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1. A Deep Learning-Based Real-time Seizure Detection System

   https://doi.org/10.1109/SPMB50085.2020.9353623  

   Shawki, N. ; Elseify, T. ; Cap, T. ; Shah, V. ; Obeid, I. ; Picone, J. ( December 2020 , Proceedings of the IEEE Signal Processing in Medicine and Biology Symposium (SPMB))

   Obeid, Iyad Selesnick (Ed.)

   Electroencephalography (EEG) is a popular clinical monitoring tool used for diagnosing brain-related disorders such as epilepsy [1]. As monitoring EEGs in a critical-care setting is an expensive and tedious task, there is a great interest in developing real-time EEG monitoring tools to improve patient care quality and efficiency [2]. However, clinicians require automatic seizure detection tools that provide decisions with at least 75% sensitivity and less than 1 false alarm (FA) per 24 hours [3]. Some commercial tools recently claim to reach such performance levels, including the Olympic Brainz Monitor [4] and Persyst 14 [5]. In this abstract, we describe our efforts to transform a high-performance offline seizure detection system [3] into a low latency real-time or online seizure detection system. An overview of the system is shown in Figure 1. The main difference between an online versus offline system is that an online system should always be causal and has minimum latency which is often defined by domain experts. The offline system, shown in Figure 2, uses two phases of deep learning models with postprocessing [3]. The channel-based long short term memory (LSTM) model (Phase 1 or P1) processes linear frequency cepstral coefficients (LFCC) [6] features from each EEG channel separately. We use the hypotheses generated by the P1 model and create additional features that carry information about the detected events and their confidence. The P2 model uses these additional features and the LFCC features to learn the temporal and spatial aspects of the EEG signals using a hybrid convolutional neural network (CNN) and LSTM model. Finally, Phase 3 aggregates the results from both P1 and P2 before applying a final postprocessing step. The online system implements Phase 1 by taking advantage of the Linux piping mechanism, multithreading techniques, and multi-core processors. To convert Phase 1 into an online system, we divide the system into five major modules: signal preprocessor, feature extractor, event decoder, postprocessor, and visualizer. The system reads 0.1-second frames from each EEG channel and sends them to the feature extractor and the visualizer. The feature extractor generates LFCC features in real time from the streaming EEG signal. Next, the system computes seizure and background probabilities using a channel-based LSTM model and applies a postprocessor to aggregate the detected events across channels. The system then displays the EEG signal and the decisions simultaneously using a visualization module. The online system uses C++, Python, TensorFlow, and PyQtGraph in its implementation. The online system accepts streamed EEG data sampled at 250 Hz as input. The system begins processing the EEG signal by applying a TCP montage [8]. Depending on the type of the montage, the EEG signal can have either 22 or 20 channels. To enable the online operation, we send 0.1-second (25 samples) length frames from each channel of the streamed EEG signal to the feature extractor and the visualizer. Feature extraction is performed sequentially on each channel. The signal preprocessor writes the sample frames into two streams to facilitate these modules. In the first stream, the feature extractor receives the signals using stdin. In parallel, as a second stream, the visualizer shares a user-defined file with the signal preprocessor. This user-defined file holds raw signal information as a buffer for the visualizer. The signal preprocessor writes into the file while the visualizer reads from it. Reading and writing into the same file poses a challenge. The visualizer can start reading while the signal preprocessor is writing into it. To resolve this issue, we utilize a file locking mechanism in the signal preprocessor and visualizer. Each of the processes temporarily locks the file, performs its operation, releases the lock, and tries to obtain the lock after a waiting period. The file locking mechanism ensures that only one process can access the file by prohibiting other processes from reading or writing while one process is modifying the file [9]. The feature extractor uses circular buffers to save 0.3 seconds or 75 samples from each channel for extracting 0.2-second or 50-sample long center-aligned windows. The module generates 8 absolute LFCC features where the zeroth cepstral coefficient is replaced by a temporal domain energy term. For extracting the rest of the features, three pipelines are used. The differential energy feature is calculated in a 0.9-second absolute feature window with a frame size of 0.1 seconds. The difference between the maximum and minimum temporal energy terms is calculated in this range. Then, the first derivative or the delta features are calculated using another 0.9-second window. Finally, the second derivative or delta-delta features are calculated using a 0.3-second window [6]. The differential energy for the delta-delta features is not included. In total, we extract 26 features from the raw sample windows which add 1.1 seconds of delay to the system. We used the Temple University Hospital Seizure Database (TUSZ) v1.2.1 for developing the online system [10]. The statistics for this dataset are shown in Table 1. A channel-based LSTM model was trained using the features derived from the train set using the online feature extractor module. A window-based normalization technique was applied to those features. In the offline model, we scale features by normalizing using the maximum absolute value of a channel [11] before applying a sliding window approach. Since the online system has access to a limited amount of data, we normalize based on the observed window. The model uses the feature vectors with a frame size of 1 second and a window size of 7 seconds. We evaluated the model using the offline P1 postprocessor to determine the efficacy of the delayed features and the window-based normalization technique. As shown by the results of experiments 1 and 4 in Table 2, these changes give us a comparable performance to the offline model. The online event decoder module utilizes this trained model for computing probabilities for the seizure and background classes. These posteriors are then postprocessed to remove spurious detections. The online postprocessor receives and saves 8 seconds of class posteriors in a buffer for further processing. It applies multiple heuristic filters (e.g., probability threshold) to make an overall decision by combining events across the channels. These filters evaluate the average confidence, the duration of a seizure, and the channels where the seizures were observed. The postprocessor delivers the label and confidence to the visualizer. The visualizer starts to display the signal as soon as it gets access to the signal file, as shown in Figure 1 using the “Signal File” and “Visualizer” blocks. Once the visualizer receives the label and confidence for the latest epoch from the postprocessor, it overlays the decision and color codes that epoch. The visualizer uses red for seizure with the label SEIZ and green for the background class with the label BCKG. Once the streaming finishes, the system saves three files: a signal file in which the sample frames are saved in the order they were streamed, a time segmented event (TSE) file with the overall decisions and confidences, and a hypotheses (HYP) file that saves the label and confidence for each epoch. The user can plot the signal and decisions using the signal and HYP files with only the visualizer by enabling appropriate options. For comparing the performance of different stages of development, we used the test set of TUSZ v1.2.1 database. It contains 1015 EEG records of varying duration. The any-overlap performance [12] of the overall system shown in Figure 2 is 40.29% sensitivity with 5.77 FAs per 24 hours. For comparison, the previous state-of-the-art model developed on this database performed at 30.71% sensitivity with 6.77 FAs per 24 hours [3]. The individual performances of the deep learning phases are as follows: Phase 1’s (P1) performance is 39.46% sensitivity and 11.62 FAs per 24 hours, and Phase 2 detects seizures with 41.16% sensitivity and 11.69 FAs per 24 hours. We trained an LSTM model with the delayed features and the window-based normalization technique for developing the online system. Using the offline decoder and postprocessor, the model performed at 36.23% sensitivity with 9.52 FAs per 24 hours. The trained model was then evaluated with the online modules. The current performance of the overall online system is 45.80% sensitivity with 28.14 FAs per 24 hours. Table 2 summarizes the performances of these systems. The performance of the online system deviates from the offline P1 model because the online postprocessor fails to combine the events as the seizure probability fluctuates during an event. The modules in the online system add a total of 11.1 seconds of delay for processing each second of the data, as shown in Figure 3. In practice, we also count the time for loading the model and starting the visualizer block. When we consider these facts, the system consumes 15 seconds to display the first hypothesis. The system detects seizure onsets with an average latency of 15 seconds. Implementing an automatic seizure detection model in real time is not trivial. We used a variety of techniques such as the file locking mechanism, multithreading, circular buffers, real-time event decoding, and signal-decision plotting to realize the system. A video demonstrating the system is available at: https://www.isip.piconepress.com/projects/nsf_pfi_tt/resources/videos/realtime_eeg_analysis/v2.5.1/video_2.5.1.mp4. The final conference submission will include a more detailed analysis of the online performance of each module. ACKNOWLEDGMENTS Research reported in this publication was most recently supported by the National Science Foundation Partnership for Innovation award number IIP-1827565 and the Pennsylvania Commonwealth Universal Research Enhancement Program (PA CURE). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the official views of any of these organizations. REFERENCES [1] A. Craik, Y. He, and J. L. Contreras-Vidal, “Deep learning for electroencephalogram (EEG) classification tasks: a review,” J. Neural Eng., vol. 16, no. 3, p. 031001, 2019. https://doi.org/10.1088/1741-2552/ab0ab5. [2] A. C. Bridi, T. Q. Louro, and R. C. L. Da Silva, “Clinical Alarms in intensive care: implications of alarm fatigue for the safety of patients,” Rev. Lat. Am. Enfermagem, vol. 22, no. 6, p. 1034, 2014. https://doi.org/10.1590/0104-1169.3488.2513. [3] M. Golmohammadi, V. Shah, I. Obeid, and J. Picone, “Deep Learning Approaches for Automatic Seizure Detection from Scalp Electroencephalograms,” in Signal Processing in Medicine and Biology: Emerging Trends in Research and Applications, 1st ed., I. Obeid, I. Selesnick, and J. Picone, Eds. New York, New York, USA: Springer, 2020, pp. 233–274. https://doi.org/10.1007/978-3-030-36844-9_8. [4] “CFM Olympic Brainz Monitor.” [Online]. Available: https://newborncare.natus.com/products-services/newborn-care-products/newborn-brain-injury/cfm-olympic-brainz-monitor. [Accessed: 17-Jul-2020]. [5] M. L. Scheuer, S. B. Wilson, A. Antony, G. Ghearing, A. Urban, and A. I. Bagic, “Seizure Detection: Interreader Agreement and Detection Algorithm Assessments Using a Large Dataset,” J. Clin. Neurophysiol., 2020. https://doi.org/10.1097/WNP.0000000000000709. [6] A. Harati, M. Golmohammadi, S. Lopez, I. Obeid, and J. Picone, “Improved EEG Event Classification Using Differential Energy,” in Proceedings of the IEEE Signal Processing in Medicine and Biology Symposium, 2015, pp. 1–4. https://doi.org/10.1109/SPMB.2015.7405421. [7] V. Shah, C. Campbell, I. Obeid, and J. Picone, “Improved Spatio-Temporal Modeling in Automated Seizure Detection using Channel-Dependent Posteriors,” Neurocomputing, 2021. [8] W. Tatum, A. Husain, S. Benbadis, and P. Kaplan, Handbook of EEG Interpretation. New York City, New York, USA: Demos Medical Publishing, 2007. [9] D. P. Bovet and C. Marco, Understanding the Linux Kernel, 3rd ed. O’Reilly Media, Inc., 2005. https://www.oreilly.com/library/view/understanding-the-linux/0596005652/. [10] V. Shah et al., “The Temple University Hospital Seizure Detection Corpus,” Front. Neuroinform., vol. 12, pp. 1–6, 2018. https://doi.org/10.3389/fninf.2018.00083. [11] F. Pedregosa et al., “Scikit-learn: Machine Learning in Python,” J. Mach. Learn. Res., vol. 12, pp. 2825–2830, 2011. https://dl.acm.org/doi/10.5555/1953048.2078195. [12] J. Gotman, D. Flanagan, J. Zhang, and B. Rosenblatt, “Automatic seizure detection in the newborn: Methods and initial evaluation,” Electroencephalogr. Clin. Neurophysiol., vol. 103, no. 3, pp. 356–362, 1997. https://doi.org/10.1016/S0013-4694(97)00003-9. 

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2. Deep Learning Approaches for Automatic Seizure Detection from Scalp Electroencephalograms

   https://doi.org/10.1007/978-3-030-36844-9  

   Golmohammadi, Meysam ; Shah, Vinit ; Obeid, Iyad ; Picone, Joseph ( April 2020 , Signal Processing in Medicine and Biology: Emerging Trends in Research and Applications)

   Obeid, Iyad ; Selesnick, Ivan ; Picone, Joseph (Ed.)

   Scalp electroencephalograms (EEGs) are the primary means by which phy-sicians diagnose brain-related illnesses such as epilepsy and seizures. Au-tomated seizure detection using clinical EEGs is a very difficult machine learning problem due to the low fidelity of a scalp EEG signal. Neverthe-less, despite the poor signal quality, clinicians can reliably diagnose ill-nesses from visual inspection of the signal waveform. Commercially avail-able automated seizure detection systems, however, suffer from unaccepta-bly high false alarm rates. Deep learning algorithms that require large amounts of training data have not previously been effective on this task due to the lack of big data resources necessary for building such models and the complexity of the signals involved. The evolution of big data science, most notably the release of the Temple University EEG (TUEG) Corpus, has mo-tivated renewed interest in this problem. In this chapter, we discuss the application of a variety of deep learning ar-chitectures to automated seizure detection. Architectures explored include multilayer perceptrons, convolutional neural networks (CNNs), long short-term memory networks (LSTMs), gated recurrent units and residual neural networks. We use the TUEG Corpus, supplemented with data from Duke University, to evaluate the performance of these hybrid deep structures. Since TUEG contains a significant amount of unlabeled data, we also dis-cuss unsupervised pre-training methods used prior to training these com-plex recurrent networks. Exploiting spatial and temporal context is critical for accurate disambigua-tion of seizures from artifacts. We explore how effectively several conven-tional architectures are able to model context and introduce a hybrid system that integrates CNNs and LSTMs. The primary error modalities observed by this state-of-the-art system were false alarms generated during brief delta range slowing patterns such as intermittent rhythmic delta activity. A varie-ty of these types of events have been observed during inter-ictal and post-ictal stages. Training models on such events with diverse morphologies has the potential to significantly reduce the remaining false alarms. This is one reason we are continuing our efforts to annotate a larger portion of TUEG. Increasing the data set size significantly allows us to leverage more ad-vanced machine learning methodologies. 

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3. Automated seizure activity tracking and onset zone localization from scalp EEG using deep neural networks

   https://doi.org/10.1371/journal.pone.0264537  

   Craley, Jeff ; Jouny, Christophe ; Johnson, Emily ; Hsu, David ; Ahmed, Raheel ; Venkataraman, Archana ( February 2022 , PLOS ONE)

   Bernhardt, Boris C (Ed.)

   We propose a novel neural network architecture, SZTrack, to detect and track the spatio-temporal propagation of seizure activity in multichannel EEG. SZTrack combines a convolutional neural network encoder operating on individual EEG channels with recurrent neural networks to capture the evolution of seizure activity. Our unique training strategy aggregates individual electrode level predictions for patient-level seizure detection and localization. We evaluate SZTrack on a clinical EEG dataset of 201 seizure recordings from 34 epilepsy patients acquired at the Johns Hopkins Hospital. Our network achieves similar seizure detection performance to state-of-the-art methods and provides valuable localization information that has not previously been demonstrated in the literature. We also show the cross-site generalization capabilities of SZTrack on a dataset of 53 seizure recordings from 14 epilepsy patients acquired at the University of Wisconsin Madison. SZTrack is able to determine the lobe and hemisphere of origin in nearly all of these new patients without retraining the network . To our knowledge, SZTrack is the first end-to-end seizure tracking network using scalp EEG. 

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4. The Temple University Artifact Corpus: An Annotated Corpus of EEG Artifacts

   Hamid, Ahmed ; Gagliano, Katherine ; Rahman, Safwanur ; Tulin, Nikita ; Tchiong, Vincent ; Obeid, Iyad ; Picone, Joseph ( December 2020 , IEEE Signal Processing in Medicine and Biology Symposium SPMB)

   Obeid, Iyad ; Selesnick, Ivan ; Picone, Joseph (Ed.)

   The Neural Engineering Data Consortium has recently developed a new subset of its popular open source EEG corpus – TUH EEG (TUEG) [1]. The TUEG Corpus is the world’s largest open source corpus of EEG data and currently has over 3,300 subscribers. There are several valuable subsets of this data, including the TUH Seizure Detection Corpus (TUSZ) [2], which was featured in the Neureka 2020 Epilepsy Challenge [3]. In this poster, we present a new subset of the TUEG Corpus – the TU Artifact Corpus. This corpus contains 310 EEG files in which every artifact has been annotated. This data can be used to evaluate artifact reduction technology. Since TUEG is comprised of actual clinical data, the set of artifacts appearing in the data is rich and challenging. EEG artifacts are defined as waveforms that are not of cerebral origin and may be affected by numerous external and or physiological factors. These extraneous signals are often mistaken for seizures due to their morphological similarity in amplitude and frequency [4]. Artifacts often lead to raised false alarm rates in machine learning systems, which poses a major challenge for machine learning research. Most state-of-the-art systems use some form of artifact reduction technology to suppress these events. The corpus was annotated using a five-way classification that was developed to meet the needs of our constituents. Brief descriptions of each form of the artifact are provided in Ochal et al. [4]. The five basic tags are: • Chewing (CHEW): An artifact resulting from the tensing and relaxing of the jaw muscles. Chewing is a subset of the muscle artifact class. Chewing has the same characteristic high frequency sharp waves with 0.5 sec baseline periods between bursts. This artifact is generally diffuse throughout the different regions of the brain. However, it might have a higher level of activity in one hemisphere. Classification of a muscle artifact as chewing often depends on whether the accompanying patient report mentions any chewing, since other muscle artifacts can appear superficially similar to chewing artifact. • Electrode (ELEC): An electrode artifact encompasses various electrode related artifacts. Electrode pop is an artifact characterized by channels using the same electrode “spiking” with an electrographic phase reversal. Electrostatic is an artifact caused by movement or interference of electrodes and or the presence of dissimilar metals. A lead artifact is caused by the movement of electrodes from the patient’s head and or poor connection of electrodes. This results in disorganized and high amplitude slow waves. • Eye Movement (EYEM): A spike-like waveform created during patient eye movement. This artifact is usually found on all of the frontal polar electrodes with occasional echoing on the frontal electrodes. • Muscle (MUSC): A common artifact with high frequency, sharp waves corresponding to patient movement. These waveforms tend to have a frequency above 30 Hz with no specific pattern, often occurring because of agitation in the patient. • Shiver (SHIV): A specific and sustained sharp wave artifact that occurs when a patient shivers, usually seen on all or most channels. Shivering is a relatively rare subset of the muscle artifact class. Since these artifacts can overlap in time, a concatenated label format was implemented as a compromise between the limitations of our annotation tool and the complexity needed in an annotation data structure used to represent these overlapping events. We distribute an XML format that easily handles overlapping events. Our annotation tool [5], like most annotation tools of this type, is limited to displaying and manipulating a flat or linear annotation. Therefore, we encode overlapping events as a series of concatenated names using symbols such as: • EYEM+CHEW: eye movement and chewing • EYEM+SHIV: eye movement and shivering • CHEW+SHIV: chewing and shivering An example of an overlapping annotation is shown below in Figure 1. This release is an update of TUAR v1.0.0, which was a partially annotated database. In v1.0.0, a similar five way system was used as well as an additional “null” tag. The “null” tag covers anything that was not annotated, including instances of artifact. Only a limited number of artifacts were annotated in v1.0.0. In this updated version, every instance of an artifact is annotated; ultimately, this provides the user with confidence that any part of the record that is not annotated with one of the five classes does not contain an artifact. No new files, patients, or sessions were added in v2.0.0. However, the data was reannotated with these standards. The total number of files remains the same, but the number of artifact events increases significantly. Complete statistics will be provided on the corpus once annotation is complete and the data is released. This is expected to occur in early July – just after the IEEE SPMB submission deadline. The TUAR Corpus is an open-source database that is currently available for use by any registered member of our consortium. To register and receive access, please follow the instructions provided at this web page: https://www.isip.piconepress.com/projects/tuh_eeg/html/downloads.shtml. The data is located here: https://www.isip.piconepress.com/projects/tuh_eeg/downloads/tuh_eeg_artifact/v2.0.0/. 

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5. Beta oscillations in the sensorimotor cortex correlate with disease and remission in benign epilepsy with centrotemporal spikes

   https://doi.org/10.1002/brb3.1237  

   Song, Dan Y. ; Stoyell, Sally M. ; Ross, Erin E. ; Ostrowski, Lauren M. ; Thorn, Emily L. ; Stufflebeam, Steven M. ; Morgan, Amy K. ; Emerton, Britt C. ; Kramer, Mark A. ; Chu, Catherine J. ( February 2019 , Brain and Behavior)

   Benign epilepsy with centrotemporal spikes (BECTS) is a common form of childhood epilepsy with the majority of those afflicted remitting during their early teenage years. Seizures arise from the lower half of the sensorimotor cortex of the brain (e.g. seizure onset zone) and the abnormal epileptiform discharges observed increase during NREM sleep. To date no clinical factors reliably predict disease course, making determination of ongoing seizure risk a significant challenge. Prior work in BECTS have shown abnormalities in beta band (14.9–30 Hz) oscillations during movement and rest. Oscillations in this frequency band are modulated by state of consciousness and thought to reflect intrinsic inhibitory mechanisms.

   We used high density EEG and source localization techniques to examine beta band activity in the seizure onset zone (sensorimotor cortex) in a prospective cohort of children with BECTS and healthy controls during sleep. We hypothesized that beta power in the sensorimotor cortex would be different between patients and healthy controls, and that beta abnormalities would improve with resolution of disease in this self‐limited epilepsy syndrome. We further explored the specificity of our findings and correlation with clinical features. Statistical testing was performed using logistic and standard linear regression models.

   We found that beta band power in the seizure onset zone is different between healthy controls and BECTS patients. We also found that a longer duration of time spent seizure‐free (corresponding to disease remission) correlates with lower beta power in the seizure onset zone. Exploratory spatial analysis suggests this effect is not restricted to the sensorimotor cortex. Exploratory frequency analysis suggests that this phenomenon is also observed in alpha and gamma range activity. We found no relationship between beta power and the presence or rate of epileptiform discharges in the sensorimotor cortex or a test of sensorimotor performance.

   These results provide evidence that cortical beta power in the seizure onset zone may provide a dynamic physiological biomarker of disease in BECTS.

    

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