Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation

Abstract

We investigated the synchronization of fast spontaneous oscillations (mainly 30–40 Hz) in anesthetized and behaving cats by means of simultaneous extra- and intracellular recordings from multiple neocortical areas. Fast Fourier transforms, auto- and cross- correlations, and spike- or wave-triggered averages were used to determine the frequency and temporal coherence of fast oscillations that outlasted the stimulation of ascending activating systems or that occurred naturally during behavioral states of waking and rapid eye movement (REM) sleep but also appeared during the depolarizing phases of slow sleep oscillations. In 90% of microelectrode tracks, the fast oscillations did not show field reversal at any depth of the cortex and were not observable in the underlying white matter. The negative field potentials of the fast oscillations were associated at all depths with neuronal firing. This field potential property of fast oscillations was in sharp contrast to the reversal of slow sleep oscillation or evoked potentials at depths of 0.25–0.5 mm. The coherence of fast spontaneous rhythms was spatially limited, being confined within a cortical column and among closely located neocortical sites, in contrast to the long- range synchronization of slow sleep rhythms. Depolarizing current pulses elicited spike-bursts (200–400 Hz) recurring at a frequency of 30–40 Hz. Our experiments demonstrate that the conventional notion of a totally desynchronized cortical activity upon arousal should be revised as fast rhythms are enhanced and synchronized within intracortical networks during brain activation. Spontaneously occurring, subthreshold membrane potential depolarizing oscillations may bias cortical and thalamic neurons to respond synchronously, at fast frequencies, to relevant stimuli in the wake state or to internally generated drives in REM sleep.