High frequency oscillations are associated with cognitive processing in human recognition memory

Abstract

High frequency oscillations are associated with normal brain function, but also increasingly recognized as potential biomarkers of the epileptogenic brain. Their role in human cognition has been predominantly studied in classical gamma frequencies (30-100 Hz), 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. Here we investigate high frequency oscillations spanning the high gamma (50-125 Hz), ripple (125-250 Hz) and fast ripple (250-500 Hz) frequency bands using intracranial recordings from 12 patients (five males and seven females, age 21-63 years) during memory encoding and recall of a series of affectively charged images. 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. 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.

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

“…5 The relationship between network activity and IEDs has recently been applied to study the effect of cognitively induced oscillations on IED suppression, 9 opening a possibility for treating interictal pathophysiology. Further research will show whether the gamma-IEDs, physiological HFOs associated with normal function, 10 and seizures share common network processes and thus drive new treatments and therapeutic strategies.…”

A study on spike focus dependence of high‐frequency activity in idiopathic focal epilepsy in childhood

“…It is known that the primary sensory area and the occipital cortex generate physiological HFOs 28, 29. Therefore, it is possible that epileptic HFA/HFOs are prone to be detected from these regions as in the case of physiological ones.…”

High frequency oscillations are less frequent but more specific to epileptogenicity during rapid eye movement sleep

“…In this study, the non-epileptogenic zone was defined as areas outside the resection, anatomical epileptogenic lesion, eloquent cortex, hippocampus, and interictal spike zone in patients with seizure freedom after surgery. Physiological HFOs are more detectable in eloquent cortex and hippocampus (Hashimoto, 2000;Girardeau and Zugaro, 2011;Kucewicz et al, 2014). A total of 196 electrodes were located in the non-epileptogenic zone in four patients with postoperative seizure freedom (40-63 electrodes per patient).…”

“…For example, hippocampal ripples are important in memory consolidation (Girardeau and Zugaro, 2011). Memory processing is associated with HFOs distributed over the amygdala, hippocampus and specific neocortical areas in humans (Kucewicz et al, 2014). HFOs can be evoked by visual stimuli in the occipital cortex (Nagasawa et al, 2012) and by somatosensory stimuli in the somatosensory cortex (Hashimoto, 2000).…”