An electronic neuromorphic system for real-time detection of high frequency oscillations (HFO) in intracranial EEG.
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ABSTRACT:
SUBMITTER: Sharifshazileh M
PROVIDER: S-EPMC8149394 | biostudies-literature | 2021 May
REPOSITORIES: biostudies-literature
Publications
An electronic neuromorphic system for real-time detection of high frequency oscillations (HFO) in intracranial EEG.
Sharifshazileh Mohammadali M Burelo Karla K Sarnthein Johannes J Indiveri Giacomo G
Nature communications 20210525 1
The analysis of biomedical signals for clinical studies and therapeutic applications can benefit from embedded devices that can process these signals locally and in real-time. An example is the analysis of intracranial EEG (iEEG) from epilepsy patients for the detection of High Frequency Oscillations (HFO), which are a biomarker for epileptogenic brain tissue. Mixed-signal neuromorphic circuits offer the possibility of building compact and low-power neural network processing systems that can ana ...[more]
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Project description:Interictal high-frequency oscillations (HFO) detected in electroencephalography recordings have been proposed as biomarkers of epileptogenesis, seizure propensity, disease severity, and treatment response. Automatic HFO detectors typically analyze the data offline using complex time-consuming algorithms, which limits their clinical application. Neuromorphic circuits offer the possibility of building compact and low-power processing systems that can analyze data on-line and in real time. In this review, we describe a fully automated detection pipeline for HFO that uses, for the first time, spiking neural networks and neuromorphic technology. We demonstrated that our HFO detection pipeline can be applied to recordings from different modalities (intracranial electroencephalography, electrocorticography, and scalp electroencephalography) and validated its operation in a custom-designed neuromorphic processor. Our HFO detection approach resulted in high accuracy and specificity in the prediction of seizure outcome in patients implanted with intracranial electroencephalography and electrocorticography, and in the prediction of epilepsy severity in patients recorded with scalp electroencephalography. Our research provides a further step toward the real-time detection of HFO using compact and low-power neuromorphic devices. The real-time detection of HFO in the operation room may improve the seizure outcome of epilepsy surgery, while the use of our neuromorphic processor for non-invasive therapy monitoring might allow for more effective medication strategies to achieve seizure control. Therefore, this work has the potential to improve the quality of life in patients with epilepsy by improving epilepsy diagnostics and treatment.
| S-EPMC9205405 | biostudies-literature
Project description:The rate of interictal high frequency oscillations (HFOs) is a promising biomarker of the seizure onset zone, though little is known about its consistency over hours to days. Here we test whether the highest HFO-rate channels are consistent across different 10-min segments of EEG during sleep. An automated HFO detector and blind source separation are applied to nearly 3000 total hours of data from 121 subjects, including 12 control subjects without epilepsy. Although interictal HFOs are significantly correlated with the seizure onset zone, the precise localization is consistent in only 22% of patients. The remaining patients either have one intermittent source (16%), different sources varying over time (45%), or insufficient HFOs (17%). Multiple HFO networks are found in patients with both one and multiple seizure foci. These results indicate that robust HFO interpretation requires prolonged analysis in context with other clinical data, rather than isolated review of short data segments.
| S-EPMC5984620 | biostudies-literature
Project description: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.
| S-EPMC7971186 | biostudies-literature
Project description:ObjectiveHigh-frequency oscillations (HFOs) are a promising biomarker for the epileptogenic zone. However, no physiological definition of an HFO has been established, so detection relies on the empirical definition of an HFO derived from visual observation. This can bias estimates of HFO features such as amplitude and duration, thereby hindering their utility as biomarkers. Therefore, we set out to develop an algorithm that detects high-frequency events in the intracranial EEG that are morphologically distinct from background without requiring assumptions about event amplitude or shape.MethodWe propose the anomaly detection algorithm (ADA), which uses unsupervised machine learning to identify segments of data that are distinct from the background. We apply ADA and a standard HFO detector using a root mean square amplitude threshold to intracranial EEG from 11 patients undergoing evaluation for epilepsy surgery. The rate, amplitude, and duration of the detected events and the percent overlap between the two detectors are compared.ResultIn the seizure onset zone (SOZ), ADA detected a subset of conventional HFOs. In non-SOZ channels, ADA detected at least twice as many events as the standard approach, including some conventional HFOs; however, ADA also identified many low and intermediate amplitude events missed by the standard amplitude-based method. The rate of ADA events was similar across all channels; however, the amplitude of ADA events was significantly higher in SOZ channels (P < .0045), and the amplitude measurement was more stable over time than the HFO rate, as indicated by a lower coefficient of variation (P < .0125).SignificanceADA does not require human supervision, parameter optimization, or prior assumptions about event shape, amplitude, or duration. Our results suggest that the algorithm's estimate of event amplitude may differentiate SOZ and non-SOZ channels. Further studies will examine the utility of HFO amplitude as a biomarker for epilepsy surgical outcome.
| S-EPMC7278560 | biostudies-literature
Project description:High-frequency oscillations >80 Hz (HFOs) have unique features distinguishing them from spikes and artifactual components that can be well-evidenced in the time-frequency representations. We introduce an unsupervised HFO detector that uses computer-vision algorithms to detect HFO landmarks on two-dimensional (2D) time-frequency maps. To validate the detector, we introduce an analytical model of the HFO based on a sinewave having a Gaussian envelope, for which analytical equations in time-frequency space can be derived, allowing us to establish a direct correspondence between common HFO detection criteria in the time domain with the ones in the frequency domain, used by the computer-vision detection algorithm. The detector identifies potential HFO events on the time-frequency representation, which are classified as true HFOs if criteria regarding the HFO's frequency, amplitude, and duration are met. The detector is validated on simulated HFOs according to the analytical model, in the presence of noise, with different signal-to-noise ratios (SNRs) ranging from -9 to 0 dB. The detector's sensitivity was 0.64 at an SNR of -9 dB, 0.98 at -6 dB, and >0.99 at -3 dB and 0 dB, while its positive prediction value was >0.95, regardless of the SNR. Using the same simulation dataset, our detector is benchmarked against four previously published HFO detectors. The F-measure, a combined metric that takes into account both sensitivity and positive prediction value, was used to compare detection algorithms. Our detector surpassed the other detectors at -6, -3, and 0 dB and had the second best F-score at -9 dB SNR after the MNI detector (0.77 vs. 0.83). The ability to detect HFOs in clinical recordings has been tested on a set of 36 intracranial electroencephalogram (EEG) channels in six patients, with 89% of the detections being validated by two independent reviewers. The results demonstrate that the unsupervised detection of HFOs based on their 2D features in time-frequency maps is feasible and has a performance comparable or better than the most used HFO detectors.
| S-EPMC7104802 | biostudies-literature
Project description:Electrical stimulation (ES) is used during intracranial electroencephalography (EEG) investigations to delineate epileptogenic areas and seizure-onset zones (SOZs) by provoking afterdischarges (ADs) or patients' typical seizure. High frequency oscillations (HFOs--ripples, 80-250 Hz; fast ripples, 250-500 Hz) are linked to seizure onset. This study investigates whether interictal HFOs are more frequent in areas with a low threshold to provoke ADs or seizures.Intracranial EEG studies were filtered at 500 Hz and sampled at 2,000 Hz. HFOs were visually identified. Twenty patients underwent ES, with gradually increasing currents. Results were interpreted as agreeing or disagreeing with the intracranial study (clinical-EEG seizure onset defined the SOZ). Current thresholds provoking an AD or seizure were correlated with the rate of HFOs of each channel.ES provoked a seizure in 12 and ADs in 19 patients. Sixteen patients showed an ES response inside the SOZ, and 10 had additional areas with ADs. The response was more specific for mesiotemporal than for neocortical channels. HFO rates were negatively correlated with thresholds for ES responses; especially in neocortical regions; areas with low threshold and high HFO rate were colocalized even outside the SOZ.Areas showing epileptic HFOs colocalize with those reacting to ES. HFOs may represent a pathologic correlate of regions showing an ES response; both phenomena suggest a more widespread epileptogenicity.
| S-EPMC3775780 | biostudies-literature
Project description:Objective.High-frequency oscillations (HFOs) are considered a biomarker of the epileptogenic zone in intracranial EEG recordings. However, automated HFO detectors confound true oscillations with spurious events caused by the presence of artifacts.Approach.We hypothesized that, unlike pseudo-HFOs with sharp transients or arbitrary shapes, real HFOs have a signal characteristic that can be represented using a small number of oscillatory bases. Based on this hypothesis using a sparse representation framework, this study introduces a new classification approach to distinguish true HFOs from the pseudo-events that mislead seizure onset zone (SOZ) localization. Moreover, we further classified the HFOs into ripples and fast ripples by introducing an adaptive reconstruction scheme using sparse representation. By visualizing the raw waveforms and time-frequency representation of events recorded from 16 patients, three experts labeled 6400 candidate events that passed an initial amplitude-threshold-based HFO detector. We formed a redundant analytical multiscale dictionary built from smooth oscillatory Gabor atoms and represented each event with orthogonal matching pursuit by using a small number of dictionary elements. We used the approximation error and residual signal at each iteration to extract features that can distinguish the HFOs from any type of artifact regardless of their corresponding source. We validated our model on sixteen subjects with thirty minutes of continuous interictal intracranial EEG recording from each.Main results.We showed that the accuracy of SOZ detection after applying our method was significantly improved. In particular, we achieved a 96.65% classification accuracy in labeled events and a 17.57% improvement in SOZ detection on continuous data. Our sparse representation framework can also distinguish between ripples and fast ripples.Significance.We show that by using a sparse representation approach we can remove the pseudo-HFOs from the pool of events and improve the reliability of detected HFOs in large data sets and minimize manual artifact elimination.
| S-EPMC9901915 | biostudies-literature
Project description:BackgroundApproaches to predictably control neural oscillations are needed to understand their causal role in brain function in healthy or diseased states and to advance the development of neuromodulation therapies.ObjectiveWe present a closed-loop neural control and optimization framework to actively suppress or amplify low-frequency neural oscillations observed in local field potentials in real-time by using electrical stimulation. The rationale behind this control approach and our working hypothesis is that neural oscillatory activity evoked by electrical pulses can suppress or amplify spontaneous oscillations via destructive or constructive interference when the pulses are continuously delivered with appropriate amplitudes and at precise phases of the modulated oscillations in a closed-loop scheme.MethodsWe tested our hypothesis in two nonhuman primates that exhibited a robust increase in low-frequency (8-30 Hz) oscillatory power in the subthalamic nucleus (STN) following administration of the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). To test our neural control approach, we targeted 8-17 Hz oscillations and used electrode arrays and electrical stimulation waveforms similar to those used in humans chronically implanted with brain stimulation systems. Stimulation parameters that maximize the suppression or amplification of neural oscillations were predicted using mathematical models of the stimulation evoked oscillations.ResultsOur neural control and optimization approach was capable of actively and robustly suppressing or amplifying oscillations in the targeted frequency band (8-17 Hz) in real-time in the studied subjects.ConclusionsThe results from this study support our hypothesis and suggest that the proposed neural control framework allows one to characterize in controlled experiments the functional role of frequency-specific neural oscillations by using electrodes and stimulation waveforms currently being employed in humans.
| S-EPMC7722151 | biostudies-literature
Project description:This work presents the first simulation of a large-scale, bio-physically constrained cerebellum model performed on neuromorphic hardware. A model containing 97,000 neurons and 4.2 million synapses is simulated on the SpiNNaker neuromorphic system. Results are validated against a baseline simulation of the same model executed with NEST, a popular spiking neural network simulator using generic computational resources and double precision floating point arithmetic. Individual cell and network-level spiking activity is validated in terms of average spike rates, relative lead or lag of spike times, and membrane potential dynamics of individual neurons, and SpiNNaker is shown to produce results in agreement with NEST. Once validated, the model is used to investigate how to accelerate the simulation speed of the network on the SpiNNaker system, with the future goal of creating a real-time neuromorphic cerebellum. Through detailed communication profiling, peak network activity is identified as one of the main challenges for simulation speed-up. Propagation of spiking activity through the network is measured, and will inform the future development of accelerated execution strategies for cerebellum models on neuromorphic hardware. The large ratio of granule cells to other cell types in the model results in high levels of activity converging onto few cells, with those cells having relatively larger time costs associated with the processing of communication. Organizing cells on SpiNNaker in accordance with their spatial position is shown to reduce the peak communication load by 41%. It is hoped that these insights, together with alternative parallelization strategies, will pave the way for real-time execution of large-scale, bio-physically constrained cerebellum models on SpiNNaker. This in turn will enable exploration of cerebellum-inspired controllers for neurorobotic applications, and execution of extended duration simulations over timescales that would currently be prohibitive using conventional computational platforms.
| S-EPMC8202688 | biostudies-literature
Project description:High-frequency oscillations (HFO) are promising EEG biomarkers of epileptogenicity. While the evidence supporting their significance derives mainly from invasive recordings, recent studies have extended these observations to HFO recorded in the widely accessible scalp EEG. Here, we investigated whether scalp HFO in drug-resistant focal epilepsy correspond to epilepsy severity and how they are affected by surgical therapy. In eleven children with drug-resistant focal epilepsy that underwent epilepsy surgery, we prospectively recorded pre- and postsurgical scalp EEG with a custom-made low-noise amplifier (LNA). In four of these children, we also recorded intraoperative electrocorticography (ECoG). To detect clinically relevant HFO, we applied a previously validated automated detector. Scalp HFO rates showed a significant positive correlation with seizure frequency (R2?=?0.80, p?<?0.001). Overall, scalp HFO rates were higher in patients with active epilepsy (19 recordings, p?=?0.0066, PPV?=?86%, NPV?=?80%, accuracy?=?84% CI [62% 94%]) and decreased following successful epilepsy surgery. The location of the highest HFO rates in scalp EEG matched the location of the highest HFO rates in ECoG. This study is the first step towards using non-invasively recorded scalp HFO to monitor disease severity in patients affected by epilepsy.
| S-EPMC6851354 | biostudies-literature