Abstracts

Rationale: High frequency oscillations are associated with normal brain function, but also increasingly recognized as a potential biomarker of epileptogenic brain. Their role in human cognition has been predominantly studied in classical gamma frequencies (30-100Hz), which reflect neuronal network coordination involved in attention, learning and memory. Invasive brain recordings in animals and humans demonstrate that physiological oscillations extend beyond the gamma frequency range, but their function in human cognitive processing has not been fully elucidated. Methods: We investigated  high frequency oscillations spanning the high gamma (50-125Hz), ripple (125-250Hz) and fast ripple (250-500Hz) frequency bands using intracranial recordings from twelve patients (five males and seven females, age 21-63 years) during memory encoding and recall of a series of affectively charged images. Significant power increases in the gamma, ripple and fast ripple bands were detected using a Hilbert transform-based method and corroborated with a multi-taper Fast Fourier Transform analysis (for more details see Kucewicz et al., Brain 2014). Individual detections of high frequency oscillations were characterized in terms of peak amplitude, frequency, duration and latency from image presentation, and quantified during the encoding and recall trials of the task. Results: Presentation of the images induced high frequency oscillations in all three studied bands within the primary visual, limbic and higher order cortical regions in a sequence consistent with the visual processing stream. These induced oscillations were detected on individual electrodes localized in the amygdala, hippocampus and specific neocortical areas, revealing discrete oscillations of characteristic frequency, duration and latency from image presentation. Memory encoding and recall significantly modulated the number of induced high gamma, ripple and fast ripple detections in the studied structures, which was greater in the primary sensory areas during the encoding (Wilcoxon rank sum test, P = 0.002) and in the higher-order cortical association areas during the recall (Wilcoxon rank sum test, P = 0.001) of memorized images. Furthermore, the induced high gamma, ripple and fast ripple responses discriminated the encoded and the affectively charged images. Conclusions: In summary, our results show that high frequency oscillations, spanning a wide range of frequencies, are associated with memory processing and generated along distributed cortical and limbic brain regions. These findings support an important role for fast network synchronization in human cognition and extend our understanding of normal physiological brain activity during memory processing.