Skip to main content
Log in

Impaired interhemispheric synchrony and effective connectivity in right temporal lobe epilepsy

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

The brain functional network plays a crucial role in cognitive impairment in temporal lobe epilepsy (TLE). Based on voxel-mirrored homotopic connectivity (VMHC), this study explored how directed functional connectivity changes and is associated with impaired cognition in right TLE (rTLE).

Methods

Twenty-seven patients with rTLE and twenty-seven healthy controls were included to perform VMHC and Granger causality analysis (GCA). Correlation analysis was performed based on GCA and cognitive function.

Results

Bilateral middle frontal gyrus (MFG), middle temporal gyrus, dorsolateral superior frontal gyrus (SFGdor), and supramarginal gyrus (SMG) exhibited decreased VMHC values in the rTLE group. Brain regions with altered VMHC had abnormal directed functional connectivity with multiple brain regions, mainly belonging to the default mode network, sensorimotor network, and visual network. Besides, the Montreal Cognitive Assessment (MoCA) score was positively correlated with the connectivity from the left SFGdor to the right cerebellum crus2 and was negatively correlated with the connectivity from the left SMG to the right supplementary motor area (SMA) before correction. Before correction, both phasic and intrinsic alertness reaction time were positively correlated with the connectivity from the left MFG to the left precentral gyrus (PreCG), connectivity from the left SMG to the right PreCG, and the connectivity from the left SMG to the right SMA. The executive control effect reaction time was positively correlated with the connectivity from the left MFG to the left calcarine fissure surrounding cortex before correction.

Conclusion

The disordered functional network tended to be correlated with cognition impairment in rTLE.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Data is available upon request.

References

  1. Dumlu SN, Ademoglu A, Sun W (2020) Investigation of functional variability and connectivity in temporal lobe epilepsy: a resting state fMRI study. Neurosci Lett 733:135076. https://doi.org/10.1016/j.neulet.2020.135076

    Article  CAS  PubMed  Google Scholar 

  2. Cataldi M, Avoli M, de Villers-Sidani E (2013) Resting state networks in temporal lobe epilepsy. Epilepsia 54:2048–2059. https://doi.org/10.1111/epi.12400

    Article  PubMed  PubMed Central  Google Scholar 

  3. Gao Y, Xiong Z, Wang X et al (2022) Abnormal degree centrality as a potential imaging biomarker for right temporal lobe epilepsy: a resting-state functional magnetic resonance imaging study and support vector machine analysis. Neuroscience 487:198–206. https://doi.org/10.1016/j.neuroscience.2022.02.004

    Article  CAS  PubMed  Google Scholar 

  4. Besson P, Dinkelacker V, Valabregue R et al (2014) Structural connectivity differences in left and right temporal lobe epilepsy. Neuroimage 100:135–144. https://doi.org/10.1016/j.neuroimage.2014.04.071

    Article  PubMed  Google Scholar 

  5. Lemkaddem A, Daducci A, Kunz N et al (2014) Connectivity and tissue microstructural alterations in right and left temporal lobe epilepsy revealed by diffusion spectrum imaging. Neuroimage Clin 5:349–358. https://doi.org/10.1016/j.nicl.2014.07.013

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  7. Mancuso L, Costa T, Nani A et al (2019) The homotopic connectivity of the functional brain: a meta-analytic approach. Sci Rep 9:3346. https://doi.org/10.1038/s41598-019-40188-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Shi K, Pang X, Wang Y, Li C, Long Q, Zheng J (2021) Altered interhemispheric functional homotopy and connectivity in temporal lobe epilepsy based on fMRI and multivariate pattern analysis. Neuroradiology 63:1873–1882. https://doi.org/10.1007/s00234-021-02706-x

    Article  PubMed  Google Scholar 

  9. Marinazzo D, Liao W, Chen H, Stramaglia S (2011) Nonlinear connectivity by Granger causality. Neuroimage 58:330–338. https://doi.org/10.1016/j.neuroimage.2010.01.099

    Article  PubMed  Google Scholar 

  10. Burianova H, Faizo NL, Gray M, Hocking J, Galloway G, Reutens D (2017) Altered functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res 137:45–52. https://doi.org/10.1016/j.eplepsyres.2017.09.001

    Article  PubMed  Google Scholar 

  11. Jokeit H, Luerding R, Ebner A (2000) Cognitive impairment in temporal-lobe epilepsy. Lancet 355:1018–1019. https://doi.org/10.1016/S0140-6736(05)74765-6

    Article  CAS  PubMed  Google Scholar 

  12. Sun YM, Peng YX, Wen Q et al (2021) Resting-state fMRI in temporal lobe epilepsy patients with cognitive impairment: a protocol for systematic review and meta-analysis. Medicine (Baltimore) 100:e27249. https://doi.org/10.1097/MD.0000000000027249

    Article  PubMed  Google Scholar 

  13. Raz A, Buhle J (2006) Typologies of attentional networks. Nat Rev Neurosci 7:367–379. https://doi.org/10.1038/nrn1903

    Article  CAS  PubMed  Google Scholar 

  14. Posner MI, Petersen SE (1990) The attention system of the human brain. Annu Rev Neurosci 13:25–42. https://doi.org/10.1146/annurev.ne.13.030190.000325

    Article  CAS  PubMed  Google Scholar 

  15. Fan J, McCandliss BD, Fossella J, Flombaum JI, Posner MI (2005) The activation of attentional networks. Neuroimage 26:471–479. https://doi.org/10.1016/j.neuroimage.2005.02.004

    Article  PubMed  Google Scholar 

  16. Fan J, Bernardi S, Van Dam NT et al (2012) Functional deficits of the attentional networks in autism. Brain Behav 2:647–660. https://doi.org/10.1002/brb3.90

    Article  PubMed  PubMed Central  Google Scholar 

  17. Zhou X, Zhang Z, Liu J, Qin L, Pang X, Zheng J (2019) Disruption and lateralization of cerebellar-cerebral functional networks in right temporal lobe epilepsy: a resting-state fMRI study. Epilepsy Behav 96:80–86. https://doi.org/10.1016/j.yebeh.2019.03.020

    Article  PubMed  Google Scholar 

  18. Fan J, McCandliss BD, Sommer T, Raz A, Posner MI (2002) Testing the efficiency and independence of attentional networks. J Cogn Neurosci 14:340–347. https://doi.org/10.1162/089892902317361886

    Article  PubMed  Google Scholar 

  19. Posner MI (2008) Measuring alertness. Ann N Y Acad Sci 1129:193–199. https://doi.org/10.1196/annals.1417.011

    Article  PubMed  Google Scholar 

  20. Shi Y, Liu W, Liu R et al (2019) Investigation of the emotional network in depression after stroke: a study of multivariate Granger causality analysis of fMRI data. J Affect Disord 249:35–44. https://doi.org/10.1016/j.jad.2019.02.020

    Article  PubMed  Google Scholar 

  21. Qiao PF, Niu GM (2017) Resting-state fMRI findings in patients with first-episode idiopathic epilepsy before and after treatment. Neurosciences (Riyadh) 22:316–319. https://doi.org/10.17712/nsj.2017.4.20160650

    Article  PubMed  Google Scholar 

  22. Zhang Z, Zhou X, Liu J et al (2020) Longitudinal assessment of resting-state fMRI in temporal lobe epilepsy: a two-year follow-up study. Epilepsy Behav 103:106858. https://doi.org/10.1016/j.yebeh.2019.106858

    Article  PubMed  Google Scholar 

  23. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202. https://doi.org/10.1146/annurev.neuro.24.1.167

    Article  CAS  PubMed  Google Scholar 

  24. Michalski LJ, Demers CH, Baranger DAA et al (2017) Perceived stress is associated with increased rostral middle frontal gyrus cortical thickness: a family-based and discordant-sibling investigation. Genes Brain Behav 16:781–789. https://doi.org/10.1111/gbb.12404

    Article  CAS  PubMed  Google Scholar 

  25. Yang H, Zhang C, Liu C et al (2018) Brain network alteration in patients with temporal lobe epilepsy with cognitive impairment. Epilepsy Behav 81:41–48. https://doi.org/10.1016/j.yebeh.2018.01.024

    Article  PubMed  Google Scholar 

  26. Zhang C, Yang H, Qin W et al (2017) Characteristics of resting-state functional connectivity in intractable unilateral temporal lobe epilepsy patients with impaired executive control function. Front Hum Neurosci 11:609. https://doi.org/10.3389/fnhum.2017.00609

    Article  PubMed  PubMed Central  Google Scholar 

  27. Thiebaut de Schotten M, Urbanski M, Valabregue R, Bayle DJ, Volle E (2014) Subdivision of the occipital lobes: an anatomical and functional MRI connectivity study. Cortex 56:121–137. https://doi.org/10.1016/j.cortex.2012.12.007

    Article  PubMed  Google Scholar 

  28. Gong L, Xu R, Liu D et al (2020) Abnormal functional connectivity density in patients with major depressive disorder with comorbid insomnia. J Affect Disord 266:417–423. https://doi.org/10.1016/j.jad.2020.01.088

    Article  PubMed  Google Scholar 

  29. Huang Q, Xiao M, Ai M et al (2021) Disruption of neural activity and functional connectivity in adolescents with major depressive disorder who engage in non-suicidal self-injury: a resting-state fMRI study. Front Psychiatry 12:571532. https://doi.org/10.3389/fpsyt.2021.571532

    Article  PubMed  PubMed Central  Google Scholar 

  30. Yang YL, Deng HX, Xing GY, Xia XL, Li HF (2015) Brain functional network connectivity based on a visual task: visual information processing-related brain regions are significantly activated in the task state. Neural Regen Res 10:298–307. https://doi.org/10.4103/1673-5374.152386

    Article  PubMed  PubMed Central  Google Scholar 

  31. Zhang Z, Lu G, Zhong Y et al (2009) Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI. J Neurol 256:1705–1713. https://doi.org/10.1007/s00415-009-5187-2

    Article  PubMed  Google Scholar 

  32. Ji GJ, Zhang Z, Zhang H et al (2013) Disrupted causal connectivity in mesial temporal lobe epilepsy. PLoS ONE 8:e63183. https://doi.org/10.1371/journal.pone.0063183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Power JD, Cohen AL, Nelson SM et al (2011) Functional network organization of the human brain. Neuron 72:665–678. https://doi.org/10.1016/j.neuron.2011.09.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Zhang R, Volkow ND (2019) Brain default-mode network dysfunction in addiction. Neuroimage 200:313–331. https://doi.org/10.1016/j.neuroimage.2019.06.036

    Article  CAS  PubMed  Google Scholar 

  35. Mohan A, Roberto AJ, Mohan A et al (2016) The significance of the default mode network (DMN) in neurological and neuropsychiatric disorders: a review. Yale J Biol Med 89:49–57

    PubMed  PubMed Central  Google Scholar 

  36. MacEachern SJ, Santoro JD, Hahn KJ et al (2020) Children with epilepsy demonstrate macro- and microstructural changes in the thalamus, putamen, and amygdala. Neuroradiology 62:389–397. https://doi.org/10.1007/s00234-019-02332-8

    Article  PubMed  Google Scholar 

  37. Li W, Qin W, Liu H et al (2013) Subregions of the human superior frontal gyrus and their connections. Neuroimage 78:46–58. https://doi.org/10.1016/j.neuroimage.2013.04.011

    Article  PubMed  Google Scholar 

  38. Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23–32. https://doi.org/10.1007/s002210000397

    Article  CAS  PubMed  Google Scholar 

  39. Desgranges B, Baron JC, Eustache F (1998) The functional neuroanatomy of episodic memory: the role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage 8:198–213. https://doi.org/10.1006/nimg.1998.0359

    Article  CAS  PubMed  Google Scholar 

  40. Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324. https://doi.org/10.1016/j.neuron.2008.04.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Buckner RL (2013) The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 80:807–815. https://doi.org/10.1016/j.neuron.2013.10.044

    Article  CAS  PubMed  Google Scholar 

  42. Guell X, Gabrieli JDE, Schmahmann JD (2018) Triple representation of language, working memory, social and emotion processing in the cerebellum: convergent evidence from task and seed-based resting-state fMRI analyses in a single large cohort. Neuroimage 172:437–449. https://doi.org/10.1016/j.neuroimage.2018.01.082

    Article  PubMed  Google Scholar 

  43. Hoche F, Guell X, Vangel MG, Sherman JC, Schmahmann JD (2018) The cerebellar cognitive affective/Schmahmann syndrome scale. Brain 141:248–270. https://doi.org/10.1093/brain/awx317

    Article  PubMed  Google Scholar 

  44. Schmahmann JD, Guell X, Stoodley CJ, Halko MA (2019) The theory and neuroscience of cerebellar cognition. Annu Rev Neurosci 42:337–364. https://doi.org/10.1146/annurev-neuro-070918-050258

    Article  CAS  PubMed  Google Scholar 

  45. Schmahmann JD, Macmore J, Vangel M (2009) Cerebellar stroke without motor deficit: clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience 162:852–861. https://doi.org/10.1016/j.neuroscience.2009.06.023

    Article  CAS  PubMed  Google Scholar 

  46. Chen Z, Zhang R, Huo H, Liu P, Zhang C, Feng T (2022) Functional connectome of human cerebellum. Neuroimage 251:119015. https://doi.org/10.1016/j.neuroimage.2022.119015

    Article  PubMed  Google Scholar 

  47. Zanao TA, Lopes TM, de Campos BM, Yasuda CL, Cendes F (2021) Patterns of default mode network in temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsy Behav 121:106523. https://doi.org/10.1016/j.yebeh.2019.106523

    Article  PubMed  Google Scholar 

  48. Vaccaro MG, Trimboli M, Scarpazza C et al (2018) Neuropsychological profile of mild temporal lobe epilepsy. Epilepsy Behav 85:222–226. https://doi.org/10.1016/j.yebeh.2018.06.013

    Article  PubMed  Google Scholar 

  49. Labate A, Aguglia U, Tripepi G et al (2016) Long-term outcome of mild mesial temporal lobe epilepsy: a prospective longitudinal cohort study. Neurology 86:1904–1910. https://doi.org/10.1212/WNL.0000000000002674

    Article  PubMed  Google Scholar 

  50. Lopez SM, Aksman LM, Oxtoby NP et al (2022) Event-based modeling in temporal lobe epilepsy demonstrates progressive atrophy from cross-sectional data. Epilepsia 63:2081–2095. https://doi.org/10.1111/epi.17316

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to express their gratitude to EditSprings (https://www.editsprings.com/) for the expert linguistic services provided. A previous version of this manuscript has been preprinted on Authorea (https://doi.org/10.22541/au.167146514.42115408/v1).

Funding

The work is supported by the Natural Science Foundation of Guangxi Province (2018GXNSFAA050149).

Author information

Authors and Affiliations

Authors

Contributions

The contributions are as follows. Ke Shi: data analysis and writing of the paper draft. Lu Yu: methodology and modification of paper draft. Yiling Wang: literature research and visualization. Zhekun Li, Chunyan Li, and Qijia Long: data acquisition. Jinou Zheng: conceptualization, study design, and supervision.

Corresponding author

Correspondence to Jinou Zheng.

Ethics declarations

Ethical approval

This study was approved by the Medical Research Ethics Committee of the First Affiliated Hospital of Guangxi Medical University (2020-KY-GUOJI-010).

Conflict of interest

The authors declare no competing interests.

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 (XLSX 11 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, K., Yu, L., Wang, Y. et al. Impaired interhemispheric synchrony and effective connectivity in right temporal lobe epilepsy. Neurol Sci 45, 2211–2221 (2024). https://doi.org/10.1007/s10072-023-07198-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-023-07198-6

Keywords

Navigation