Abstract
Human High-Frequency-Oscillations (HFO) in the ripple band are oscillatory brain activity in the frequency range between 80 and 250 Hz. HFOs may comprise different subgroups that either play a role in physiologic or pathologic brain functions. An exact differentiation between physiologic and pathologic HFOs would help elucidate their relevance for cognitive and epileptogenic brain mechanisms, but the criteria for differentiating between physiologic and pathologic HFOs remain controversial. In particular, the separation of pathologic HFOs from physiologic HFOs could improve the identification of epileptogenic brain regions during the pre-surgical evaluation of epilepsy patients. In this study, we performed intracranial electroencephalography recordings from the hippocampus of epilepsy patients before, during, and after the patients completed a spatial navigation task. We isolated hippocampal ripples from the recordings and categorized the ripples into the putative pathologic group iesRipples, when they coincided with interictal spikes, and the putative physiologic group isolRipples, when they did not coincide with interictal spikes. We found that the occurrence of isolRipples significantly decreased during the task as compared to periods before and after the task. The rate of iesRipples was not modulated by the task. In patients who completed the spatial navigation task on two consecutive days, we furthermore examined the occurrence of ripples in the intervening night. We found that the rate of ripples that coincided with sleep spindles and were therefore putatively physiologic correlated with the performance improvement on the spatial navigation task, whereas the rate of all ripples did not show this relationship. Together, our results suggest that the differentiation of HFOs into putative physiologic and pathologic subgroups may help identify their role for spatial memory and memory consolidation processes. Conversely, excluding putative physiologic HFOs from putative pathologic HFOs may improve the HFO-based identification of epileptogenic brain regions in future studies.
Highlights
High Frequency Oscillations (HFO) are an electrographic manifestation of hyper-synchronized neurons and are subdivided into Ripples and Fast-Ripples according to the frequency range of the oscillations (80–250 and 250–500 Hz, respectively) [1, 2]
In the subgroup of the 9 patients conducting the paradigm on two consecutive days, the maximum, minimum and mean performance on day 1 corresponded to 86%, 48%
We presented evidence supporting the role of sleep spindle-coincident ripples in memory consolidation processes, which may contribute to better understand the neural interactions allowing the storage of newly acquired information in the brain
Summary
High Frequency Oscillations (HFO) are an electrographic manifestation of hyper-synchronized neurons and are subdivided into Ripples and Fast-Ripples according to the frequency range of the oscillations (80–250 and 250–500 Hz, respectively) [1, 2]. In the field of epilepsy, Ripples and Fast-Ripples were initially considered improved biomarkers of epileptogenic networks [3,4,5,6,7,8]. Recent research has drawn a more complex picture [9,10,11] and has highlighted the importance of being able to differentiate between physiologic and pathologic HFOs. Interictal Epileptic Spikes (IES) are another type of epileptic biomarker. IES are common in patients with epilepsy, have a waveform of a fast transient, are commonly generated in epileptic cortex and reflect a hyper-excitability of neural networks [12]
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