| Literature DB >> 33820942 |
Michael L Martini1, Aly A Valliani1, Claire Sun1,2, Anthony B Costa1, Shan Zhao3, Fedor Panov1, Saadi Ghatan1, Kanaka Rajan4, Eric Karl Oermann5,6,7.
Abstract
Real-time seizure detection is a resource intensive process as it requires continuous monitoring of patients on stereoelectroencephalography. This study improves real-time seizure detection in drug resistant epilepsy (DRE) patients by developing patient-specific deep learning models that utilize a novel self-supervised dynamic thresholding approach. Deep neural networks were constructed on over 2000 h of high-resolution, multichannel SEEG and video recordings from 14 DRE patients. Consensus labels from a panel of epileptologists were used to evaluate model efficacy. Self-supervised dynamic thresholding exhibited improvements in positive predictive value (PPV; difference: 39.0%; 95% CI 4.5-73.5%; Wilcoxon-Mann-Whitney test; N = 14; p = 0.03) with similar sensitivity (difference: 14.3%; 95% CI - 21.7 to 50.3%; Wilcoxon-Mann-Whitney test; N = 14; p = 0.42) compared to static thresholds. In some models, training on as little as 10 min of SEEG data yielded robust detection. Cross-testing experiments reduced PPV (difference: 56.5%; 95% CI 25.8-87.3%; Wilcoxon-Mann-Whitney test; N = 14; p = 0.002), while multimodal detection significantly improved sensitivity (difference: 25.0%; 95% CI 0.2-49.9%; Wilcoxon-Mann-Whitney test; N = 14; p < 0.05). Self-supervised dynamic thresholding improved the efficacy of real-time seizure predictions. Multimodal models demonstrated potential to improve detection. These findings are promising for future deployment in epilepsy monitoring units to enable real-time seizure detection without annotated data and only minimal training time in individual patients.Entities:
Year: 2021 PMID: 33820942 PMCID: PMC8021582 DOI: 10.1038/s41598-021-86891-y
Source DB: PubMed Journal: Sci Rep ISSN: 2045-2322 Impact factor: 4.379
Figure 1Overview of the workflow for continuous monitoring with video and SEEG and real-time analysis in the epilepsy monitoring unit. Patients with DRE receive continuous monitoring of their intracranial SEEG leads (red) and simultaneous video recording in their hospital beds (blue). A convolutional LSTM autoencoder (CNN + LSTM) was applied to the video recordings to calculate a regularity score for each frame over time. This regularity score time series and the SEEG time series (green sequence, bottom left) were then separately fed into an LSTM network to reconstruct their signals (blue sequence, bottom middle) and calculate a reconstruction error (red sequence, bottom right) which was then subjected to a self-supervised dynamically thresholding method to identify anomalous events in real-time.
Figure 2Design of crossover experiments to assess patient-specificity of models. LSTM models were trained on recordings from one patient and tested on recordings from another patient.
Figure 3Crossover testing produces a large increase in the number of false positive results. This indicates that trained models are attuned to the unique electrical signal of a given patient. Green shading refers to prediction mismatches that correspond to correctly identified anomalies whereas red shading refers to prediction mismatches that correspond to false positives.
Figure 4Self-supervised error thresholding for real-time detection of anomalies in SEEG and video data. An LSTM network is trained to predict the next window of values in the test time series sequence (A, blue). These values are compared to the actual values (A, orange), and a smoothed error is calculated for each value in the sequence (B, red sequence). Prediction mismatches (A, purple) manifest as higher errors. A self-supervised dynamic threshold (B, magenta line) enables effective local classification of true anomalous sequences (B, green bar) while omitting many of the false positives (B, red bars) that result from traditional static thresholding methods (B, blue line). Concurrently acquired video recordings for each patient were considerably noisier and signal reconstruction was not as robust, demonstrated by the higher reconstruction errors (C, red sequence). While video sequences captured all of the true seizure events in the study population (C, middle, green bar), they also captured several false positive events, such as nurse visits (C, far right, red bars).
Characteristics of the patient population.
| Age (mean ± SEM) | 24.5 ± 2.0 years |
| Female (%) | 8 (57%) |
| Duration of recording in hospital (mean ± SEM) | 6.1 ± 0.4 days |
| Taking antiepileptic drugs (%) | 10 (71%) |
| Number of leads (total; mean ± SEM) | 204; 14.6 ± 0.6 |
| Supplementary motor area (SMA) | 8 (4%) |
| Amygdala | 25 (12%) |
| Cingulate | 55 (27%) |
| Frontal | 11 (5%) |
| Hippocampus | 25 (12%) |
| Insula | 10 (5%) |
| Orbitofrontal | 28 (14%) |
| Parietal | 7 (3%) |
| Premotor | 5 (3%) |
| Temporal | 28 (14%) |
| Thalamus | 2 (1%) |
| Number of channels (total; mean ± SEM) | 2055; 146.8 ± 7.6 |
SEM standard error of the mean.
Neural network specifications and results.
| Train:test ratio (mean ± SEM) | 0.41 ± 0.03 |
| Time used to train model (mean ± SEM) | 11.2 ± 1.5 min |
| Train recordings with events (%) | 4 (29%) |
| Test recordings with events (%) | 12 (86%) |
| MAPE for dynamic threshold (mean ± SEM) | 0.7 ± 0.2% |
| MAPE for static threshold (mean ± SEM) | 0.7 ± 0.1% |
| MAPE for crossover experiments with dynamic threshold (mean ± SEM) | 2.7 ± 0.8% |
| MAPE for video recordings (mean ± SEM) | 19.9 ± 0.8% |
| Sensitivity (mean ± SEM) | 64.3 ± 13.3% |
| Positive predictive value (mean ± SEM) | 34.4 ± 13.9% |
| F1 Score (mean ± SEM) | 0.61 ± 0.12 |
| Sensitivity (mean ± SEM) | 78.6 ± 11.4% |
| Positive predictive value (mean ± SEM) | 89.6 ± 9.2% |
| F1 Score (mean ± SEM) | 0.92 ± 0.08 |
| Sensitivity (mean ± SEM) | 83.3 ± 16.7% |
| Positive predictive value (mean ± SEM) | 15.3 ± 10.6% |
| F1 Score (mean ± SEM) | 0.54 ± 0.11 |
| Sensitivity (mean ± SEM) | 100.0 ± 0% |
| Positive predictive value (mean ± SEM) | 19.1 ± 7.1% |
| F1 Score (mean ± SEM) | 0.44 ± 0.07 |
| Sensitivity (mean ± SEM) | 100.0 ± 0% |
| Positive predictive value (mean ± SEM) | 65.6 ± 9.2% |
| F1 Score (mean ± SEM) | 0.65 ± 0.09 |
MAPE mean absolute percent error, SEEG stereoelectroencephalography, SEM standard error of the mean.
Patient-specific clinical and electrophysiologic seizure manifestations, as well as model performance on individual patient recordings.
| Pt # | Clinical seizure findings | EEG seizure findings | SEEG, dynamic thresholding (PPV, sensitivity) | SEEG, static thresholding (PPV, sensitivity) | Video alone, dynamic thresholding (PPV, sensitivity) | SEEG + video, dynamic thresholding (PPV, sensitivity) |
|---|---|---|---|---|---|---|
| 1 | Generalized tonic seizure with abduction of both arms and extensor posturing of her legs. | Generalized desynchronization of the EEG background with superimposed beta frequency activity. | 92.3, 100 | 9.7, 100 | 100, 100 | 100, 100 |
| 2 | Absence seizures with repetitive eye blinking and staring. | Generalized, repetitive, spikes and polyspikes of 2 Hz. | 50.0, 100 | 0, 0 | 50.0, 100 | 50.0, 100 |
| 3 | Bilateral motor manifestations involving extension of both arms and legs. | Sentinal spike in the left amygdala followed by a slow buildup of rhythmic theta. Activity spreads to left medial temporal, parietal, and insular regions. Semi-rhythmic theta with admixed spikes in left anterior and medial cingulate. | 100, 100 | 27.7, 100 | 25.0, 100 | 88.0, 100 |
| 4 | Ictal cry with head movements and bilateral clonic body movements obscured by blankets. Arms are held in dystonic posture bilaterally with forceful jerking movements superimposed. | Starts as low amplitude beta activity in the left hippocampus with spread to left amygdala and left medial temporal lobe. Evolves to high amplitude spiky alpha and spiky theta activities. Later spread to the medial olfactory cortex. | 100, 100 | 0, 0 | 25.0, 100 | 25.0, 100 |
| 5 | Oral and head movements with vocalizations and bilateral extremity flexion. Later progresses to tonic–clonic. | Continuous atypical, generalized spike-and-wave discharges at 4 Hz in bilateral frontal, cingulate, and hippocampal regions. Subsequent burst of spike and wave activity. | 100, 100 | 100, 100 | 20.0, 100 | 90.7, 100 |
| 6 | Notable eye movement, vocalization, and some bilateral extremity movements. Eventually tonic–clonic. | Atypical, generalized spike-and-wave discharges at 4 Hz in bilateral frontal and cingulate regions followed by rhythmic spiking diffusely. | 100, 100 | No events detected | 20.0, 100 | 33.3, 100 |
| 7 | Multiple subclinical seizures. Clinically, all seizures are hypermotor, and begin with a rapid movement in the hands. | Slightly different onsets but nearly always maximal involvement in left lateral temporal. Begins with spike and wave, or gamma/beta activity there. Often has several minutes of very subtle epileptic spasms with diffuse slow waves in left lateral temporal. | 100, 100 | 100, 100 | 20.0, 100 | 60.0, 100 |
| 8 | Versive head movements with right arm flexion and extension, followed by tonic–clonic movements of both arms. | Rhythmic fast activity in right medial cingulate and temporal areas. Sharply contoured theta develops in left hippocampus, which evolves to spike and slow wave morphology and spreads to bilateral medial cingulate and left temporal areas. | 100, 100 | 100, 100 | 25.0, 100 | 40.0, 100 |
| 9 | Oral movements with ictal cry and right facial contraction. Later generalized clonic jerking and posturing before generalized tonic–clonic seizures. | Desynchronization with superimposed low voltage fast beta/gamma activity over left medial cingulate. Later, ictal discharge of repetitive spikes become wide spread, involving cingulate, temporal, and amygdala areas bilaterally. | No events detected | No events detected | 16.7, 100 | 16.7, 100 |
| 10 | Right arm movements with subtle leg movements. Some head movement with eyes looking up and left. Later, jerking movements, vocalization, and tonic posturing. | Rhythmic alpha activity in right amygdala and hippocampus that slows to the theta range. | No events detected | No events detected | 16.7, 100 | 16.7, 100 |
| 11 | Lower extremity bicycling movements under bed sheets. | High amplitude right hippocampal activity. Several seconds into the seizure, there is spread to right insula, cingulate, and temporal regions. | 100, 100 | 59.0, 100 | 33.3, 100 | 50.0, 100 |
| 12 | Motionless at onset. At times will look around and turn head slowly left. | Subtle low amplitude gamma buzz at left SMA. Some rhythmic beta in left premotor region. | 100, 100 | 40.0, 100 | 40.0, 100 | 70.0, 100 |
| 13 | Subtle bilateral automatisms in hands. Will then raise left hand with some tremulous movements. Later has rapid eye blinking and smile. | Right premotor area becomes rhythmic near onset but bilateral activity seen. Activity builds in amplitude and then slows to delta with admixed spikes/gamma. Some spread to left SMA. | 16.7, 100 | 20.0, 100 | 50.0, 100 | 90.0. 100 |
| 14 | Brief oral automatisms with faint vocalization. Right hand clenched into fist. Subtle clonic jerking of the right hand and arm. | Onset of repetitive spikes of 1 Hz at left hippocampus and amygdala. Spikes increase in frequency to 2–3 Hz and evolve into alpha frequency discharge. Ictal discharge spreads to left cingulate, olfactory, and temporal areas. | No events detected | No events detected | 6.3, 100 | 6.25, 100 |
EEG electroencephalographic, Pt patient, SEEG stereoelectroencephalography, SMA supplementary motor area, SEM standard error of the mean.