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Unité de Neurosciences Intégratives et Computationnelles, Centre National de la Recherche Scientifique, Gif-sur-Yvette, France; Howard Hughes Medical Institute and the Salk Institute; Department of Biology, University of California at San Diego, La Jolla, California
Destexhe, A., and T. J. Sejnowski. Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations. Physiol Rev 83: 1401-1453, 2003; 10.1152/physrev.00012.2003.—Neurons of the central nervous system display a broad spectrum of intrinsic electrophysiological properties that are absent in the traditional "integrate-and-fire" model. A network of neurons with these properties interacting through synaptic receptors with many time scales can produce complex patterns of activity that cannot be intuitively predicted. Computational methods, tightly linked to experimental data, provide insights into the dynamics of neural networks. We review this approach for the case of bursting neurons of the thalamus, with a focus on thalamic and thalamocortical slow-wave oscillations. At the single-cell level, intrinsic bursting or oscillations can be explained by interactions between calcium- and voltage-dependent channels. At the network level, the genesis of oscillations, their initiation, propagation, termination, and large-scale synchrony can be explained by interactions between neurons with a variety of intrinsic cellular properties through different types of synaptic receptors. These interactions can be altered by neuromodulators, which can dramatically shift the large-scale behavior of the network, and can also be disrupted in many ways, resulting in pathological patterns of activity, such as seizures. We suggest a coherent framework that accounts for a large body of experimental data at the ion-channel, single-cell, and network levels. This framework suggests physiological roles for the highly synchronized oscillations of slow-wave sleep.
2 Computer-generated animations of the membrane voltage are available at http://cns.iaf.cnrs-gif.fr or http://www.salk.edu/~alain.
3 Heterogeneity was created by randomizing the values of the Ih conductance, such that the majority of TC cells was resting around -60 mV, while only a small minority were spontaneous oscillators, similar to the proportion found in vitro (191). This minority served as "initiators" of the oscillation in the entire network.
4 It is also conceivable that RE cells coupled through gap junctions could induce bursts in each other if their resting level is hyperpolarized enough to deinactivate the IT. In this case, oscillations should be observed in slices of the RE nucleus, where the level of RE cells is typically very hyperpolarized (see, for example, Ref. 337). Such oscillations have, however, never been reported.
5 Bicuculline was later shown to also block the apamin-sensitive calcium-dependent current in RE cells (76). Because this current is important for controlling burst generation in RE cells (17), bicuculline therefore does not exert specific effects on GABAA receptors. Other antagonists are used, such as picrotoxin, that also induce slow thalamic oscillations, showing that this oscillation is generated through antagonist actions on GABAA receptors in the RE nucleus (266).
6 This may also be described as an afterdepolarization (ADP) following the spindle wave, which is actually the terminology used in the in vitro experiments (19).
7 Inhibitory dominance was not by itself a prediction, given the large body of experimental evidence showing that cortical stimulation primarily evoke IPSPs in TC cells (4, 45, 66, 82, 196, 263, 315, 330, 359).
8 This is converse to the claims that the low-threshold spike in TC cells is not involved in generating seizures in GAERS rats (251).
9 This is possible in slices from the visual thalamus, in which the corticothalamic and retinal fibers are both accessible (18, 334).
Address for reprint requests and other correspondence: A. Destexhe, Unité de Neurosciences Intégratives et Computation-nelles, CNRS, UPR-2191, Avenue de la Terrasse, Bat. 33, 91198 Gif-sur-Yvette, France (E-mail: Destexhe{at}iaf.cnrs-gif.fr).
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