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Article

Evaluation of Unsupervised Anomaly Detection Techniques in Labelling Epileptic Seizures on Human EEG

1
National Medical and Surgical Center named after N.I. Pirogov, Ministry of Healthcare of the Russian Federation, 105203 Moscow, Russia
2
Baltic Center for Neurotechnology and Artificial Intelligence, Immanuel Kant Baltic Federal University, 236041 Kaliningrad, Russia
3
Research and Production Company “Immersmed”, 105203 Moscow, Russia
*
Author to whom correspondence should be addressed.
Submission received: 22 March 2023 / Revised: 1 May 2023 / Accepted: 2 May 2023 / Published: 4 May 2023
(This article belongs to the Special Issue Artificial Intelligence (AI) in Neuroscience)

Abstract

:
Automated labelling of epileptic seizures on electroencephalograms is an essential interdisciplinary task of diagnostics. Traditional machine learning approaches operate in a supervised fashion requiring complex pre-processing procedures that are usually labour intensive and time-consuming. The biggest issue with the analysis of electroencephalograms is the artefacts caused by head movements, eye blinks, and other non-physiological reasons. Similarly to epileptic seizures, artefacts produce rare high-amplitude spikes on electroencephalograms, complicating their separability. We suggest that artefacts and seizures are rare events; therefore, separating them from the rest data seriously reduces information for further processing. Based on the occasional nature of these events and their distinctive pattern, we propose using anomaly detection algorithms for their detection. These algorithms are unsupervised and require minimal pre-processing. In this work, we test the possibility of an anomaly (or outlier) detection algorithm to detect seizures. We compared the state-of-the-art outlier detection algorithms and showed how their performance varied depending on input data. Our results evidence that outlier detection methods can detect all seizures reaching 100% recall, while their precision barely exceeds 30%. However, the small number of seizures means that the algorithm outputs a set of few events that could be quickly classified by an expert. Thus, we believe that outlier detection algorithms could be used for the rapid analysis of electroencephalograms to save the time and effort of experts.

1. Introduction

Epilepsy is a neurological disease that affects about 1 % of the world’s population [1]. A key feature of epilepsy is seizures—rare episodes of abnormal activity [2]. On the behavioural level, seizures may either induce uncontrollable convulsions (e.g., tonic–clonic seizures) or loss of consciousness (e.g., absence seizures) [3]. On the neural activity level, seizures are accompanied by rhythmic low-frequency neural oscillations with a high amplitude reflecting synchronous activity in large neuronal populations [4].
In general, seizures are accompanied by a state of incapacity that leads to dangerous situations for patients and other people. Epilepsy can also cause cognitive and behavioural deficits [5]. Thus, antiepileptic treatment is highly important, and it starts with diagnostics [6]. Epileptic seizures occur unpredictably and alternate with long periods of normal activity. The rare nature of these events complicates their diagnostics in hospital settings. To collect a sufficient amount of epileptiform activity, patients undergo prolonged electroencephalogram (EEG) monitoring in hospital [7]. As a result, this procedure generates big data comprising hours of normal activity and several seizures with a total duration of a few minutes in total. Usually, this EEG data becomes a subject of manual processing by epileptologists, who spend many hours inspecting EEG signals to label the fragments containing seizures [8]. Machine learning (ML) algorithms are often implemented in EEG data processing, which includes seizure detection [9,10,11,12]. These algorithms can be used to reduce the routine work of experts, helping them label seizures faster, and decreasing the number of errors caused by the human factor.
The application of the ML approach in seizure labelling commonly results in classifiers capable of detecting two classes: “seizures” and “normal activity” [13]. Each classifier falls into one of two broad categories: supervised and unsupervised [14]. The supervised ML algorithm undergoes training using the labelled data of some patients before labelling data from a new patient. Using EEG recordings with manually labelled seizures, these algorithms may learn the distinctive features of epileptiform patterns to detect them on unseen EEG signals [15]. A supervised approach to epilepsy detection has shown promising results and includes state-of-the-art techniques such as deep learning (DL) [16], recurrent neural networks (RNNs) [17], and its modified version—long short-term memory (LSTM) [18]. The majority of ML methods for seizure labelling are supervised [19]. However, some limitations of supervised ML algorithms are often overlooked. Firstly, supervised methods require a large amount of pre-labelled data. The acquisition of such a dataset can be a challenging task in itself. Epileptic patterns are known to be high variable, originating from physiological features of different types of epilepsy and further exacerbated by differences in experimental conditions, and hard- and software acquisition. Secondly, one of the most prominent problems in epileptic data is class imbalance: hour and day recordings usually only contain several epileptic episodes with a total length in minutes. In many cases, the class imbalance leads to overfitting.
Unsupervised ML algorithms are commonly less effective in classification but can provide other benefits, for instance, when working with imbalanced data [20]. Additionally, unsupervised methods do not require data pre-labelling and tend to be more explainable [21]. The ultimate goal of our work was to propose a decision support system (DSS) for epilepsy diagnostics as explainability is highly important in medicine. Thus, we decided to use unsupervised ML methods specifically designed to work with imbalanced data and perform anomaly detection. A literature search showed that some unsupervised methods rely on complex pre-processing [22] or invasive techniques [23], neither of which are acceptable for rapid clinical diagnostics in human patients. In this research, we decided to use EEG data with minimal pre-processing to devise a system capable of operating in a clinical setting. The main goal of our work was to estimate the performance of unsupervised anomaly detection models as a system for automatic pre-labelling of epileptic seizures on human EEGs.
Recently, we showed that EEG data with epileptic seizures are not only imbalanced but also demonstrate features of extreme event behaviour [24,25]. We used this knowledge to apply anomaly detection techniques to label epileptic EEG data. These techniques belong to unsupervised ML algorithms that operate without training data. We tested a one-class support-vector machine (SVM), a popular outlier detection algorithm, on the data of 83 patients and reported 77 % sensitivity and 12 % precision [26].
Here, we further investigate the ability of outlier detection algorithms to detect seizures. We start by introducing popular algorithms for outlier detection, including SVM, ensemble method, and distance-based methods, and adjust their hyperparameters to ensure the best score. Then, we trained these algorithms using various features of EEG signals, including two frequency ranges and three types of spectral power: full spectrum, mean, and principal components (PCs). With the obtained results, we tested two hypotheses: (i) the algorithm type and features impact performance; (ii) predicted performance based on prior knowledge about the algorithm type and features.
The remainder of this paper is organized as follows. Section 2 presents the materials and methods, describing the used dataset, details on the following data processing, and feature engineering procedures. Section 2 also includes information on the proposed methods: Block diagram, details on the different ML algorithms tested, and a description of processes for evaluation and hyperparameter optimization. Section 3 presents the results and discussion, including the results of hyperparameter optimization and an evaluation of the models with optimal hyperparameters. Section 3 also includes the results of statistical comparisons of different algorithms as well as different features. Section 4 presents the conclusion.

2. Materials and Methods

2.1. Dataset

We studied data from the National Medical and Surgical Center named after N. I. Pirogov of the Russian Healthcare Ministry (Moscow, Russia). The dataset included anonymized results from patients under long-term monitoring from the Department of Neurology and Clinical Neurophysiology in 2017–2019. This procedure aimed to record samples of epileptic activity and verify epileptogenic zones for further clinical treatment. During monitoring, patients kept a regular daily routine with a normal sleep–wake cycle and regular physiological trials. The trials included photic stimulation and hyperventilation, commonly used to stimulate the emergence of epileptiform activity. However, no of the seizures were triggered by these trials, i.e., all epileptic seizures in the resulting dataset were spontaneous. The length of recording varied between patients from 8 to 84 h and depended on the patient’s condition. The number of recorded epileptic seizures varied between patients from 1 to 5. All medical procedures followed the Helsinki Declaration and the Center’s medical regulations. Patients provided written informed consent before participation.
EEG signals were recorded with a “Micromed” recorder (Micromed S.p.A., Italy). The dataset for each patient consisted of 25 EEG channels with a sampling rate of 128 Hz. During the recording, EEG electrodes were arranged according to a“10–20” scheme with the ground electrode on the forehead and reference electrodes on the ears. EEG signals were examined and labelled by an experienced epileptologist.
Here, we used EEG data of 80 patients diagnosed pathologically with focal epilepsy. However, there was no uniformity of the diagnosis: in different patients, epileptic focus points were found in frontal, temporal, or parietal areas of one or both hemispheres.

2.2. Data Processing

Data processing mainly followed the pipeline described in our previous work [25]. EEG signals are highly susceptible to external and internal noises, and this becomes even more prominent during long-term recording [27]. To increase the quality of EEG data, we applied two steps of pre-processing. Firstly, we filtered EEG data with band-pass (1–60 Hz) and notch (50 Hz) filters. High-pass filter restrained low-frequency artefacts caused by stray effects or breathing, while the low-pass filter reduced high-frequency components, usually related to muscle activity during everyday routine or seizure convulsions [28]. The notch filter suppressed 50 Hz noise from the power grid. Secondly, we used an artefact-removal approach based on independent component analysis (ICA) to mainly remove blinking artefacts.
Further data processing included time–frequency analysis. For this purpose, we used continuous wavelet transform (CWT) with Morlet mother wavelet [29]. We calculated wavelet power (WP) as it is one of the most common CWT-based characteristics for describing the time–frequency structure of EEGs [30]. We chose 1–30 Hz as the frequency band of interest since it is acceptable for studying both normal and pathological EEG activity [31]. CWT can produce a lot of WP data that is difficult to process and use as features for ML methods, so we performed additional steps to reduce data complexity. Firstly, we reduced the spatial dimensionality by averaging the WP over all EEG channels. Secondly, we divided the WP time series into a set of non-overlapping 60 s intervals and calculated the median value inside each interval, hence providing downsampling in the temporal domain. Thus, we obtained WPs averaged over all EEG channels and time intervals and used this data for further feature engineering.

2.3. Feature Engineering

Here, we extended the feature engineering approach from our papers [25,26] by introducing additional features of the EEG signals. Each 60 s interval was considered as an event characterized by a vector of 300 values. These values correspond to the spectrum of WP in the 1–30 Hz band divided into bins with a 0.1 Hz step.
To reduce the complexity of the data, we implemented principal component analysis (PCA) [32]. In PCA, it is important to assess the number of PCs for the output; however, those components must have high explained variance of the original data. Thus, we applied the following algorithm: we decomposed the data into several PCs, introduced a threshold for explained variance— 90 % , then chose a minimum number of components that could explain a high enough variance. The dependence of the minimum explained variance on the number of PCs is shown in Figure 1. The number of PCs was chosen to be four. Together four PCs could explain at least 98 % and 90 % of the variance in the original data for the 3 Hz and 30 Hz frequency bands, respectively. In practice, we do not need to use all 300 values of initial WP, but instead can use only four PCs to train the model. This approach simplifies the work of the model, since the number of features used for classification is reduced, while we lose a fairly low percentage of initial information.
Based on the data, we proposed several features for the ML algorithm, including ones obtained through PCA:
  • 30 Hz raw—the vector of all 300 values of the WP in the 1–30 Hz band;
  • 3 Hz raw—the sub-vector of 30 values of the WP in the 1–3 Hz band;
  • 30 Hz mean—the mean value of the WP in the 1–30 Hz band;
  • 3 Hz mean—the mean value of the WP in the 1–3 Hz band;
  • 30 Hz PCA—PCA-based feature obtained after decomposing the WP in the 1–30 Hz band and considering four PCs that explain 90 % of the variance;
  • 3 Hz PCA—PCA-based feature obtained after decomposing the WP in the 1–3 Hz band and considering four PCs that explain 98 % of the variance.
We explain chosen features with the following reasoning. It is a well-known fact that epileptic seizures represent abnormal excessive neuronal activity in the brain [2]. Abnormality suggests that EEG signals during seizure episodes differ greatly from normal EEG signals. Hence, the properties of the EEG spectrum should reflect these differences as well. Thus, for spectrum properties, we considered:
  • the overall distribution of the WP across frequencies reflected by the feature 30 Hz raw;
  • the mean value of the WP in the spectrum reflected by the feature 30 Hz mean;
  • the WP values at dominant frequencies reflected by the feature 30 Hz PCA.
Recent works have demonstrated that epileptic activity is associated with characteristic frequency bands in both animal [33] and human subjects [24,25,26]. For human epilepsy, the band is considered to be 1–3 Hz, so we added three features to reflect spectrum properties in this band: 3 Hz raw, 3 Hz mean, and 3 Hz PCA.

2.4. Machine Learning Methods

We used outlier detection methods, a subgroup of unsupervised ML algorithms. Generally, we considered three different approaches: distance-based methods, SVM, and random forest. Below, we give a brief overview of these methods and describe their main hyperparameters. For a more detailed description, see the recent work of Urs Lenz, Peralta, and Cornelis [34]. Figure 2 shows a block diagram of the method.

2.4.1. One-Class Support Vector Machine

A one-class support vector machine (OCSVM) was chosen as the first ML method because it has already demonstrated a good performance in the analysis of EEG data [22,35]. SVM takes the data to a higher dimensional space and then aims to find the hyperplane that separates the vectors into two classes. OCSVM, on the other hand, learns to separate normal data from abnormal data. This model has four hyperparameters:
  • Kernel type is similar to one used in standard SVM classifiers;
  • Threshold parameter (nu) indicates the expected percentage of outliers in the data;
  • Kernel coefficient (gamma) determines the degree of wrapping of the vectors by the plane;
  • Stopping criterion (tol) implies that the algorithm stops running when the difference between old and new loss values becomes less than tol.

2.4.2. k-Nearest Neighbors

The k-nearest neighbours (kNN) method works on a simple principle—it calculates the distances from each data vector to its k-nearest vectors and compares these distances to some predefined threshold [36]. kNN has three hyperparameters:
  • Algorithm is a parameter responsible for the method used for distance calculation;
  • n_neighbors defines the number of nearest neighbors;
  • Threshold defines a decision boundary, i.e., the data with a distance exceeding the threshold is referred to as an outlier.

2.4.3. Local Nearest Neighbors Distance

The local nearest neighbours distance (LNND) [37] relies on the same principle as kNN: once the distance to the data exceeds a predefined threshold, these data are marked as outliers. The main difference is that the LNND distance in the attribute space is not valued equally everywhere, but instead it is compared to the local distance between nearby training instances. For instance, if A is a given point and B is its kth nearest neighbour, then the localized distance is the distance from A to B, divided by the distance from B to its kth nearest neighbour. Hyperparameters for LNND are the same as the ones for kNN.

2.4.4. Local Outlier Factor

The local outlier factor (LOF) method is based on the concept of local density, which reflects how close the neighbours are to a given point [38]. Based on the distances to the nearest neighbours, the algorithm calculates the local density for each data vector and then extracts the vectors whose density is lower than their neighbour’s. This method has three hyperparameters:
  • Algorithm defines a distance measure;
  • n_neighbors is the number of neighbours;
  • Contamination sets the percentage of outliers in the dataset.

2.4.5. Isolation Forest

Isolation forest (IF) is an adaptation of the random forest classifier for one-class classification. Its central idea is that instances that are more isolated from the target class should be easier to separate from the training instances. This idea is transferred to the model by constructing randomized search trees on the target data and measuring the average number of steps required to pass through these trees. IF has one hyperparameter—contamination [39].

2.5. Evaluation and Hyperparameter Optimization

For ML algorithms, we adjusted hyperparameters to maximize the F1-score [40]. Due to EEG variety, we trained an algorithm on the data of a single patient and calculated the corresponding F1-score using the equation:
F 1 = 2 × p r e c i s i o n × r e c a l l p r e c i s i o n + r e c a l l × 100 % ,
where precision and recall are calculated based on the number of true ( T P ) and false ( F P ) positives, and false negatives ( F N ) as follows:
p r e c i s i o n = T P T P + F P × 100 % ,
r e c a l l = T P T P + F N × 100 % ,
Then, we averaged individual F1-scores across participants and chose hyperparameters that minimized this averaged F1-score. To choose parameters, we used the GridSearch function in Python. GridSearch is a simple function for hyperparameter tuning that sorts through all possible combinations of hyperparameters. It trains models with every possible combination and selects one model with the best metric result given as a target parameter.
Of course, such an approach is much more time-consuming than Bayesian optimization, since its computational cost is calculated as
O = i = 1 n l i ,
where l i is the length of the array of values for the i-th hyperparameter. However with GridSearch we can be fully confident that every combination of hyperparameters has been considered and we have received the best variant. In our work, the GridSearch function aimed to maximize the F1-score. Parameters were marked as optimal if the model showed the best result averaged in a group of patients. The range of values after hyperparameter tuning by the GridSearch function are shown in Table 1.
Finally, to generate precision–recall curves, we calculated the probabilities for each event to be classified as a seizure and varied the decision boundary.
We tested the differences in F1-score between the algorithms using the Friedman test. For the post hoc analysis, we used the non-parametric Conover’s test [41].
For performance evaluation, we used the criteria most suitable for the considered epileptic EEG data characterized by a high level of class imbalance. Accuracy and specificity would always be high since only 2 % of the data would be positive, so these metrics would not reflect the real quality of the ML models. We chose sensitivity (recall) and precision, as these two metrics reflect the ability of the model to search the seizures. These metrics are shown in the form of precision–recall curves. Since GridSearch can only focus on one metric, we combined precision and recall into the F1-score, helping to properly assess the quality of the trained models.

3. Results and Discussion

We started with hyperparameter optimization for all algorithms and all types of input data (Table 2). We tested the models with different types of distance estimation metrics, and the GridSearch method chose the Euclidean distance as the best metric.
Therefore, we proceeded with the Euclidean distance in all calculations. The OCSVM performed better with the rbf kernel when the gamma was set to scale. The obtained results provided the following insights. First, the LNND and LOF required more neighbours than kNN. Second, the parameters of the OCSVM did not depend on the type of input data. Third, in the distance-based methods the threshold had the smallest value for PCA and the highest value for the 30 Hz and 3 Hz spectral power.
After finding the optimal combination of hyperparameters, an individual model was trained for each patient, i.e., 80 models were obtained for each ML method. Then, the recall, precision, and F1-score were calculated, and these values were averaged for a group of patients (see Table 3). These results show that OCSVM, kNN, and IF reach the highest performance on the raw data, while the LNND and LOF perform better on PCAs. The best results were demonstrated by the LNND trained using 30 Hz PCAs.
To test if the F1-score changed between algorithms, we used the non-parametric Friedman test.
For the mean value in the 3 Hz band, there was a statistically significant difference in the F1-score depending on which algorithm was used, χ 2 ( 4 ) = 91.731 , p < 0.001 . Post hoc analysis with Conover’s tests was conducted with a Bonferroni correction applied, resulting in a significance level set at p < 0.01 . There was a significant difference in the F1-score between the LNND and other algorithms (Table 4).
For the mean value in the 30 Hz band, there was a statistically significant difference in the F1-score depending on which algorithm was used, χ 2 ( 4 ) = 56.151 , p < 0.001 . Post hoc analysis with Conover’s tests was conducted with a Bonferroni correction applied, resulting in a significance level set at p < 0.01 . There was a significant difference in the F1-score between the LNND and other algorithms (Table 5).
For the PCA in the 3 Hz band, there was no statistically significant difference in the F1-score between the algorithms, χ 2 ( 4 ) = 6.616 , p < 0.158 .
For the PCA in the 30 Hz band, there was no statistically significant difference in the F1-score between the algorithms, χ 2 ( 4 ) = 0.988 , p < 0.912 .
For the RAW data in the 3 Hz band, there was no statistically significant difference in the F1-score between the algorithms, χ 2 ( 4 ) = 4.934 , p < 0.212 .
For the RAW data in the 30 Hz band, there was no statistically significant difference in the F1-score between the algorithms, χ 2 ( 4 ) = 3.253 , p < 0.516 .
The F1-scores appeared to be low; however, there are certain reasons for this. Firstly, in unsupervised ML, we cannot compare predicted values to true values and change the parameters of the method to improve the performance. Since unsupervised methods aim to separate anomalies from the rest of the data, the main way to affect performance is to estimate the percentage of outliers in the data. Secondly, EEG data contains a lot of artefacts that can also be marked as anomalies, and since the data is not pre-labelled, we have limited options to avoid them. The presence of artefacts affects the threshold value for the method, so in highly contaminated data, the F1-score can be lower. Nonetheless, even these F1-scores can be beneficial for DSS, where the final decision is made by a human. The proposed system could be used for express analyses of the EEG to save the time and effort of experts.
In the next step, we considered the precision–recall curves for all algorithms trained using the optimal hyperparameters from Table 2 on the different types of input data (Figure 3). Each sub-figure shows the precision–recall curves for all algorithms (different colours).
The obtained results provided the following insights. First, the lowest areas under the precision–recall curves were achieved at 30 Hz mean (Figure 3B). This indicates that the overall power may not be a reliable marker of a seizure. In particular, the precision is low, indicating a large number of false detections. The possible explanation is that there are many events characterized by an increase in overall power, such as artefacts or sleep-related patterns [42]. Second, using 3 Hz mean improves the precision–recall curves (Figure 3A). This illustrates that seizures produce an outlier in a specific frequency band rather than increasing the overall power. In line with our previous results, this confirms that extreme behaviour occurs in a certain frequency range [24,33]. Third, the mean spectral power provides the worst results for the LOF and LNND algorithms (red and green curves). Moreover, the transition to the specific frequency band of 3 Hz barely improves the performance of these methods. We see that the green and red curves practically do not change between Figure 3A,B, while the others show higher precision. Note that LOF and LNND are distance-based methods, working similarly to kNN but using a different distance measure. Knowing that kNN improves performance when switching from 30 Hz mean to 3 Hz mean, we hypothesize that the distance measure affects the separability between the classes. Fourth, using the entire 30 Hz range provides the widest feature space in which we see that the LOF and LNND perform better. The possible reason for this is that the boundary between the classes changes its configuration in the different feature spaces. Fifth, the best precision–recall curve is achieved using the LNND trained on 30 Hz PCA (Figure 3F). Interestingly, the LNND improves its performance when using PCAs in the 30 Hz range rather than 3 Hz. An intuitively clear explanation is that extending the frequency range provides more distinguishing features together with an increasing amount of unnecessary information and correlated features, therefore limiting the ability to improve. Using PCAs reduces the amount of unnecessary information and rejects correlations between features but leaves the advantage of using a wide frequency range.
Finally, we analysed the effect of the distance measure in the distance-based algorithms on the separability between seizures and normal activity in the feature space. We introduced distance between the classes, a normalized difference between the median distances to seizures and normal states, and tested if it was dependent on the algorithm, frequency band, or feature (see Figure 4). The median distances did not follow a normal distribution in the group of patients (according to the Shapiro–Wilk test), having long tails over the high values. Therefore, we removed 5 % of patients with the highest values and transformed the rest data using the root-mean-square. Resulting values underwent repeated measures of analysis of variances (rm ANOVA) with two within-subject factors: frequency band (3 Hz and 30 Hz) and feature (raw, mean, PCA) separately for three ML algorithms (LNND, kNN, and LOF).
For the LNND, the rm ANOVA reveals a significant main effect of the feature: F(2,106) = 11.468, p < 0.001. The main effect of the frequency band was insignificant: F(1,53) = 1.472, p = 0.23. Finally, the interaction effect feature × frequency band was also insignificant: F(2,106) = 1.365, p < 0.26. These results evidence that the distance between the classes depends on the feature in a similar way for both frequency bands. The direction of change is shown in Figure 4A. Note that since the effect of frequency and the feature × frequency band interaction were both insignificant, the distance between classes in Figure 4A is presented as an average between the 30 Hz and 3 Hz bands. Using the mean value as a feature provides the smallest distance between the seizures and normal states. Raw and PCA ensure a greater distance but it barely differs between them.
For the LOF, the rm ANOVA reveals a significant main effect of the feature: F(2,78) = 53.738, p < 0.001, and an insignificant main effect of the frequency band: F(1,39) = 3.757, p = 0.06. In contrast, there was a significant feature × frequency band interaction effect: F(2,78) = 23.109, p < 0.001. These results evidence that the distance between the classes depends on the feature and the way it changes depends on the frequency band. The direction of change is shown in Figure 4B for 30 Hz and 3 Hz. For the 3 Hz band, the distance between the classes hardly changes between the different features. For the 30 Hz band, the mean value provides the highest distance, and raw data provides the lowest distance.
For the kNN, the rm ANOVA reveals a significant main effect of the feature: F(2,114) = 35.854, p < 0.001, and an insignificant main effect of the frequency band: F(1,57) = 1.312, p = 0.257. There was a significant feature × frequency band interaction effect: F(2,114) = 19.894, p < 0.001. These results evidence that the distance between the classes depends on the feature and the way it changes depends on the frequency band. The direction of change is shown in Figure 4C for 30 Hz and 3 Hz. When using the mean as a feature, the distance differs between 3 Hz and 30 Hz, for the raw and PCA this difference disappears.
Combining the results of outlier detection (Figure 3) and the analysis of distances (Figure 4), we find similar tendencies in the dependence of the precision–recall curve and distance in the LNND on the frequency band and feature. First, the lowest precision–recall curve is observed for the mean value and grows when we use raw data and PCA. Second, this tendency remains similar for 3 Hz and 30 Hz. Therefore, we conclude that in the LNND, the structure of the feature space affects the distance between the classes (i.e., separability). Estimating the separability may give prior knowledge about the performance of the LNND, therefore enabling the selection of features to ensure the best performance.
In terms of achievable performance rates, the obtained results are consistent with modern studies, which also propose novel methods for automated seizure identification in EEG signals using different supervised ML-based approaches. Amiri et al., proposed [9] a method utilizing sparse common spatial patterns (sCSPs) and adaptive short-time Fourier transform-based synchrosqueezing transforms (adaptive FSSTs) to enhance the time–frequency representation of multi-component EEG signals and reduce noise and interferences. They method achieved outstanding performance with high sensitivity, specificity, and accuracy in detecting seizures, demonstrating the potential of their proposed method for epilepsy diagnosis. Malekzadeh et al., utilized [10] a computer-aided diagnosis system (CADS) for the automatic diagnosis of epileptic seizures in EEG signals, involving pre-processing, feature extraction, and classification steps. They used tunable-Q wavelet transforms (TQWTs) for EEG signal decomposition and extracted various linear and non-linear features from TQWT sub-bands. They employed different approaches based on conventional ML and DL for classification and achieved high accuracy (up to 99 % ) in detecting seizures using their proposed DL method based on convolutional neural network (CNN) and RNN. Jiwani et al., proposed [11] an LSTM-CNN model for epileptic seizure detection using EEG signals, highlighting the need for automated techniques due to the lengthy process and shortage of specialists for the visual inspection of EEG reports. Their proposed model combined LSTM and CNN for feature extraction and classification, and they achieved promising results in detecting seizures.
Thus, our findings provide valuable insights into the performance of outlier detection algorithms for epileptic seizure detection in EEG signals and highlight the potential of distance-based methods, particularly when combined with PCA, for achieving high performance in this task. These findings are consistent with current studies [9,10,11,12]. Further research in this area could potentially lead to the development of more effective and efficient computer-aided tools for epilepsy diagnosis, reducing the interpretation load on specialists and improving patient care.

4. Conclusions

We tested the performance of popular outlier detection algorithms in labelling epileptic seizures in human EEGs. We showed that distance-based methods may outperform SVMs and random forests if the distance calculation and feature space are properly defined. Thus, we obtained the best score from the LNND trained on four PCAs explaining 90 % of the variance in the spectral power in the 1–30 Hz frequency range. Finally, we tested if the distance between the classes (separability) in feature space, a core of the distance-based algorithm, predicts its performance. We observed that PCA provided better separability regardless of the frequency band. Therefore, we suggest that estimating the distance between the classes may predict the algorithm’s performance providing opportunities for feature selection.

Author Contributions

Conceptualization, O.E.K., D.A.A. and A.E.H.; data curation, O.E.K., V.V.G. and N.U.; formal analysis, V.A.M.; funding acquisition, D.A.A. and A.E.H.; investigation, M.S.K.; methodology, O.E.K., S.A.K., V.A.M. and A.E.H.; project administration, O.E.K. and D.A.A.; resources, O.E.K., N.U. and D.A.A.; software, M.S.K. and V.V.G.; supervision, A.E.H.; validation, V.A.M., V.V.G., S.A.K., M.S.K. and A.E.H.; visualization, S.A.K. and M.S.K.; writing—original draft, V.A.M. and V.V.G.; writing—review and editing, O.E.K., S.A.K. and A.E.H. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Academic Leadership Program “PRIORITY-2030” of Immanuel Kant Baltic Federal University of Ministry of Science and Education of Russian Federation. AEH thanks the Leading Scientific School Support Program (grant NSH-589.2022.1.2). SAK thanks the Doctor Support Program (grant MD-590.2022.1.2).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of Immanuel Kant Baltic Federal University (protocol code 7/2022 of 27 June 2022).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data that support the findings of this study are available from the National Medical and Surgical Center named after N. I. Pirogov of Russian Healthcare Ministry but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of the National Medical and Surgical Center named after N. I. Pirogov of Russian Healthcare Ministry.

Conflicts of Interest

The authors declare no conflict of interest. The funders and organizations had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

Abbreviations

The following abbreviations are used in this manuscript:
EEGElectroencephalogram
MLMachine learning
DLDeep learning
RNNRecurrent neural networks
LSTMLong short-term memory
DSSDecision support system
SVMSupport vector machine
PCPrinciple component
ICAIndependent component analysis
CWTContinuous wavelet transform
WPWavelet power
PCAPrinciple component analysis
OCSVMOne-class support vector machine
kNNk-Nearest neighbours
LNNDLocal nearest neighbours distance
LOFLocal outlier factor
IFIsolation forest
TPTrue positive
FPFalse positive
FNFalse negative
rm ANOVARepeated measures analysis of variances
sCSPSparse common spatial pattern
FSSTFourier transform-based synchrosqueezing transform
CADSComputer-aided diagnosis system
TQWTTunable-Q wavelet transform
CNNConvolutional neural network

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Figure 1. The dependence of the minimum explained variance on the number of PCs for the 3 Hz (green line) and 30 Hz (blue line) frequency bands.
Figure 1. The dependence of the minimum explained variance on the number of PCs for the 3 Hz (green line) and 30 Hz (blue line) frequency bands.
Applsci 13 05655 g001
Figure 2. Block diagram of the proposed ML method.
Figure 2. Block diagram of the proposed ML method.
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Figure 3. Precision–recall curves for the different outlier detection algorithms are shown in different colours. Each panel reflects the type of input data as stated in the panel caption: (A) 3 Hz mean; (B) 30 Hz mean; (C) 3 Hz raw; (D) 30 Hz raw; (E) 3 Hz PCA; (F) 30 Hz PCA.
Figure 3. Precision–recall curves for the different outlier detection algorithms are shown in different colours. Each panel reflects the type of input data as stated in the panel caption: (A) 3 Hz mean; (B) 30 Hz mean; (C) 3 Hz raw; (D) 30 Hz raw; (E) 3 Hz PCA; (F) 30 Hz PCA.
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Figure 4. Distance between the seizures and normal states (group mean and 95 % CI) in the feature space depending on the frequency band and feature. Sub-figures correspond to the different distance-based ML algorithms: LNND (A); LOF (B); kNN (C).
Figure 4. Distance between the seizures and normal states (group mean and 95 % CI) in the feature space depending on the frequency band and feature. Sub-figures correspond to the different distance-based ML algorithms: LNND (A); LOF (B); kNN (C).
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Table 1. The range hyperparameter values examined by the GridSearch method.
Table 1. The range hyperparameter values examined by the GridSearch method.
AlgorithmHyperparameterRange of Values
OCSVMNu10 i , i [−6, −1]
Gamma10 i , i [−6, −1], and ‘scale’
Tol10 i , i [−6, −1]
Kernel type‘rbf’, ‘poly’, ’sigmoid’
kNN, LNND, LOFN_neighbors i [1, 20]
Algorithm‘Euclidean’, ‘manhattan’, ‘cosine’
Threshold (for kNN, LNND), % j × 10 i , i [−4, 1], j 1, 5
Contamination (For LOF) j × 10 i , i [−6, −1], j 1, 5
IFContamination j × 10 i , i [−6, −1], j 1, 5
Table 2. The optimal hyperparameters that provide the highest F1-score for the different algorithms and types of input data.
Table 2. The optimal hyperparameters that provide the highest F1-score for the different algorithms and types of input data.
AlgorithmHyperparameterInput Data
30 Hz3 Hz30 Hz Mean3 Hz Mean30 Hz PCA3 Hz PCA
OCSVMNu0.10.10.10.10.10.1
Gammascale
Tol0.10.10.10.10.10.1
Kernel typerbf
kNNN_neighbors334443
Threshold, %0.50.50.10.10.10.1
AlgorithmEuclidean
LNNDN_neighbors589997
Threshold, %0.50.50.50.50.10.1
AlgorithmEuclidean
LOFN_neighbors788883
Contamination0.0050.0050.0010.0050.0010.0001
AlgorithmEuclidean
IFContamination0.0010.0050.0010.0010.0010.005
Table 3. The maximum F1-score for all models trained on the different types of input data using the optimal parameters from Table 2. Results are shown as a group mean and 95% confidence intervals (bold text indicates the best results of the models).
Table 3. The maximum F1-score for all models trained on the different types of input data using the optimal parameters from Table 2. Results are shown as a group mean and 95% confidence intervals (bold text indicates the best results of the models).
FeatureAlgorithm
OCSVMkNNLNNDLOFIF
3 Hz Raw0.305 ± 0.0570.316 ± 0.0550.281 ± 0.0550.297 ± 0.0550.304 ± 0.057
30 Hz Raw0.307 ± 0.0600.312 ± 0.0600.331 ± 0.0560.330 ± 0.0540.271 ± 0.073
3 Hz mean0.255 ± 0.0710.282 ± 0.0740.116 ± 0.0400.278 ± 0.0730.282 ± 0.074
30 Hz mean0.245 ± 0.0710.270 ± 0.0730.135 ± 0.0460.254 ± 0.0530.270 ± 0.073
3 Hz PCA0.273 ± 0.0720.300 ± 0.0750.250 ± 0.0710.292 ± 0.0750.276 ± 0.073
30 Hz PCA0.300 ± 0.0580.313 ± 0.0770.338 ± 0.0770.331 ± 0.0800.304 ± 0.061
Table 4. 3 Hz mean (Conover’s post hoc comparisons).
Table 4. 3 Hz mean (Conover’s post hoc comparisons).
T-Statdf W i W j p p bonf p holm
OCSVMkNN 0.039 316 264.000 263.500 0.969 1.000 1.000
LNND 7.883 316 264.000 163.500 <0.001<0.001<0.001
LOF 1.294 316 264.000 247.500 0.197 1.000 1.000
IF 0.196 316 264.000 261.500 0.845 1.000 1.000
kNNLNND 7.844 316 263.500 163.500 <0.001<0.001<0.001
LOF 1.255 316 263.500 247.500 0.210 1.000 1.000
IF 0.157 316 263.500 261.500 0.875 1.000 1.000
LNNDLOF 6.589 316 163.500 247.500 <0.001<0.001<0.001
IF 7.687 316 163.500 261.500 <0.001<0.001<0.001
LOFIF 1.098 316 247.500 261.500 0.273 1.000 1.000
Table 5. 30 Hz mean (Conover’s post hoc comparisons).
Table 5. 30 Hz mean (Conover’s post hoc comparisons).
T-Statdf W i W j p p bonf p holm
OCSVMkNN 1.013 316 244.000 254.000 0.312 1.000 1.000
LNND 5.115 316 244.000 193.500 <0.001<0.001<0.001
LOF 0.861 316 244.000 252.500 0.390 1.000 1.000
IF 1.215 316 244.000 256.000 0.225 1.000 1.000
kNNLNND 6.128 316 254.000 193.500 <0.001<0.001<0.001
LOF 0.152 316 254.000 252.500 0.879 1.000 1.000
IF 0.203 316 254.000 256.000 0.840 1.000 1.000
LNNDLOF 5.976 316 193.500 252.500 <0.001<0.001<0.001
IF 6.331 316 193.500 256.000 <0.001<0.001<0.001
LOFIF 0.355 316 252.500 256.000 0.723 1.000 1.000
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Karpov, O.E.; Khoymov, M.S.; Maksimenko, V.A.; Grubov, V.V.; Utyashev, N.; Andrikov, D.A.; Kurkin, S.A.; Hramov, A.E. Evaluation of Unsupervised Anomaly Detection Techniques in Labelling Epileptic Seizures on Human EEG. Appl. Sci. 2023, 13, 5655. https://0-doi-org.brum.beds.ac.uk/10.3390/app13095655

AMA Style

Karpov OE, Khoymov MS, Maksimenko VA, Grubov VV, Utyashev N, Andrikov DA, Kurkin SA, Hramov AE. Evaluation of Unsupervised Anomaly Detection Techniques in Labelling Epileptic Seizures on Human EEG. Applied Sciences. 2023; 13(9):5655. https://0-doi-org.brum.beds.ac.uk/10.3390/app13095655

Chicago/Turabian Style

Karpov, Oleg E., Matvey S. Khoymov, Vladimir A. Maksimenko, Vadim V. Grubov, Nikita Utyashev, Denis A. Andrikov, Semen A. Kurkin, and Alexander E. Hramov. 2023. "Evaluation of Unsupervised Anomaly Detection Techniques in Labelling Epileptic Seizures on Human EEG" Applied Sciences 13, no. 9: 5655. https://0-doi-org.brum.beds.ac.uk/10.3390/app13095655

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