Negative effects of interictal spikes on theta rhythm in human temporal lobe epilepsy

Fu, Xiaoxuan; Wang, Youhua; Ge, Manling; Wang, Danhong; Gao, Rongguang; Wang, Long; Guo, Jundan; Liu, Hesheng

doi:10.1016/j.yebeh.2018.07.014

Cited by 20 publications

(16 citation statements)

References 43 publications

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“…Even though running speed was consistent around the time of the pHFO (median speed change from baseline to before the pHFO 0 cm/s; IQR −2–3 cm/s; from baseline to after the pHFO, 0 cm/s; IQR −3–3 cm/s), LFP recorded in stratum radiatum was characterized by robust theta oscillations leading up to the pHFO (median power change between baseline and the period immediately preceding the pHFO, 10.9 μV 2 ; IQR, −51.5–74.6 μV 2 , n.s., p = 0.08, z-value = 1.6, Wilcoxon signed rank test) followed by a transient suppression of theta oscillations for several hundred ms after the event (median reduction from baseline, 98.0 μV 2 ; IQR, 21.3–206.2 μV 2 , p = 4.7×10 −29 , z-value = 11.2, Wilcoxon signed rank test) (Figure 3C & D). These results are consistent with previous reports that observe theta suppression after interictal spikes in humans (Fu et al, 2018). Indeed, in stratum radiatum, the most prominent feature of the interictal event is the interictal spike, consistent with the notion that the interictal spike/pHFO complex also suppresses theta in the rat model.…”

Section: Resultssupporting

confidence: 94%

The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy

Ewell

Fischer

Leibold

et al. 2019

eLife

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In epilepsy, brain networks generate pathological high-frequency oscillations (pHFOs) during interictal periods. To understand how pHFOs differ from normal oscillations in overlapping frequency bands and potentially perturb hippocampal processing, we performed high-density single unit and local field potential recordings from hippocampi of behaving rats with and without chronic epilepsy. In epileptic animals, we observed two types of co-occurring fast oscillations, which by comparison to control animals we could classify as ‘ripple-like’ or ‘pHFO’. We compared their spectral characteristics, brain state dependence, and cellular participants. Strikingly, pHFO occurred irrespective of brain state, were associated with interictal spikes, engaged distinct subnetworks of principal neurons compared to ripple-like events, increased the sparsity of network activity, and initiated both general and immediate disruptions in spatial information coding. Taken together, our findings suggest that events that result in pHFOs have an immediate impact on memory processes, corroborating the need for proper classification of pHFOs to facilitate therapeutic interventions that selectively target pathological activity.

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Section: Resultssupporting

confidence: 94%

The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy

Ewell

Fischer

Leibold

et al. 2019

eLife

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“…15,16 Similarly, interictal spikes also suppress theta rhythms in the human hippocampus. 17 Interictal spikes often (but not always) co-occur with pHFA. 10 Thus, it is likely that pHFA in humans is also disrupting theta rhythms and impairing performance on memory tasks.…”

Section: Commentarymentioning

confidence: 99%

Ripple While You Walk, and You May Get Lost: Pathological High-Frequency Activity Can Alter Spatial Navigation Circuits

Brennan¹,

Ahmed²

2019

Epilepsy Curr

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The Impact of Pathological High-frequency Oscillations on Hippocampal Network Activity in Rats With Chronic Epilepsy. Ewell LA, Fischer KB, Leibold C, Leutgeb S, Leutgeb JK. eLIFE. 2019;8:pii: e42148. doi: 10.7554/eLife.42148. PMID: 30794155 In epilepsy, brain networks generate pathological high-frequency oscillations (pHFOs) during interictal periods. To understand how pHFOs differ from normal oscillations in overlapping frequency bands and potentially perturb hippocampal processing, we performed high-density single unit and local field potential recordings from hippocampi of behaving rats with and without chronic epilepsy. In epileptic animals, we observed 2 types of co-occurring fast oscillations that by comparison to control animals could be classified as “ripple-like” or “pHFO.” We compared their spectral characteristics, brain state dependence, and cellular participants. Strikingly, pHFO occurred irrespective of brain state, were associated with interictal spikes, engaged distinct subnetworks of principal neurons compared to ripple-like events, increased the sparsity of network activity, and initiated both general and immediate disruptions in spatial information coding. Taken together, our findings suggest that events that result in pHFOs have an immediate impact on memory processes, corroborating the need for proper classification of pHFOs to facilitate therapeutic interventions that selectively target pathological activity.

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“…Emerging from our experiments we can conclude that the emotional disturbances can be considered as the emergence of instinctive behavior with an adaptive significance of defence and as a by-product of the inhibitory processes that build-up to protect against the future occurrence of seizures, that gives support that interictal spikes have a significant negative impact on theta rhythm in human temporal lobe epilepsy [10]. Therefore, seizure-Theta antagonism in our experiments could be interpreted as an adjustment of the inhibitory mechanisms when the theta rhythm is evoked.…”

Section: Discussionmentioning

confidence: 52%

Interaction between Seizure and Theta Rhythm

Nanobashvili¹,

Bilanishvili²,

Barbakadze³

et al. 2020

JBBS

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Recently it was shown by us that combined stimulation of hippocampus and dorsomedial hypothalamus resulted in suppression of the electroencephalographic seizure reactions and, respectively, manifestations of behavioral seizures reduced. It is expected, that augmentation of inhibitory processes in hippocampal neurons in the course of dorsomedial hypothalamus stimulation can trigger mechanisms preventing the development of epileptiform activity. Because of two important characteristics of the hippocampus-theta rhythm and epileptogenesis-these appear to be interrelated in respect of their cellular substrates, and as far as theta rhythm may modulate hippocampal excitability, a study of the functional relationship between theta rhythm and seizure activity was endeavored. The purpose of this study is to test this proposal by determining the effects on seizures of induction or suppression of hippocampal theta activity. Our findings show that: 1) against background of strong unusual sound stimulation (in our case-sound) blockade of local seizure reactions induced by hippocampal stimulation occurred; 2) the frequency of hippocampal interictal epileptiform dischargers increased with the transition from the awake state to drowsiness and a slow-wave sleep phase. After the animal came from slow-wave sleep to paradoxical sleep, epileptiform activity completely disappeared; 3) at threshold stimulation of hypothalamus when electrohippocampogram shows augmentation of the theta rhythm there is a significant reduction of seizure durations. When at hypothalamus stimulation instead of theta rhythm the electrical activity is desynchronized, there occurs a considerable intensification of seizure activity. Therefore, seizure-theta antagonism in our experiments could be interpreted as an adjustment of the inhibitory mechanisms when the theta rhythm is evoked.

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Negative effects of interictal spikes on theta rhythm in human temporal lobe epilepsy

Cited by 20 publications

References 43 publications

The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy

The impact of pathological high-frequency oscillations on hippocampal network activity in rats with chronic epilepsy

Ripple While You Walk, and You May Get Lost: Pathological High-Frequency Activity Can Alter Spatial Navigation Circuits

Interaction between Seizure and Theta Rhythm

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