Large-Scale Microelectrode Recordings of High-Frequency Gamma Oscillations in Human Cortex during Sleep

Abstract

Gamma oscillations (40-120 Hz), usually associated with waking functions, can be recorded in the deepest stages of sleep in animals. The full details of their large-scale coordination across multiple cortical networks are still unknown. Furthermore, it is not known whether oscillations with similar characteristics are also present in the human brain. In this study, we examined the existence of gamma oscillations during polysomnographically defined sleep-wake states using large-scale microelectrode recordings (up to 56 channels), with single-cell and spike-time precision, in epilepsy patients. We report that low (40-80 Hz) and high (80-120 Hz) gamma oscillations recurrently emerged over time windows of several hundreds of milliseconds in all investigated cortical areas during slow-wave sleep. These patterns were correlated with positive peaks of EEG slow oscillations and marked increases in local cellular discharges, suggesting that they were associated with cortical UP states. These gamma oscillations frequently appeared at approximately the same time in many different cortical areas, including homotopic regions, forming large spatial patterns. Coincident firings with millisecond precision were strongly enhanced during gamma oscillations but only between cells within the same cortical area. Furthermore, in a significant number of cases, cortical gamma oscillations tended to occur within 100 ms after hippocampal ripple/sharp wave complexes. These data confirm and extend earlier animal studies reporting that gamma oscillations are transiently expressed during UP states during sleep. We speculate that these high-frequency patterns briefly restore "microwake" activity and are important for consolidation of memory traces acquired during previous awake periods.