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Journal of Neuroscience, Vol 11, 3200-3217, Copyright © 1991 by Society for Neuroscience
Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression
M Steriade, RC Dossi and A Nunez
Laboratoire de Neurophysiologie, Faculte de Medecine, Universite Laval, Quebec, Canada.
A slow (0.5-4 Hz) oscillation of thalamic neurons was recently described
and attributed to the interplay of two intrinsic currents. In this study,
we investigated the network modulation of this intrinsic thalamic
oscillation within the frequency range of EEG sleep delta- waves. We
performed intracellular and extracellular recordings of antidromically
identified thalamocortical cells (n = 305) in sensory, motor,
associational, and intralaminar nuclei of anesthetized cats. At the resting
membrane potential, Vm (-60.3 +/- 0.4 mV, mean +/- SE), cortical
stimulation induced spindle-like oscillations (7-14 Hz), whereas at Vm more
negative than -65 mV the same stimuli triggered an oscillation within the
EEG delta-frequency (0.5-4 Hz), consisting of low-threshold spikes (LTSs)
followed by after hyperpolarizing potentials (AHPs). The LTS-AHP sequences
outlasted cortical stimuli as a self-sustained rhythmicity at 1-2 Hz.
Corticothalamic stimuli were able to transform subthreshold slow (0.5-4 Hz)
oscillations, occurring spontaneously at Vm more negative than -65 mV, into
rhythmic LTSs crowned by bursts of Na+ spikes that persisted for 10-20 sec
after cessation of cortical volleys. Cortical volleys also revived a
hyperpolarization-activated slow oscillation when it dampened after a few
cycles. Auto- and crosscorrelograms of neuronal pairs revealed that
unrelated cells became synchronized after a series of corticothalamic
stimuli, with both neurons displaying rhythmic (1-2 Hz) bursts or spike
trains. Since delta-thalamic oscillations, prevailing during late sleep
stages, are triggered at more negative Vm than spindles characterizing the
early sleep stage, we postulate a progressive hyperpolarization of
thalamocortical neurons with the deepening of the behavioral state of
EEG-synchronized sleep. In view of the evidence that cortical-elicited slow
oscillations depend on synaptically induced hyperpolarization of
thalamocortical cells, we propose that the potentiating influence of the
corticothalamic input results from the engagement of two GABAergic thalamic
cell classes, reticular and local-circuit neurons. The
thalamocorticothalamic loop would transfer the spike bursts of thalamic
oscillating cells to cortical targets, which in turn would reinforce the
oscillation by direct pathways and/or indirect projections relayed by
reticular and local-circuit thalamic cells. Stimulation of mesopontine
cholinergic [peribrachial (PB) and laterodorsal tegmental (LDT)] nuclei in
monoamine-depleted animals had an effect that was opposite to that exerted
by corticothalamic volleys. PB/LDT stimulation reduced or suppressed the
slow (1-4 Hz) oscillatory bursts of high- frequency spikes in thalamic
cells.(ABSTRACT TRUNCATED AT 400 WORDS)
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