scholarly journals Dual mechanisms of ictal high frequency oscillations in human rhythmic onset seizures

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Elliot H. Smith ◽  
Edward M. Merricks ◽  
Jyun-You Liou ◽  
Camilla Casadei ◽  
Lucia Melloni ◽  
...  

Abstract High frequency oscillations (HFOs) are bursts of neural activity in the range of 80 Hz or higher, recorded from intracranial electrodes during epileptiform discharges. HFOs are a proposed biomarker of epileptic brain tissue and may also be useful for seizure forecasting. Despite such clinical utility of HFOs, the spatial context and neuronal activity underlying these local field potential (LFP) events remains unclear. We sought to further understand the neuronal correlates of ictal high frequency LFPs using multielectrode array recordings in the human neocortex and mesial temporal lobe during rhythmic onset seizures. These multiscale recordings capture single cell, multiunit, and LFP activity from the human brain. We compare features of multiunit firing and high frequency LFP from microelectrodes and macroelectrodes during ictal discharges in both the seizure core and penumbra (spatial seizure domains defined by multiunit activity patterns). We report differences in spectral features, unit-local field potential coupling, and information theoretic characteristics of high frequency LFP before and after local seizure invasion. Furthermore, we tie these time-domain differences to spatial domains of seizures, showing that penumbral discharges are more broadly distributed and less useful for seizure localization. These results describe the neuronal and synaptic correlates of two types of pathological HFOs in humans and have important implications for clinical interpretation of rhythmic onset seizures.

2020 ◽  
Author(s):  
Elliot H. Smith ◽  
Edward M. Merricks ◽  
Jyun-You Liou ◽  
Camilla Casadei ◽  
Lucia Melloni ◽  
...  

ABSTRACTHigh frequency oscillations (HFOs) recorded from intracranial electrodes during epileptiform discharges are a proposed biomarker of epileptic brain tissue and may also be useful for seizure forecasting, with mixed results. Despite such potential for HFOs, there is limited investigation into the spatial context of HFOs and their relationship to simultaneously recorded neuronal activity. We sought to further understand the biophysical underpinnings of ictal HFOs using unit recordings in the human neocortex and mesial temporal lobe during rhythmic onset seizures. We compare features of ictal discharges in both the seizure core and penumbra (spatial seizure domains defined by multiunit activity patterns). We report differences in spectral features, unit-local field potential coupling, and information theoretic characteristics of HFOs before and after local seizure invasion. Furthermore, we tie these timing-related differences to spatial domains of seizures, showing that penumbral discharges are widely distributed and less useful for seizure localization.


Author(s):  
Elliot H. Smith ◽  
Edward M. Merricks ◽  
Jyun-You Liou ◽  
Camilla Casadei ◽  
Lucia Melloni ◽  
...  

ABSTRACTObjectiveHigh frequency oscillations (HFOs) recorded from intracranial electrodes during epileptiform discharges have been proposed as a biomarker of epileptic brain sites and may also be a useful feature for seizure forecasting, with mixed results. Currently, pathological subclasses of HFOs have been defined primarily by frequency characteristics. Despite this, there has been limited investigation into the spatial context of HFOs with recruitment of local cortex into seizure discharging. We sought to further understand the biophysical underpinnings of ictal HFOs.MethodsHere we examine ictal HFOs from multi-scale electrophysiological recordings during spontaneous human rhythmic onset seizures. We compare features of ictal discharges in both the seizure core and penumbra, as defined by multiunit activity patterns.ResultsWe show marked differences in spectral features, unit coupling, and information theoretic characteristics of HFOs during ictal discharges before and after local seizure invasion. Furthermore, we tie these timing-related differences to different spatial domains of seizures, showing that eccentric, penumbral discharges are widely distributed and less useful for seizure localization, which may explain the variable utility of HFOs in seizure localization and forecasting.InterpretationWe thus identify two distinct classes of ictal HFOs, implying two different mechanisms underlying pathological HFOs with contrasting significance for seizure localization.


2021 ◽  
Author(s):  
Hiroshi Tamura

AbstractNeuron activity in the sensory cortices mainly depends on feedforward thalamic inputs. High-frequency activity of a thalamic input can be temporally integrated by a neuron in the sensory cortex and is likely to induce larger depolarization. However, feedforward inhibition (FFI) and depression of excitatory synaptic transmission in thalamocortical pathways attenuate depolarization induced by the latter part of high-frequency spiking activity and the temporal summation may not be effective. The spiking activity of a thalamic neuron in a specific temporal pattern may circumvent FFI and depression of excitatory synapses. The present study determined the relationship between the temporal pattern of spiking activity of a single thalamic neuron and the degree of cortical activation as well as that between the firing rate of spiking activity of a single thalamic neuron and the degree of cortical activation. Spiking activity of a thalamic neuron was recorded extracellularly from the lateral geniculate nucleus (LGN) in male Long-Evans rats. Degree of cortical activation was assessed by simultaneous recording of local field potential (LFP) from the visual cortex. A specific temporal pattern appearing in three consecutive spikes of an LGN neuron induced larger cortical LFP modulation than high-frequency spiking activity during a short period. These findings indicate that spiking activity of thalamic inputs is integrated by a synaptic mechanism sensitive to an input temporal pattern.Significance StatementSensory cortical activity depends on thalamic inputs. Despite the importance of thalamocortical transmission, how spiking activity of thalamic inputs is integrated by cortical neurons remains unclear. Feedforward inhibition and synaptic depression of excitatory transmission may not allow simple temporal summation of membrane potential induced by consecutive spiking activity of a thalamic neuron. A specific temporal pattern appearing in three consecutive spikes of a thalamic neuron induced larger cortical local field potential modulation than high-frequency spiking activity during a short period. The findings indicate the importance of the temporal pattern of spiking activity of a single thalamic neuron on cortical activation.


2013 ◽  
Vol 133 (8) ◽  
pp. 1493-1500 ◽  
Author(s):  
Ryuji Kano ◽  
Kenichi Usami ◽  
Takahiro Noda ◽  
Tomoyo I. Shiramatsu ◽  
Ryohei Kanzaki ◽  
...  

Sign in / Sign up

Export Citation Format

Share Document