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BMC Neurology
Published in: BMC Neurology 1/2020

01-12-2020 | Epilepsy | Research article

Functional brain network mechanism of executive control dysfunction in temporal lobe epilepsy

Authors: Yanping Ren, Liping Pan, Xueyun Du, Yuying Hou, Xun Li, Yijun Song

Published in: BMC Neurology | Issue 1/2020

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Abstract

Background

Executive control dysfunction is observed in a sizable number of patients with temporal lobe epilepsy (TLE). Neural oscillations in the theta band are increasingly recognized as having a crucial role in executive control network. The purpose of this study was to investigate the alterations in the theta band in executive control network and explore the functional brain network mechanisms of executive control dysfunction in TLE patients.

Methods

A total of 20 TLE patients and 20 matched healthy controls (HCs) were recruited in the present study. All participants were trained to perform the executive control task by attention network test while the scalp electroencephalogram (EEG) data were recorded. The resting state signals were collected from the EEG in the subjects with quiet and closed eyes conditions. Functional connectivity among EEGs in the executive control network and resting state network were respectively calculated.

Results

We found the significant executive control impairment in the TLE group. Compared to the HCs, the TLE group showed significantly weaker functional connectivity among EEGs in the executive control network. Moreover, in the TLE group, we found that the functional connectivity was significantly positively correlated with accuracy and negatively correlated with EC_effect. In addition, the functional connectivity of the executive control network was significantly higher than that of the resting state network in the HCs. In the TLE group, however, there was no significant change in functional connectivity strengths between the executive control network and resting state network.

Conclusion

Our results indicate that the decreased functional connectivity in theta band may provide a potential mechanism for executive control deficits in TLE patients.
Literature
1.
Oyegbile TO, VanMeter JW, Motamedi G, Zecavati N, Santos C, Chun CLE, Gaillard WD, Hermann B. Executive dysfunction is associated with an altered executive control network in pediatric temporal lobe epilepsy. Epilepsy Behav. 2018;86:145–52.PubMedCrossRefPubMedCentral
2.
Oyegbile TO, Dow C, Jones J, Bell B, Rutecki P, Sheth R, Seidenberg M, Hermann BP. The nature and course of neuropsychological morbidity in chronic temporal lobe epilepsy. Neurology. 2004;62(10):1736–42.PubMedCrossRef
3.
Posner MI, Petersen SE. The attention system of the human brain. Annu Rev Neurosci. 1990;13(1):25–42.PubMedCrossRef
4.
Agah E, Asgari-Rad N, Ahmadi M, Tafakhori A, Aghamollaii V. Evaluating executive function in patients with temporal lobe epilepsy using the frontal assessment battery. Epilepsy Res. 2017;133:22.PubMedCrossRef
5.
6.
7.
Reyes A, Uttarwar VS, Chang YA, Balachandra AR, Pung CJ, Hagler DJ Jr, Paul BM, McDonald CR. Decreased neurite density within frontostriatal networks is associated with executive dysfunction in temporal lobe epilepsy. Epilepsy Behav. 2018;78:187–93.PubMedCrossRef
8.
9.
Van Diessen E, Diederen SJ, Braun KP, Jansen FE, Stam CJ. Functional and structural brain networks in epilepsy: what have we learned? Epilepsia. 2013;54(11):1855–65.PubMedCrossRef
10.
Tuchscherer V, Seidenberg M, Pulsipher D, Lancaster M, Guidotti L, Hermann B. Extrahippocampal integrity in temporal lobe epilepsy and cognition: thalamus and executive functioning. Epilepsy Behav. 2010;17(4):478–82.PubMedCrossRef
11.
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.PubMedCrossRef
12.
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007;27(9):2349–56.PubMedPubMedCentralCrossRef
13.
14.
Hae-Jeong P, Karl F. Structural and functional brain networks: from connections to cognition. Science. 2013;342(6158):579.
15.
Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med. 2010;34(4):537–41.CrossRef
16.
Smith SM, Miller KL, Salimi-Khorshidi G, Webster M, Beckmann CF, Nichols TE, Ramsey JD, Woolrich MW. Network modelling methods for FMRI. NeuroImage. 2011;54(2):875–91.PubMedCrossRef
17.
Granger CWJ. Investigating causal relations by econometric models and cross-spectral methods. Econometrica. 1969;37(3):424–38.CrossRef
18.
19.
20.
Wilke C, Worrell G, He B. Graph analysis of epileptogenic networks in human partial epilepsy. Epilepsia. 2011;52(1):84–93.PubMedCrossRef
21.
Van de Steen F, Faes L, Karahan E, Songsiri J, Valdes-Sosa PA, Marinazzo D. Critical comments on EEG sensor space dynamical connectivity analysis. Brain Topogr. 2016;32(4):643–54.PubMedCrossRef
22.
Zhang D, Zhao H, Bai W, Tian X. Functional connectivity among multi-channel EEGs when working memory load reaches the capacity. Brain Res. 1631;2016:101–12.
23.
Blinowska KJ, Kaminski M, Brzezicka A, Kaminski J. Application of directed transfer function and network formalism for the assessment of functional connectivity in working memory task. Philos Trans A Math Phys Eng Sci. 2013;371(1997):20110614.PubMedCrossRef
24.
Sauseng P, Hoppe J, Klimesch W, Gerloff C, Hummel FC. Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range. Eur J Neurosci. 2007;25(2):587–93.PubMedCrossRef
25.
Mas-Herrero E, Marco-Pallares J. Theta oscillations integrate functionally segregated sub-regions of the medial prefrontal cortex. NeuroImage. 2016;143:166–74.PubMedCrossRef
26.
Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313(5793):1626–8.PubMedPubMedCentralCrossRef
27.
Fan J, Byrne J, Worden MS, Guise KG, McCandliss BD, Fossella J, Posner MI. The relation of brain oscillations to attentional networks. J Neurosci. 2007;27(23):6197–206.PubMedPubMedCentralCrossRef
28.
Li X, Hou Y, Ren Y, Tian X, Song Y. Alterations of theta oscillation in executive control in temporal lobe epilepsy patients. Epilepsy Res. 2018;140:148–54.PubMedCrossRef
29.
Leyden KM, Kucukboyaci NE, Puckett OK, Lee D, Loi RQ, Paul B, Mcdonald CR. What does diffusion tensor imaging (DTI) tell us about cognitive networks in temporal lobe epilepsy? Quant ImagingMed Surg. 2015;5(2):247.
30.
Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P. Small-world networks and functional connectivity in Alzheimer's disease. Cereb Cortex. 2007;17(1):92–9.PubMedCrossRef
31.
Fisher RS. An overview of the 2017 ILAE operational classification of seizure types. Epilepsy Behav. 2017;70(Pt A):271–3.PubMedCrossRef
32.
Riley JD, Moore S, Cramer SC, Lin JJ. Caudate atrophy and impaired frontostriatal connections are linked to executive dysfunction in temporal lobe epilepsy. Epilepsy Behav. 2011;21(1):80–7.PubMedPubMedCentralCrossRef
33.
Giesbrecht B, Woldorff MG, Song AW, Mangun GR. Neural mechanisms of top-down control during spatial and feature attention. NeuroImage. 2003;19(3):496–512.PubMedCrossRef
34.
Slagter HA, Giesbrecht B, Kok A, Weissman DH, Kenemans JL, Woldorff MG, Mangun GR. fMRI evidence for both generalized and specialized components of attentional control. Brain Res. 2007;1177:90–102.PubMedPubMedCentralCrossRef
35.
Jiang J, Zhang Q, van Gaal S. Conflict awareness dissociates theta-band neural dynamics of the medial frontal and lateral frontal cortex during trial-by-trial cognitive control. NeuroImage. 2015;116:102–11.PubMedCrossRef
36.
Zhang C, Yang H, Qin W, Liu C, Qi Z, Chen N, Li K. Characteristics of resting-state functional connectivity in intractable unilateral temporal lobe epilepsy patients with impaired executive control function. Front Hum Neurosci. 2017;11:609.PubMedPubMedCentralCrossRef
37.
Vlooswijk MC, Jansen JF, Jeukens CR, Majoie HJ, Hofman PA, de Krom MC, Aldenkamp AP, Backes WH. Memory processes and prefrontal network dysfunction in cryptogenic epilepsy. Epilepsia. 2011;52(8):1467–75.PubMedCrossRef
38.
Bell B, Lin JJ, Seidenberg M, Hermann B. The neurobiology of cognitive disorders in temporal lobe epilepsy. Na Rev Neurol. 2011;7(3):154–64.CrossRef
39.
Keller SS, Baker G, Downes JJ. Roberts N; quantitative MRI of the prefrontal cortex and executive function in patients with temporal lobe epilepsy. Epilepsy Behav. 2009;15(2):186–95.PubMedCrossRef
40.
Takaya S, Mikuni N, Mitsueda T, Satow T, Taki J, Kinoshita M, Miyamoto S, Hashimoto N, Ikeda A, Fukuyama H. Improved cerebral function in mesial temporal lobe epilepsy after subtemporal amygdalohippocampectomy. Brain. 2009;132(Pt 1):185–94.PubMedCrossRef
41.
Berger J, Plotkin M, Demin K, Holtkamp M, Bengner T. The relationship between structural MRI, FDG-PET, and memory in temporal lobe epilepsy: preliminary results. Epilepsy Behav. 2018;80:61–7.PubMedCrossRef
42.
Rodriguez-Cruces R, Velazquez-Perez L, Rodriguez-Leyva I, Velasco AL, Trejo-Martinez D, Barragan-Campos HM, Camacho-Tellez V, Concha L. Association of white matter diffusion characteristics and cognitive deficits in temporal lobe epilepsy. Epilepsy Behav. 2018;79:138–45.PubMedCrossRef
43.
Yang H, Zhang C, Liu C, Yu T, Zhang G, Chen N, Li K. Brain network alteration in patients with temporal lobe epilepsy with cognitive impairment. Epilepsy Behav. 2018;81:41–8.PubMedCrossRef
44.
Dinkelacker V, Valabregue R, Thivard L, Lehericy S, Baulac M, Samson S, Dupont S. Hippocampal-thalamic wiring in medial temporal lobe epilepsy: enhanced connectivity per hippocampal voxel. Epilepsia. 2015;56(8):1217–26.PubMedCrossRef
45.
Voytek B, Kayser AS, Badre D, Fegen D, Chang EF, Crone NE, Parvizi J, Knight RT, D'Esposito M. Oscillatory dynamics coordinating human frontal networks in support of goal maintenance. Nat Neurosci. 2015;18(9):1318–24.PubMedPubMedCentralCrossRef
46.
Roux F, Uhlhaas PJ. Working memory and neural oscillations. Alpha-gamma versus theta-gamma codes for distinct WM information? Trends Cogn Sci. 2014;18(1):16–25.PubMedCrossRef
47.
Sellers KK, Yu C, Zhou ZC, Stitt I, Li Y, Radtke-Schuller S, Alagapan S, Frohlich F. Oscillatory dynamics in the Frontoparietal attention network during sustained attention in the ferret. Cell Rep. 2016;16(11):2864–74.PubMedPubMedCentralCrossRef
48.
49.
Rutishauser U, Ross IB, Mamelak AN, Schuman EM. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature. 2010;464(7290):903–7.PubMedCrossRef
50.
Fellrath J, Mottaz A, Schnider A, Guggisberg AG, Ptak R. Theta-band functional connectivity in the dorsal fronto-parietal network predicts goal-directed attention. Neuropsychologia. 2016;92:20–30.PubMedCrossRef
51.
Fleck JI, Kuti J, Brown J, Mahon JR, Gayda-Chelder C. Frontal-posterior coherence and cognitive function in older adults. Int J Psychophysiol. 2016;110:217–30.PubMedCrossRef
52.
Angelidis A, van der Does W, Schakel L, Putman P. Frontal EEG theta/beta ratio as an electrophysiological marker for attentional control and its test-retest reliability. Biol Psychol. 2016;121(Pt A):49–52.PubMedCrossRef
53.
Shah SA, Goldin Y, Conte MM, Goldfine AM, Mohamadpour M, Fidali BC, Cicerone K, Schiff ND. Executive attention deficits after traumatic brain injury reflect impaired recruitment of resources. NeuroImage Clin. 2017;14:233–41.PubMedPubMedCentralCrossRef
54.
Howe WM, Gritton HJ, Lusk NA, Roberts EA, Hetrick VL, Berke JD, Sarter M. Acetylcholine release in prefrontal cortex promotes gamma oscillations and Theta-gamma coupling during Cue detection. J Neurosci. 2017;37(12):3215–30.PubMedPubMedCentralCrossRef
Metadata
Title
Functional brain network mechanism of executive control dysfunction in temporal lobe epilepsy
Authors
Yanping Ren
Liping Pan
Xueyun Du
Yuying Hou
Xun Li
Yijun Song
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Epilepsy
Published in
BMC Neurology / Issue 1/2020
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-020-01711-6

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