Top

Published in:

01-05-2019 | Original Paper

Altered Dynamic Functional Network Connectivity in Frontal Lobe Epilepsy

Authors: Benjamin Klugah-Brown, Cheng Luo, Hui He, Sisi Jiang, Gabriel Kofi Armah, Yu Wu, Jianfu Li, Wenjie Yin, Dezhong Yao

Published in: Brain Topography | Issue 3/2019

Abstract

Frontal lobe epilepsy has recently been associated with disrupted brain functional connectivity; variations among various resting-state networks (RSNs) across time remains largely unclear. This study applied dynamic functional network connectivity (dFNC) analysis to investigate functional patterns in the temporal and spatial domains of various functional systems in FLE. Resting-state fMRI data were acquired from 19 FLE patients and 18 controls. Independent component analysis was used to decompose RSNs, which were grouped into seven functional systems. Sliding windows and clustering approach were used to identify the dFNC patterns. Then, state-specific connectivity pattern and dynamic functional state interactions (dFSIs) were evaluated. Compared with healthy controls, FLE patients exhibited decreased dFNC in almost all four patterns, changes that were mostly related to the frontoparietal system, suggesting a disturbed communication of the frontoparietal system with other systems in FLE. Additionally, regarding the fundamental connectivity pattern (state 3 in this study), FLE showed decreased time spent in this state. Moreover, the duration positively correlated with seizure onset. Furthermore, significantly reduced dynamic connections in this state were observed in the frontoparietal system linked to the cerebellar and subcortical systems. These findings imply abnormal fundamental dynamic interactions and dysconnectivity associated with the subcortical and cerebellar regulation of dysfunctions in frontoparietal regions in FLE. Finally, based on the developed FSI analysis, temporal dynamic abnormalities among states were observed in FLE. Therefore, this altered dynamic FNC extended our understanding of the abnormalities in the frontoparietal system in FLE. The dynamic FNC provided novel insight into the fundamental pathophysiological mechanisms in FLE.

Available only for authorised users

Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2011) Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 24:663–676CrossRef

An D, Dubeau F, Gotman J (2015) BOLD responses related to focal spikes and widespread bilateral synchronous discharges generated in the frontal lobe. Epilepsia 56(3):366–374CrossRef

Beckmann CF, Mackay CE, Filippini N, Smith SM (2009) Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. NeuroImage 47:S39–S41. https://doi.org/10.1016/S1053-8119(09)71511-3 CrossRef

Beleza P, Pinho J (2011) Frontal lobe epilepsy. J Clin Neurosci 18(5):593–600CrossRefPubMed

Braakman H, Vaessen M, Hofman P, Debeij-van Hall M, Backes W, Vles J, Aldenkamp A (2011) Cognitive and behavioral complications of frontal lobe epilepsy in children: a review of the literature. Epilepsia 52:849–856CrossRefPubMed

Braakman H, Vaessen M, Jansen J, Debeij-van Hall M, de Louw A, Hofman P et al (2013) Frontal lobe connectivity and cognitive impairment in pediatric frontal lobe epilepsy. Epilepsia 54:446–454CrossRefPubMed

Chang C, Glover G (2010) Time frequency dynamics of resting state brain connectivity measured with fMRI. Neuroimage 50:81–98. https://doi.org/10.1016/j.neuroimage.2009.12.001 CrossRefPubMed

Damaraju E, Allen E, Belger A, Ford J, McEwen S, Mathalon D et al (2014) Dynamic functional connectivity analysis reveals transient states of dysconnectivity in schizophrenia. NeuroImage:Clinical 5:298–308CrossRefPubMedPubMedCentral

Deco G, Ponce-Alvarez A, Mantini D, Romani G, Hagmann P, Corbetta M (2013) Resting-state functional connectivity emerges from structural and dynamically shaped slow linear fluctuation. J Neurosci 33:11239–11252CrossRefPubMedPubMedCentral

Direito B, Teixeira CA, Sales F, Castelo-Branco M, Dourado A (2017) A realistic seizure prediction study based on multiclass SVM. Int J Neural Syst 27(3):1750006. https://doi.org/10.1142/S012906571750006X CrossRefPubMed

Doelken M, Mennecke A, Huppertz H (2012) Multimodality approach in cryptogenic epilepsy with focus on morphometric 3T MRI. J Neuroradiol 39(2):87–96CrossRefPubMed

Dong L, Wang P, Peng R, Jiang S, Klugah-Brown B, Luo C, Yao D (2016) Altered basal ganglia-cortical functional connections in frontal lobe epilepsy: a resting-state fMRI study. Epilepsy Res 128:12–20CrossRefPubMed

Dong L, Luo C, Liu X, Jiang S, Feng H, Li J, Gong D, Yao D (2018) Neuroscience information toolbox: an open source toolbox for EEG-fMRI multimodal fusion analysis. Front Neuroinform 12:56CrossRefPubMedPubMedCentral

Engel J Jr, International League Against Epilepsy (ILAE) (2001) A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 42(6):796–803CrossRefPubMed

Exner C, Boucsein K, Lange C, Winter H, Weniger G, Steinhoff B, Irle E (2002) Neuropsychological performance in frontal lobe epilepsy. Seizure 11:20–32CrossRefPubMed

Fletcher P, Henson R (2001) Henson, frontal lobes and human memory. Brain 124:849–881CrossRefPubMed

Geier C, Lehnertz K (2017) Which brain regions are important for seizure dynamics in epileptic networks? Influence of link identification and EEG recording montage on node centralities. Int J Neural Syst 27(1):1550035. https://doi.org/10.1142/S0129065715500355 CrossRef

Graña M, Ozaeta L, Chyzhyk D (2017) Resting state effective connectivity allows auditory hallucination discrimination. Int J Neural Syst 27(05):1750019. https://doi.org/10.1142/S0129065717500198 CrossRefPubMed

Jafri M, GD P, Stevens M, Calhoun V (2008) A method for functional network connectivity among spatially independent resting-state components in schizophrenia. Neuroimage 39:1666–1681CrossRefPubMed

Jiang S, Luo C, Gong J, Peng R, Ma S, Tan S et al (2017) Aberrant thalamocortical connectivity in juvenile myoclonic epilepsy. Int J Neural Syst. https://doi.org/10.1142/S0129065717500344 CrossRefPubMed

Jiang Y, Luo C, Li X, Li Y, Yang H, Li J, Chang X, Li H, Yang H, Wang J, Duan M, Yao D (2018) White-matter functional networks changes in patients with schizophrenia. Neuroimage. https://doi.org/10.1016/j.neuroimage.2018.1004.1018 CrossRefPubMedPubMedCentral

Kellinghaus C, Lüders HO (2004) Frontal lobe epilepsy. Epileptic Disord 6(4):223–239

Kros L, Eelkman RO, De Zeeuw C, Hoebeek F (2015a) Controlling cerebellar output to treat refractory epilepsy. Trends Neurosci 38(12):787–799. https://doi.org/10.1016/j.tins.2015.10.002 CrossRefPubMed

Kros L, Eelkman ROH, Spanke JK, Alva P, van Dongen MN, Karapatis A et al (2015b) Cerebellar output controls generalized spike-and-wave discharge occurrence. Ann Neurol. https://doi.org/10.1002/ana.24399 CrossRefPubMedPubMedCentral

Li Q, Cao W, Liao X, Chen Z, Yang T, Gong Q et al (2015) Altered resting state functional network connectivity in children absence epilepsy. J Neurol Sci 354(1–2):79–85CrossRefPubMed

Li J, Zhou W, Yuan S, Zhang Y, Li C, Wu Q (2016) An Improved sparse representation over learned dictionary method for seizure detection. Int J Neural Syst 26(1):1750006. https://doi.org/10.1142/S012906571750006X CrossRef

Li Q, Chen Y, Wei Y, Chen S, Ma L, He Z, Chen Z (2017a) Functional network connectivity patterns between idiopathic generalized epilepsy with myoclonic and absence seizures. Front Comput Neurosci. https://doi.org/10.3389/fncom.2017.00038. (ecollection)CrossRefPubMedPubMedCentral

Li R, Ji GJ, Yu Y, Yu Y, Ding MP, Tang YL, Chen H, Liao W (2017b) Epileptic discharge related functional connectivity within and between networks in benign epilepsy with centrotemporal spikes. Int J Neural Syst 27(7):1750018. https://doi.org/10.1142/S0129065717500186 CrossRefPubMed

Luo C, Qiu C, Guo Z, Fang J, Li Q, Lei X et al (2012) Disrupted functional brain connectivity in partial epilepsy: a resting-state fMRI study. PLoS ONE 7:e28196CrossRefPubMedCentral

Luo C, An D, Yao D, Gotman J (2014) Patient-specific connectivity pattern of epileptic network in frontal lobe epilepsy. Neuroimage Clin 4:668–675CrossRefPubMedPubMedCentral

Luo C, Zhang Y, Cao W, Huang Y, Yang F, Wang J et al (2015) Altered structural and functional feature of striato-cortical circuit in benign epilepsy with centrotemporal spikes. Int J Neural Syst 25(6): 1550027CrossRefPubMed

Mayo Clinic (2008) Mayoclinic. http://Mayoclinic.com. Accessed Sept 2017

McAvoy M, Larson-Prior L, Nolan T, Vaishnavi S, Raichle M, d’Avossa G (2008) Resting states affect spontaneous BOLD oscillation in sensory and paralimbic cortex. J Neurophysiol 100:922–931CrossRefPubMedPubMedCentral

Norden A, Blumenfeld H (2002) The role of subcortical structures in human epilepsy. Epilepsy Behav 3:219–231CrossRefPubMed

Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefPubMed

Rashid B, Damaraju E, Pearlson GD, Calhoun VD (2014) Dynamic connectivity states estimated from resting fMRI Identify differences among Schizophrenia, bipolar disorder, and healthy control subjects. Front Hum Neurosci 8:897. https://doi.org/10.3389/fnhum.2014.00897. (eCollection 2014)CrossRefPubMedPubMedCentral

Shen K, Hutchison R, Bezgin G, Everling S, McIntosh A (2015) Network structure shapes spontaneous functional connectivity dynamics. J Neurosci 35:5579–5588CrossRefPubMedPubMedCentral

Tan Y, Tan J, Deng J, Cui W, He H, Yang F et al (2015) Alteration of basal ganglia and right frontoparietal network in early drug-naive Parkinson’s disease during heat pain stimuli and resting state. Front Hum Neurosci 9:467CrossRefPubMedPubMedCentral

Tracy J, Doucet G (2015) Resting-state functional connectivity in epilepsy: growing relevance for clinical decision making. Curr Opin Neurol 28(2):158–165CrossRefPubMed

Wang L, Liu Q, Shen H, Li H, Hu D (2015) Large-scale functional brain network changes in taxi drivers: evidence from resting state fMRI. Hum Brain Mapp 36:862–871CrossRefPubMed

Williamson P, Jobst B (2000) Frontal lobe epilepsy. In: Williamson P, Siegel A, Roberts D, Thadani V, Gazzaniga M, (eds) Advances in neurology. Raven Press, Philadelphia pp 215–251

Xiaobo C, Han Z, Yue G, Chong-Yaw W, Gang L, Dinggang S, the Alzheimer’s Disease Neuroimaging Initiative (2016) High-order resting-state functional connectivity network for MCI classification. Hum Brain Mapp 37: 3282–3296CrossRef

Zhang H, Chen X, Zhang Y, Shen D (2017) Test-Retest Reliability of “high-order” functional connectivity in young healthy adults. Front Neurosci 11:439. https://doi.org/10.3389/fnins.2017.00439 CrossRefPubMedPubMedCentral

Zhong C, Liu R, Luo C, Jiang S, Dong L, Peng R, Guo F, Wang P (2018) Altered structural and functional connectivity of juvenile myoclonic epilepsy: an fMRI study. Neural Plast. https://doi.org/10.1155/2018/7392187 CrossRefPubMedPubMedCentral

Title: Altered Dynamic Functional Network Connectivity in Frontal Lobe Epilepsy
Authors: Benjamin Klugah-Brown
Cheng Luo
Hui He
Sisi Jiang
Gabriel Kofi Armah
Yu Wu
Jianfu Li
Wenjie Yin
Dezhong Yao
Publication date: 01-05-2019
Publisher: Springer US
Published in: Brain Topography / Issue 3/2019
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-018-0678-z

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Altered Dynamic Functional Network Connectivity in Frontal Lobe Epilepsy

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2019

MEG Assessment of Expressive Language in Children Evaluated for Epilepsy Surgery

Brain Activity Mapping from MEG Data via a Hierarchical Bayesian Algorithm with Automatic Depth Weighting

Cortical Inhibition of Face and Jaw Muscle Activity and Discomfort Induced by Repetitive and Paired-Pulse TMS During an Overt Object Naming Task

Towards the Neuromotor Control Processes of Steady-State and Speed-Matched Treadmill and Overground Walking

A Comparison of Evoked and Non-evoked Functional Networks

Altered Oscillatory Responses to Feedback in Borderline Personality Disorder are Linked to Symptom Severity