Skip to main content
SpringerLink
Log in

Disrupted functional connectivity in white matter resting-state networks in unilateral temporal lobe epilepsy

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Unilateral temporal lobe epilepsy (TLE) is the most common type of focal epilepsy characterized by foci in the unilateral temporal lobe grey matters of regions such as the hippocampus. However, it remains unclear how the functional features of white matter are altered in TLE. In the current study, resting-state functional magnetic resonance imaging (fMRI) was performed on 71 left TLE (LTLE) patients, 79 right TLE (RTLE) patients and 47 healthy controls (HC). Clustering analysis was used to identify fourteen white matter networks (WMN). The functional connectivity (FC) was calculated among WMNs and between WMNs and grey matter. Furthermore, the FC laterality of hemispheric WMNs was assessed. First, both patient groups showed decreased FCs among WMNs. Specifically, cerebellar white matter illustrated decreased FCs with the cerebral superficial WMNs, implying a dysfunctional interaction between the cerebellum and the cerebral cortex in TLE. Second, the FCs between WMNs and the ipsilateral hippocampus (grey matter foci) were also reduced in patient groups, which may suggest insufficient functional integration in unilateral TLE. Interestingly, RTLE showed more severe abnormalities of white matter FCs, including links to the bilateral hippocampi and temporal white matter, than LTLE. Taken together, these findings provide functional evidence of white matter abnormalities, extending the understanding of the pathological mechanism of white matter impairments in unilateral TLE.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agcaoglu, O., et al. (2015). Lateralization of resting state networks and relationship to age and gender. NeuroImage, 104, 310–325.

    CAS  PubMed  Google Scholar 

  • Bellec, P., et al. (2010). Multi-level bootstrap analysis of stable clusters in resting-state fMRI. NeuroImage, 51(3), 1126–1139.

    PubMed  Google Scholar 

  • Bernhardt, B. C., et al. (2016). The spectrum of structural and functional imaging abnormalities in temporal lobe epilepsy. Annals of Neurology, 80(1), 142–153.

    PubMed  Google Scholar 

  • Bonilha, L., et al. (2004). Voxel-based morphometry reveals gray matter network atrophy in refractory medial temporal lobe epilepsy. Archives of Neurology, 61(9), 1379–1384.

    PubMed  Google Scholar 

  • Cataldi, M., Avoli, M., & de Villers-Sidani, E. (2013). Resting state networks in temporal lobe epilepsy. Epilepsia, 54(12), 2048–2059.

    PubMed  PubMed Central  Google Scholar 

  • Craddock, R. C., et al. (2012). A whole brain fMRI atlas generated via spatially constrained spectral clustering. Human Brain Mapping, 33(8), 1914–1928.

    PubMed  Google Scholar 

  • DeSalvo, M. N., et al. (2014). Altered structural connectome in temporal lobe epilepsy. Radiology, 270(3), 842–848.

    PubMed  Google Scholar 

  • Desikan, R. S., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980.

    PubMed  Google Scholar 

  • Diehl, B., et al. (2008). Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia, 49(8), 1409–1418.

    PubMed  Google Scholar 

  • Ding, Z. H., et al. (2018). Detection of synchronous brain activity in white matter tracts at rest and under functional loading. Proceedings of the National Academy of Sciences of the United States of America, 115(3), 595–600.

    CAS  PubMed  Google Scholar 

  • Dupont, S., et al. (2000). Episodic memory in left temporal lobe epilepsy: A functional MRI study. Brain, 123, 1722–1732.

    PubMed  Google Scholar 

  • Engel, J., Jr., & International League Against Epilepsy. (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), 796–803.

  • Fabri, M., et al. (2011). Topographical organization of human corpus callosum: An fMRI mapping study. Brain Research, 1370, 99–111.

    CAS  PubMed  Google Scholar 

  • Fan, Y. S., et al. (2019). Impaired interactions among white-matter functional networks in antipsychotic-naive first-episode schizophrenia. Human Brain Mapping, 41(1), 230–240.

    PubMed  PubMed Central  Google Scholar 

  • Focke, N. K., et al. (2008). Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. NeuroImage, 40(2), 728–737.

    PubMed  Google Scholar 

  • Gawryluk, J. R., Mazerolle, E. L., & D’Arcy, R. C. N. (2014). Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions. Frontiers in Neuroscience. https://doi.org/10.3389/fnins.2014.00239

    Article  PubMed  PubMed Central  Google Scholar 

  • He, H., et al. (2019). Reduction in gray matter of cerebellum in schizophrenia and its influence on static and dynamic connectivity. Human Brain Mapping, 40(2), 517–528.

    PubMed  Google Scholar 

  • Ji, G. J., et al. (2019). Regional and network properties of white matter function in Parkinson’s disease. Human Brain Mapping, 40(4), 1253–1263.

    PubMed  Google Scholar 

  • Jia, X., et al. (2019). Reconfiguration of dynamic large-scale brain network functional connectivity in generalized tonic-clonic seizures. Human Brain Mapping, 41(1), 67–79.

    PubMed  PubMed Central  Google Scholar 

  • Jiang, Y., et al. (2019a). Aberrant prefrontal-thalamic-cerebellar circuit in schizophrenia and depression: Evidence from a possible causal connectivity. International Journal of Neural Systems, 29(5), 1850032.

    PubMed  Google Scholar 

  • Jiang, S., et al. (2018). Aberrant thalamocortical connectivity in juvenile myoclonic epilepsy. International Journal of Neural Systems, 28(1), 1750034.

    CAS  PubMed  Google Scholar 

  • Jiang, Y. C., et al. (2019b). White-matter functional networks changes in patients with schizophrenia. NeuroImage, 190, 172–181.

    PubMed  Google Scholar 

  • Jiang, Y. C., et al. (2019c). Dysfunctional white-matter networks in medicated and unmedicated benign epilepsy with centrotemporal spikes. Human Brain Mapping, 40(10), 3113–3124.

    PubMed  PubMed Central  Google Scholar 

  • Kelly, C., et al. (2012). A convergent functional architecture of the insula emerges across imaging modalities. NeuroImage, 61(4), 1129–1142.

    PubMed  Google Scholar 

  • Klugah-Brown, B., et al. (2019a). Altered dynamic functional network connectivity in frontal lobe epilepsy. Brain Topography, 32(3), 394–404.

    PubMed  Google Scholar 

  • Klugah-Brown, B., et al. (2019b). Altered structural and causal connectivity in frontal lobe epilepsy. Bmc Neurology. https://doi.org/10.1186/s12883-019-1300-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, E., et al. (2006). Temporal and extratemporal BOLD responses to temporal lobe interictal spikes. Epilepsia, 47(2), 343–354.

    PubMed  Google Scholar 

  • Kros, L., et al. (2015a). Controlling cerebellar output to treat refractory epilepsy. Trends in Neurosciences, 38(12), 787–799.

    CAS  PubMed  Google Scholar 

  • Kros, L., et al. (2015b). Cerebellar output controls generalized spike-and-wave discharge occurrence. Annals of Neurology, 77(6), 1027–1049.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lange, T., et al. (2004). Stability-based validation of clustering solutions. Neural Computation, 16(6), 1299–1323.

    PubMed  Google Scholar 

  • Li, W., et al. (2019a). Different patterns of white matter changes after successful surgery of mesial temporal lobe epilepsy. Neuroimage: Clinical, 21, 101631.

    Google Scholar 

  • Li, J., et al. (2019b). Exploring the functional connectome in white matter. Human Brain Mapping, 40(15), 4331–4344.

    PubMed  PubMed Central  Google Scholar 

  • Li, H., et al. (2017). Reorganization of anterior and posterior hippocampal networks associated with memory performance in mesial temporal lobe epilepsy. Clinical Neurophysiology, 128(5), 830–838.

    PubMed  Google Scholar 

  • Lorio, S., et al. (2016). New tissue priors for improved automated classification of subcortical brain structures on MRI. NeuroImage, 130, 157–166.

    CAS  PubMed  Google Scholar 

  • Luo, C., et al. (2012). Disrupted functional brain connectivity in partial epilepsy: A resting-state fMRI study. PLoS ONE, 7(1), e28196.

    CAS  PubMed Central  Google Scholar 

  • Marussich, L., et al. (2017). Mapping white-matter functional organization at rest and during naturalistic visual perception. NeuroImage, 146, 1128–1141.

    PubMed  Google Scholar 

  • McDonald, C. R., et al. (2008). Subcortical and cerebellar atrophy in mesial temporal lobe epilepsy revealed by automatic segmentation. Epilepsy Research, 79(2–3), 130–138.

    PubMed  PubMed Central  Google Scholar 

  • McIntyre, D. C., & Gilby, K. L. (2008). Mapping seizure pathways in the temporal lobe. Epilepsia, 49(Suppl 3), 23–30.

    PubMed  Google Scholar 

  • Morgan, V. L., Abou-Khalil, B., & Rogers, B. P. (2015). Evolution of functional connectivity of brain networks and their dynamic interaction in temporal lobe epilepsy. Brain Connect, 5(1), 35–44.

    PubMed  PubMed Central  Google Scholar 

  • Morgan, V. L., et al. (2019). Divergent network properties that predict early surgical failure versus late recurrence in temporal lobe epilepsy. Journal of Neurosurgery, 132(5), 1324–1333.

    PubMed  Google Scholar 

  • Peer, M., et al. (2017). Evidence for functional networks within the human brain’s white matter. Journal of Neuroscience, 37(27), 6394–6407.

    CAS  PubMed  Google Scholar 

  • Qin, Y., et al. (2019). BOLD-fMRI activity informed by network variation of scalp EEG in juvenile myoclonic epilepsy. NeuroImage: Clinical, 22, 101759.

    Google Scholar 

  • Rodrigo, S., et al. (2007). Uncinate fasciculus fiber tracking in mesial temporal lobe epilepsy. Initial findings. European Radiology, 17(7), 1663–1668.

    CAS  PubMed  Google Scholar 

  • Schuck, N. W., et al. (2016). Human orbitofrontal cortex represents a cognitive map of state space. Neuron, 91(6), 1402–1412.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tellez-Zenteno, J. F., & Hernandez-Ronquillo, L. (2012). A review of the epidemiology of temporal lobe epilepsy. Epilepsy Research and Treatment, 2012, 630853.

    PubMed  Google Scholar 

  • Tzourio-Mazoyer, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289.

    CAS  PubMed  Google Scholar 

  • Umeoka, S. C., et al. (2012). Requirement of longitudinal synchrony of epileptiform discharges in the hippocampus for seizure generation: A pilot study. Journal of Neurosurgery, 116(3), 513–524.

    PubMed  Google Scholar 

  • Voets, N. L., et al. (2012). Structural substrates for resting network disruption in temporal lobe epilepsy. Brain, 135, 2350–2357.

    PubMed  Google Scholar 

  • Wei, W., et al. (2016). more severe extratemporal damages in mesial temporal lobe epilepsy with hippocampal sclerosis than that with other lesions: A multimodality MRI study. Medicine, 95(10), e3020.

    PubMed  PubMed Central  Google Scholar 

  • Wu, X., et al. (2017). Functional connectivity and activity of white matter in somatosensory pathways under tactile stimulations. NeuroImage, 152, 371–380.

    PubMed  Google Scholar 

  • Xu, S. W., et al. (2018). Cognitive decline and white matter changes in mesial temporal lobe epilepsy. Medicine (Baltimore), 97(33), e11803.

    Google Scholar 

  • Yeo, B. T., et al. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106(3), 1125–1165.

    PubMed  Google Scholar 

  • Zhou, X., et al. (2019). Disruption and lateralization of cerebellar-cerebral functional networks in right temporal lobe epilepsy: A resting-state fMRI study. Epilepsy & Behavior, 96, 80–86.

    Google Scholar 

  • Zhu, X., et al. (2018). Altered spontaneous brain activity in MRI-negative refractory temporal lobe epilepsy patients with major depressive disorder: A resting-state fMRI study. Journal of the Neurological Sciences, 386, 29–35.

    PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by grants from the National Nature Science Foundation of China (Grant Number: 61933003, 81771402, 81701076, 81771822, 81960249, 81861128001), and the ‘111’ Project (B12027). We gratefully acknowledge the participation of the study subjects and investigators.

Author information

Author notes

  1. Xuan Li and Yuchao Jiang have contributed equally to this work.

Authors and Affiliations

  1. The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, Center for Information in Medicine, School of Life Science and Technology, University of Electronic Science and Technology of China, Second North Jianshe Road, Chengdu, 610054, People’s Republic of China

    Xuan Li, Yuchao Jiang, Zhiliang Li, Yan Chen, Xiaojun Zuo, Dezhong Yao & Cheng Luo

  2. Department of Neurology, West China Hospital, Sichuan University, Chengdu, 610054, People’s Republic of China

    Wei Li, Yingjie Qin, Xin Tong, Fenglai Xiao, Dong Zhou & Dongmei An

  3. Huaxi MR Research Center, Department of Radiology, West China Hospital, Sichuan University, Chengdu, 610054, People’s Republic of China

    Qiyong Gong

Authors
  1. Xuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuchao Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yingjie Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhiliang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xin Tong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fenglai Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiaojun Zuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qiyong Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Dong Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Dezhong Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Dongmei An
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Cheng Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cheng Luo.

Ethics declarations

Conflict of interest

There is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1656 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., Jiang, Y., Li, W. et al. Disrupted functional connectivity in white matter resting-state networks in unilateral temporal lobe epilepsy. Brain Imaging and Behavior 16, 324–335 (2022). https://doi.org/10.1007/s11682-021-00506-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-021-00506-8

Keywords

Search

Navigation