High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery.
TL;DR: This work investigated whether HFOs can delineate epileptogenic areas even outside the SOZ by correlating the resection of HFO‐generating areas with surgical outcome.
Abstract: Thirty percent to 40% of patients with focal epilepsy are medically intractable,1 and for some, surgical removal of epileptogenic areas is the best option to gain seizure freedom. Intracranial electroencephalographic (iEEG) investigations are indicated for patients in whom noninvasive methods fail to identify a single focal seizure generator.2
iEEG is used to define the seizure onset zone (SOZ).3 Removal of the SOZ alone, however, does not always predict the surgical benefit.4,5 It is uncertain whether the outcome can be improved by removing areas of interictal spiking, often more widespread than the SOZ.6,7 Intracranial studies also have limitations, as their results depend on electrode location and type of implantation (intracortical vs subdural). For instance, iEEG electrodes only record neuronal activity in their direct vicinity and are blind for other areas,8 making it hard to judge whether the activity at seizure onset really represents the seizure generator or is the result of propagation from else-where. Thus the actual focus and its extent may be missed, leading to unsuccessful surgery.
Microelectrode-recorded high-frequency oscillations (HFOs), ripples (80 –250Hz), and fast ripples (FRs, 250 –500Hz), were found predominantly in epileptogenic tissue.9 –11 They can also be recorded with macroelectrodes during clinical iEEG investigation.12,13 HFOs were more specific in indicating the SOZ than spikes.14 Additionally, they were linked to the SOZ independently of the underlying lesion and were infrequent in lesional areas outside the SOZ.15 Evidence therefore suggests that HFOs are good markers of epileptic tissue and may help to identify epileptogenic areas. We hypothesize that removing areas generating HFOs results in good surgical outcome. The correlation between removal of HFO-generating areas and seizure outcome was compared to that coming from spikes and to the current gold standard, removing the SOZ.
Citations
More filters
TL;DR: Alteration of the physiological mechanisms supporting SPW‐Rs leads to their pathological conversion, “p‐ripples,” which are a marker of epileptogenic tissue and can be observed in rodent models of schizophrenia and Alzheimer's Disease.
Abstract: Sharp wave ripples (SPW-Rs) represent the most synchronous population pattern in the mammalian brain. Their excitatory output affects a wide area of the cortex and several subcortical nuclei. SPW-Rs occur during "off-line" states of the brain, associated with consummatory behaviors and non-REM sleep, and are influenced by numerous neurotransmitters and neuromodulators. They arise from the excitatory recurrent system of the CA3 region and the SPW-induced excitation brings about a fast network oscillation (ripple) in CA1. The spike content of SPW-Rs is temporally and spatially coordinated by a consortium of interneurons to replay fragments of waking neuronal sequences in a compressed format. SPW-Rs assist in transferring this compressed hippocampal representation to distributed circuits to support memory consolidation; selective disruption of SPW-Rs interferes with memory. Recently acquired and pre-existing information are combined during SPW-R replay to influence decisions, plan actions and, potentially, allow for creative thoughts. In addition to the widely studied contribution to memory, SPW-Rs may also affect endocrine function via activation of hypothalamic circuits. Alteration of the physiological mechanisms supporting SPW-Rs leads to their pathological conversion, "p-ripples," which are a marker of epileptogenic tissue and can be observed in rodent models of schizophrenia and Alzheimer's Disease. Mechanisms for SPW-R genesis and function are discussed in this review.
1,173 citations
TL;DR: The lives of most people with epilepsy continue to be adversely affected by gaps in knowledge, diagnosis, treatment, advocacy, education, legislation, and research and Concerted actions to address these challenges are urgently needed.
674 citations
TL;DR: In this review, the spectral, spatial, and temporal characteristics of muscle artifacts are compared with those described (so far) for high-frequency neural activity and several of the techniques that are being developed to help suppress muscle artifacts in MEG/EEG are reviewed.
Abstract: In recent years high-frequency brain activity in the gamma-frequency band (30–80 Hz) and above has become the focus of a growing body of work in MEG/EEG research. Unfortunately, high-frequency neural activity overlaps entirely with the spectral bandwidth of muscle activity (~20–300 Hz). It is becoming appreciated that artifacts of muscle activity may contaminate a number of non-invasive reports of high-frequency activity. In this review, the spectral, spatial, and temporal characteristics of muscle artifacts are compared with those described (so far) for high-frequency neural activity. In addition, several of the techniques that are being developed to help suppress muscle artifacts in MEG/EEG are reviewed. Suggestions are made for the collection, analysis, and presentation of experimental data with the aim of reducing the number of publications in the future that may contain muscle artifacts.
535 citations
Cites background from "High-frequency electroencephalograp..."
...…because they appear to be generated near the zone of seizure onset (Jacobs et al., 2008; Zijlmans et al., 2009) and because the removal of the areas that generate pathological fast-oscillations have been shown to be a good predictor of surgical outcome (Jacobs et al., 2010; Wu et al., 2010)....
[...]
TL;DR: High‐frequency HFOs appear excellent markers for the epileptogenic zone and show promise for improving surgical outcome and accelerating intracranial EEG investigations, which needs to be assessed by future research.
Abstract: The discovery that electroencephalography (EEG) contains useful information at frequencies above the traditional 80Hz limit has had a profound impact on our understanding of brain function. In epilepsy, high-frequency oscillations (HFOs, >80Hz) have proven particularly important and useful. This literature review describes the morphology, clinical meaning, and pathophysiology of epileptic HFOs. To record HFOs, the intracranial EEG needs to be sampled at least at 2,000Hz. The oscillatory events can be visualized by applying a high-pass filter and increasing the time and amplitude scales, or EEG time-frequency maps can show the amount of high-frequency activity. HFOs appear excellent markers for the epileptogenic zone. In patients with focal epilepsy who can benefit from surgery, invasive EEG is often required to identify the epileptic cortex, but current information is sometimes inadequate. Removal of brain tissue generating HFOs has been related to better postsurgical outcome than removing the seizure onset zone, indicating that HFOs may mark cortex that needs to be removed to achieve seizure control. The pathophysiology of epileptic HFOs is challenging, probably involving populations of neurons firing asynchronously. They differ from physiological HFOs in not being paced by rhythmic inhibitory activity and in their possible origin from population spikes. Their link to the epileptogenic zone argues that their study will teach us much about the pathophysiology of epileptogenesis and ictogenesis. HFOs show promise for improving surgical outcome and accelerating intracranial EEG investigations. Their potential needs to be assessed by future research.
415 citations
TL;DR: Overall, iEEG research on HFA should play an increasing role in cognitive neuroscience in humans, because it can be explicitly linked to basic research in animals, and the future evolution of this field is discussed.
393 citations
Cites background from "High-frequency electroencephalograp..."
..., 2007), and have demonstrated a significant correlation between the resection of regions with epileptiform HFOs and postsurgical seizure-free outcomes (Jacobs et al., 2010; Ochi et al., 2007)....
[...]
References
More filters
TL;DR: A subset of 'observers who demonstrate a high level of interobserver agreement can be identified by using pairwise agreement statistics betweeni each observer and the internal majority standard opinion on each subject.
Abstract: This paper presents a general statistical methodology for the anialysis of mnultivariate categorical data involving agreement among nmore than two observers Since these situations give rise to very large contingency tables in which mi0ost of the observed cell frequencies are zero, procedures based on indicator variables of the raw data for individual subjects are used to genierate first-order margins and main diagonal sums from the conceptual multidinmenisional contingency table From these quantities, estimates are generated to reflect the strenlgth of'an internlal mlajority decision on each subject Moreover, a subset of 'observers who demonstrate a high level of interobserver agreement can be identified by using pairwise agreement statistics betweeni each observer and the internal majority standard opinion on each subject These procedures are all illustrated within the context of'a clinical diagnosis examiiple involving seven pathologists
2,870 citations
01 Jan 1993
2,670 citations
"High-frequency electroencephalograp..." refers methods in this paper
...Surgical outcomes are given according to Engel’ classification.(20) Patient #13 underwent a palliative approach, because his seizure onset was within his speech area....
[...]
TL;DR: The current diagnostic techniques used in the definition of these cortical zones, such as video-EEG monitoring, MRI and ictal single photon emission computed tomography, are discussed and possible future developments that might lead to a more direct definition of the epileptogenic zone are presented.
Abstract: An overview of the following six cortical zones that have been defined in the presurgical evaluation of candidates for epilepsy surgery is given: the symptomatogenic zone; the irritative zone; the seizure onset zone; the epileptogenic lesion; the epileptogenic zone; and the eloquent cortex. The stepwise historical evolution of these different zones is described. The current diagnostic techniques used in the definition of these cortical zones, such as video-EEG monitoring, MRI and ictal single photon emission computed tomography, are discussed. Established diagnostic tests are set apart from procedures that should still be regarded as experimental, such as magnetoencephalography, dipole source localization and spike-triggered functional MRI. Possible future developments that might lead to a more direct definition of the epileptogenic zone are presented.
1,416 citations
"High-frequency electroencephalograp..." refers methods in this paper
...iEEG is used to define the seizure onset zone (SOZ).(3) Removal of the SOZ alone, however, does not always predict the surgical benefit....
[...]
TL;DR: Property of oscillations with frequencies >100 Hz were studied in kainic acid (KA)‐treated rats and compared with those recorded in normal and kindled rats as well as in patients with epilepsy to determine differences associated with epilepsy.
Abstract: Summary: Purpose: Properties of oscillations with frequencies >100 Hz were studied in kainic acid (KA)-treated rats and compared with those recorded in normal and kindled rats as well as in patients with epilepsy to determine differences associated with epilepsy.
Methods: Prolonged in vivo wideband recordings of electrical activity were made in hippocampus and entorhinal cortex (EC) of (a) normal rats, (b) kindled rats, (c) rats having chronic recurrent spontaneous seizures after intrahippocampal KA injections, and (d) patients with epilepsy undergoing depth electrode evaluation in preparation for surgical treatment.
Results: Intermittent oscillatory activity ranging from 100 to 200 Hz in frequency and 50–150 ms in duration was recorded in CA1 and EC of all three animal groups, and in epileptic human hippocampus and EC. This activity had the same characteristics in all groups, resembled previously observed “ripples” described by Buzsaki et al., and appeared to represent field potentials of inhibitory postsynaptic potentials (IPSPs) on principal cells. Unexpectedly, higher frequency intermittent oscillatory activity ranging from 200 to 500 Hz and 10–100 ms in duration was encountered only in KA-treated rats and patients with epilepsy. These oscillations, termed fast ripples (FRs), were found only adjacent to the epileptogenic lesion in hippocampus, EC, and dentate gyrus, and appeared to represent field potential population spikes. Their local origin was indicated by correspondence with the negative phase of burst discharges of putative pyramidal cells.
Conclusions: The persistence of normal-appearing ripples in epileptic brain support the view that inhibitory processes are preserved. FRs appear to be field potentials reflecting hypersynchronous bursting of excitatory neurons and provide an opportunity to study the role of this pathophysiologic phenomenon in epilepsy and seizure initiation. Furthermore, if FR activity is unique to brain areas capable of generating spontaneous seizures, its identification could be a powerful functional indicator of the epileptic region in patients evaluated for surgical treatment.
681 citations
TL;DR: The outcomes of surgery in adults and children with epilepsy are considered and studies of neurological and cognitive sequelae, psychiatric and behavioural outcomes, and overall health-related quality of life are reviewed.
Abstract: Summary Surgery is widely accepted as an effective therapy for selected individuals with medically refractory epilepsy. Numerous studies in the past 20 years have reported seizure freedom for at least 1 year in 53–84% of patients after anteromesial temporal lobe resections for mesial temporal lobe sclerosis, in 66–100% of patients with dual pathology, in 36–76% of patients with localised neocortical epilepsy, and in 43–79% of patients after hemispherectomies. Reported rates for non-resective surgery have been less impressive in terms of seizure freedom; however, the benefit is more apparent when reported in terms of significant seizure reductions. In this Review, we consider the outcomes of surgery in adults and children with epilepsy and review studies of neurological and cognitive sequelae, psychiatric and behavioural outcomes, and overall health-related quality of life.
660 citations
"High-frequency electroencephalograp..." refers background in this paper
...They decrease with antiepileptic medication withdrawal.(24) The weakness of spikes as epileptogenic markers raises the question of whether interictal HFOs are independent enough of spikes to be better markers....
[...]