Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance [published erratum appears in Cereb Cortex 1997 Dec;7(8):779]

Abstract

The cerebral cortex and thalamus constitute a unified oscillatory machine displaying different spontaneous rhythms that are dependent on the behavioral state of vigilance. In vivo multi-site recordings from a variety of neocortical areas and related thalamic nuclei in cat, including dual simultaneous intracellular recordings, demonstrate that corticofugal volleys are effective in synchronizing fast (20-50 Hz) and low-frequency (<15 Hz) oscillations In thalamocortical networks, characterizing activated and deafferented states. (i) Fast spontaneous oscillations depend on the depolarization of thalamic and cortical cells and appear in a sustained manner during waking and REM sleep. Corticothalamic neurons, discharging high-frequency (400 Hz) spike bursts at 30-40 Hz, are good candidates to synchronize fast oscillations in reentrant thalamocortical loops. Weakly synchronized, fast spontaneous oscillations may be reset and become robustly coherent after relevant sensory stimuli in waking or internal signals during the dreaming state. (ii) During quiescent sleep, the long-range synchronization of brain electrical activity results from synchronous hyperpolarizations in forebrain neurons. The corticothalamic inputs during the depolarizing component of the slow oscillation (<1 Hz) are effective in grouping the thalamic-generated sleep rhythms (spindles at 7-14 Hz and delta at 1-4 Hz) into complex wave-sequences. These inputs also control the shape of spindles, and favor the long-range synchronization and nearly simultaneous appearance of spindles. (iii) The cortical control of thalamic activity is also demonstrated in spike-wave seizures developing from sleep patterns. More than half of thalamocortical neurons are silent during spike-wave seizures, being tonically hyperpolarized, and display IPSPs (closely related to the paroxysmal depolarizing shifts of cortical cells) that are determined by the pattern of activities in thalamic reticular cells. All these data congruently show the power of cortical control upon thalamic oscillators.