Fast oscillations could be devided on 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.
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).
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