00035.2008 · Cited by 1,939 · see citing works
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 · see citing works
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model
Wang, X., & Buzsáki, G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-20-06402.1996 · Cited by 1,571 · see citing works
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · see citing works
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 · see citing works
Self-citationHu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · see citing works
The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network
van Strien, N. M., Cappaert, N. L. M., & Witter, M. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2614 · Cited by 1,041 · see citing works
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 · see citing works
Inhibition-based rhythms: experimental and mathematical observations on network dynamics
Whittington, M. A., Traub, R. D., Kopell, N., Ermentrout, B., & Buhl, E. (2000) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(00)00173-2 · Cited by 953 · see citing works
Intracellular Features Predicted by Extracellular Recordings in the Hippocampus In Vivo
Henze, D. A., Borhegyi, Z., Csicsvari, J., Mamiya, A., Harris, K. D., & Buzsáki, G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.1.390 · Cited by 942 · see citing works
Defined types of cortical interneurone structure space and spike timing in the hippocampus
Somogyi, P., & Klausberger, T. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.078915 · Cited by 927 · see citing works
Barthó, P., Hirase, H., Monconduit, L., Zugaro, M. B., Harris, K. D., & Buzsáki, G. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01170.2003 · Cited by 888 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks
Buzsáki, G., & Chrobak, J. J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80012-3 · Cited by 878 · see citing works
Somogyi, P., Tamás, G., Luján, R., & Buhl, E. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00061-1 · Cited by 860 · see citing works
Farahani, F. V., Karwowski, W., & Lighthall, N. R. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00585 · Cited by 719 · see citing works
A mechanism for generation of long-range synchronous fast oscillations in the cortex
Traub, R. D., Whittington, M. A., Stanford, I. M., & Jefferys, J. G. R. (1996) · Nature · doi:10.1038/383621a0 · Cited by 701 · see citing works
Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo
Traub, R. D., Whittington, M. A., Colling, S. B., Buzsáki, G., & Jefferys, J. G. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021397 · Cited by 607 · see citing works
Reliability and State Dependence of Pyramidal Cell–Interneuron Synapses in the Hippocampus
Csicsvari, J., Hirase, H., Czurko, A., & Buzsáki, G. (1998) · Neuron · doi:10.1016/s0896-6273(00)80525-5 · Cited by 606 · see citing works
Gamma Oscillations in the Entorhinal Cortex of the Freely Behaving Rat
Chrobak, J. J., & Buzsáki, G. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00388.1998 · Cited by 590 · see citing works
Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition
Atallah, B. V., & Scanziani, M. (2009) · Neuron · doi:10.1016/j.neuron.2009.04.027 · Cited by 588 · see citing works
Chrobak, J. J., & Buzsáki, G. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-03056.1996 · Cited by 587 · see citing works
Presynaptic Specificity of Endocannabinoid Signaling in the Hippocampus
Wilson, R. I., Kunos, G., & Nicoll, R. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00372-5 · Cited by 543 · see citing works
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 · see citing works
Bartos, M., Vida, I., Frotscher, M., Meyer, A. H., Monyer, H., Geiger, J. R. P., & Jónás, P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192233099 · Cited by 529 · see citing works
Emerging principles of altered neural circuitry in schizophrenia
Benes, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00041-7 · Cited by 513 · see citing works
Gulyás, A. I., Hájos, N., & Freund, T. F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03397.1996 · Cited by 512 · see citing works
Maccaferri, G., & McBain, C. J. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021754 · Cited by 503 · see citing works
Oliva, A. A., Jiang, M., Lam, T., Smith, K. L., & Swann, J. W. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-09-03354.2000 · Cited by 498 · see citing works
Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons
Buzsáki, G., Geisler, C. E., Henze, D. A., & Wang, X. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.02.007 · Cited by 483 · see citing works
Korotkova, T., Fuchs, E. C., Ponomarenko, A., von Engelhardt, J., & Monyer, H. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.017 · Cited by 480 · see citing works
Buzsáki, G., Kai, K.-L., & Raichle, M. (2007) · Neuron · doi:10.1016/j.neuron.2007.11.008 · Cited by 56 · see citing works
Small-world human brain networks: Perspectives and challenges
Liao, X., Vasilakos, A. V., & Yong He, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.018 · Cited by 431 · see citing works
Transcranial Electric Stimulation Entrains Cortical Neuronal Populations in Rats
Irmak, S. O., Sirota, A., Belluscio, M., Anastassiou, C. A., Stark, E., Christof Koch, A., & Buzsáki, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5252-09.2010 · Cited by 414 · see citing works
Wulff, P., Ponomarenko, A. A., Bartos, M., Korotkova, T. M., Fuchs, E. C., Bähner, F., Both, M., Tort, A. B. L., Kopell, N. J., Wisden, W., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813176106 · Cited by 400 · see citing works
Nusser, Z., Sieghart, W., Benke, D., Fritschy, J., & Somogyi, P. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11939 · Cited by 386 · see citing works
Distal Initiation and Active Propagation of Action Potentials in Interneuron Dendrites
Martina, M., Vida, I., & Jonas, P. (2000) · Science · doi:10.1126/science.287.5451.295 · Cited by 375 · see citing works
Bezaire, M. J., & Soltesz, I. (2013) · Hippocampus · doi:10.1002/hipo.22141 · Cited by 373 · see citing works
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 · see citing works
Paradoxical Effects of External Modulation of Inhibitory Interneurons
Tsodyks, M. V., Skaggs, W. E., B, T. J. S. A., & McNaughton, B. L. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-11-04382.1997 · Cited by 364 · see citing works
Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro
Traub, R. D., Bibbig, A., LeBeau, F. E. N., Buhl, E. H., & Whittington, M. A. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144303 · Cited by 358 · see citing works
Maccaferri, G., David, J., Roberts, B., Szucs, P., Cottingham, C. A., & Somogyi, P. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-3-00091.x · Cited by 357 · see citing works
Traub, R. D., Kopell, N., Bibbig, A., Buhl, E. H., LeBeau, F. E. N., & Whittington, M. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09478.2001 · Cited by 357 · see citing works
Witter, M. P., & Amaral, D. G. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50022-5 · Cited by 344 · see citing works
Vida, I., Bartos, M., & Jónás, P. (2006) · Neuron · doi:10.1016/j.neuron.2005.11.036 · Cited by 343 · see citing works
Distributed Encoding and Retrieval of Spatial Memory in the Hippocampus
Moser, M., & Moser, E. I. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07535.1998 · Cited by 333 · see citing works
Clathrin regenerates synaptic vesicles from endosomes
Watanabe, S., Trimbuch, T., Camacho-Pérez, M., Rost, B. R., Brokowski, B., Söhl-Kielczynski, B., Felies, A., Davis, M. W., Rosenmund, C., & Jorgensen, E. M. (2014) · Nature · doi:10.1038/nature13846 · Cited by 333 · see citing works
Sustained activation of hippocampal pyramidal cells by ‘space clamping’ in a running wheel
Czurkó, A., Hirase, H., Csicsvari, J. L., & Buzsáki, G. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00446.x · Cited by 326 · see citing works
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network
Bartos, M., Vida, I., Frotscher, M., Geiger, J. R. P., & Jonas, P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02687.2001 · Cited by 325 · see citing works
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 310 · see citing works
Acsády, L., Görcs, T. J., & Freund, T. F. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00609-5 · Cited by 310 · see citing works
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 296 · see citing works
Self-citationKann, O., Papageorgiou, I. E., & Draguhn, A. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.104 · Cited by 295 · see citing works
Gap Junctions Linking the Dendritic Network of GABAergic Interneurons in the Hippocampus
Fukuda, T., & Kosaka, T. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-04-01519.2000 · Cited by 293 · see citing works
Meyer, A. H., Katona, I., Blatow, M., Rozov, A. V., & Monyer, H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07055.2002 · Cited by 286 · see citing works
A Blueprint for the Spatiotemporal Origins of Mouse Hippocampal Interneuron Diversity
Tricoire, L., Pelkey, K. A., Erkkila, B. E., Jeffries, B. W., Yuan, X., & McBain, C. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0323-11.2011 · Cited by 292 · see citing works
A model of gamma‐frequency network oscillations induced in the rat CA3 region by carbachol in vitro
Traub, R. D., Bibbig, A., Fisahn, A., LeBeau, F. E. N., Whittington, M. A., & Buhl, E. H. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00300.x · Cited by 283 · see citing works
Thomson, A. M., West, D. C., Hahn, J. D., & Deuchars, J. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021667 · Cited by 275 · see citing works
Functional nicotinic ACh receptors on interneurones in the rat hippocampus
Jones, S., & Yakel, J. L. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.603bd.x · Cited by 271 · see citing works
Activity-Dependent Redistribution and Essential Role of Cortactin in Dendritic Spine Morphogenesis
Hering, H., & Sheng, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-37-11759.2003 · Cited by 269 · see citing works
Jónás, P., Bischofberger, J., Fricker, D., & Miles, R. (2003) · Trends in Neurosciences · doi:10.1016/j.tins.2003.10.010 · Cited by 266 · see citing works
The interneuron energy hypothesis: Implications for brain disease
Kann, O. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.08.005 · Cited by 266 · see citing works
Pawelzik, H., Hughes, D. I., & Thomson, A. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10118 · Cited by 262 · see citing works
GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus
Klausberger, T. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06913.x · Cited by 260 · see citing works
Dendritic Spikes Are Enhanced by Cooperative Network Activity in the Intact Hippocampus
Kamondi, A., Acsády, L., & Buzsáki, G. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03919.1998 · Cited by 252 · see citing works
Multiple origins of the cortical gamma rhythm
Whittington, M. A., Cunningham, M. O., LeBeau, F. E. N., Racca, C., & Traub, R. D. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20814 · Cited by 253 · see citing works
Traub, R. D., & Bibbig, A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02086.2000 · Cited by 250 · see citing works
Postnatal Differentiation of Basket Cells from Slow to Fast Signaling Devices
Doischer, D., Aurel Hosp, J., Yanagawa, Y., Obata, K., Jonas, P., Vida, I., & Bartos, M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2890-08.2008 · Cited by 248 · see citing works
Probabilistic cell typing enables fine mapping of closely related cell types in situ
Qian, X., Harris, K. D., Hauling, T., Nicoloutsopoulos, D., Muñoz‐Manchado, A. B., Skene, N., Hjerling‐Leffler, J., & Nilsson, M. F. (2019) · Nature Methods · doi:10.1038/s41592-019-0631-4 · Cited by 230 · see citing works
Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat
Tamás, G., Somogyi, P., & Buhl, E. H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04255.1998 · Cited by 242 · see citing works
Alkondon, M., & Albuquerque, E. X. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.6.3043 · Cited by 240 · see citing works
Nicotinic Receptor Activation Excites Distinct Subtypes of Interneurons in the Rat Hippocampus
McQuiston, A. R., & Madison, D. V. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-08-02887.1999 · Cited by 239 · see citing works
Buzsáki, G., Penttonen, M., Nádasdy, Z., & Bragin, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.18.9921 · Cited by 239 · see citing works
Self-citationOrthogonal arrangement of rhythm-generating microcircuits in the hippocampus
Gloveli, T., Dugladze, T., Rotstein, H. G., Traub, R. D., Monyer, H., Heinemann, U., Whittington, M. A., & Kopell, N. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506259102 · Cited by 232 · see citing works
Gloveli, 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 231 · see citing works
Intrinsic and extrinsic wiring of CA3: Indications for connectional heterogeneityPreprint
Witter, M. P. (2007) · Learning & Memory · doi:10.1101/lm.725207 · Cited by 234 · see citing works
Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”
Fishell, G., & Rudy, B. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113717 · Cited by 233 · see citing works
Ognjanovski, N., Schaeffer, S. M., Wu, J., Mofakham, S., Maruyama, D., Żochowski, M., & Aton, S. J. (2017) · Nature Communications · doi:10.1038/ncomms15039 · Cited by 221 · see citing works
Ji, D., & Dani, J. A. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2682 · Cited by 231 · see citing works
Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice
Whittington, M. A., Stanford, I. M., Colling, S. B., Jefferys, J. G. R., & Traub, R. D. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.591bj.x · Cited by 224 · see citing works
Bienkowski, M. S., Bowman, I., Song, M. Y., Gou, L., Ard, T., Cotter, K., Zhu, M., Benavidez, N. L., Yamashita, S., Abu-Jaber, J., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0241-y · Cited by 224 · see citing works
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 · see citing works
Venero, C., Guadaño‐Ferraz, A., Herrero, A. I., Nordström, K., Manzano, J., de Escobar, G. M., Bernal, J., & Vennström, B. (2005) · Genes & Development · doi:10.1101/gad.346105 · Cited by 222 · see citing works
Neurotrophins and activity-dependent plasticity of cortical interneurons
Marty, S., da, M., & Berninger, B. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01026-0 · Cited by 221 · see citing works
Prefrontal neuronal assemblies temporally control fear behaviour
Déjean, C., Courtin, J., Karalis, N., Chaudun, F., Wurtz, H., Bienvenu, T., & Herry, C. (2016) · Nature · doi:10.1038/nature18630 · Cited by 218 · see citing works
A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning
Li, Y., Xu, J., Liu, Y., Zhu, J., Liu, N., Zeng, W., Huang, N., Rasch, M. J., Jiang, H., Gu, X., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4517 · Cited by 210 · see citing works
Ramos, B., Baglietto‐Vargas, D., del Río, J. C., Moreno‐González, I., Santa‐María, C., Jiménez, S., Caballero, C., Lopez-Tellez, J. F., Khan, Z. U., Ruano, D., et al. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.09.022 · Cited by 213 · see citing works
Calcium Microdomains in Aspiny Dendrites
Goldberg, J. H., Tamas, G., Aronov, D., & Yuste, R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00714-1 · Cited by 212 · see citing works
Morphological diversity and connectivity of hippocampal interneurons
Booker, S. A., & Vida, I. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2882-2 · Cited by 210 · see citing works
Hájos, N., Papp, E., Acsády, L., Levey, A. I., & Freund, T. F. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00300-x · Cited by 210 · see citing works
Fukuda, T., Kosaka, T., Singer, W., & Galuske, R. A. W. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4076-05.2006 · Cited by 209 · see citing works
The fractions of short- and long-range connections in the visual cortex
Stepanyants, A., Martinez, L. M., Ferecskó, A. S., & Kisvárday, Z. F. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810390106 · Cited by 208 · see citing works
Dinocourt, C., Petanjek, Z., Freund, T. F., Ben‐Ari, Y., & Esclapez, M. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10622 · Cited by 208 · see citing works
- 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
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