Fast oscillations

• Dr. Roger D. Traub, SUNY Downstate Medical Center, Brooklyn, NY

Fast oscillations (greater than 20 Hz) in cortical networks of the brain have been implicated in cognitive processes, sleep, and seizures.

Cellular Mechanisms

Fast oscillations could be divided between fast (beta–gamma) and ultrafast (>100 Hz, ripples). Fast oscillations have been implicated in cognitive processes (Gray and Singer, 1989; MacKay and Mendonça, 1995); they also form a prominent part of sleep EEG signals, when intracortical electrodes are used (Grenier et al. 2001; Steriade et al. 1996); and they occur in association with seizures (Traub et al. 2001a). Ultrafast oscillations could be found during sharp waves and sleep (Ylinen et al., 1995, Grenier et al. 2001), the ripples are prominent in the onset of seizures (Grenier et al. 2003, Allen et al., 1992. Bragin A et al., 1999).

There are two major categories of fast oscillations:

• (Homogeneous) Those which occur in a homogeneous collection of neurons, all of the same type, for example CA1 pyramidal neurons;
• (Heterogeneous) Those which require synaptic interactions between two or more populations of neurons, for example CA1 pyramidal neurons together with fast-spiking CA1 interneurons.

Oscillations of Homogeneous Population

Mechanisms of fast and ultrafast oscillations were investigated in vitro. Homogeneous fast oscillations, in vitro, include the following types:

• ~200 Hz oscillations that occur amongst CA1 pyramidal neurons in nominally zero [Ca²⁺]₀ media, that is, in conditions in which chemical synaptic transmission is blocked, and cells have increased excitability (Draguhn et al. 1998). Such oscillations can be accounted for with a network model in which a collection of neurons are sparsely connected by gap junctions between their axons, in a locally random topology; and where, in addition, action potentials occur spontaneously (at low rates), with the property that an action potential can cross from axon to axon across the gap junctions (Traub et al. 1999b, 2003). The mechanisms may be similar to ~200 Hz “ripples” in vivo (Buzsáki et al. 1992; Traub and Bibbig 2000).
• 20-30 Hz "beta 2" oscillations in intrinsically bursting pyramidal cells of layer 5 somatosensory cortex (Roopun et al., in press). Beta 2 requires gap junctions, but – remarkably - not synaptic currents. The period is determined by an intrinsic K⁺ current, probably the M-current.
• Interneuron network gamma ("ING", 30-70 Hz), in neuronal networks where ionotropic glutamate receptors have been blocked, while the interneurons themselves are tonically depolarized, for example by metabotropic glutamate receptors (Whittington et al. 1995). The oscillation period of ING is primarily determined by mutual IPSPs generated by the interneurons amongst each other, but the oscillation is critically stabilized by dendritic gap junctions between the interneurons (Traub et al. 2001b). Such gap junctions compensate for the heterogeneity (Wang and Buzsáki 1996) produced by varying neuronal depolarizations, axonal conduction delays, and spatial localization of the axonal interconnections.

Figure 1: Experiments were performed in CA1 minislices (cartoon in a), bathed in kainate. This drug evokes gamma oscillations evident in field potential recordings in stratum oriens. Filtering the field potential signal at 100 to 1000 Hz shows that bursts of very high frequency activity are separated by gamma periods, each lasting tens of ms. This pattern of activity is apparent in the color coded spectrogram. After a cut that isolates stratum oriens, which contains the axonal collaterals of the CA1 pyramidal cells (cartoon in b), only continuous very fast oscillation occurs. Similar patterns of activity are seen in a network model based on hypothesize gap junctions between pyramidal cell axons, along with conventional types of synaptic interactions. Scale bars: 0.2 mV, 100 ms in I; 10 and 40 mV, 100 ms in II. From Traub et al. (2003).

Oscillations via Interplay of Distinct Populations

Fast oscillations in vitro, that involve interplay between distinct types of neurons, include these:

• Gamma (30-70 Hz) oscillations evoked by tetanic stimulation in the hippocampus (CA1) (Traub et al. 1996; Whittington et al. 1997a; Traub et al. 1999a). The electrical stimulus produces a strong, but transient, depolarization of both pyramidal cells and interneurons, mediated in part by metabotropic glutamate receptors. Gap junctions do not appear to be needed. The phasing of the oscillation requires IPSPs. This type of gamma may be an experimental model for sensory evoked gamma (Gray and Singer 1989). It is both interesting and complex because
  • it displays long-range synchrony in the presence of significant axonal conduction delays, explicable by interneuron doublets (Traub et al. 1996), and
  • because strong 2-site stimulation can produce a gamma to beta "switch", associated with synaptic plasticity (in form of long-lasting potentiation of recurrent excitatory synapses) between pyramidal cells (Whittington et al. 1997b). On the other hand, the experimental model has the limitation that it does not appear to work in neocortical slices.

• Persistent gamma in hippocampus and entorhinal cortex (Fisahn et al. 1998; Cunningham et al. 2003). This type of gamma is notable for the sparse firing of pyramidal cell somata, despite the prominent presence of IPSPs in pyramidal cells, and the dependence of the oscillation on synaptic inhibition. Additionally, phasic EPSPs and gap junctions are also required; the experimental evidence suggests that axonal electrical coupling between pyramidal cells is an absolute requirement, while interneuronal electrical coupling plays a modulatory role (Traub et al. 2003; Hormuzdi et al. 2001). Persistent gamma is usually induced by bath application of an appropriate drug, such as kainate or carbachol, and can last for hours. Power spectra of the field oscillation reveal both a gamma peak, and also a faster, but non-harmonic, peak at >70 Hz (Traub et al. 2003; Cunningham et al. 2004b). Remarkably, the pyramidal cell axonal plexus, in the hippocampal CA1 region, when it is surgically separated from pyramidal cell somata, generates a continuous very fast oscillation, rather than gamma (Figure 1). It is thought that the mechanism for this continuous very fast oscillation is similar to the mechanism for the first type of "homogeneous" fast oscillation described above. It is apparent that very fast oscillations (>70 Hz) and persistent gamma oscillations are intimately related.

• Persistent gamma in superficial layers (i.e. layers 2 and 3) of neocortex. This oscillation is similar to hippocampal and entorhinal gamma in its dependence on gap junctions, EPSPs and IPSPs; but it is different in that spontaneous very fast (>70 Hz) oscillations in the axonal plexus may not be essential for oscillation generation. Rather, this type of cortical gamma appears to require a small sub-population of fast rhythmic bursting (chattering) pyramidal and non-pyramidal cells (Gray, McCormich, 1996, Steriade et al., 1998), and these cells must be depolarized enough to be spontaneously active at near gamma frequency (Cunningham et al. 2004a).

References

• Allen PJ, Fish DR, and Smith SJ. (1992) Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. Electroencephalogr Clin Neurophysiol 82: 155-159.
• Bragin A, Engel J, Jr., Wilson CL, Fried I, and Mathern GW. (1999) Hippocampal and entorhinal cortex high-frequency oscillations (100--500 Hz) in human epileptic brain and in kainic acid--treated rats with chronic seizures. Epilepsia 40: 127-137.
• Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025-1027.
• Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA (2003) Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. J. Neurosci. 23: 9761-9769.
• Cunningham MO, Whittington MA, Bibbig A, Roopun A, LeBeau FEN, Vogt A, Monyer H, Buhl EH, Traub RD (2004a) A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. Proc. Natl. Acad. Sci. USA 101: 7152-7157.
• Cunningham MO, Halliday DM, Davies CH, Traub RD, Buhl EH, Whittington MA (2004b) Coexistence of gamma and high-frequency oscillations in the medial entorhinal cortex in vitro. J. Physiol. 559: 347-353.
• Draguhn A, Traub RD, Schmitz D, Jefferys JGR (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394: 189-192.
• Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394: 186-189.
• Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci. USA 86: 1698-1702.
• Gray CM and McCormick DA. (1996) Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science 274: 109-113.
• Grenier F, Timofeev I, Steriade M (2001) Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. J. Neurophysiol. 86: 1884-1898.
• Grenier F, Timofeev I, Steriade M (2003) Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates. J. Neurophysiol. 89: 841-852.
• Hormuzdi SG, Pais I, LeBeau FEN, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H (2001) Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31: 487-495.
• MacKay WA, Mendonça AJ (1995) Field potential oscillatory bursts in parietal cortex before and during reach. Brain Res. 704: 167-174.
• Roopun A, Middleton SJ, Cunningham MO, LeBeau FEN, Bibbig A, Whittington MA, Traub RD (In press) A beta2-frequency (20-30 Hz) oscillation in non-synaptic networks of somatosensory cortex. Proc. Natl. Acad. Sci. USA
• Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez RE, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31: 831-840.
• Steriade M, Contreras D, Amzica F, Timofeev I (1996) Synchronization of fast (30-40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J. Neurosci. 16: 2788-2808.
• Steriade M, Timofeev I, Dürmüller N, and Grenier F. (1998) Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. J Neurophysiol 79: 483-490.
• Traub RD, Whittington MA, Stanford IM, Jefferys JGR (1996) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383: 621-624.
• Traub RD, Jefferys JGR, Whittington MA (1999a) Fast Oscillations in Cortical Circuits. MIT Press, Cambridge, MA.
• Traub RD, Schmitz D, Jefferys JGR, Draguhn A (1999b) High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions. Neuroscience 92: 407-426.
• Traub RD, Bibbig A (2000) A model of high-frequency ripples in the hippocampus, based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J. Neurosci. 20: 2086-2093.
• Traub RD, Bibbig A, Fisahn A, LeBeau FEN, Whittington MA, Buhl EH (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur. J. Neurosci. 12: 4093-4106.
• Traub RD, Whittington MA, Buhl EH, LeBeau FEN, Bibbig A, Boyd S, Cross H, Baldeweg T (2001a) 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.
• Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FEN, Whittington MA (2001b) Gap junctions between interneuron dendrites can enhance long-range synchrony of gamma oscillations. J. Neurosci. 21: 9478-9486.
• Traub RD, Cunningham MO, Gloveli T, LeBeau FEN, Bibbig A, Buhl EH, Whittington MA (2003) GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations. Proc. Natl. Acad. Sci. USA 100: 11047-11052.
• Traub, R.D., Contreras, D., Cunningham, M.O., Murray, H., LeBeau, F.E.N., Roopun, A., Bibbig, A., Wilent, W.B., Higley, MJ. and Whittington, M.A. (2005) Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles and epileptogenic bursts. J. Neurophysiol. 93: 2194-2232.
• Wang X-J, Buzsáki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16: 6402-6413.
• Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615.
• Whittington MA, Stanford IM, Colling SB, Jefferys JGR, Traub RD (1997a) Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J. Physiol. 502: 591-607.
• Whittington MA, Traub RD, Faulkner HJ, Stanford IM, Jefferys JGR (1997b) Recurrent excitatory postsynaptic potentials induced by synchronized fast cortical oscillations. Proc. Natl. Acad. Sci. USA 94: 12198-12203.

Internal references

• Eugene M. Izhikevich (2006) Bursting. Scholarpedia, 1(3):1300.
• Jeff Moehlis, Kresimir Josic, Eric T. Shea-Brown (2006) Periodic orbit. Scholarpedia, 1(7):1358.
• Maxim Bazhenov and Igor Timofeev (2006) Thalamocortical oscillations. Scholarpedia, 1(6):1319.

External links

Roger Traub webpage

See also

Cortex, Binding by Synchrony, Hippocampus, Interneurons, Periodic Orbit, Synchronization, Thalamocortical oscillations

Sponsored by: Eugene M. Izhikevich, Editor-in-Chief of Scholarpedia, the peer-reviewed open-access encyclopedia

Reviewed by: Anonymous

Accepted on: 2006-12-18 21:42:03 GMT