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Fast oscillations in activated neocortical brain slices: an in vitro continuation of the pioneering in vivo studies of Mircea Steriade and colleagues

Published online by Cambridge University Press:  23 January 2008

Roger D. Traub ,
Mark Cunningham  and
Miles A. Whittington
Roger D. Traub*
Affiliation:
Depts of Physiology and Pharmacology, and Neurology, SUNY Downstate Medical Center, Brooklyn, NY, USA
Mark Cunningham
Affiliation:
School of Neurology, Neurobiology and Psychiatry, The Medical School, University of Newcastle, UK
Miles A. Whittington
Affiliation:
School of Neurology, Neurobiology and Psychiatry, The Medical School, University of Newcastle, UK
*
Correspondence shoud be addressed to: Roger D. Traub, MD, SUNY Downstate Medical Center, 450 Clarkson Ave., Box 31, Brooklyn, NY 11203U.S.A. email: roger.traub@downstate.edu
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Abstract

The seminal in vivo work of Mircea Steriade and his colleagues has, as is always the case with the most insightful and creative scientists, raised many serious questions: questions, for example, of the detailed cellular and molecular mechanisms of the phenomena they discovered. In our tribute to this great investigator, we shall present some examples, based on our in vitro and modeling work, that shed light on some of his remarkable breakthroughs: the slow oscillation of sleep (<1 Hz); the several types of fast oscillations that are superimposed on the intracellular depolarizing, or active, phases of the slow oscillation; and the transition from slow oscillation to seizure via a period of very fast (>70 Hz) oscillations.

Keywords

slow oscillationvery fast oscillationgap junctionspikeletkainate
Type
Review Article
Information
Thalamus & Related Systems , Volume 4 , Issue 1 , March 2008 , pp. 79 - 86
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Amzica, F. and Steriade, M. (1995) Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. Journal of Neuroscience 15, 4658–4677.CrossRefGoogle ScholarPubMed
Brumberg, J.C., Nowak, L.G. and McCormick, D.A. (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. Journal of Neuroscience 20, 4829–4843.CrossRefGoogle ScholarPubMed
Buhl, E.H., Tamás, G. and Fisahn, A. (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. Journal of Physiology 513, 117–126.CrossRefGoogle ScholarPubMed
Connors, B.W., Benardo, L.S. and Prince, D.A. (1983) Coupling between neurons of the developing rat neocortex. Journal of Neuroscience 3, 773–782.CrossRefGoogle ScholarPubMed
Contractor, A., Swanson, G.T., Sailer, A., O'Gorman, S. and Heinemann, S.F. (2000) Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. Journal of Neuroscience 20, 8269–8278.CrossRefGoogle ScholarPubMed
Contreras, D., Timofeev, I. and Steriade, M. (1996) Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. Journal of Physiology 494, 251–264.CrossRefGoogle ScholarPubMed
Cunningham, M.O., Whittington, M.A., Bibbig, A., Roopun, A., LeBeau, F.E.N., Vogt, A. et al. (2004) A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. Proceedings of the National Academy of Sciences of the USA 101, 7152–7157.CrossRefGoogle Scholar
Cunningham, M.O., Pervouchine, D., Racca, C., Kopell, N.J., Davies, C.H., Jones, R.S.G. et al. (2006) Neuronal metabolism governs cortical response state. Proceedings of the National Academy of Sciences of the USA 103, 5597–5601.CrossRefGoogle Scholar
Draguhn, A., Traub, R.D., Schmitz, D. and Jefferys, J.G.R. (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189–192.CrossRefGoogle ScholarPubMed
Fisahn, A., Pike, F.G., Buhl, E.H. and Paulsen, O. (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394, 186–189.CrossRefGoogle ScholarPubMed
Gasparini, S., Migliore, M. and Magee, J.C. (2004) On the initiation and propagation of dendritic spikes in CA1 pyamidal neurons. Journal of Neuroscience 24, 11046–11056.CrossRefGoogle ScholarPubMed
Grenier, F., Timofeev, I. and Steriade, M. (2001) Focal synchronization of ripples (80–200 Hz) in neocortex and their neuronal correlates. Journal of Neurophysiology 86, 1884–1898.CrossRefGoogle ScholarPubMed
Grenier, F., Timofeev, I. and Steriade, M. (2003) Neocortical very fast oscillations (ripples, 80–200 Hz) during seizures: intracellular correlates. Journal of Neurophysiology 89, 841–852.CrossRefGoogle ScholarPubMed
Gribble, F.M., Ashfield, R., Ammala, C. and Ashcroft, F.M. (1997) Properties of cloned ATP-sensitive K+ channels expressed in Xenopus oocytes. Journal of Physiology 498, 87–98.CrossRefGoogle ScholarPubMed
Gutnick, M.J., Lobel-Yaakov, R. and Rimon, G. (1985) Incidence of neuronal dye-coupling in neocortical slices depends on the plane of section. Neuroscience 15, 659–666.CrossRefGoogle ScholarPubMed
Hamzei-Sichani, F., Janssen, W.G., Hof, P.R., Wearne, S.L., Stewart, M.G., Whittington, M.A. and Traub, R.D. (2006) Gap junctions couple hippocampal mossy fiber axons to each other and to CA3 pyramidal cell dendrites. Society for Neuroscience Abstracts 132.9.Google Scholar
Hamzei-Sichani, F., Kamasawa, N., Janssen, W.G.M., Yasumura, T., Davidson, K.G.V., Hof, P.R., Wearne, S.L., Stewart, M.G., Young, S.R., Whittington, M.A., Rash, J.E. and Traub, R.D. (2007) Gap junctions on hippocampal mossy fiber axons demonstrated by thin-section electron microscopy and freeze-fracture replica immunogold labeling. Proceedings of the National Academy of Sciences of the USA 104, 12548–12553.CrossRefGoogle ScholarPubMed
Montana, V., Malarkey, E.B., Verderio, C., Matteoli, M. and Parpura, V. (2006) Vesicular transmitter release from astrocytes. Glia 54, 700–715.CrossRefGoogle ScholarPubMed
Peinado, A., Yuste, R. and Katz, L.C. (1993) Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10, 103–114.CrossRefGoogle ScholarPubMed
Roopun, A., Middleton, S.J., Cunningham, M.O., LeBeau, F.E.N., Bibbig, A., Whittington, M.A. et al. (2006) A beta2-frequency (20–30 Hz) oscillation in non-synaptic networks of somatosensory cortex. Proceedings of the National Academy of Sciences of the USA 103, 15646–15650.CrossRefGoogle Scholar
Sakura, H., Ammala, C., Smith, P.A., Gribble, F.M. and Ashcroft, F.M. (1995) Cloning and functional expression of the cDNA encoding a novel ATP-sensitive potassium channel subunit expressed in pancreatic beta-cells, brain, heart and skeletal muscle. FEBS Letters 377, 338–344.Google ScholarPubMed
Sanchez-Vives, M.V. and McCormick, D.A. (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nature Neuroscience 3, 1027–1034.CrossRefGoogle ScholarPubMed
Schmitz, D., Schuchmann, S., Fisahn, A., Draguhn, A., Buhl, E.H., Petrasch-Parwez, R.E. et al. (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31, 831–840.CrossRefGoogle ScholarPubMed
Spencer, W.A. and Kandel, E.R. (1961) Electrophysiology of hippocampal neurons IV. Fast prepotentials. Journal of Neurophysiology 24, 272–285.CrossRefGoogle ScholarPubMed
Steriade, M. and Contreras, D. (1998) Spike-wave complexes and fast components of cortically generated seizures. I. Role of neocortex and thalamus. Journal of Neurophysiology 80, 1439–1455.CrossRefGoogle ScholarPubMed
Steriade, M., Amzica, F. and Contreras, D. (1996) Synchronization of fast (30–40 Hz) spontaneous cortical rhythms during brain activation. Journal of Neuroscience 16, 392–417.CrossRefGoogle ScholarPubMed
Steriade, M., Amzica, F., Neckelmann, D. and Timofeev, I. (1998) Spike-wave complexes and fast components of cortically generated seizures. II. Extra- and intracellular pattens. Journal of Neurophysiology 80, 1456–1479.CrossRefGoogle Scholar
Steriade, M., Curró Dossi, R., Paré, D. and Oakson, G. (1991) Fast oscillations (20–40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proceedings of the National Academy of Sciences of the USA 88, 4396–4400.CrossRefGoogle Scholar
Steriade, M., Nuñez, A. and Amzica, F. (1993a) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. Journal of Neuroscience 13, 3252–3265.CrossRefGoogle ScholarPubMed
Steriade, M., Nuñez, A. and Amzica, F. (1993b) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. Journal of Neuroscience 13, 3266–3283.CrossRefGoogle ScholarPubMed
Suh, B.C. and Hille, B. (2002) Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35, 507–520.CrossRefGoogle ScholarPubMed
Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T.J. and Steriade, M. (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cerebral Cortex 10, 1185–1199.CrossRefGoogle ScholarPubMed
Traub, R.D. and Bibbig, A. (2000) A model of high-frequency ripples in the hippocampus, based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. Journal of Neuroscience 20, 2086–2093.CrossRefGoogle Scholar
Traub, R.D., Bibbig, A., Fisahn, A., LeBeau, F.E.N., Whittington, M.A. and Buhl, E.H. (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. European Journal of Neuroscience 12, 4093–4106.CrossRefGoogle Scholar
Traub, R.D., Whittington, M.A., Buhl, E.H., LeBeau, F.E.N., Bibbig, A., Boyd, S. et al. (2001) A possible role for gap junctions in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia 42, 153–170.Google ScholarPubMed
Traub, R.D., Buhl, E.H., Gloveli, T. and Whittington, M.A. (2003) Fast rhythmic bursting can be induced in layer 2/3 cortical neurons by enhancing persistent Na+ conductance or by blocking BK channels. Journal of Neurophysiology 89, 909–921.CrossRefGoogle ScholarPubMed
Traub, R.D., Contreras, D., Cunningham, M.O., Murray, H., LeBeau, F.E.N., Roopun, A. et al. (2005) Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles and epileptogenic bursts. Journal of Neurophysiology 93, 2194–2232.CrossRefGoogle ScholarPubMed
Traub, R.D., Cunningham, M.O., Gloveli, T., LeBeau, F.E.N., Bibbig, A., Buhl, E.H. et al. (2003) GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations. Proceedings of the National Academy of Sciences of the USA 100, 11047–11052.CrossRefGoogle Scholar
Worrell, G.A., Parish, L., Cranstoun, S.D., Jonas, R., Baltuch, G. and Litt, B. (2004) High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 127, 1496–1506.CrossRefGoogle ScholarPubMed
Yasargil, G.M. and Sandri, C. (1990) Topography and ultrastructure of commissural interneurons that may establish reciprocal inhibitory connections of the Mauthner axons in the spinal cord of the tench, Tinca tinca L. Journal of Neurocytology 19, 111–126.CrossRefGoogle ScholarPubMed