Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro
Abstract
Coherent oscillations, in which ensembles of neurons fire in a repeated and synchronous manner, are thought to be important in higher brain functions. In the hippocampus, these discharges are categorized according to their frequency as theta (4-10Hz), gamma (20-80 Hz) and high-frequency (approximately 200 Hz) discharges, and they occur in relation to different behavioural states. The synaptic bases of theta and gamma rhythms have been extensively studied but the cellular bases for high-frequency oscillations are not understood. Here we report that high-frequency network oscillations are present in rat brain slices in vitro, occurring as a brief series of repetitive population spikes at 150-200 Hz in all hippocampal principal cell layers. Moreover, this synchronous activity is not mediated through the more commonly studied modes of chemical synaptic transmission, but is in fact a result of direct electrotonic coupling of neurons, most likely through gap-junctional connections. Thus high-frequency oscillations synchronize the activity of electrically coupled subsets of principal neurons within the well-documented synaptic network of the hippocampus.
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Beginning in 1998, evidence began to show that gamma synchrony, the best measurable correlate of consciousness, depended on gap junctions, particularly dendritic-dendritic gap junctions.
“Beginning in 1998, evidence began to show that gamma synchrony, the best measurable correlate of consciousness, depended on gap junctions, particularly dendritic-dendritic gap junctions [49][50][51][52][53][54].”
From Consciousness in the universe (2014) · cites this paper as [50]
Cites
Hamill, O. P., Marty, A., Neher, E., Sakmann, B., & Sigworth, F. J. (1981) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00656997 · Cited by 18,436 · see citing works
Hippocampal electrical activity and voluntary movement in the rat
Vanderwolf, C. H. (1969) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(69)90092-3 · Cited by 1,928 · see citing works
Whittington, M. A., Traub, R. D., & Jefferys, J. G. R. (1995) · Nature · doi:10.1038/373612a0 · Cited by 1,613 · see citing works
Self-citationSynchronization of neuronal activity in hippocampus by individual GABAergic interneurons
Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., & Somogyi, P. (1995) · Nature · doi:10.1038/378075a0 · Cited by 1,498 · see citing works
High-frequency network oscillation in the hippocampus
Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J. F., & Wise, K. D. (1992) · Science · doi:10.1126/science.1589772 · Cited by 1,223 · 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
Electrotonic coupling between neurons in cat inferior olive.
Llinas, R. H., Baker, R. G. V., & Sotelo, C. (1974) · Journal of Neurophysiology · doi:10.1152/jn.1974.37.3.560 · Cited by 661 · 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
ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: IV. FAST PREPOTENTIALS
Spencer, W. A., & Kandel, E. R. (1961) · Journal of Neurophysiology · doi:10.1152/jn.1961.24.3.272 · Cited by 502 · see citing works
Gap Junctional Conductance Is a Simple and Sensitive Function of Intracellular p H
Spray, D. C., Harris, A. L., & Bennett, M. V. L. (1981) · Science · doi:10.1126/science.6779379 · Cited by 485 · see citing works
Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission
Jefferys, J. G. R., & Haas, H. L. (1982) · Nature · doi:10.1038/300448a0 · Cited by 436 · see citing works
Self-citationTHOMAS, R. C. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015397 · Cited by 350 · see citing works
Synchronous Neural Afterdischarges in Rat Hippocampal Slices Without Active Chemical Synapses
Taylor, C. P., & Dudek, F. E. (1982) · Science · doi:10.1126/science.7134978 · Cited by 343 · see citing works
Electrotonic Coupling Between Pyramidal Cells: A Direct Demonstration in Rat Hippocampal Slices
MacVicar, B. A., & Dudek, F. E. (1981) · Science · doi:10.1126/science.6266013 · Cited by 329 · 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
Self-citationElectrophysiology of Hippocampal Neurons
Schwartzkroin, P. A., & Mueller, A. L. (1987) · Cerebral cortex · doi:10.1007/978-1-4615-6616-8_8 · Cited by 300 · see citing works
Perez-Velazquez, J. L., Valiante, T. A., & Carlen, P. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-07-04308.1994 · Cited by 276 · see citing works
Influence of electric fields on the excitability of granule cells in guinea‐pig hippocampal slices.
Jefferys, J. G. R. (1981) · The Journal of Physiology · doi:10.1113/jphysiol.1981.sp013897 · Cited by 205 · see citing works
Self-citationThe fast component in the electrical activity of rabbit's hippocampus
Stumpf, C. (1965) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(65)90128-8 · Cited by 155 · see citing works
Strata, F., Atzori, M., Molnar, M., Ugolini, G., Tempia, F., & Cherubini, E. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-04-01435.1997 · Cited by 141 · see citing works
Coupling potentials in CA1 neurons during calcium-free-induced field burst activity
Valiante, T. A., Velazquez, J. P., Jahromi, S., et al. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06946.1995 · Cited by 126 · see citing works
Church, J., & Baimbridge, K. G. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-10-03289.1991 · Cited by 124 · see citing works
Visually evoked calcium action potentials in cat striate cortex
Hirsch, J. A., Alonso, J., & Reid, R. C. (1995) · Nature · doi:10.1038/378612a0 · Cited by 110 · see citing works
Pinault, D. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(95)00004-m · Cited by 101 · see citing works
Electrotonic coupling between rat sympathetic preganglionic neurones in vitro.
Logan, S. D., Pickering, A. E., Gibson, I. C., et al. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021609 · Cited by 84 · see citing works
Traub, R. D. (1995) · Journal of Computational Neuroscience · doi:10.1007/bf00961440 · Cited by 83 · see citing works
Self-citationThe coupling pattern of axon-bearing horizontal cells in the mammalian retina
Vaney, D. I. (1993) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1993.0051 · Cited by 70 · see citing works
Expression of connexin43 mRNA in adult rodent brain
Simbürger, E., Stang, A., Kremer, M., & Dermietzel, R. (1997) · Histochemistry and Cell Biology · doi:10.1007/s004180050097 · Cited by 64 · see citing works
Uncoupling of CA3 pyramidal neurons by propionate
MacVicar, B. A., & Jahnsen, H. (1985) · Brain Research · doi:10.1016/0006-8993(85)90015-0 · Cited by 52 · see citing works
Rho, M.-J., Cabana, T., & Drew, T. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19971117)388:2 · Cited by 50 · see citing works
Patrylo, P. R., KUHN, A. J., SCHWEITZER, J. S., et al. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00111-x · Cited by 14 · see citing works
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Self-citationNeural synchrony in brain disorders: Relevance for cognitive dysfunctions and pathophysiology
Uhlhaas, P. J., & Singer, W. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.020 · Cited by 2,194 · see citing works
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Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Hameroff, S., & Penrose, R. (2014) · Physics of Life Reviews · doi:10.1016/j.plrev.2013.08.002 · Cited by 983 · see citing works
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BackgroundOscillatory 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
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Connors, B. W., & Long, M. A. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131128 · Cited by 784 · see citing works
The role of locus coeruleus in the regulation of cognitive performance
Usher, M., Cohen, J. D., Servan-Schreiber, D., Rajkowski, J., & Aston-Jones, G. (1999) · Science · doi:10.1126/science.283.5401.549 · Cited by 715 · see citing works
Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons
Tamás, G., Buhl, E. H., Lörincz, A., & Somogyi, P. (2000) · Nature Neuroscience · doi:10.1038/73936 · Cited by 648 · see citing works
Uhlhaas, P. J., Haenschel, C., Nikolic, D., & Singer, W. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn062 · Cited by 629 · see citing works
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Hughes, S. W., & Crunelli, V. (2005) · The Neuroscientist · doi:10.1177/1073858405277450 · Cited by 565 · see citing works
McBain, C. J., & Fisahn, A. (2001) · Nature Reviews Neuroscience · doi:10.1038/35049047 · Cited by 581 · see citing works
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Uhlhaas, P. J., Roux, F., Rodriguez, E., Rotarska-Jagiela, A., & Singer, W. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.12.002 · Cited by 532 · see citing works
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Hormuzdi, S. G., Pais, I., LeBeau, F. E. N., Towers, S. K., Rozov, A., Buhl, E. H., Whittington, M. A., & Monyer, H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00387-7 · Cited by 522 · see citing works
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Galarreta, M., & Hestrin, S. (2001) · Nature Reviews Neuroscience · doi:10.1038/35077566 · Cited by 434 · see citing works
Ripples in the medial temporal lobe are relevant for human memory consolidation
Axmacher, N., Elger, C. E., & Fell, J. (2008) · Brain · doi:10.1093/brain/awn103 · Cited by 372 · see citing works
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Nagy, J. I., Dudek, F. E., & Rash, J. E. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.05.005 · Cited by 375 · see citing works
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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
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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
Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish
Edwards, D. H., Heitler, W. J., & Krasne, F. B. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01340-x · Cited by 334 · see citing works
Kann, 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
Self-citationSlow waves, sharp waves, ripples, and REM in sleeping dragons
Shein-Idelson, M., Ondracek, J. M., Liaw, H.-P., Reiter, S., & Laurent, G. (2016) · Science · doi:10.1126/science.aaf3621 · Cited by 274 · see citing works
O'Neill, J., Senior, T., & Csicsvari, J. (2006) · Neuron · doi:10.1016/j.neuron.2005.10.037 · Cited by 281 · see citing works
Connexin expression in electrically coupled postnatal rat brain neurons
Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D., & Monyer, H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160037097 · Cited by 273 · see citing works
The spatial dimensions of electrically coupled networks of interneurons in the neocortex
Amitai, Y., Gibson, J. R., Beierlein, M., Patrick, S. L., Ho, A. M., Connors, B. W., & Golomb, D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-10-04142.2002 · Cited by 235 · see citing works
Juszczak, G. R., & Swiergiel, A. H. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2008.12.014 · Cited by 211 · see citing works
Sipilä, S. T., Huttu, K., Soltesz, I., Voipio, J., & Kaila, K. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0378-05.2005 · Cited by 190 · see citing works
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Maier, N., Tejero-Cantero, Á., Dorrn, A. L., Winterer, J., Beed, P. S., Morris, G., Kempter, R., Poulet, J. F. A., Leibold, C., & Schmitz, D. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.016 · Cited by 126 · see citing works
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- Authors
- Draguhn, A., Traub, R. D., Schmitz, D., & Jefferys, J. G. R.
- Affiliations
- University of Birmingham (GB)
- Humboldt-Universität zu Berlin (DE)
- Corresponding author
- Draguhn, A.
- Venue
- Nature
- Published
- 1998-07
- Volume
- 394
- Issue
- 6689
- Pages
- 189-192
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2030670571
- Cited by
- 703
- References
- 31
- Citations by year
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- FWCI
- 20.80
- 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)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Funders
- Wellcome Trust
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- high-frequency oscillations, hippocampus, electrical coupling, gap junctions, neuronal synchronization, population spike, gamma oscillations, theta oscillations, brain slices
- MeSH terms
- Action Potentials, Animals, Bicuculline, Calcium, Female, Hippocampus, Male, Neurons, Oscillometry, Rats, Wistar, Gap Junctions, Excitatory Amino Acid Antagonists, GABA Antagonists, Rats, In Vitro Techniques
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