AI-Based Electroencephalogram Analysis in Rodent Models of Epilepsy: A Systematic Review
Source abstract
Abstract
About 70 million people globally have been diagnosed with epilepsy. Electroencephalogram (EEG) devices are the primary method for identifying and monitoring seizures. The use of EEG expands the preclinical research involving the long-term recording of neuro-activities in rodent models of epilepsy targeted towards the efficient testing of prospective antiseizure medications. Typically, trained epileptologists visually analyse long-term EEG recordings, which is time-consuming and subject to expert variability. Automated epileptiform discharge detection using machine learning or deep learning methods is an effective approach to tackling these challenges. This systematic review examined and summarised the last 30 years of research on detecting epileptiform discharge in rodent models of epilepsy using machine learning and deep learning methods. A comprehensive literature search was conducted on two databases, PubMed and Google Scholar. Following the PRISMA protocol, the 3021 retrieved articles were filtered to 21 based on inclusion and exclusion criteria. An additional article was obtained through the reference list. Hence, 22 articles were selected for critical analysis in this review. These articles revealed the seizure type, features and feature engineering, machine learning and deep learning methods, training methodologies, evaluation metrics so far explored, and models deployed for real-world validation. Although these studies have advanced the field of epilepsy research, the majority of the models are experimental. Further studies are required to fill in the identified gaps and expedite preclinical research in epilepsy, ultimately leading to translational research.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: EEG and Brain-Computer Interfaces · Neuroscience and Neuropharmacology Research · Epilepsy research and treatment
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
School of Computer Science, University College Dublin, D04 V1W8 Dublin, Ireland
FutureNeuro SFI Research Centre, School of Computer Science, University College Dublin, D04 V1W8 Dublin, Ireland
Funding
European Union’s Horizon 2020 Research and Innovation Programme · Science Foundation Ireland (SFI) · European Regional Development Fund · FutureNeuro
References (100+)
Show source-provided references
1. ILAE official report: A practical clinical definition of epilepsy10.1111/epi.12550 ↗
2. The neurobiology of epilepsy10.1007/s11910-007-0053-z ↗
3. Shimizu, H., Morimoto, Y., Yamamoto, N., Tayama, T., Ozawa, H., and Imamura, A. (2022). Overlap between epilepsy and neurodevelopmental disorders: Insights from clinical and genetic studies. Epilepsy.10.36255/exon-publications-epilepsy-neurodevelopmental-disorders ↗
4. Emerging insights into the genesis of epilepsy10.1038/399a015 ↗
5. Operational classification of seizure types by the International League against Epilepsy: Position Paper of the ILAE Commission for Classification and Terminology10.1111/epi.13670 ↗
6. How many patients with psychogenic nonepileptic seizures also have epilepsy?10.1212/WNL.57.5.915 ↗
7. Frequency of a false positive diagnosis of epilepsy: A systematic review of observational studies10.1016/j.seizure.2016.08.005 ↗
8. MCC950 alleviates seizure severity and angiogenesis by inhibiting NLRP3/IL-1β signaling pathway-mediated pyroptosis in mouse model of epilepsy10.1016/j.intimp.2023.111236 ↗
9. The consequences of refractory epilepsy and its treatment10.1016/j.yebeh.2014.05.031 ↗
10. Global, regional, and national burden of epilepsy, 1990–2016: A systematic analysis for the Global Burden of Disease Study 201610.1016/S1474-4422(18)30454-X ↗
11. Prevalence and incidence of epilepsy: A systematic review and meta-analysis of international studies10.1212/WNL.0000000000003509 ↗
12. Drug resistance in epilepsy: Clinical impact, potential mechanisms, and new innovative treatment options10.1124/pr.120.019539 ↗
13. Animal models of epilepsy: Use and limitations10.2147/NDT.S50371 ↗
14. Singh, R., Farooq, S., Mannan, A., Singh, T., Najda, A., Grażyna, Z., Albadrani, G., Sayed, A., and Abdel-Daim, M. (2022). Animal models of diabetic microvascular complications: Relevance to clinical features. Biomed. Pharmacother., 145.10.1016/j.biopha.2021.112305 ↗
15. Edoho, M., Mamad, O., Henshall, D.C., Mooney, C., and Wei, L. (2023, January 9–12). Prediction of Epilepsy Phenotype in Intra-amygdala Kainic Acid Mouse Model of Epilepsy. Proceedings of the 2023 10th International Conference on Biomedical and Bioinformatics Engineering, Kyoto, Japan.10.1145/3637732.3637740 ↗
16. Animal models of neurodegenerative diseases10.1038/s41593-018-0236-8 ↗
17. Animal models in epilepsy research: Legacies and new directions10.1038/nn.3934 ↗
18. Animal models of epilepsy: A phenotype-oriented review10.14336/AD.2021.0723 ↗
19. The validity of animal models of depression10.1007/BF00427414 ↗
20. The significance of meaning: Why do over 90% of behavioral neuroscience results fail to translate to humans, and what can we do to fix it?10.1093/ilar/ilu047 ↗
21. Trends in EEG-BCI for daily-life: Requirements for artifact removal10.1016/j.bspc.2016.09.005 ↗
22. Slimen, I., Boubchir, L., and Seddik, H. (2020). Epileptic seizure prediction based on EEG spikes detection of ictal-preictal states. J. Biomed. Res., 34.10.7555/JBR.34.20190097 ↗
23. Seneviratne, U., Boston, R., Cook, M., and D’Souza, W. (2018). Characteristics of epileptiform discharge duration and interdischarge interval in genetic generalized epilepsies. Front. Neurol., 9.10.3389/fneur.2018.00036 ↗
24. Human interictal epileptiform discharges are bidirectional traveling waves echoing ictal discharges10.7554/eLife.73541 ↗
25. Clinical utility of EEG in diagnosing and monitoring epilepsy in adults10.1016/j.clinph.2018.01.019 ↗
26. Sablok, S., Gururaj, G., Shaikh, N., Shiksha, I., and Choudhary, A. (2020, January 13–15). Interictal spike detection in EEG using time series classification. Proceedings of the 2020 4th International Conference on Intelligent Computing and Control Systems (ICICCS), Madurai, India.10.1109/ICICCS48265.2020.9120928 ↗
27. Detection of interictal epileptiform discharges in an extended scalp EEG array and high-density EEG—A prospective multicenter study10.1111/epi.17246 ↗
28. Prasanth, T., Thomas, J., Yuvaraj, R., Jing, J., Cash, S., Chaudhari, R., Leng, T., Rathakrishnan, R., Rohit, S., and Saini, V. (2020, January 20–24). Deep learning for interictal epileptiform spike detection from scalp EEG frequency sub bands. Proceedings of the 2020 42nd Annual International Conference of the IEEE Engineering in Medicine & Biology Society (EMBC), Montréal, QC, Canada.10.1109/EMBC44109.2020.9175644 ↗
29. Selim, S., Elhinamy, E., Othman, H., Abouelsaadat, W., and Salem, M. (2019, January 17–18). A review of machine learning approaches for epileptic seizure prediction. Proceedings of the 2019 14th International Conference on Computer Engineering and Systems (ICCES), Cairo, Egypt.10.1109/ICCES48960.2019.9068190 ↗
30. Dynamic preictal discharges in patients with mesial temporal lobe epilepsy10.1097/WNP.0000000000000486 ↗
31. Epilepsy seizure prediction with few-shot learning method10.1186/s40708-022-00170-8 ↗
32. Clinical features of the postictal state: Correlation with seizure variables10.1016/j.yebeh.2010.06.039 ↗
33. Postictal symptoms help distinguish patients with epileptic seizures from those with non-epileptic seizures10.1053/seiz.1999.0270 ↗
34. Detection of spontaneous seizures in EEGs in multiple experimental mouse models of epilepsy10.1088/1741-2552/ac2ca0 ↗
35. Proposal for revised clinical and electroencephalographic classification of epileptic seizures10.1111/j.1528-1157.1981.tb06159.x ↗
36. The new classification of seizures by the International League Against Epilepsy 201710.1007/s11910-017-0758-6 ↗
37. Epilepsy: Diagnosis, classification and management10.1016/j.mpmed.2020.05.001 ↗
38. Introduction to the epilepsy syndrome papers10.1111/epi.17262 ↗
39. Epilepsy: A clinical overview10.1016/j.amjmed.2021.01.038 ↗
40. The kainic acid models of temporal lobe epilepsy10.1523/ENEURO.0337-20.2021 ↗
41. Modelling epilepsy in the mouse: Challenges and solutions10.1242/dmm.047449 ↗
42. New insights from the use of pilocarpine and kainate models10.1016/S0920-1211(02)00072-4 ↗
43. A permanent change in brain function resulting from daily electrical stimulation10.1016/0014-4886(69)90128-9 ↗
44. Status epilepticus10.4103/0972-2327.56312 ↗
45. Limbic seizures produced by pilocarpine in rats: Behavioural, electroencephalographic and neuropathological study10.1016/0166-4328(83)90136-5 ↗
46. Changes in interictal spike features precede the onset of temporal lobe epilepsy10.1002/ana.23549 ↗
47. Long-term seizure suppression and optogenetic analyses of synaptic connectivity in epileptic mice with hippocampal grafts of GABAergic interneurons10.1523/JNEUROSCI.0005-14.2014 ↗
48. Animal models of temporal lobe epilepsy following systemic chemoconvulsant administration10.1016/j.jneumeth.2015.03.009 ↗
49. Griffin, A., Hamling, K., Hong, S., Anvar, M., Lee, L., and Baraban, S. (2018). Preclinical animal models for Dravet syndrome: Seizure phenotypes, comorbidities and drug screening. Front. Pharmacol., 9.10.3389/fphar.2018.00573 ↗
50. Fit for purpose application of currently existing animal models in the discovery of novel epilepsy therapies10.1016/j.eplepsyres.2016.05.016 ↗
51. Seizures induce obstructive apnea in DBA/2J audiogenic seizure-prone mice: Lifesaving impact of tracheal implants10.1111/epi.16431 ↗
52. Bosco, F., Guarnieri, L., Leo, A., Tallarico, M., Gallelli, L., Rania, V., Citraro, R., and De Sarro, G. (2023). Audiogenic epileptic DBA/2 mice strain as a model of genetic reflex seizures and SUDEP. Front. Neurol., 14.10.3389/fneur.2023.1223074 ↗
53. The genetic absence epilepsy rat from Strasbourg as a model to decipher the neuronal and network mechanisms of generalized idiopathic epilepsies10.1016/j.jneumeth.2015.05.022 ↗
54. Scn1a gene reactivation after symptom onset rescues pathological phenotypes in a mouse model of Dravet syndrome10.1038/s41467-021-27837-w ↗
55. Life-span characterization of epilepsy and comorbidities in Dravet syndrome mice carrying a targeted deletion of exon 1 of the Scn1a gene10.1016/j.expneurol.2022.114090 ↗
56. Reduced sodium channel Nav1.1 levels in BACE1-null mice10.1074/jbc.M110.134692 ↗
57. High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research10.1016/j.pneurobio.2012.06.008 ↗
58. Promises and limitations of human intracranial electroencephalography10.1038/s41593-018-0108-2 ↗
59. Large-scale recording of neuronal ensembles10.1038/nn1233 ↗
60. Mechanisms of action of antiepileptic drugs10.1016/S0074-7742(06)81006-8 ↗
61. Invasive electroencephalography monitoring: Indications and presurgical planning10.4103/0972-2327.128668 ↗
62. Signal quality of simultaneously recorded invasive and non-invasive EEG10.1016/j.neuroimage.2009.02.028 ↗
63. Fisher, R., Scharfman, H., and DeCurtis, M. (2014). How can we identify ictal and interictal abnormal activity?. Issues in Clinical Epileptology: A View from the Bench, Springer.10.1007/978-94-017-8914-1_1 ↗
64. Invasive recordings from the human brain: Clinical insights and beyond10.1038/nrn1585 ↗
65. Brienza, M., Davassi, C., and Mecarelli, O. (2019). Artifacts. Clin. Electroencephalogr., 109–130.10.1007/978-3-030-04573-9_8 ↗
66. Invasive or noninvasive: Understanding brain-machine interface technology10.1109/MEMB.2009.935475 ↗
67. Protocol for recording epileptiform discharges of EEG and behavioral seizures in freely moving mice10.1016/j.xpro.2022.101245 ↗
68. Standards for data acquisition and software-based analysis of in vivo electroencephalography recordings from animals. A TASK 1-WG 5 report of the AES/ILAE Translational Task Force of the ILAE10.1111/epi.13909 ↗
69. Nayak, C., and Anilkumar, A. (2020). EEG Normal Waveforms. Updated 31 July 2020. StatPearls, StatPearls Publishing. Available online: http://www.ncbi.nlm.nih.gov.
70. Sucholeiki, R., and Louis, S. (2008). Normal EEG waveforms. E-Med., 1–7.
71. A review of electroencephalogram signal processing methods for brain-controlled robots10.1016/j.cogr.2021.07.001 ↗
72. High-frequency oscillations as a new biomarker in epilepsy10.1002/ana.22548 ↗
73. Epileptic seizure focus detection from interictal electroencephalogram: A survey10.1007/s11571-022-09816-z ↗
74. High-frequency oscillations: What is normal and what is not?10.1111/j.1528-1167.2008.01917.x ↗
75. Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy10.1016/0013-4694(94)00286-T ↗
76. The correlation between electroencephalography amplitude and interictal abnormalities: Audit study
77. Transfer Learning for the Identification of Paediatric EEGs with Interictal Epileptiform Abnormalities10.1109/ACCESS.2024.3415786 ↗
78. Wei, L., Mchugh, J.C., and Mooney, C. (2023, January 9–12). Interictal Epileptiform Discharge Classification for the Prediction of Epilepsy Type in Children. Proceedings of the 2023 10th International Conference on Biomedical and Bioinformatics Engineering, Kyoto, Japan.10.1145/3637732.3637737 ↗
79. Nayak, C., and Anilkumar, A. (2023). EEG normal waveforms. Updated 24 July 2023. StatPearls [Internet], StatPearls Publishing.
80. A review on machine learning for EEG signal processing in bioengineering10.1109/RBME.2020.2969915 ↗
81. Automated EEG artifact elimination by applying machine learning algorithms to ICA-based features10.1088/1741-2552/aa69d1 ↗
82. A brain-computer interface based on a few-channel EEG-fNIRS bimodal system10.1109/ACCESS.2016.2637409 ↗
83. EMG and EOG artifacts in brain computer interface systems: A survey10.1016/j.clinph.2006.10.019 ↗
84. Effect of EOG signal filtering on the removal of ocular artifacts and EEG-based brain-computer interface: A comprehensive study10.1155/2018/4853741 ↗
85. A new ICA-based fingerprint method for the automatic removal of physiological artifacts from EEG recordings10.7717/peerj.4380 ↗
86. Sanei, S., and Chambers, J. (2013). EEG Signal Processing, John Wiley & Sons.
87. Azlan, W., and Low, Y. (2014, January 8–10). Feature extraction of Electroencephalogram (EEG) signal—A review. Proceedings of the 2014 IEEE Conference on Biomedical Engineering and Sciences (IECBES), Kuala Lumpur, Malaysia.
88. Classification of EEG signals: An interpretable approach using functional data analysis10.1016/j.jneumeth.2022.109609 ↗
89. Tong, S., and Thankor, N. (2009). Quantitative EEG Analysis Methods and Clinical Applications, Artech House.
90. Analysis of EEG signals using nonlinear dynamics and chaos: A review
91. Feature selection: A data perspective
92. Priyanka, S., Dema, D., and Jayanthi, T. (2017, January 1–2). Feature selection and classification of Epilepsy from EEG signal. Proceedings of the 2017 International Conference on Energy, Communication, Data Analytics and Soft Computing (ICECDS), Chennai, India.10.1109/ICECDS.2017.8389880 ↗
93. Sánchez-Hernández, S., Salido-Ruiz, R., Torres-Ramos, S., and Román-Godinez, I. (2022). Evaluation of feature selection methods for classification of epileptic seizure EEG signals. Sensors, 22.10.3390/s22083066 ↗
94. Boubchir, L., Daachi, B., and Pangracious, V. (2017, January 5–7). A review of feature extraction for EEG epileptic seizure detection and classification. Proceedings of the 2017 40th International Conference on Telecommunications and Signal Processing (TSP), Barcelona, Spain.10.1109/TSP.2017.8076027 ↗
95. Machine learning for predicting epileptic seizures using EEG signals: A review10.1109/RBME.2020.3008792 ↗
96. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement
97. Google Scholar, Web of Science, and Scopus: A systematic comparison of citations in 252 subject categories
98. Google Scholar to overshadow them all? Comparing the sizes of 12 academic search engines and bibliographic databases10.1007/s11192-018-2958-5 ↗
99. An overview of the functionalities of PubMed10.1177/14782715221088906 ↗
100. Shin, J., Smith, D., Swiniarski, R., Dudek, F., White, A., Staley, K., and Cios, K. (2009, January 18–22). Analysis of EEG epileptic signals with rough sets and support vector machines. Proceedings of the Artificial Intelligence in Medicine: 12th Conference on Artificial Intelligence in Medicine, AIME 2009, Verona, Italy. Proceedings 12.10.1007/978-3-642-02976-9_45 ↗