Brain activation, then (1949) and now: coherent fast rhythms in corticothalamic networks

The hypothesis of forebrain activation elicited by brainstem reticular core stimulation, formulated almost a half century ago, is now fully substantiated at the intracellular level of thalamic and neocortical neurons. Data show that stimulation of mesopontine cholinergic nuclei induces a prolonged muscarinic depolarization of thalamocortical neurons, associated with an increase in their apparent input resistance (that explains the enhanced probability of thalamic responses to incoming volleys upon arousal) and accompanied by a long-lasting activation of cortical rhythms. Activation also includes the preservation or even enhancement of short-lasting sculpturing inhibitory processes in thalamic and neocortical cells, a basic requirement for discrimination purposes. The notion of activation, that was erroneously termed as a "desynchronized" activity in thalamocortical networks, is now demonstrated to include spontaneously occurring, synchronous fast (20-40 Hz) rhythms. While the spatial coherence of sleep rhythms extends over wide territories, fast oscillations during brain arousal are synchronous within a cortical column and among closely spaced cortical areas, thalamic nuclei, and corticothalamic systems. Fast oscillations do not exclusively characterize brain-active states of waking and REM sleep, as they are also present during the depolarizing phase of the slow sleep oscillation in both cortical and thalamic cells. The subthreshold fast depolarizing spontaneous oscillations may bias thalamic and cortical cells to respond synchronously, at fast frequencies, to external stimuli in the wake state and to internal drives (such as ponto-geniculo-occipital signals) during REM sleep.