Modulation of γ and spindle-range power by slow oscillations in scalp sleep EEG of children

Deep sleep is characterized by slow waves of electrical activity in the cerebral cortex. They represent alternating down states and up states of, respectively, hyperpolarization with accompanying neuronal silence and depolarization during which neuronal firing resumes. The up states give rise to faster oscillations, notably spindles and gamma activity which appear to be of major importance to the role of sleep in brain function and cognition. Unfortunately, while spindles are easily detectable, gamma oscillations are of very small amplitude. No previous sleep study has succeeded in demonstrating modulations of gamma power along the time course of slow waves in human scalp EEG. As a consequence, progress in our understanding of the functional role of gamma modulation during sleep has been limited to animal studies and exceptional human studies, notably those of intracranial recordings in epileptic patients. Because high synaptic density, which peaks some time before puberty depending on the brain region (Huttenlocher and Dabholkar, 1997), generates oscillations of larger amplitude, we considered that the best chance to demonstrate a modulation of gamma power by slow wave phase in regular scalp sleep EEG would be in school-aged children. Sleep EEG was recorded in 30 healthy children (aged 10.7 ± 0.8 years; mean ± s.d.). Time-frequency analysis was applied to evaluate the time course of spectral power along the development of a slow wave. Moreover, we attempted to modify sleep architecture and sleep characteristics through automated acoustic stimulation coupled to the occurrence of slow waves in one subset of the children. Gamma power increased on the rising slope and positive peak of the slow wave. Gamma and spindle activity is strongly suppressed during the negative peak. There were no differences between the groups who received and did not receive acoustic stimulation in the sleep parameters and slow wave-locked time-frequency analysis. Our findings show, for the first time in scalp EEG in humans, that gamma activity is associated with the up-going slope and peak of the slow wave. We propose that studies in children provide a uniquely feasible opportunity to conduct investigations into the role of gamma during sleep.