Assessing the Effectiveness of Neurofeedback for Drug-Resistant Focal Epilepsy: A Preliminary MRI Study
-
Donya Abolghasemkhah Salmasi
,
Alireza Fallahi
,
Narges Hoseini-Tabatabaei
,
Seyed-Sohrab Hashemi-Fesharaki
,
Reza Rostami
,
Mohammad-Reza Nazem-Zadeh
Abstract
Purpose: Evidence shows that Neurofeedback (NF) can reduce seizure frequency and enhance Sensorimotor Rhythm (SMR) in patients with drug-resistant focal epilepsy, but the neural mechanisms underlying such effects are not well understood. The objective of this study was to investigate the neuromodulatory effects of SMR NF training on functional and structural connectivity in patients with drug-resistant focal epilepsy.
Materials and Methods: Four patients with drug-resistant focal epilepsy underwent functional Magnetic Resonance Imaging (fMRI), diffusion MRI (dMRI), Quantitative Electroencephalogram (QEEG), and Integrated Visual and Auditory (IVA-2) test before and after 6 to 8 weeks of SMR NF training. We assessed alterations in functional and structural connectivity within and between six brain networks based on the Automated Anatomical Labeling (AAL) atlas.
Results: All four patients showed a reduction of a minimum of 35% in seizure frequency after SMR NF training, with two patients experiencing a reduction within the first week of treatment. IVA-2 scores increased for all patients compared to the pre-treatment baseline, indicating cognitive improvement. Post-treatment fMRI revealed no significant differences in functional connectivity between patients and control cases, despite significant differences in some brain networks observed in pre-treatment fMRI. We also found increased Fractional Anisotropy (FA) values between subcortical and auditory networks after SMR training.
Conclusion: Our study provides promising evidence for the neural basis of SMR NF training in the treatment of drug-resistant focal epilepsy. The observed reductions in seizure frequency, improvements in cognitive abilities, and increased FA values suggest that SMR NF training may be an effective treatment for patients with drug-resistant focal epilepsy.
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27- M Barry Sterman, "Basic concepts and clinical findings in the treatment of seizure disorders with EEG operant conditioning." Clinical electroencephalography, Vol. 31 (No. 1), pp. 45-55, (2000).
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30- N. Tzourio-Mazoyer et al., "Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain." (in eng), Neuroimage, Vol. 15 (No. 1), pp. 273-89, (2002).
31- AJBSJJDK Leemans, Ben Jeurissen, Jan Sijbers, and Derek K Jones, "ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data." in Proc Intl Soc Mag Reson Med, Vol. 17 (No. 1), p. 3537, (2009).
32- Josien PW Pluim, JB Antoine Maintz, and Max A Viergever, "Mutual-information-based registration of medical images: a survey." IEEE transactions on medical imaging, Vol. 22 (No. 8), pp. 986-1004, (2003).
33- Alexander Leemans and Derek K Jones, "The B‐matrix must be rotated when correcting for subject motion in DTI data." Magnetic Resonance in Medicine: An Official Journal of the International Society for Magnetic Resonance in Medicine, Vol. 61 (No. 6), pp. 1336-49, (2009).
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35- An Effect Size Primer: A Guide for Clinicians and Researchers." Professional Psychology: Research and Practice, Vol. 40pp. 532-38, (2009).
2- Zhibin Chen, Martin J. Brodie, Danny Liew, and Patrick Kwan, "Treatment Outcomes in Patients With Newly Diagnosed Epilepsy Treated With Established and New Antiepileptic Drugs: A 30-Year Longitudinal Cohort Study." (in eng), JAMA neurology, Vol. 75 (No. 3), pp. 279-86, (2018).
3- R. Joshi, M. Tripathi, P. Gupta, S. Gulati, and Y. K. Gupta, "Adverse effects & drug load of antiepileptic drugs in patients with epilepsy: Monotherapy versus polytherapy." (in eng), Indian J Med Res, Vol. 145 (No. 3), pp. 317-26, (2017).
4- Y. Nagai et al., "Epileptic seizures are reduced by autonomic biofeedback therapy through enhancement of fronto-limbic connectivity: A controlled trial and neuroimaging study." (in eng), EBioMedicine, Vol. 27pp. 112-22, (2018).
5- R. Michaelis et al., "Psychological treatments for people with epilepsy." (in eng), Cochrane Database Syst Rev, Vol. 10 (No. 10), p. Cd012081, (2017).
6- S. Åkerlund, E. Varkey, J. Klecki, J. Zelano, and E. Ben-Menachem, "Randomized controlled trial of moderate cardiovascular exercise for patients with drug-resistant epilepsy." (in eng), Epilepsy Behav, Vol. 124p. 108335, (2021).
7- J. B. Allendorfer and R. M. Arida, "Role of Physical Activity and Exercise in Alleviating Cognitive Impairment in People With Epilepsy." (in eng), Clin Ther, Vol. 40 (No. 1), pp. 26-34, (2018).
8- N. Feter, R. Alt, C. A. Häfele, M. C. da Silva, and A. J. Rombaldi, "Effect of combined physical training on cognitive function in people with epilepsy: Results from a randomized controlled trial." (in eng), Epilepsia, Vol. 61 (No. 8), pp. 1649-58, (2020).
9- G. Tan et al., "Meta-analysis of EEG biofeedback in treating epilepsy." (in eng), Clin EEG Neurosci, Vol. 40 (No. 3), pp. 173-9, (2009).
10- JL Koberda and LC Frey, "Application of Z-score LORET A Neurofeedback in therapy of epilepsy." Journal of Neurology and Neurobiology, Vol. 1 (No. 1), (2015).
11- M. B. Sterman and T. Egner, "Foundation and practice of neurofeedback for the treatment of epilepsy." (in eng), Appl Psychophysiol Biofeedback, Vol. 31 (No. 1), pp. 21-35, (2006).
12- T. Egner and M. B. Sterman, "Neurofeedback treatment of epilepsy: from basic rationale to practical application." (in eng), Expert Rev Neurother, Vol. 6 (No. 2), pp. 247-57, (2006).
13- Gary H. Glover, "Overview of functional magnetic resonance imaging." (in eng), Neurosurgery clinics of North America, Vol. 22 (No. 2), pp. 133-vii, (2011).
14- Medana Luca, Christian Beckmann, Nicola De Stefano, Paul Matthews, and S. M. Smith, "FMRI resting state networks define distinct modes of long-distance interactions in the human brain." Neuroimage, Vol. 29pp. 1359-67, (2006).
15- Saba Amiri et al., "Graph theory application with functional connectivity to distinguish left from right temporal lobe epilepsy." Epilepsy Res, Vol. 167, (2020).
16- Maryam Afzali et al., "The sensitivity of diffusion MRI to microstructural properties and experimental factors." (in eng), Journal of neuroscience methods, Vol. 347pp. 108951-51, (2021).
17- E. Silvagni, A. Bortoluzzi, M. Borrelli, A. Bianchi, E. Fainardi, and M. Govoni, "Cerebral Microstructure Analysis by Diffusion-Based MRI in Systemic Lupus Erythematosus: Lessons Learned and Research Directions." (in eng), Brain Sci, Vol. 12 (No. 1), (2021).
18- Neil G. Simon and Michel Kliot, "Diffusion weighted MRI and tractography for evaluating peripheral nerve degeneration and regeneration." (in eng), Neural regeneration research, Vol. 9 (No. 24), pp. 2122-24, (2014).
19- Yang Jiang, Reza Abiri, and Xiaopeng Zhao, "Tuning Up the Old Brain with New Tricks: Attention Training via Neurofeedback." (in English), Frontiers in Aging Neuroscience, Mini Review Vol. 9, (2017).
20- T. Egner and J. H. Gruzelier, "Learned self-regulation of EEG frequency components affects attention and event-related brain potentials in humans." (in eng), Neuroreport, Vol. 12 (No. 18), pp. 4155-9, (2001).
21- T. Egner and J. H. Gruzelier, "EEG biofeedback of low beta band components: frequency-specific effects on variables of attention and event-related brain potentials." (in eng), Clin Neurophysiol, Vol. 115 (No. 1), pp. 131-9, (2004).
22- Timothy P. Tinius, "The Integrated Visual and Auditory Continuous Performance Test as a neuropsychological measure." Archives of Clinical Neuropsychology, Vol. 18 (No. 5), pp. 439-54, (2003).
23- Cong Fu, Aikedan Aisikaer, Zhijuan Chen, Qing Yu, Jianzhong Yin, and Weidong Yang, "Different Functional Network Connectivity Patterns in Epilepsy: A Rest-State fMRI Study on Mesial Temporal Lobe Epilepsy and Benign Epilepsy With Centrotemporal Spike." (in English), Frontiers in Neurology, Original Research Vol. 122021-May-28, (2021).
24- René M. H. Besseling et al., "Reduced functional integration of the sensorimotor and language network in rolandic epilepsy." NeuroImage: Clinical, Vol. 2pp. 239-46, (2013)
25- Christopher J. Ferguson, "An effect size primer: A guide for clinicians and researchers." 40 doi:10.1037/a0015808, American Psychological Association, US, (2009).
26- Gonzalo Rojas, Carolina Alvarez, Carlos Montoya Moya, Maria de la Iglesia Vaya, Jaime Cisternas, and Marcelo Gálvez, "Study of Resting-State Functional Connectivity Networks Using EEG Electrodes Position As Seed." Frontiers in Neuroscience, Vol. 1203/26 (2018).
27- M Barry Sterman, "Basic concepts and clinical findings in the treatment of seizure disorders with EEG operant conditioning." Clinical electroencephalography, Vol. 31 (No. 1), pp. 45-55, (2000).
28- Hengameh Marzbani, Hamid Reza Marateb, and Marjan Mansourian, "Neurofeedback: a comprehensive review on system design, methodology and clinical applications." Basic and clinical neuroscience, Vol. 7 (No. 2), p. 143 ,(2016).
29- Chao-Gan Yan, Xin-Di Wang, Xi-Nian Zuo, and Yu-Feng Zang, "DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging." Neuroinformatics, Vol. 14 (No. 3), pp. 339-51, (2016).
30- N. Tzourio-Mazoyer et al., "Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain." (in eng), Neuroimage, Vol. 15 (No. 1), pp. 273-89, (2002).
31- AJBSJJDK Leemans, Ben Jeurissen, Jan Sijbers, and Derek K Jones, "ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data." in Proc Intl Soc Mag Reson Med, Vol. 17 (No. 1), p. 3537, (2009).
32- Josien PW Pluim, JB Antoine Maintz, and Max A Viergever, "Mutual-information-based registration of medical images: a survey." IEEE transactions on medical imaging, Vol. 22 (No. 8), pp. 986-1004, (2003).
33- Alexander Leemans and Derek K Jones, "The B‐matrix must be rotated when correcting for subject motion in DTI data." Magnetic Resonance in Medicine: An Official Journal of the International Society for Magnetic Resonance in Medicine, Vol. 61 (No. 6), pp. 1336-49, (2009).
34- H. X. Barnhart and D. P. Barboriak, "Applications of the repeatability of quantitative imaging biomarkers: a review of statistical analysis of repeat data sets." (in eng), Transl Oncol, Vol. 2 (No. 4), pp. 231-5, (2009).
35- An Effect Size Primer: A Guide for Clinicians and Researchers." Professional Psychology: Research and Practice, Vol. 40pp. 532-38, (2009).
| Files | ||
| Issue | Vol 12 No 2 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/fbt.v12i2.18284 | |
| Keywords | ||
| Drug-Resistant Epilepsy Neurofeedback Sensorimotor Rhythm Resting-State functional Magnetic Resonance Imaging Diffusion Magnetic Resonance Imaging Functional Connectivity Structural Connectivity Brain Networks | ||
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How to Cite
1.
Abolghasemkhah Salmasi D, Fallahi A, Hoseini-Tabatabaei N, Hashemi-Fesharaki S-S, Rostami R, Nazem-Zadeh M-R. Assessing the Effectiveness of Neurofeedback for Drug-Resistant Focal Epilepsy: A Preliminary MRI Study. Frontiers Biomed Technol. 2025;12(2):399-415.
