Physiology of functional and effective networks in epilepsy
2014, Clinical Neurophysiology
https://doi.org/10.1016/J.CLINPH.2014.09.009Abstract
The relationships between functional and structural networks provide insights into brain abnormalities that are observed in epilepsy. Functional and effective connectivity methods have been used to identify the ictal onset zone as well as to characterize the onset, spread, and termination of seizures. Studies of the dynamics of epileptic networks suggest mechanisms that may explain the sudden onset and termination of seizures.
References (109)
- Ansari-Asl K, Senhadji L, Bellanger JJ, Wendling F. Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. Phys Rev E Stat Nonlin Soft Matter Phys 2006;74:031916.
- Aoki T, Aoyagi T. Self-organized network of phase oscillators coupled by activity- dependent interactions. Phys Rev E Stat Nonlin Soft Matter Phys 2011;84:066109.
- Bak P, Paczuski M. Complexity, contingency, and criticality. Proc Natl Acad Sci USA 1995;92:6689-96.
- Bak P, Tang C, Wiesenfeld K. Self-organized criticality: an explanation of the 1/f noise. Phys Rev Lett 1987;59:381-4.
- Beggs JM, Plenz D. Neuronal avalanches in neocortical circuits. J Neurosci 2003;23:11167-77.
- Beggs JM, Plenz D. Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 2004;24:5216-29.
- Bernhardt BC, Hong S, Bernasconi A, Bernasconi N. Imaging structural and functional brain networks in temporal lobe epilepsy. Front Hum Neurosci 2013;7:624.
- Bettus G, Bartolomei F, Confort-Gouny S, Guedj E, Chauvel P, Cozzone PJ, et al. Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 2010;81:1147-54.
- Bialonski S, Horstmann MT, Lehnertz K. From brain to earth and climate systems: small-world interaction networks or not? Chaos 2010;20:013134.
- 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 1995;34:537-41.
- Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, et al. Toward discovery science of human brain function. Proc Natl Acad Sci USA 2010;107:4734-9.
- Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang DU. Complex networks: structure and dynamics. Phys Rep 2006;424:175-308.
- Bogaard A, Parent J, Zochowski M, Booth V. Interaction of cellular and network mechanisms in spatiotemporal pattern formation in neuronal networks. J Neurosci 2009;29:1677-87.
- Brazier MA. Spread of seizure discharges in epilepsy: anatomical and electrophysiological considerations. Exp Neurol 1972;36:263-72.
- Breakspear M, Stam CJ. Dynamics of a neural system with a multiscale architecture. Philos Trans R Soc Lond B Biol Sci 2005;360:1051-74.
- Brovelli A, Ding M, Ledberg A, Chen Y, Nakamura R, Bressler SL. Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc Natl Acad Sci USA 2004;101:9849-54.
- Buchel C, Friston K. Assessing interactions among neuronal systems using functional neuroimaging. Neural Netw 2000;13:871-82.
- Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008;1124:1-38.
- Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009;10:186-98.
- Burns SP, Santaniello S, Anderson WS, Sarma SV. State dynamics of the epileptic brain. In: Proceedings of the 6th ASME annual dynamic systems and control conference (DSCC), Palo Alto, CA; 2013. p. V002T22A001.
- Burns SP, Sritharan D, Jouny C, Bergey G, Crone N, Anderson WS, et al. A network analysis of the dynamics of seizure. Conf Proc IEEE Eng Med Biol Soc 2012;2012:4684-7.
- Ching S, Brown EN, Kramer MA. Distributed control in a mean-field cortical network model: implications for seizure suppression. Phys Rev E Stat Nonlin Soft Matter Phys 2012;86:021920.
- Conner CR, Ellmore TM, DiSano MA, Pieters TA, Potter AW, Tandon N. Anatomic and electro-physiologic connectivity of the language system: a combined DTI-CCEP study. Comput Biol Med 2011;41:1100-9.
- Constable RT, Scheinost D, Finn ES, Shen X, Hampson M, Winstanley FS, et al. Potential use and challenges of functional connectivity mapping in intractable epilepsy. Front Neurol 2013;4:39.
- Craddock RC, James GA, Holtzheimer 3rd PE, Hu XP, Mayberg HS. A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum Brain Mapp 2012;33:1914-28.
- David O, Bastin J, Chabardes S, Minotti L, Kahane P. Studying network mechanisms using intracranial stimulation in epileptic patients. Front Syst Neurosci 2010;4:148.
- David O, Job AS, De Palma L, Hoffmann D, Minotti L, Kahane P. Probabilistic functional tractography of the human cortex. Neuroimage 2013;80:307-17.
- Deco G, Jirsa VK, Robinson PA, Breakspear M, Friston K. The dynamic brain: from spiking neurons to neural masses and cortical fields. PLoS Comput Biol 2008;4:e1000092.
- Deco G, Senden M, Jirsa V. How anatomy shapes dynamics: a semi-analytical study of the brain at rest by a simple spin model. Front Comput Neurosci 2012;6:68.
- Duncan JS, Sander JW, Sisodiya SM, Walker MC. Adult epilepsy. Lancet 2006;367:1087-100.
- Enatsu R, Bulacio J, Nair DR, Bingaman W, Najm I, Gonzalez-Martinez J. Posterior cingulate epilepsy: clinical and neurophysiological analysis. J Neurol Neurosurg Psychiatry 2014;85:44-50.
- Enatsu R, Jin K, Elwan S, Kubota Y, Piao Z, O'Connor T, et al. Correlations between ictal propagation and response to electrical cortical stimulation: a cortico- cortical evoked potential study. Epilepsy Res 2012a;101:76-87.
- Enatsu R, Piao Z, O'Connor T, Horning K, Mosher J, Burgess R, et al. Cortical excitability varies upon ictal onset patterns in neocortical epilepsy: a cortico- cortical evoked potential study. Clin Neurophysiol 2012b;123:252-60.
- Entz L, Toth E, Keller CJ, Bickel S, Groppe DM, Fabo D, et al. Evoked effective connectivity of the human neocortex. Hum Brain Mapp 2014. http://dx.doi.org/ 10.1002/hbm.22581.
- Fisher RS, van Emde Boas W, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005;46:470-2.
- Friston KJ. Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 1994;2:56-78.
- Friston KJ. Functional and effective connectivity: a review. Brain Connect 2011;1:13-36.
- Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Functional connectivity: the principal- component analysis of large (PET) data sets. J Cereb Blood Flow Metab 1993;13:5-14.
- Gomez-Gardenes J, Gomez S, Arenas A, Moreno Y. Explosive synchronization transitions in scale-free networks. Phys Rev Lett 2011;106:128701.
- Gotman J. Measurement of small time differences between EEG channels: method and application to epileptic seizure propagation. Electroencephalogr Clin Neurophysiol 1983;56:501-14.
- Greicius MD, Krasnow B, Reiss AL, Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 2003;100:253-8.
- Guye M, Regis J, Tamura M, Wendling F, McGonigal A, Chauvel P, et al. The role of corticothalamic coupling in human temporal lobe epilepsy. Brain 2006;129:1917-28.
- Hagmann P. From diffusion MRI to brain connectomics [Ph.D. dissertation].
- Lausanne, CH: EPFL; 2005.
- Haneef Z, Lenartowicz A, Yeh HJ, Levin HS, Engel Jr J, Stern JM. Functional connectivity of hippocampal networks in temporal lobe epilepsy. Epilepsia 2014;55:137-45.
- He B, Liu Z. Multimodal functional neuroimaging: integrating functional MRI and EEG/MEG. IEEE Rev Biomed Eng 2008;1:23-40.
- Hobbs JP, Smith JL, Beggs JM. Aberrant neuronal avalanches in cortical tissue removed from juvenile epilepsy patients. J Clin Neurophysiol 2010;27:380-6.
- Honey CJ, Kotter R, Breakspear M, Sporns O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci USA 2007;104:10240-5.
- Iwasaki M, Enatsu R, Matsumoto R, Novak E, Thankappen B, Piao Z, et al. Accentuated cortico-cortical evoked potentials in neocortical epilepsy in areas of ictal onset. Epileptic Disord 2010;12:292-302.
- Keller CJ, Bickel S, Entz L, Ulbert I, Milham MP, Kelly C, et al. Intrinsic functional architecture predicts electrically evoked responses in the human brain. Proc Natl Acad Sci USA 2011;108:10308-13.
- Keller CJ, Bickel S, Honey CJ, Groppe DM, Entz L, Craddock RC, et al. Neurophysiological investigation of spontaneous correlated and anticorrelated fluctuations of the BOLD signal. J Neurosci 2013;33:6333-42.
- Keller CJ, Honey CJ, Entz L, Bickel S, Groppe DM, Toth E, et al. Corticocortical evoked potentials reveal projectors and integrators in human brain networks. J Neurosci 2014a;34:9152-63.
- Keller CJ, Honey CJ, Mégevand P, Entz L, Ulbert I, Mehta AD. Mapping human brain networks with cortico-cortical evoked potentials. Philos Trans R Soc B 2014. http://dx.doi.org/10.1098/rstb.2013.0528.
- Kiebel SJ, Garrido MI, Moran R, Chen CC, Friston KJ. Dynamic causal modeling for EEG and MEG. Hum Brain Mapp 2009;30:1866-76.
- Kokkonen SM, Nikkinen J, Remes J, Kantola J, Starck T, Haapea M, et al. Preoperative localization of the sensorimotor area using independent component analysis of resting-state fMRI. Magn Reson Imaging 2009;27:733-40.
- Kramer MA, Cash SS. Epilepsy as a disorder of cortical network organization. Neuroscientist 2012;18:360-72.
- Kramer MA, Eden UT, Kolaczyk ED, Zepeda R, Eskandar EN, Cash SS. Coalescence and fragmentation of cortical networks during focal seizures. J Neurosci 2010;30:10076-85.
- Kramer MA, Kolaczyk ED, Kirsch HE. Emergent network topology at seizure onset in humans. Epilepsy Res 2008;79:173-86.
- Lacruz ME, Garcia Seoane JJ, Valentin A, Selway R, Alarcon G. Frontal and temporal functional connections of the living human brain. Eur J Neurosci 2007;26:1357-70.
- Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001;13:534-46.
- Lehnertz K, Bialonski S, Horstmann MT, Krug D, Rothkegel A, Staniek M, et al. Synchronization phenomena in human epileptic brain networks. J Neurosci Methods 2009;183:42-8.
- Lepage KQ, Kramer MA, Chu CJ. A statistically robust EEG re-referencing procedure to mitigate reference effect. J Neurosci Methods 2014;235c:101-16.
- Lieb JP, Hoque K, Skomer CE, Song XW. Inter-hemispheric propagation of human mesial temporal lobe seizures: a coherence/phase analysis. Electroencephalogr Clin Neurophysiol 1987;67:101-19.
- Matsumoto R, Nair DR, LaPresto E, Najm I, Bingaman W, Shibasaki H, et al. Functional connectivity in the human language system: a cortico-cortical evoked potential study. Brain 2004;127:2316-30.
- Matsuzaki N, Juhasz C, Asano E. Cortico-cortical evoked potentials and stimulation- elicited gamma activity preferentially propagate from lower-to higher-order visual areas. Clin Neurophysiol 2013;124:1290-6.
- McCormick C, Quraan M, Cohn M, Valiante TA, McAndrews MP. Default mode network connectivity indicates episodic memory capacity in mesial temporal lobe epilepsy. Epilepsia 2013;54:809-18.
- Meisel C, Kuehn C. Scaling effects and spatio-temporal multilevel dynamics in epileptic seizures. PLoS One 2012;7:e30371.
- Meisel C, Storch A, Hallmeyer-Elgner S, Bullmore E, Gross T. Failure of adaptive self- organized criticality during epileptic seizure attacks. PLoS Comput Biol 2012;8:e1002312.
- Minati L, Aquino D. Probing neural connectivity through diffusion tensor imaging DTI. In: Trappl R, editor. Cybernetics and systems 2006. Austrian Society for Cybernetics Studies; 2006. p. 263-8.
- Mitchell TJ, Hacker CD, Breshears JD, Szrama NP, Sharma M, Bundy DT, et al. A novel data-driven approach to preoperative mapping of functional cortex using resting-state functional magnetic resonance imaging. Neurosurgery 2013;73:969-82. discussion 982-3.
- Morgan RJ, Soltesz I. Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc Natl Acad Sci USA 2008;105:6179-84.
- Negishi M, Martuzzi R, Novotny EJ, Spencer DD, Constable RT. Functional MRI connectivity as a predictor of the surgical outcome of epilepsy. Epilepsia 2011;52:1733-40.
- Netoff TI, Clewley R, Arno S, Keck T, White JA. Epilepsy in small-world networks. J Neurosci 2004;24:8075-83.
- Netoff TI, Schiff SJ. Decreased neuronal synchronization during experimental seizures. J Neurosci 2002;22:7297-307.
- Newman MEJ. Networks: an introduction. Oxford, New York: Oxford University Press; 2010.
- Percha B, Dzakpasu R, Zochowski M, Parent J. Transition from local to global phase synchrony in small world neural network and its possible implications for epilepsy. Phys Rev E Stat Nonlin Soft Matter Phys 2005;72:031909.
- Pereira FR, Alessio A, Sercheli MS, Pedro T, Bilevicius E, Rondina JM, et al. Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci 2010;11:66.
- Perucca P, Dubeau F, Gotman J. Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 2014;137:183-96.
- Ponten SC, Bartolomei F, Stam CJ. Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 2007;118:918-27.
- Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012;59:2142-54.
- Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc Natl Acad Sci USA 2001;98:676-82.
- Raichle ME, Snyder AZ. A default mode of brain function: a brief history of an evolving idea. Neuroimage 2007;37:1083-90. discussion 1097-9.
- Richardson MP. New observations may inform seizure models: very fast and very slow oscillations. Prog Biophys Mol Biol 2011;105:5-13.
- Richardson MP. Large scale brain models of epilepsy: dynamics meets connectomics. J Neurol Neurosurg Psychiatry 2012;83:1238-48.
- Schevon CA, Cappell J, Emerson R, Isler J, Grieve P, Goodman R, et al. Cortical abnormalities in epilepsy revealed by local EEG synchrony. Neuroimage 2007;35:140-8.
- Schindler K, Leung H, Elger CE, Lehnertz K. Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. Brain 2007;130:65-77.
- Schindler KA, Bialonski S, Horstmann MT, Elger CE, Lehnertz K. Evolving functional network properties and synchronizability during human epileptic seizures. Chaos 2008;18:033119.
- Sporns O. Networks of the brain. Cambridge, MA: MIT Press; 2011.
- Sporns O. The human connectome: origins and challenges. Neuroimage 2013;80:53-61.
- Sporns O, Tononi G, Kotter R. The human connectome: a structural description of the human brain. PLoS Comput Biol 2005;1:e42.
- Sritharan D, Sarma SV. Fragility in dynamic networks: application to neural networks in the epileptic cortex. Neural Comput 2014. http://dx.doi.org/ 10.1162/NECO_a_00644:1-34.
- Stefan H, Lopes da Silva FH. Epileptic neuronal networks: methods of identification and clinical relevance. Front Neurol 2013;4:8.
- Strogatz SH. Exploring complex networks. Nature 2001;410:268-76.
- Stufflebeam SM, Liu H, Sepulcre J, Tanaka N, Buckner RL, Madsen JR. Localization of focal epileptic discharges using functional connectivity magnetic resonance imaging. J Neurosurg 2011;114:1693-7.
- Timofeev I, Steriade M. Neocortical seizures: initiation, development and cessation. Neuroscience 2004;123:299-336.
- Topolnik L, Steriade M, Timofeev I. Hyperexcitability of intact neurons underlies acute development of trauma-related electrographic seizures in cats in vivo. Eur J Neurosci 2003;18:486-96.
- Truccolo W, Donoghue JA, Hochberg LR, Eskandar EN, Madsen JR, Anderson WS, et al. Single-neuron dynamics in human focal epilepsy. Nat Neurosci 2011;14:635-41.
- Valentin A, Anderson M, Alarcon G, Seoane JJ, Selway R, Binnie CD, et al. Responses to single pulse electrical stimulation identify epileptogenesis in the human brain in vivo. Brain 2002;125:1709-18.
- van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE. Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 2009;30:3127-41.
- Vogels TP, Rajan K, Abbott LF. Neural network dynamics. Annu Rev Neurosci 2005;28:357-76.
- Warren CP, Hu S, Stead M, Brinkmann BH, Bower MR, Worrell GA. Synchrony in normal and focal epileptic brain: the seizure onset zone is functionally disconnected. J Neurophysiol 2010;104:3530-9.
- Watts DJ, Strogatz SH. Collective dynamics of 'small-world' networks. Nature 1998;393:440-2.
- Wendling F, Ansari-Asl K, Bartolomei F, Senhadji L. From EEG signals to brain connectivity: a model-based evaluation of interdependence measures. J Neurosci Methods 2009;183:9-18.
- Whalen AJ, Brennan SN, Sauer TD, Schiff SJ. Observability of neuronal network motifs. In: 46th annual conference on information sciences and systems (CISS); 2012. p. 1-5.
- Wurina, Zang YF, Zhao SG. Resting-state fMRI studies in epilepsy. Neurosci Bull 2012;28:449-55.
- Yaffe R, Burns S, Gale J, Park HJ, Bulacio J, Gonzalez-Martinez J, et al. Brain state evolution during seizure and under anesthesia: a network-based analysis of stereotaxic eeg activity in drug-resistant epilepsy patients. Conf Proc IEEE Eng Med Biol Soc 2012;2012:5158-61.
- Zapperi S, Baekgaard Lauritsen K, Stanley HE. Self-organized branching processes: mean-field theory for avalanches. Phys Rev Lett 1995;75:4071-4.
- Zhang D, Johnston JM, Fox MD, Leuthardt EC, Grubb RL, Chicoine MR, et al. Preoperative sensorimotor mapping in brain tumor patients using spontaneous fluctuations in neuronal activity imaged with functional magnetic resonance imaging: initial experience. Neurosurgery 2009;65:226-36.
- Zhang Z, Lu G, Zhong Y, Tan Q, Liao W, Wang Z, et al. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res 2010;1323:152-60.