Mechanisms underlying the synchronizing action of corticothalamic
feedback through inhibition of thalamic relay cells
Alain Destexhe, Diego Contreras and Mircea Steriade
Journal of Neurophysiology 79: 999-1016 (1998)
Abstract
Early studies have shown that spindle oscillations are generated in the
thalamus and are synchronized over wide cortical territories. More recent
experiments have shown that this large-scale synchrony depends on the
integrity of corticothalamic feedback. Previously proposed mechanisms
emphasized exclusively intrathalamic mechanisms to generate the synchrony of
these oscillations. In the present paper, we propose a cellular mechanism in
which the synchrony is dependent of a mutual interaction between cortex and
thalamus. This cellular mechanism is tested by computational models
consisting of pyramidal cells, interneurons, thalamic reticular (RE) and
thalamocortical (TC) relay cells, based on voltage-clamp data on intrinsic
currents and synaptic receptors present in the circuitry. The model suggests
that corticothalamic feedback must operate on the thalamus mainly through
excitation of GABAergic RE neurons, therefore recruiting relay cells
essentially through inhibition and rebound. We provide experimental evidence
for such dominant inhibition in the lateral posterior nucleus. In these
conditions, the model shows that cortical discharges optimally evoked thalamic
oscillations. This feature is essential to the present cellular mechanism and
is also consistently observed experimentally. The model further shows that,
with this type of corticothalamic feedback, cortical discharges recruited
large areas of the thalamus due to the divergent cortex-to-RE and RE-to-TC
axonal projections. Consequently, the thalamocortical network generated
patterns of oscillations and synchrony similar to in vivo recordings. The
model also emphasizes the important role of the modulation of the Ih current
by calcium in TC cells. This property conferred a relative refractoriness to
the entire network, a feature also observed experimentally, as we show here.
Further, the same property accounted for various spatiotemporal features of
oscillations, such as systematic propagation following low-intensity cortical
stimulation, local oscillations, and more generally, a high variability in the
patterns of spontaneous oscillations, similar to in vivo recordings. We
propose that the large-scale synchrony of spindle oscillations in vivo is due
to thalamo-cortical interactions in which the corticothalamic feedback acts
predominantly through the RE nucleus. Several predictions are suggested to
test the validity of this model.
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