Skip to main content
Top
Published in: BMC Neurology 1/2022

Open Access 01-12-2022 | Epilepsy | Research

A study of brain functional network and alertness changes in temporal lobe epilepsy with and without focal to bilateral tonic–clonic seizures

Authors: Liluo Nie, Yanchun Jiang, Zongxia Lv, Xiaomin Pang, Xiulin Liang, Weiwei Chang, Jinou Zheng

Published in: BMC Neurology | Issue 1/2022

Login to get access

Abstract

Background

Temporal lobe epilepsy (TLE) is commonly refractory. Epilepsy surgery is an effective treatment strategy for refractory epilepsy, but patients with a history of focal to bilateral tonic-clonic seizures (FBTCS) have poor outcomes. Previous network studies on epilepsy have found that TLE and idiopathic generalized epilepsy with generalized tonic-clonic seizures (IGE-GTCS) showed altered global and nodal topological properties. Alertness deficits also were found in TLE. However, FBTCS is a common type of seizure in TLE, and the implications for alertness as well as the topological rearrangements associated with this seizure type are not well understood.

Methods

We obtained rs-fMRI data and collected the neuropsychological assessment data from 21 TLE patients with FBTCS (TLE- FBTCS), 18 TLE patients without FBTCS (TLE-non- FBTCS) and 22 controls, and constructed their respective functional brain networks. The topological properties were analyzed using the graph theoretical approach and correlations between altered topological properties and alertness were analyzed.

Results

We found that TLE-FBTCS patients showed more serious impairment in alertness effect, intrinsic alertness and phasic alertness than the patients with TLE-non-FBTCS. They also showed significantly higher small-worldness, normalized clustering coefficient (γ) and a trend of higher global network efficiency (gE) compared to TLE-non-FBTCS patients. The gE showed a significant negative correlation with intrinsic alertness for TLE-non-FBTCS patients.

Conclusion

Our findings show different impairments in brain network information integration, segregation and alertness between the patients with TLE-FBTCS and TLE-non-FBTCS, demonstrating that impairments of the brain network may underlie the disruptions in alertness functions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512–21.CrossRef Scheffer IE, Berkovic S, Capovilla G, Connolly MB, French J, Guilhoto L, et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58:512–21.CrossRef
2.
go back to reference Englot DJ, Lee AT, Tsai C, Halabi C, Barbaro NM, Auguste KI, et al. Seizure types and frequency in patients who “fail” temporal lobectomy for intractable epilepsy. Neurosurgery. 2013;73:838–44.CrossRef Englot DJ, Lee AT, Tsai C, Halabi C, Barbaro NM, Auguste KI, et al. Seizure types and frequency in patients who “fail” temporal lobectomy for intractable epilepsy. Neurosurgery. 2013;73:838–44.CrossRef
3.
go back to reference Englot DJ, Rutkowski MJ, Ivan ME, Sun PP, Kuperman RA, Chang EF, et al. Effects of temporal lobectomy on consciousness-impairing and consciousness-sparing seizures in children. Childs Nerv Syst. 2013;29:1915–22.CrossRef Englot DJ, Rutkowski MJ, Ivan ME, Sun PP, Kuperman RA, Chang EF, et al. Effects of temporal lobectomy on consciousness-impairing and consciousness-sparing seizures in children. Childs Nerv Syst. 2013;29:1915–22.CrossRef
4.
go back to reference Caciagli L, Bernasconi A, Wiebe S, Koepp MJ, Bernasconi N, Bernhardt BC. A meta-analysis on progressive atrophy in intractable temporal lobe epilepsy: time is brain? Neurology. 2017;89:506–16.CrossRef Caciagli L, Bernasconi A, Wiebe S, Koepp MJ, Bernasconi N, Bernhardt BC. A meta-analysis on progressive atrophy in intractable temporal lobe epilepsy: time is brain? Neurology. 2017;89:506–16.CrossRef
5.
go back to reference Keller SS, Richardson MP, Schoene-Bake JC, O’Muircheartaigh J, Elkommos S, Kreilkamp B, et al. Thalamotemporal alteration and postoperative seizures in temporal lobe epilepsy. Ann Neurol. 2015;77:760–74.CrossRef Keller SS, Richardson MP, Schoene-Bake JC, O’Muircheartaigh J, Elkommos S, Kreilkamp B, et al. Thalamotemporal alteration and postoperative seizures in temporal lobe epilepsy. Ann Neurol. 2015;77:760–74.CrossRef
7.
go back to reference Ryvlin P, Rheims S. Predicting epilepsy surgery outcome. Curr Opin Neurol. 2016;29:182–8.CrossRef Ryvlin P, Rheims S. Predicting epilepsy surgery outcome. Curr Opin Neurol. 2016;29:182–8.CrossRef
8.
go back to reference Yang L, Li H, Zhu L, Yu X, Jin B, Chen C, et al. Localized shape abnormalities in the thalamus and pallidum are associated with secondarily generalized seizures in mesial temporal lobe epilepsy. Epilepsy Behav. 2017;70:259–64.CrossRef Yang L, Li H, Zhu L, Yu X, Jin B, Chen C, et al. Localized shape abnormalities in the thalamus and pallidum are associated with secondarily generalized seizures in mesial temporal lobe epilepsy. Epilepsy Behav. 2017;70:259–64.CrossRef
9.
go back to reference Blumenfeld H, Varghese GI, Purcaro MJ, Motelow JE, Enev M, McNally KA, et al. Cortical and subcortical networks in human secondarily generalized tonicclonic seizures. Brain. 2009;132:999–1012.CrossRef Blumenfeld H, Varghese GI, Purcaro MJ, Motelow JE, Enev M, McNally KA, et al. Cortical and subcortical networks in human secondarily generalized tonicclonic seizures. Brain. 2009;132:999–1012.CrossRef
10.
go back to reference Chen C, Li H, Ding F, Yang L, Huang P, Wang S, et al. Alterations in the hippocampal-thalamic pathway underlying secondarily generalized tonic–clonic seizures in mesial temporal lobe epilepsy: a diffusion tensor imaging study. Epilepsia. 2019;60:121–30.CrossRef Chen C, Li H, Ding F, Yang L, Huang P, Wang S, et al. Alterations in the hippocampal-thalamic pathway underlying secondarily generalized tonic–clonic seizures in mesial temporal lobe epilepsy: a diffusion tensor imaging study. Epilepsia. 2019;60:121–30.CrossRef
11.
go back to reference He X, Doucet GE, Sperling M, Sharan A, Tracy JI. Reduced thalamocortical functional connectivity in temporal lobe epilepsy. Epilepsia. 2015;56:1571–9.CrossRef He X, Doucet GE, Sperling M, Sharan A, Tracy JI. Reduced thalamocortical functional connectivity in temporal lobe epilepsy. Epilepsia. 2015;56:1571–9.CrossRef
12.
go back to reference Bernhardt BC, Fadaie F, Liu M, Caldairou B, Gu S, Jefferies E, et al. Temporal lobe epilepsy: hippocampal pathology modulates connectome topology and controllability. Neurology. 2019;92:E2209–20.CrossRef Bernhardt BC, Fadaie F, Liu M, Caldairou B, Gu S, Jefferies E, et al. Temporal lobe epilepsy: hippocampal pathology modulates connectome topology and controllability. Neurology. 2019;92:E2209–20.CrossRef
13.
go back to reference He X, Chaitanya G, Asma B, Caciagli L, Bassett DS, Tracy JI, et al. Disrupted basal ganglia-thalamocortical loops in focal to bilateral tonic-clonic seizures. Brain. 2020;143:175–90.CrossRef He X, Chaitanya G, Asma B, Caciagli L, Bassett DS, Tracy JI, et al. Disrupted basal ganglia-thalamocortical loops in focal to bilateral tonic-clonic seizures. Brain. 2020;143:175–90.CrossRef
14.
go back to reference Chiang S, Haneef Z. Graph theory findings in the pathophysiology of temporal lobe epilepsy. Clin Neurophysiol. 2014;125:1295–305.CrossRef Chiang S, Haneef Z. Graph theory findings in the pathophysiology of temporal lobe epilepsy. Clin Neurophysiol. 2014;125:1295–305.CrossRef
15.
go back to reference Jiang W, Li J, Chen X, Ye W, Zheng J. Disrupted structural and functional networks and their correlation with alertness in right temporal lobe epilepsy: a graph theory study. Front Neurol. 2017;8:179. Jiang W, Li J, Chen X, Ye W, Zheng J. Disrupted structural and functional networks and their correlation with alertness in right temporal lobe epilepsy: a graph theory study. Front Neurol. 2017;8:179.
16.
go back to reference Yasuda CL, Chen Z, Beltramini GC, Coan AC, Morita ME, Kubota B, et al. Aberrant topological patterns of brain structural network in temporal lobe epilepsy. Epilepsia. 2015;56:1992–2002.CrossRef Yasuda CL, Chen Z, Beltramini GC, Coan AC, Morita ME, Kubota B, et al. Aberrant topological patterns of brain structural network in temporal lobe epilepsy. Epilepsia. 2015;56:1992–2002.CrossRef
17.
go back to reference Zhang Z, Liao W, Chen H, Mantini D, Ding JR, Xu Q, et al. Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain. 2011;134:2912–28.CrossRef Zhang Z, Liao W, Chen H, Mantini D, Ding JR, Xu Q, et al. Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain. 2011;134:2912–28.CrossRef
20.
go back to reference Zhou X, Zhang Z, Liu J, Qin L, Pang X, Zheng J. Disruption and lateralization of cerebellar–cerebral functional networks in right temporal lobe epilepsy: a resting-state fMRI study. Epilepsy Behav. 2019;96:80–6.CrossRef Zhou X, Zhang Z, Liu J, Qin L, Pang X, Zheng J. Disruption and lateralization of cerebellar–cerebral functional networks in right temporal lobe epilepsy: a resting-state fMRI study. Epilepsy Behav. 2019;96:80–6.CrossRef
24.
go back to reference Mei CX, Hong HD, Rong CZ, Ye W, Xia LZ, Ou ZJ. Temporal lobe epilepsy: decreased thalamic resting-state functional connectivity and their relationships with alertness performance. Epilepsy Behav. 2015;44:47–54.CrossRef Mei CX, Hong HD, Rong CZ, Ye W, Xia LZ, Ou ZJ. Temporal lobe epilepsy: decreased thalamic resting-state functional connectivity and their relationships with alertness performance. Epilepsy Behav. 2015;44:47–54.CrossRef
27.
go back to reference Vlooswijk MCG, Jansen JFA, Reijs RP, de Krom MCTFM, Kooi ME, Majoie HJM, et al. Cognitive fMRI and neuropsychological assessment in patients with secondarily generalized seizures. Clin Neurol Neurosurg. 2008;110:441–50.CrossRef Vlooswijk MCG, Jansen JFA, Reijs RP, de Krom MCTFM, Kooi ME, Majoie HJM, et al. Cognitive fMRI and neuropsychological assessment in patients with secondarily generalized seizures. Clin Neurol Neurosurg. 2008;110:441–50.CrossRef
28.
go back to reference Thompson PJ, Duncan JS. Cognitive decline in severe intractable epilepsy. Epilepsia. 2005;46:1780–7.CrossRef Thompson PJ, Duncan JS. Cognitive decline in severe intractable epilepsy. Epilepsia. 2005;46:1780–7.CrossRef
29.
go back to reference Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55:475–82.CrossRef Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia. 2014;55:475–82.CrossRef
32.
go back to reference Walser G, Unterberger I, Dobesberger J, Embacher N, Falkenstetter T, Larch J, et al. Asymmetric seizure termination in primary and secondary generalized tonic-clonic seizures. Epilepsia. 2009;50:2035–9.CrossRef Walser G, Unterberger I, Dobesberger J, Embacher N, Falkenstetter T, Larch J, et al. Asymmetric seizure termination in primary and secondary generalized tonic-clonic seizures. Epilepsia. 2009;50:2035–9.CrossRef
33.
go back to reference Chianga S, Sternb JM, Engel JJ, Levin HS, Haneef Z. Differences in graph theory functional connectivity in left and right temporal lobe epilepsy. Epilepsy Res. 2014;108:1770–81.CrossRef Chianga S, Sternb JM, Engel JJ, Levin HS, Haneef Z. Differences in graph theory functional connectivity in left and right temporal lobe epilepsy. Epilepsy Res. 2014;108:1770–81.CrossRef
34.
go back to reference Niaz FE, Abou-Khalil B, Fakhoury T. The generalized tonic-clonic seizure in partial versus generalized epilepsy: Semiologic differences. Epilepsia. 1999;40:1664–6.CrossRef Niaz FE, Abou-Khalil B, Fakhoury T. The generalized tonic-clonic seizure in partial versus generalized epilepsy: Semiologic differences. Epilepsia. 1999;40:1664–6.CrossRef
35.
go back to reference Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.CrossRef Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.CrossRef
36.
go back to reference Fan J, Mccandliss BD, Sommer T, Raz A, Posner MI. Testing the efficiency and independence of attentional networks. J Cogn Neurosci. 2002;14(3):340–7. Fan J, Mccandliss BD, Sommer T, Raz A, Posner MI. Testing the efficiency and independence of attentional networks. J Cogn Neurosci. 2002;14(3):340–7.
37.
go back to reference Liu J, Zhou X, Zhang Z, Qin L, Ye W, Zheng J. Disrupted functional network in patients with temporal lobe epilepsy with impaired alertness. Epilepsy Behav. 2019;101(Pt A):106573. Liu J, Zhou X, Zhang Z, Qin L, Ye W, Zheng J. Disrupted functional network in patients with temporal lobe epilepsy with impaired alertness. Epilepsy Behav. 2019;101(Pt A):106573.
38.
go back to reference Zhou M, Jiang W, Zhong D, Zheng J. Resting-state brain entropy in right temporal lobe epilepsy and its relationship with alertness. Brain Behav. 2019;9:1–12. Zhou M, Jiang W, Zhong D, Zheng J. Resting-state brain entropy in right temporal lobe epilepsy and its relationship with alertness. Brain Behav. 2019;9:1–12.
39.
go back to reference Westlye LT, Grydeland H, Walhovd KB, Fjell AM. Associations between regional cortical thickness and attentional networks as measured by the attention network test. Cereb Cortex. 2011;21:345–56.CrossRef Westlye LT, Grydeland H, Walhovd KB, Fjell AM. Associations between regional cortical thickness and attentional networks as measured by the attention network test. Cereb Cortex. 2011;21:345–56.CrossRef
40.
go back to reference Wang J, Wang X, Xia M, Liao X, Evans A, He Y. GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci. 2015;9:386. Wang J, Wang X, Xia M, Liao X, Evans A, He Y. GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci. 2015;9:386.
41.
go back to reference Prajapati R, Emerson IA. Global and regional connectivity analysis of resting-state function MRI brain images using graph theory in Parkinson’s disease. Int J Neurosci. 2020;131(2):105–15. Prajapati R, Emerson IA. Global and regional connectivity analysis of resting-state function MRI brain images using graph theory in Parkinson’s disease. Int J Neurosci. 2020;131(2):105–15.
42.
go back to reference Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci. 2006;26:63–72.CrossRef Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci. 2006;26:63–72.CrossRef
43.
go back to reference Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, et al. Functional connectivity and brain networks in schizophrenia. J Neurosci. 2010;30:9477–87.CrossRef Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, et al. Functional connectivity and brain networks in schizophrenia. J Neurosci. 2010;30:9477–87.CrossRef
44.
go back to reference Chen LT, Le FX, Li HJ, Nie S, Gong HH, Zhang W, et al. Disrupted small-world brain functional network topology in male patients with severe obstructive sleep apnea revealed by resting-state fMRI. Neuropsychiatr Dis Treat. 2017;13:1471–82.CrossRef Chen LT, Le FX, Li HJ, Nie S, Gong HH, Zhang W, et al. Disrupted small-world brain functional network topology in male patients with severe obstructive sleep apnea revealed by resting-state fMRI. Neuropsychiatr Dis Treat. 2017;13:1471–82.CrossRef
48.
go back to reference Sinha N, Peternell N, Schroeder GM, de Tisi J, Vos SB, Winston GP, et al. Focal to bilateral tonic-clonic seizures are associated with widespread network abnormality in temporal lobe epilepsy. Epilepsia. 2020;2020:1–13. Sinha N, Peternell N, Schroeder GM, de Tisi J, Vos SB, Winston GP, et al. Focal to bilateral tonic-clonic seizures are associated with widespread network abnormality in temporal lobe epilepsy. Epilepsia. 2020;2020:1–13.
49.
go back to reference Sutula TP. Mechanisms of epilepsy progression: current theories and perspectives from neuroplasticity in adulthood and development. Epilepsy Res. 2004;60:161–71.CrossRef Sutula TP. Mechanisms of epilepsy progression: current theories and perspectives from neuroplasticity in adulthood and development. Epilepsy Res. 2004;60:161–71.CrossRef
51.
go back to reference Yang D, Huang L, Luo C, Li M, Qin R, Ma J, et al. Impaired structural network properties caused by white matter Hyperintensity related to cognitive decline. Front Neurol. 2020;11:250. Yang D, Huang L, Luo C, Li M, Qin R, Ma J, et al. Impaired structural network properties caused by white matter Hyperintensity related to cognitive decline. Front Neurol. 2020;11:250.
52.
go back to reference Zhang Y, Li M, Wang R, Bi Y, Li Y, Yi Z, et al. Abnormal brain white matter network in young smokers: a graph theory analysis study. Brain Imaging Behav. 2018;12:345–56.CrossRef Zhang Y, Li M, Wang R, Bi Y, Li Y, Yi Z, et al. Abnormal brain white matter network in young smokers: a graph theory analysis study. Brain Imaging Behav. 2018;12:345–56.CrossRef
53.
go back to reference Lee K, Khoo HM, Lina JM, Dubeau F, Gotman J, Grova C. Disruption, emergence and lateralization of brain network hubs in mesial temporal lobe epilepsy. NeuroImage Clin. 2018;20:71–84.CrossRef Lee K, Khoo HM, Lina JM, Dubeau F, Gotman J, Grova C. Disruption, emergence and lateralization of brain network hubs in mesial temporal lobe epilepsy. NeuroImage Clin. 2018;20:71–84.CrossRef
55.
go back to reference Vuong J, Devergnas A. The role of the basal ganglia in the control of seizure. J Neural Transm. 2018;125:531–45.CrossRef Vuong J, Devergnas A. The role of the basal ganglia in the control of seizure. J Neural Transm. 2018;125:531–45.CrossRef
56.
go back to reference Výtvarová E, Mareček R, Fousek J, Strýček O, Rektor I. Large-scale cortico-subcortical functional networks in focal epilepsies: the role of the basal ganglia. NeuroImage Clin. 2017;14:28–36.CrossRef Výtvarová E, Mareček R, Fousek J, Strýček O, Rektor I. Large-scale cortico-subcortical functional networks in focal epilepsies: the role of the basal ganglia. NeuroImage Clin. 2017;14:28–36.CrossRef
59.
go back to reference Haneef Z, Levin HS, Chiang S. Brain graph topology changes associated with anti-epileptic drug use. Brain Connect. 2015;5:284–91.CrossRef Haneef Z, Levin HS, Chiang S. Brain graph topology changes associated with anti-epileptic drug use. Brain Connect. 2015;5:284–91.CrossRef
61.
go back to reference Gutierrez-Colina AM, Vannest J, Maloney T, Wade SL, Combs A, Horowitz-Kraus T, et al. The neural basis of executive functioning deficits in adolescents with epilepsy: a resting-state fMRI connectivity study of working memory. Brain Imaging Behav. 2020;15(1):166–76. Gutierrez-Colina AM, Vannest J, Maloney T, Wade SL, Combs A, Horowitz-Kraus T, et al. The neural basis of executive functioning deficits in adolescents with epilepsy: a resting-state fMRI connectivity study of working memory. Brain Imaging Behav. 2020;15(1):166–76.
63.
go back to reference Reijmer YD, Leemans A, Caeyenberghs K, Heringa SM, Koek HL, Biessels GJ. Disruption of cerebral networks and cognitive impairment in Alzheimer disease. Neurology. 2013;80:1370–7.CrossRef Reijmer YD, Leemans A, Caeyenberghs K, Heringa SM, Koek HL, Biessels GJ. Disruption of cerebral networks and cognitive impairment in Alzheimer disease. Neurology. 2013;80:1370–7.CrossRef
66.
go back to reference Yan Y, Xie G, Zhou H, Liu H, Wan M. Altered spontaneous brain activity in patients with childhood absence epilepsy: associations with treatment effects. Neuroreport. 2020;31(8):613–8. Yan Y, Xie G, Zhou H, Liu H, Wan M. Altered spontaneous brain activity in patients with childhood absence epilepsy: associations with treatment effects. Neuroreport. 2020;31(8):613–8.
67.
go back to reference Danielson NB, Guo JN, Blumenfeld H. The default mode network and altered consciousness in epilepsy. Behav Neurol. 2011;24:55–65.CrossRef Danielson NB, Guo JN, Blumenfeld H. The default mode network and altered consciousness in epilepsy. Behav Neurol. 2011;24:55–65.CrossRef
Metadata
Title
A study of brain functional network and alertness changes in temporal lobe epilepsy with and without focal to bilateral tonic–clonic seizures
Authors
Liluo Nie
Yanchun Jiang
Zongxia Lv
Xiaomin Pang
Xiulin Liang
Weiwei Chang
Jinou Zheng
Publication date
01-12-2022
Publisher
BioMed Central
Keyword
Epilepsy
Published in
BMC Neurology / Issue 1/2022
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-021-02525-w

Other articles of this Issue 1/2022

BMC Neurology 1/2022 Go to the issue