Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy

Cimbálník, Jan; Pail, Martin; Klimeš, Petr; Travnicek, Vojtech; Román, Róbert; Vajčner, Adam; Brázdil, Milan

doi:10.3389/fneur.2020.578571

Cited by 9 publications

(18 citation statements)

References 39 publications

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“…Our analysis was focused on the hippocampus, as it plays a major role for both spatial navigation (24)(25)(26)(27)(28)(29)(30) and declarative memory formation (43)(44)(45)(46)(47)(48)(49)(50) and is a candidate region for generating epileptic activity (51,52) and is therefore often assessed for the decision making and planning for surgical epilepsy therapy.…”

Section: Discussionmentioning

confidence: 99%

“…Numerous publications have reported, for both the human and non-human brain, on the occurrence of Ripples during wakefulness and while conducting cognitive tasks ( 43 – 50 ); despite this, to our knowledge, only the studies from ( 47 ) and those from the Brázdil1 group ( 48 – 50 ), have analyzed the effects of cognitive processes on the activity of putatively physiologic and putatively pathologic Ripples during the awake state and in humans. The study from ( 50 ) presents the largest patient cohort with 36 patients and will thus be considered for further discussion. This study explored if the effect of cognitive load in the form of different tasks (visual oddball, Go/NoGo, Ultimatum Game, Mismatch Negativity) on putative-pathologic ripples (i.e., ripples from epileptic hippocampi, hereinafter referenced as pathoBrazRipples ) differed from the effect on putative-physiologic ripples (i.e., from non-epileptic hippocampi, hereinafter referred to as physioBrazRipples ).…”

Section: Discussionmentioning

confidence: 99%

“…Numerous publications have reported, for both the human and non-human brain, on the occurrence of Ripples during wakefulness and while conducting cognitive tasks (43)(44)(45)(46)(47)(48)(49)(50); despite this, to our knowledge, only the studies from (47) and those from the Brázdil1 group (48)(49)(50), have analyzed the effects of cognitive processes on the activity of putatively physiologic and putatively pathologic Ripples during the awake state and in humans. The study from (50) presents the largest patient cohort with 36 patients and will thus be considered for further discussion.…”

Section: Differentiation Of Pathologic and Physiologic Ripplesmentioning

confidence: 99%

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Effects of Spatial Memory Processing on Hippocampal Ripples

et al. 2021

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Differentiation Of Pathologic and Physiologic Ripplesmentioning

confidence: 99%

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Effects of Spatial Memory Processing on Hippocampal Ripples

et al. 2021

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“…How can this null-result be reconciled with the finding of physiological HFOs reported in other studies? Some studies use cognitive tasks and define as HFOs those oscillations in the HFO frequency band that are modulated by cognitive processing (Axmacher et al, 2008 ; Kucewicz et al, 2014 ; Jacobs et al, 2016 ; Cimbalnik et al, 2018 , 2020 ; Arnulfo et al, 2020 ; Pail et al, 2020 ). These findings are in discrepancy with our null result, where we found no evidence for rate modulation of FRandRs by the cognitive tasks.…”

Section: Discussionmentioning

confidence: 99%

“…Unfortunately, different studies use the term “HFO” for different phenomena (Noorlag et al, 2019 ). The distinction between a physiological HFO and an epileptic HFO, which indicates the EZ, is a matter of ongoing research (Cimbalnik et al, 2018 , 2020 ; Frauscher et al, 2018 ; Weiss et al, 2019 , 2020 ; Arnulfo et al, 2020 ; Gliske et al, 2020 ; Pail et al, 2020 ). Can an epileptic HFO be confounded with a physiological HFO?…”

Section: Introductionmentioning

confidence: 99%

Epileptic High-Frequency Oscillations in Intracranial EEG Are Not Confounded by Cognitive Tasks

Boran

Stieglitz

Sarnthein

2021

Front. Hum. Neurosci.

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Rationale: High-frequency oscillations (HFOs) in intracranial EEG (iEEG) are used to delineate the epileptogenic zone during presurgical diagnostic assessment in patients with epilepsy. HFOs are historically divided into ripples (80–250 Hz), fast ripples (FR, >250 Hz), and their co-occurrence (FRandR). In a previous study, we had validated the rate of FRandRs during deep sleep to predict seizure outcome. Here, we ask whether epileptic FRandRs might be confounded by physiological FRandRs that are unrelated to epilepsy.Methods: We recorded iEEG in the medial temporal lobe MTL (hippocampus, entorhinal cortex, and amygdala) in 17 patients while they performed cognitive tasks. The three cognitive tasks addressed verbal working memory, visual working memory, and emotional processing. In our previous studies, these tasks activated the MTL. We re-analyzed the data of these studies with the automated detector that focuses on the co-occurrence of ripples and FRs (FRandR).Results: For each task, we identified those channels in which the HFO rate was modulated during the task condition compared to the control condition. However, the number of these channels did not exceed the chance level. Interestingly, even during wakefulness, the HFO rate was higher for channels within the seizure onset zone (SOZ) than for channels outside the SOZ.Conclusion: Our prospective definition of an epileptic HFO, the FRandR, is not confounded by physiological HFOs that might be elicited by our cognitive tasks. This is reassuring for the clinical use of FRandR as a biomarker of the EZ.

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