• Review •
Research progress of resting state functional magnetic resonance imaging in epilepsy
Cite this article as: GUO J H, WU Q, GAO Y, et al. Research progress of resting state functional magnetic resonance imaging in epilepsy[J]. Chin J Magn Reson Imaging, 2024, 15(3): 206-211. DOI:10.12015/issn.1674-8034.2024.03.034.
| [Abstract] Epilepsy is a chronic neurological disease, its classification is wide, the mechanism is complex, has the characteristics of repeated seizures and unpredictable, which has caused a certain impact on the life of patients. Therefore, it is necessary to understand the pathophysiological mechanisms for the treatment of epilepsy and the improvement of patients' quality of life. Resting-state functional magnetic resonance imaging (rs-MRI) has become an effective method to investigate the changes of brain function in epilepsy. At present, the data analysis methods for epilepsy research based on rs-fMRI mainly include amplitude of low frequency fluctuation (ALFF), regional homogeneity (ReHo), function connection (FC) and graph theory analysis. This article provides a review of the application of various rs-fMRI analysis methods in epilepsy, aiming to provide imaging indicators for the pathophysiological mechanism, preoperative and precise clinical treatment of epilepsy. |
| [Keywords] epilepsy；magnetic resonance imaging；resting-state functional magnetic resonance imaging；amplitude of low frequency fluctuation；regional homogeneity；function connection；graph theory |
GUO Jiahui1
WU Qiong1*
GAO Yang1
ZHAO He1
XIE Shenghui1
LI Bo1
WANG Shaoyu2
ZHANG Huapeng2
WANG Yanan1
1 Department of Radiology, Affiliated Hospital of Inner Mongolia Medical University, Hohhot 010030, China
2 SIEMENS Healthineers, Shanghai 201318, China
Corresponding author: WU Q, E-mail: 33360023@qq.com
Conflicts of interest None.
| Received 2023-10-07 |
| Accepted 2024-03-04 |
| DOI: 10.12015/issn.1674-8034.2024.03.034 |
| Cite this article as: GUO J H, WU Q, GAO Y, et al. Research progress of resting state functional magnetic resonance imaging in epilepsy[J]. Chin J Magn Reson Imaging, 2024, 15(3): 206-211. DOI:10.12015/issn.1674-8034.2024.03.034. |
[1]
FISHER R S, VAN EMDE BOAS W, BLUME W, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE)[J]. Epilepsia, 2005, 46(4): 470-472.
DOI:
10.1111/j.0013-9580.2005.66104.x.
[2]
RINEY K, BOGACZ A, SOMERVILLE E, et al. International league against epilepsy classification and definition of epilepsy syndromes with onset at a variable age: position statement by the ILAE task force on nosology and definitions[J]. Epilepsia, 2022, 63(6): 1443-1474.
DOI:
10.1111/epi.17240.
[3]
FALCO-WALTER J. Epilepsy-definition, classification, pathophysiology, and epidemiology[J]. Semin Neurol, 2020, 40(6): 617-623.
DOI:
10.1055/s-0040-1718719.
[4]
MANFORD M. Recent advances in epilepsy[J]. J Neurol, 2017, 264(8): 1811-1824.
DOI:
10.1007/s00415-017-8394-2.
[5]
ASADI-POOYA A A, FARAZDAGHI M. Clinical characteristics of MRI-negative temporal lobe epilepsy[J]. Acta Neurol Belg, 2022, 123(5): 1911-1916.
DOI:
10.1007/s13760-022-02145-2.
[6]
ZHANG X, PAN W J, KEILHOLZ S. The relationship between local field potentials and the blood-oxygenation-level dependent MRI signal can be non-linear[J/OL]. Front Neurosci, 2019, 13: 1126 [2023-10-07]. https://doi.org/10.3389/fnins.2019.01126.
DOI:
10.3389/fnins.2019.01126.
[7]
DUAN Y T, CHEN Z Q, HE M W, et al. MRI study of association between the SCN1A gene rs3812718 locus polymorphism and spontaneous brain activity in temporal lobe epilepsy[J]. Chin J Radiol, 2022, 56(5): 530-535.
DOI:
10.3760/cma.j.cn112149-20210408-00344.
[8]
SAINBURG L E, LITTLE A A, JOHNSON G W, et al. Characterization of resting functional MRI activity alterations across epileptic foci and networks[J]. Cereb Cortex, 2022, 32(24): 5555-5568.
DOI:
10.1093/cercor/bhac035.
[9]
SINGH T B, AISIKAER A, HE C, et al. The assessment of brain functional changes in the temporal lobe epilepsy patient with cognitive impairment by resting-state functional magnetic resonance imaging[J/OL]. J Clin Imaging Sci, 2020, 10: 50 [2023-10-07]. https://doi.org/10.25259/JCIS_55_2020.
DOI:
10.25259/JCIS_55_2020.
[10]
ZHANG Z, ZHOU X, LIU J, et al. Aberrant executive control networks and default mode network in patients with right-sided temporal lobe epilepsy: a functional and effective connectivity study[J]. Int J Neurosci, 2020, 130(7): 683-693.
DOI:
10.1080/00207454.2019.1702545.
[11]
ZHANG Z, ZHOU X, LIU J, et al. Longitudinal assessment of resting-state fMRI in temporal lobe epilepsy: A two-year follow-up study[J/OL]. Epilepsy Behav, 2020, 103(Pt A): 106858 [2023-10-07]. https://doi.org/10.1016/j.yebeh.2019.106858.
DOI:
10.1016/j.yebeh.2019.106858.
[12]
QIN L, JIANG W, ZHENG J, et al. Alterations functional connectivity in temporal lobe epilepsy and their relationships with cognitive function: A longitudinal resting-state fMRI study[J/OL]. Front Neurol, 2020, 11: 625 [2023-10-07]. https://doi.org/10.3389/fneur.2020.00625.
DOI:
10.3389/fneur.2020.00625.
[13]
BERNHARDT B C, FADAIE F, DE WAEL R VOS, et al. Preferential susceptibility of limbic cortices to microstructural damage in temporal lobe epilepsy: A quantitative T1 mapping study[J]. NeuroImage, 2018, 182: 294-303.
DOI:
10.1016/j.neuroimage.2017.06.002.
[14]
CACIAGLI L, WANDSCHNEIDER B, XIAO F, et al. Abnormal hippocampal structure and function in juvenile myoclonic epilepsy and unaffected siblings[J]. Brain, 2019, 142(9): 2670-2687.
DOI:
10.1093/brain/awz215.
[15]
YANG F, JIA W, KUKUN H, et al. A study of spontaneous brain activity on resting-state functional magnetic resonance imaging in adults with MRI-negative temporal lobe epilepsy[J]. Neuropsychiatr Dis Treat, 2022, 18: 1107-1116.
DOI:
10.2147/NDT.S366189.
[16]
VETKAS A, FOMENKO A, GERMANN J, et al. Deep brain stimulation targets in epilepsy: Systematic review and meta‐analysis of anterior and centromedian thalamic nuclei and hippocampus[J]. Epilepsia, 2022, 63(3): 513-524.
DOI:
10.1111/epi.17157.
[17]
YU Q Q, LIU G P, XU Q, et al. Uncoupling between functional connectivity density and amplitude of low frequency fluctuation in childhood absence epilepsy[J]. Chin J Magn Reson Imaging, 2022, 13(7): 75-79, 89.
DOI:
10.12015/issn.1674-8034.2022.07.013.
[18]
WENG Y, LARIVIERE S, CACIAGLI L, et al. Macroscale and microcircuit dissociation of focal and generalized human epilepsies[J/OL]. Commun Biol, 2020, 3(1): 244 [2023-10-07]. https://doi.org/10.1038/s42003-020-0958-5.
DOI:
10.1038/s42003-020-0958-5.
[19]
ZOU Q H, ZHU C Z, YANG Y, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF[J]. J Neurosci Methods, 2008, 172(1): 137-141.
DOI:
10.1016/j.jneumeth.2008.04.012.
[20]
CHEN L C, LI X,F, SHEN L S. Self-limited focal epilepsy decreased regional brain activity in sensorimotor areas[J]. Acta Neurol Scand, 2021, 143(2): 188-194.
DOI:
10.1111/ane.13350.
[21]
YAN Y, XIE G, ZHOU H, et al. Altered spontaneous brain activity in patients with childhood absence epilepsy: associations with treatment effects[J]. Neuroreport, 2020, 31(8): 613-618.
DOI:
10.1097/WNR.0000000000001447.
[22]
LI X, CHEN Q, WANG Z, et al. Altered spontaneous brain activity as a potential imaging biomarker for generalized and focal to bilateral tonic-clonic seizures: A resting-state fMRI study[J/OL]. Epilepsy Behav, 2023, 140: 109100 [2023-10-07]. https://doi.org/10.1016/j.yebeh.2023.109100.
DOI:
10.1016/j.yebeh.2023.109100.
[23]
ZANG Y, JIANG T, LU Y, et al. Regional homogeneity approach to fMRI data analysis[J]. NeuroImage, 2004, 22(1): 394-400.
DOI:
10.1016/j.neuroimage.2003.12.030.
[24]
LIU G, LYU G, YANG N, et al. Abnormalities of diffusional kurtosis imaging and regional homogeneity in idiopathic generalized epilepsy with generalized tonic-clonic seizures[J]. Exp Ther Med, 2019, 17(1): 603-612.
DOI:
10.3892/etm.2018.7018.
[25]
CHANG W, LV Z, PANG X, et al. The local neural markers of MRI in patients with temporal lobe epilepsy presenting ictal panic: A resting resting-state postictal fMRI study[J/OL]. Epilepsy Behav, 2022, 129: 108490 [2023-10-07]. https://doi.org/10.1016/j.yebeh.2021.108490.
DOI:
10.1016/j.yebeh.2021.108490.
[26]
SCHUTTENBERG EM S J, ROSMARIN D H, et al. Forgiveness mediates the relationship between middle frontal gyrus volume and clinical symptoms in adolescents[J/OL]. Front Hum Neurosci, 2022, 16: 782893 [2023-10-07]. https://doi.org/10.3389/fnhum.2022.782893.
DOI:
10.3389/fnhum.2022.782893.
[27]
ZHU J, XU C, ZHANG X, et al. A resting-state functional MRI study on the effect of vagal nerve stimulation on spontaneous regional brain activity in drug-resistant epilepsy patients[J/OL]. Behav Brain Res, 2020, 392: 112709 [2023-10-07]. https://doi.org/10.1016/j.bbr.2020.112709.
DOI:
10.1016/j.bbr.2020.112709.
[28]
ZHU J, XU C, ZHANG X, et al. Altered amplitude of low-frequency fluctuations and regional homogeneity in drug-resistant epilepsy patients with vagal nerve stimulators under different current intensity[J]. CNS Neurosci Ther, 2021, 27(3): 320-329.
DOI:
10.1111/cns.13449.
[29]
FORNITO A, ZALESKY A, BREAKSPEAR M. The connectomics of brain disorders[J]. Nat Rev Neurosci, 2015, 16(3): 159-172.
DOI:
10.1038/nrn3901.
[30]
DAVIS K A, JIRSA V K, SCHEVON C A. Wheels within wheels: Theory and practice of epileptic networks[J/OL]. Epilepsy Curr, 2021, 21(4): 15357597211015663 [2023-10-07]. https://doi.org/10.1177/15357597211015663.
DOI:
10.1177/15357597211015663.
[31]
LIU W, YUE Q, GONG Q, et al. Regional and remote connectivity patterns in focal extratemporal lobe epilepsy[J/OL]. Ann Transl Med, 2021, 9(14): 1128 [2023-10-07]. https://dx.doi.org/10.21037/atm-21-1374.
DOI:
10.21037/atm-21-1374.
[32]
MA X Y, BAN C, ZHAO P F, et al. A fMRI study of hippocampal functional connectivity changes in benign childhood epilepsy with centrotemporal spikes[J]. Chin J Magn Reson Imaging, 2022, 13(2): 22-25.
DOI:
10.12015/issn.1674-8034.2022.02.005.
[33]
PIZZANELLI C, PESARESI I, MILANO C, et al. Distinct limbic connectivity in left and right benign mesial temporal lobe epilepsy: Evidence from a resting state functional MRI study[J/OL]. Front Neurol, 2022, 13: 943660 [2023-10-07]. https://doi.org/10.3389/fneur.2022.943660.
DOI:
10.3389/fneur.2022.943660.
[34]
AVIGAN P D, CAMMACK K, SHAPIRO M L. Flexible spatial learning requires both the dorsal and ventral hippocampus and their functional interactions with the prefrontal cortex[J]. Hippocampus, 2020, 30(7): 733-744.
DOI:
10.1002/hipo.23198.
[35]
KIM H J, LEE J H, PARK C H, et al. Role of language-related functional connectivity in patients with benign childhood epilepsy with centrotemporal spikes[J]. J Clin Neurol, 2018, 14(1): 48-57.
DOI:
10.3988/jcn.2018.14.1.48.
[36]
ROGER E, PICHAT C, TORLAY L, et al. Hubs disruption in mesial temporal lobe epilepsy. A resting-state fMRI study on a language-and-memory network[J/OL]. Hum Brain Mapp, 2020, 41(3): 779-796 [2023-10-07]. https://doi.org/10.1002/hbm.24839.
DOI:
10.1002/hbm.24839.
[37]
QIN Y, LI S, YAO D, et al. Causality analysis to the abnormal subcortical-cortical connections in idiopathic-generalized epilepsy[J/OL]. Front Neurosci, 2022, 16: 925968 [2023-10-07]. https://pubmed.ncbi.nlm.nih.gov/35844218/.
DOI:
10.3389/fnins.2022.925968.
[38]
KRISTIN E, WILLS B, HERNÁN F J, et al. People with mesial temporal lobe epilepsy have altered thalamooccipital brain networks[J/OL]. Front Neurosci, 2022, 16: 925968 [2023-10-07]. https://doi.org/10.3389/fnins.2022.925968.
DOI:
10.1016/j.yebeh.2020.107645.
[39]
ZENG Z, ZHANG T J. Study on resting-state fMRI of the central executive network in children with idiopathic generalized epilepsy[J]. Journal of Epileptology and Electroneurophysiology, 2022, 31(4): 203-208.
DOI:
10.19984/j.cnki.1674-8972.2022.04.03
[40]
BISWAL B, YETKIN F Z, HAUGHTON V M, et al. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI[J]. Magn Reson Med, 1995, 34(4): 537-541.
DOI:
10.1002/mrm.1910340409.
[41]
LI Y, QIN B, CHEN Q, et al. Impaired functional homotopy and topological properties within the default mode network of children with generalized tonic-clonic seizures: A resting-state fMRI study[J/OL]. Front Neurosci, 2022, 16: 833837 [2023-10-07]. https://doi.org/10.3389/fnins.2022.833837.
DOI:
10.3389/fnins.2022.833837.
[42]
CHU Y, WU J, WANG D, et al. Altered voxel-mirrored homotopic connectivity in right temporal lobe epilepsy as measured using resting-state fMRI and support vector machine analyses [J/OL]. Front Psychiatry, 2022, 13: 958294 [2023-10-07]. https://doi.org/10.3389/fpsyt.2022.958294.
DOI:
10.3389/fpsyt.2022.958294.
[43]
SHI K, PANG X, WANG Y, et al. Altered interhemispheric functional homotopy and connectivity in temporal lobe epilepsy based on fMRI and multivariate pattern analysis[J]. Neuroradiology, 2021, 63(11): 1873-1882.
DOI:
10.1007/s00234-021-02706-x.
[44]
SONG C, ZHANG X, HAN S, et al. Static and temporal dynamic alteration of intrinsic brain activity in MRI-negative temporal lobe epilepsy[J]. Seizure, 2023, 108: 33-42.
DOI:
10.1016/j.seizure.2023.04.004.
[45]
PANG L, FAN B, CHEN Z, et al. Disruption of cerebellar-cerebral functional connectivity in temporal lobe epilepsy and the connection to language and cognitive functions[J/OL]. Front Neurosci, 2022, 16: 871128 [2023-10-07]. https://doi.org/10.3389/fnins.2022.871128.
DOI:
10.3389/fnins.2022.871128.
[46]
WANG K, XIE F, LIU C, et al. Shared functional network abnormality in patients with temporal lobe epilepsy and their siblings[J]. CNS Neurosci Ther, 2023, 29(4): 1109-1119.
DOI:
10.1111/cns.14087.
[47]
HATLESTAD-HALL C, BRUNA R, ERICHSEN A, et al. The organization of functional neurocognitive networks in focal epilepsy correlates with domain-specific cognitive performance[J]. J Neurosci Res, 2021, 99(10): 2669-2687.
DOI:
10.1002/jnr.24896.
[48]
ZHOU X, ZHANG Z, LIU J, et al. Aberrant topological organization of the default mode network in temporal lobe epilepsy revealed by graph-theoretical analysis[J/OL]. Neurosci Lett, 2019, 708: 134351 [2023-10-07]. https://doi.org/10.1016/j.neulet.2019.134351.
DOI:
10.1016/j.neulet.2019.134351.
[49]
YU Y, CHU L, LIU C, et al. Alterations of white matter network in patients with left and right non-lesional temporal lobe epilepsy[J]. Eur Radiol, 2019, 29(12): 6750-6761.
DOI:
10.1007/s00330-019-06295-5.
[50]
MA K, ZHANG X, SONG C, et al. Altered topological properties and their relationship to cognitive functions in unilateral temporal lobe epilepsy[J/OL]. Epilepsy Behav, 2023, 144: 109247 [2023-10-07]. https://doi.org/10.1016/j.yebeh.2023.109247.
DOI:
10.1016/j.yebeh.2023.109247.
[51]
CHANG W, LIU J, NIE L, et al. The degree centrality and functional connectivity in patients with temporal lobe epilepsy presenting as ictal panic: A resting state fMRI study[J/OL]. Front Neurol, 2022, 13: 822253 [2023-10-07]. https://doi.org/10.3389/fneur.2022.822253.
DOI:
10.3389/fneur.2022.822253.
[52]
AMIRI S, MEHVARI-HABIBABADI J, MOHAMMADI-MOBARAKEH N, et al. Graph theory application with functional connectivity to distinguish left from right temporal lobe epilepsy[J/OL]. Epilepsy Res, 2020, 167: 106449 [2023-10-07]. https://doi.org/10.1016/j.eplepsyres.2020.106449.
DOI:
10.1016/j.eplepsyres.2020.106449.
[53]
TANG W Y. Study of brain functional network in intractable epilepsybased on rs-fMRI with graph theory analysis[D]. Zunyi: Zunyi Medical University, 2021.
DOI:
10.27680/d.cnki.gzyyc.2021.000022.
[54]
MA L, LIU G, ZHANG P, et al. Altered cerebro-cerebellar effective connectivity in new-onset juvenile myoclonic epilepsy[J/OL]. Brain Sci, 2022, 12(12): 1658 [2023-10-07]. https://doi.org/10.3390/brainsci12121658.
DOI:
10.3390/brainsci12121658.
