Subcortical structures and epilepsy

doi:10.3969/j.issn.1672-6731.2023.03.002

Abstract

Abstract: With the rapid development of neuroelectrophysiology, neuroimaging and other technologies, a large amount of evidence has shown the occurrence and development of epilepsy was closely related to cortico-subcortical neural network. This paper aims to review the relevant studies on the involvement of subcortical structures such as thalamus, hypothalamus, cerebellum, basal ganglia and brainstem in the occurrence and development of epilepsy, as well as some important targets of subcortical nucleus for the treatment of drug-resistant epilepsy (DRE) by neuroregulation, in order to provide help for the exploration of new intervention targets for epilepsy treatment.

Key words: Epilepsy, Cerebral cortex, Nerve net, Electric stimulation therapy, Review

摘要： 随着神经电生理学、神经影像学等技术的快速发展，已有大量证据显示癫痫的发生发展与皮质-皮质下神经网络密切相关。本文拟就丘脑、下丘脑、小脑、基底节、脑干等皮质下结构参与癫痫发生发展的相关研究，以及目前神经调控治疗耐药性癫痫所针对的重要皮质下神经核团靶点进行综述，以为发掘癫痫治疗新靶点提供帮助。

关键词: 癫痫, 大脑皮质, 神经网, 电刺激疗法, 综述

ZHANG Qiong, FENG Li. Subcortical structures and epilepsy[J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(3): 156-160.

张琼, 冯莉. 大脑皮质下结构与癫痫[J]. 中国现代神经疾病杂志, 2023, 23(3): 156-160.

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URL: http://journal11.magtechjournal.com/cjcnn/EN/10.3969/j.issn.1672-6731.2023.03.002

http://journal11.magtechjournal.com/cjcnn/EN/Y2023/V23/I3/156

References

[1] Norden AD, Blumenfeld H. The role of subcortical structures in human epilepsy[J]. Epilepsy Behav, 2002, 3:219-231.
[2] Badawy RA, Lai A, Vogrin SJ, Cook MJ. Subcortical epilepsy[J]? Neurology, 2013, 80:1901-1907.
[3] Park KM, Lee BI, Shin KJ, Ha SY, Park J, Kim SE, Kim SE. Pivotal role of subcortical structures as a network hub in focal epilepsy:evidence from graph theoretical analysis based on diffusion-tensor imaging[J]. J Clin Neurol, 2019, 15:68-76.
[4] Xu Q, Zhang Q, Yang F, Weng Y, Xie X, Hao J, Qi R, Gumenyuk V, Stufflebeam SM, Bernhardt BC, Lu G, Zhang Z. Cortico-striato-thalamo-cerebellar networks of structural covariance underlying different epilepsy syndromes associated with generalized tonic-clonic seizures[J]. Hum Brain Mapp, 2021, 42:1102-1115.
[5] Hsieh H, Xu Q, Yang F, Zhang Q, Hao J, Liu G, Liu R, Yu Q, Zhang Z, Xing W, Bernhardt BC, Lu G, Zhang Z. Distinct functional cortico-striato-thalamo-cerebellar networks in genetic generalized and focal epilepsies with generalized tonic-clonic seizures[J]. J Clin Med, 2022, 11:1612.
[6] Li Y, Wang J, Wang X, Chen Q, Qin B, Chen J. Reconfiguration of static and dynamic thalamo-cortical network functional connectivity of epileptic children with generalized tonic-clonic seizures[J]. Front Neurosci, 2022, 16:953356.
[7] Jia X, Xie Y, Dong D, Pei H, Jiang S, Ma S, Huang Y, Zhang X, Wang Y, Zhu Q, Zhang Y, Yao D, Yu L, Luo C. Reconfiguration of dynamic large-scale brain network functional connectivity in generalized tonic-clonic seizures[J]. Hum Brain Mapp, 2020, 41:67-79.
[8] Warsi NM, Yan H, Suresh H, Wong SM, Arski ON, Gorodetsky C, Zhang K, Gouveia FV, Ibrahim GM. The anterior and centromedian thalamus:anatomy, function, and dysfunction in epilepsy[J]. Epilepsy Res, 2022, 182:106913.
[9] Qin Y, Zhang N, Chen Y, Zuo X, Jiang S, Zhao X, Dong L, Li J, Zhang T, Yao D, Luo C. Rhythmic network modulation to thalamocortical couplings in epilepsy[J]. Int J Neural Syst, 2020, 30:2050014.
[10] Li R, Zhang L, Guo D, Zou T, Wang X, Wang H, Li J, Wang C, Liu D, Yang Z, Xiao B, Chen H, Feng L. Temporal lobe epilepsy shows distinct functional connectivity patterns in different thalamic nuclei[J]. Brain Connect, 2021, 11:119-131.
[11] Sathe AV, Kogan M, Kang K, Miao J, Syed M, Ailes I, Matias CM, Middleton D, Mohamed FB, Faro S, Tracy J, Sharan A, Alizadeh M. Amplitude synchronization of spontaneous activity of medial and lateral temporal gyri reveals altered thalamic connectivity in patients with temporal lobe epilepsy[J]. Sci Rep, 2022, 12:18389.
[12] Pizzo F, Roehri N, Giusiano B, Lagarde S, Carron R, Scavarda D, McGonigal A, Filipescu C, Lambert I, Bonini F, Trebuchon A, Bénar CG, Bartolomei F. The ictal signature of thalamus and basal ganglia in focal epilepsy:a SEEG study[J]. Neurology, 2021, 96:e280-293.
[13] He X, Chaitanya G, Asma B, Caciagli L, Bassett DS, Tracy JI, Sperling MR. Disrupted basal ganglia-thalamocortical loops in focal to bilateral tonic-clonic seizures[J]. Brain, 2020, 143:175-190.
[14] He X, Doucet GE, Pustina D, Sperling MR, Sharan AD, Tracy JI. Presurgical thalamic "hubness" predicts surgical outcome in temporal lobe epilepsy[J]. Neurology, 2017, 88:2285-2293.
[15] Piper RJ, Tangwiriyasakul C, Shamshiri EA, Centeno M, He X, Richardson MP, Tisdall MM, Carmichael DW. Functional connectivity of the anterior nucleus of the thalamus in pediatric focal epilepsy[J]. Front Neurol, 2021, 12:670881.
[16] Wu D, Chang F, Peng D, Xie S, Li X, Zheng W. The morphological characteristics of hippocampus and thalamus in mesial temporal lobe epilepsy[J]. BMC Neurol, 2020, 20:235.
[17] Law N, Smith ML, Widjaja E. Thalamocortical connections and executive function in pediatric temporal and frontal lobe epilepsy[J]. AJNR Am J Neuroradiol, 2018, 39:1523-1529.
[18] Martín-López D, Jiménez -Jiménez D, Cabañés-Martínez L, Selway RP, Valentín A, Alarcón G. The role of thalamus versus cortex in epilepsy:evidence from human ictal centromedian recordings in patients assessed for deep brain stimulation[J]. Int J Neural Syst, 2017, 27:1750010.
[19] Qin Y, Li S, Yao D, Luo C. Causality analysis to the abnormal subcortical -cortical connections in idiopathic-generalized epilepsy[J]. Front Neurosci, 2022, 16:925968.
[20] Qin Y, Zhang N, Chen Y, Tan Y, Dong L, Xu P, Guo D, Zhang T, Yao D, Luo C. How alpha rhythm spatiotemporally acts upon the thalamus-default mode circuit in idiopathic generalized epilepsy[J]. IEEE Trans Biomed Eng, 2021, 68:1282-1292.
[21] Bernasconi A, Bernasconi N, Natsume J, Antel SB, Andermann F, Arnold DL. Magnetic resonance spectroscopy and imaging of the thalamus in idiopathic generalized epilepsy[J]. Brain, 2003, 126(Pt 11):2447-2454.
[22] Helms G, Ciumas C, Kyaga S, Savic I. Increased thalamus levels of glutamate and glutamine (Glx) in patients with idiopathic generalised epilepsy[J]. J Neurol Neurosurg Psychiatry, 2006, 77:489-494.
[23] Hou J, Zhu H, Xiao L, Zhao CW, Liao G, Tang Y, Feng L. Alterations in cortical-subcortical metabolism in temporal lobe epilepsy with impaired awareness seizures[J]. Front Aging Neurosci, 2022, 14:849774.
[24] Assenza G, Lanzone J, Dubbioso R, Coppola A, Boscarino M, Ricci L, Insola A, Bilo L, Tombini M, Di Lazzaro V. Thalamic and cortical hyperexcitability in juvenile myoclonic epilepsy[J]. Clin Neurophysiol, 2020, 131:2041-2046.
[25] Lee HJ, Seo SA, Lee BI, Kim SE, Park KM. Thalamic nuclei volumes and network in juvenile myoclonic epilepsy[J]. Acta Neurol Scand, 2020, 141:271-278.
[26] Herrera ML, Suller-Marti A, Parrent A, MacDougall K, Burneo JG. Stimulation of the anterior nucleus of the thalamus for epilepsy:a Canadian experience[J]. Can J Neurol Sci, 2021, 48:469-478.
[27] Fasano A, Eliashiv D, Herman ST, Lundstrom BN, Polnerow D, Henderson JM, Fisher RS. Experience and consensus on stimulation of the anterior nucleus of thalamus for epilepsy[J]. Epilepsia, 2021, 62:2883-2898.
[28] Parisi V, Lundstrom BN, Kerezoudis P, Alcala Zermeno JL, Worrell GA, Van Gompel JJ. Anterior nucleus of the thalamus deep brain stimulation with concomitant vagus nerve stimulation for drug-resistant epilepsy[J]. Neurosurgery, 2021, 89:686-694.
[29] Yang JC, Bullinger KL, Dickey AS, Karakis I, Alwaki A, Cabaniss BT, Winkel D, Rodriguez-Ruiz A, Willie JT, Gross RE. Anterior nucleus of the thalamus deep brain stimulation vs temporal lobe responsive neurostimulation for temporal lobe epilepsy[J]. Epilepsia, 2022, 63:2290-2300.
[30] Alcala-Zermeno JL, Gregg NM, Wirrell EC, Stead M, Worrell GA, Van Gompel JJ, Lundstrom BN. Centromedian thalamic nucleus with or without anterior thalamic nucleus deep brain stimulation for epilepsy in children and adults:a retrospective case series[J]. Seizure, 2021, 84:101-107.
[31] Zhu J, Xu C, Zhang X, Qiao L, Wang X, Zhang X, Yan X, Ni D, Yu T, Zhang G, Li Y. The thalamus -precentral gyrus functional connectivity changes in epilepsy patients following vagal nerve stimulation[J]. Neurosci Lett, 2021, 751:135815.
[32] Hachem LD, Wong SM, Ibrahim GM. The vagus afferent network:emerging role in translational connectomics[J]. Neurosurg Focus, 2018, 45:E2.
[33] Middlebrooks EH, He X, Grewal SS, Keller SS. Neuroimaging and thalamic connectomics in epilepsy neuromodulation[J]. Epilepsy Res, 2022, 182:106916.
[34] Zhu J, Xu C, Zhang X, Qiao L, Wang X, Zhang X, Yan X, Ni D, Yu T, Zhang G, Li Y. 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, 27:320-329.
[35] Zhu J, Xu C, Zhang X, Qiao L, Wang X, Yan X, Ni D, Yu T, Zhang G, Li Y. The effect of vagal nerve stimulation on hippocampal - thalamic functional connectivity in epilepsy patients[J]. Brain Res Bull, 2020, 163:143-149.
[36] Fu C, Aisikaer A, Chen Z, Yu Q, Yin J, Yang W. Antiepileptic efficacy and network connectivity modulation of repetitive transcranial magnetic stimulation by vertex suppression[J]. Front Hum Neurosci, 2021, 15:667619.
[37] Vetkas A, Fomenko A, Germann J, Sarica C, Iorio-Morin C, Samuel N, Yamamoto K, Milano V, Cheyuo C, Zemmar A, Elias G, Boutet A, Loh A, Santyr B, Gwun D, Tasserie J, Kalia SK, Lozano AM. Deep brain stimulation targets in epilepsy:systematic review and meta-analysis of anterior and centromedian thalamic nuclei and hippocampus[J]. Epilepsia, 2022, 63:513-524. D, Tassi L,
[38] Munari C, Kahane P, Francione S, Hoffmann Cusmai R, Vigevano F, Pasquier B, Betti OO. Role of the hypothalamic hamartoma in the genesis of gelastic fits (a video-stereo-EEG study)[J]. Electroencephalogr Clin Neurophysiol, 1995, 95:154-160.
[39] Qasim BA, Mohammed AA. Hamartoma of hypothalamus presented as precocious puberty and epilepsy in a 10-year-old girl[J]. Int J Surg Case Rep, 2020, 77:170-173.
[40] van Rijckevorsel K, Abu Serieh B, de Tourtchaninoff M, Raftopoulos C. Deep EEG recordings of the mammillary body in epilepsy patients[J]. Epilepsia, 2005, 46:781-785.
[41] Zangiabadi N, Ladino LD, Sina F, Orozco-Hernández JP, Carter A, Téllez-Zenteno JF. Deep brain stimulation and drug-resistant epilepsy:a review of the literature[J]. Front Neurol, 2019, 10:601.
[42] Allen LA, Vos SB, Kumar R, Ogren JA, Harper RK, Winston GP, Balestrini S, Wandschneider B, Scott CA, Ourselin S, Duncan JS, Lhatoo SD, Harper RM, Diehl B. Cerebellar, limbic, and midbrain volume alterations in sudden unexpected death in epilepsy[J]. Epilepsia, 2019, 60:718-729.
[43] Marcián V, Mareček R, Korit'áková E, Pail M, Bareš M, Brázdil M. Morphological changes of cerebellar substructures in temporal lobe epilepsy:a complex phenomenon, not mere atrophy[J]. Seizure, 2018, 54:51-57.
[44] Li R, Hu C, Wang L, Liu D, Liu D, Liao W, Xiao B, Chen H, Feng L. Disruption of functional connectivity among subcortical arousal system and cortical networks in temporal lobe epilepsy[J]. Brain Imaging Behav, 2020, 14:762-771.
[45] Shin WC, Hong SB, Tae WS, Seo DW, Kim SE. Ictal hyperperfusion of cerebellum and basal ganglia in temporal lobe epilepsy:SPECT subtraction with MRI coregistration[J]. J Nucl Med, 2001, 42:853-858.
[46] Cooper IS. Effect of chronic stimulation of anterior cerebellum on neurological disease[J]. Lancet, 1973, 1:206.
[47] Streng ML, Krook-Magnuson E. The cerebellum and epilepsy[J]. Epilepsy Behav, 2021, 121(Pt B):106909.
[48] Vuong J, Devergnas A. The role of the basal ganglia in the control of seizure[J]. J Neural Transm (Vienna), 2018, 125:531-545.
[49] Tang Y, Su TY, Choi JY, Hu S, Wang X, Sakaie K, Murakami H, Alexopoulos A, Griswold M, Jones S, Najm I, Ma D, Wang ZI. Characterizing thalamic and basal ganglia nuclei in medically intractable focal epilepsy by MR fingerprinting[J]. Epilepsia, 2022, 63:1998-2010.
[50] MacEachern SJ, Santoro JD, Hahn KJ, Medress ZA, Stecher X, Li MD, Hahn JS, Yeom KW, Forkert ND. Children with epilepsy demonstrate macro-and microstructural changes in the thalamus, putamen, and amygdala[J]. Neuroradiology, 2020, 62:389-397.
[51] Chkhenkeli SA, Sramka M, Lortkipanidze GS, Rakviashvili TN, Bregvadze ESh, Magalashvili GE, Gagoshidze TSh, Chkhenkeli IS. Electrophysiological effects and clinical results of direct brain stimulation for intractable epilepsy[J]. Clin Neurol Neurosurg, 2004, 106:318-329.
[52] Englot DJ, Gonzalez HFJ, Reynolds BB, Konrad PE, Jacobs ML, Gore JC, Landman BA, Morgan VL. Relating structural and functional brainstem connectivity to disease measures in epilepsy[J]. Neurology, 2018, 91:e67-77.
[53] Chugani HT, Shewmon DA, Sankar R, Chen BC, Phelps ME. Infantile spasms. Ⅱ:lenticular nuclei and brain stem activation on positron emission tomography[J]. Ann Neurol, 1992, 31:212- 219.
[54] Kohsaka S, Kohsaka M, Mizukami S, Sakai T, Kobayashi K. Brainstem activates paroxysmal discharge in human generalized epilepsy[J]. Brain Res, 2001, 903:53-61.
[55] Mueller SG, Nei M, Bateman LM, Knowlton R, Laxer KD, Friedman D, Devinsky O, Goldman AM. Brainstem network disruption:a pathway to sudden unexplained death in epilepsy[J]? Hum Brain Mapp, 2018, 39:4820-4830.
[56] Liu J, Peedicail JS, Gaxiola-Valdez I, Li E, Mosher V, Wilson W, Perera T, Singh S, Teskey GC, Federico P; Calgary Comprehensive Epilepsy Program Collaborators. Postictal brainstem hypoperfusion and risk factors for sudden unexpected death in epilepsy[J]. Neurology, 2020, 95:e1694-1705.

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