Graph theory findings in the pathophysiology of temporal lobe epilepsy

Clinical Neurophysiology

Volumn 125, Issue 7, 2014, Pages 1295-1305

  Chiang, Sharon ^a   Haneef, Zulfi ^b,c  

^a Rice University   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Diffusion tensor imaging; Functional connectivity; Graph theory; Pathophysiology; Small world networks; Temporal lobe epilepsy

Indexed keywords

DIFFUSION TENSOR IMAGING; ELECTRODE IMPLANT; ELECTROENCEPHALOGRAM; EPILEPTIC DISCHARGE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; IMMUNOHISTOCHEMISTRY; LIMBIC SYSTEM; MAGNETOENCEPHALOGRAPHY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; TEMPORAL LOBE; TEMPORAL LOBE EPILEPSY; TRACTOGRAPHY; WHITE MATTER; ARTIFICIAL NEURAL NETWORK; BRAIN MAPPING; CELL CULTURE; ELECTROENCEPHALOGRAPHY; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES;

BRAIN MAPPING; CELLS, CULTURED; DIFFUSION TENSOR IMAGING; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETOENCEPHALOGRAPHY; NERVE NET; NEURAL NETWORKS (COMPUTER); TEMPORAL LOBE;

EID: 84901256627     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2014.04.004     Document Type: Review

References (85)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol 2007, 3:e17.
2. 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.
3. Alexander-Bloch A., Giedd J.N., Bullmore E. Imaging structural co-variance between human brain regions. Nat Rev Neurosci 2013, 14:322-336.
4. Bartolomei F., Bettus G., Stam C.J., Guye M. Interictal network properties in mesial temporal lobe epilepsy: A graph theoretical study from intracerebral recordings. Clin Neurophysiol 2013, 124:2345-2353.
5. Bartolomei F., Bosma I., Klein M., Baayen J.C., Reijneveld J.C., Postma T.J., et al. Disturbed functional connectivity in brain tumour patients: evaluation by graph analysis of synchronization matrices. Clin Neurophysiol 2006, 117:2039-2049.
6. Bernhardt B.C., Chen Z., He Y., Evans A.C., Bernasconi N. Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb Cortex 2011, 21:2147-2157.
7. Bernhardt B.C., Hong S., Bernasconi A., Bernasconi N. Imaging structural and functional brain networks in temporal lobe epilepsy. Front Hum Neurosci 2013, 7:624.
8. Bettus G., Bartolomei F., Confort-Gouny S., Guedj E., Chauvel P., Cozzone P.J., et al. Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 2010, 81:1147-1154.
9. Bonelli S.B., Thompson P.J., Yogarajah M., Vollmar C., Powell R.H., Symms M.R., et al. Imaging language networks before and after anterior temporal lobe resection: results of a longitudinal fMRI study. Epilepsia 2012, 53:639-650.
10. Bonilha L., Nesland T., Martz G.U., Joseph J.E., Spampinato M.V., Edwards J.C., et al. Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures. J Neurol Neurosurg Psychiatry 2012, 83:903-909.
11. Bonilha L., Rorden C., Castellano G., Cendes F., Li L.M. Voxel-based morphometry of the thalamus in patients with refractory medial temporal lobe epilepsy. Neuroimage 2005, 25:1016-1021.
12. Bonilha L., Rorden C., Halford J.J., Eckert M., Appenzeller S., Cendes F., et al. Asymmetrical extra-hippocampal grey matter loss related to hippocampal atrophy in patients with medial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 2007, 78:286-294.
13. Bourgon R., Gentleman R., Huber W. Independent filtering increases detection power for high-throughput experiments. Proc Natl Acad Sci USA 2010, 107:9546-9551.
14. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008, 1124:1-38.
15. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009, 10:186-198.
16. Bullmore E.T., Bassett D.S. Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol 2011, 7:113-140.
17. Cabral J., Hugues E., Kringelbach M.L., Deco G. Modeling the outcome of structural disconnection on resting-state functional connectivity. Neuroimage 2012, 62:1342-1353.
18. Cardanobile S., Pernice V., Deger M., Rotter S. Inferring general relations between network characteristics from specific network ensembles. PLoS One 2012, 7:e37911.
19. Case M., Soltesz I. Computational modeling of epilepsy. Epilepsia 2011, 52(Suppl. 8):12-15.
20. Chartrand G. Introductory Graph Theory 1985, Dover, Mineola.
21. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 1:623-634.
22. Constable R.T., Scheinost D., Finn E.S., Shen X., Hampson M., Winstanley F.S., et al. Potential use and challenges of functional connectivity mapping in intractable epilepsy. Front Neurol 2013, 4:39.
23. Craddock R.C., James G.A., Holtzheimer P.E., Hu X.P., Mayberg H.S. A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum Brain Mapp 2012, 33:1914-1928.
24. Douw L., van Dellen E., de Groot M., Heimans J.J., Klein M., Stam C.J., et al. Epilepsy is related to theta band brain connectivity and network topology in brain tumor patients. BMC Neurosci 2010, 11:103.
25. Duzel E., Schiltz K., Solbach T., Peschel T., Baldeweg T., Kaufmann J., et al. Hippocampal atrophy in temporal lobe epilepsy is correlated with limbic systems atrophy. J Neurol 2006, 253:294-300.
26. Dyhrfjeld-Johnsen J., Santhakumar V., Morgan R.J., Huerta R., Tsimring L., Soltesz I. Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol 2007, 97:1566-1587.
27. Engel J. Mesial temporal lobe epilepsy: what have we learned?. Neuroscientist 2001, 7:340-352.
28. Engel J., Thompson P.M., Stern J.M., Staba R.J., Bragin A., Mody I. Connectomics and epilepsy. Curr Opin Neurol 2013, 26:186-194.
29. Engelborghs S., D'Hooge R., De Deyn P.P. Pathophysiology of epilepsy. Acta Neurol Belg 2000, 100:201-213.
30. Euler L. Solutio problematis ad geometriam situs pertinentis. Commentarii academiae scientiarum Petropolitana 1741, 8:128-140.
31. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1991, 1:1-47.
32. Friedman J., Hastie T., Tibshirani R. Sparse inverse covariance estimation with the graphical lasso. Biostatistics 2008, 9:432-441.
33. Frings L., Schulze-Bonhage A., Spreer J., Wagner K. Remote effects of hippocampal damage on default network connectivity in the human brain. J Neurol 2009, 256:2021-2029.
34. Gibbs J.W. Elementary principles in statistical physics 1902, Yale University Press, New Haven.
35. Haneef Z., Lenartowicz A., Yeh H.J., Engel J., Stern J.M. Effect of lateralized temporal lobe epilepsy on the default mode network. Epilepsy Behav 2012, 25:350-357.
36. Horstmann M.T., Bialonski S., Noennig N., Mai H., Prusseit J., Wellmer J., et al. State dependent properties of epileptic brain networks: comparative graph-theoretical analyses of simultaneously recorded EEG and MEG. Clin Neurophysiol 2010, 121:172-185.
37. James G.A., Tripathi S.P., Ojemann J.G., Gross R.E., Drane D.L. Diminished default mode network recruitment of the hippocampus and parahippocampus in temporal lobe epilepsy. J Neurosurg 2013, 119:288-300.
38. Juhasz C., Nagy F., Watson C., da Silva E.A., Muzik O., Chugani D.C., et al. Glucose and [11C]flumazenil positron emission tomography abnormalities of thalamic nuclei in temporal lobe epilepsy. Neurology 1999, 53:2037-2045.
39. Kaiser M., Hilgetag C.C. Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2006, 2:e95.
40. Kobayashi Y., Amaral D.G. Macaque monkey retrosplenial cortex: II. Cortical afferents. J Comp Neurol 2003, 466:48-79.
41. Kollar D., Friedman N. Probabilistic graphical models: principles and techniques 2009, The MIT Press, Boston.
42. Kramer M.A., Cash S.S. Epilepsy as a disorder of cortical network organization. Neuroscientist 2012, 18:360-372.
43. Lauritzen S.L. Graphical Models 1996, Oxford University Press, Oxford.
44. Liao W., Zhang Z., Pan Z., Mantini D., Ding J., Duan X., et al. Altered functional connectivity and small-world in mesial temporal lobe epilepsy. PLoS One 2010, 5:e8525.
45. Lieb J.P., Dasheiff R.M., Engel J. Role of the frontal lobes in the propagation of mesial temporal lobe seizures. Epilepsia 1991, 32:822-837.
46. Luo C., Qiu C., Guo Z., Fang J., Li Q., Lei X., et al. Disrupted functional brain connectivity in partial epilepsy: a resting-state fMRI study. PLoS One 2011, 7:e28196.
47. Mankinen K., Jalovaara P., Paakki J.J., Harila M., Rytky S., Tervonen O., et al. Connectivity disruptions in resting-state functional brain networks in children with temporal lobe epilepsy. Epilepsy Res 2012, 100:168-178.
48. Margerison J., Corsellis J. Epilepsy and the temporal lobes: A clinical electroencephalographic and neuropatholoical study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 1966, 89:499-530.
49. Markov A.A. Extension of the law of large numbers to dependent quantities. Izv Fiz-Matem Obsch Kazan Univ(2nd Ser) 1906, 15:135-156.
50. McDonald C.R., Hagler D.J., Ahmadi M.E., Tecoma E., Iragui V., Gharapetian L., et al. Regional neocortical thinning in mesial temporal lobe epilepsy. Epilepsia 2008, 49:794-803.
51. Meinshausen N., Bühlmann P. High-dimensional graphs and variable selection with the lasso. Ann Stat 2006, 34:1436-1462.
52. Mueller S.G., Laxer K.D., Barakos J., Cheong I., Finlay D., Garcia P., et al. Involvement of the thalamocortical network in TLE with and without mesiotemporal sclerosis. Epilepsia 2010, 51:1436-1445.
53. Netoff T.I., Clewley R., Arno S., Keck T., White J.A. Epilepsy in small-world networks. J Neurosci 2004, 24:8075-8083.
54. Otte W.M., Dijkhuizen R.M., van Meer M.P., van der Hel W.S., Verlinde S.A., van Nieuwenhuizen O., et al. Characterization of functional and structural integrity in experimental focal epilepsy: reduced network efficiency coincides with white matter changes. PLoS One 2012, 7:e39078.
55. Pearl J. Probabilistic reasoning in intelligent systems: networks of plausible inference 1988, Morgan Kaufmann, San Francisco.
56. 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.
57. Pereira F.R., Alessio A., Sercheli M.S., Pedro T., Bilevicius E., Rondina J.M., et al. Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI. BMC Neurosci 2010, 11:66.
58. Ponten S.C., Bartolomei F., Stam C.J. Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 2007, 118:918-927.
59. Quraan M.A., McCormick C., Cohn M., Valiante T.A., McAndrews M.P. Altered resting state brain dynamics in temporal lobe epilepsy can be observed in spectral power, functional connectivity and graph theory metrics. PLoS One 2013, 8:e68609.
60. Sanchez M.M., Moghadam S., Naik P., Martin K.J., Salehi A. Hippocampal network alterations in Alzheimer's disease and Down syndrome: from structure to therapy. J Alzheimers Dis 2011, 26(Suppl. 3):29-47.
61. Scheinost D., Benjamin J., Lacadie C.M., Vohr B., Schneider K.C., Ment L.R., et al. The intrinsic connectivity distribution: a novel contrast measure reflecting voxel level functional connectivity. Neuroimage 2012, 62:1510-1519.
62. Schindler K., Leung H., Elger C.E., Lehnertz K. Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. Brain 2007, 130:65-77.
63. Sharp D.J., Beckmann C.F., Greenwood R., Kinnunen K.M., Bonnelle V., De Boissezon X., et al. Default mode network functional and structural connectivity after traumatic brain injury. Brain 2011, 134:2233-2247.
64. Shen X., Papademetris X., Constable R.T. Graph-theory based parcellation of functional subunits in the brain from resting-state fMRI data. Neuroimage 2010, 50:1027-1035.
65. Shen X., Tokoglu F., Papademetris X., Constable R.T. Groupwise whole-brain parcellation from resting-state fMRI data for network node identification. Neuroimage 2013, 82:403-415.
66. Sloviter R.S. "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 1983, 10:675-697.
67. Sloviter R.S. Hippocampal pathology and pathophysiology in temporal lobe epilepsy. Neurologia 1996, 11(Suppl. 4):29-32.
68. Spencer S.S. Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia 2002, 43:219-227.
69. Sporns O., Chialvo D.R., Kaiser M., Hilgetag C.C. Organization, development and function of complex brain networks. Trends Cogn Sci 2004, 8:418-425.
70. Sporns O., Zwi J.D. The small world of the cerebral cortex. Neuroinformatics 2004, 2:145-162.
71. Srinivas K.V., Jain R., Saurav S., Sikdar S.K. Small-world network topology of hippocampal neuronal network is lost, in an in vitro glutamate injury model of epilepsy. Eur J Neurosci 2007, 25:3276-3286.
72. Stam C.J., Jones B.F., Nolte G., Breakspear M., Scheltens P. Small-world networks and functional connectivity in Alzheimer's disease. Cereb Cortex 2007, 17:92-99.
73. Sun D.A., Sombati S., DeLorenzo R.J. Glutamate injury-induced epileptogenesis in hippocampal neurons: an in vitro model of stroke-induced "epilepsy". Stroke 2001, 32:2344-2350.
74. Sutula T., Cascino G., Cavazos J., Parada I., Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann Neurol 1989, 26:321-330.
75. Vaessen M.J., Jansen J.F., Vlooswijk M.C., Hofman P.A., Majoie H.J., Aldenkamp A.P., et al. White matter network abnormalities are associated with cognitive decline in chronic epilepsy. Cereb Cortex 2012, 22:2139-2147.
76. van Dellen E., Douw L., Baayen J.C., Heimans J.J., Ponten S.C., Vandertop W.P., et al. Long-term effects of temporal lobe epilepsy on local neural networks: a graph theoretical analysis of corticography recordings. PLoS One 2009, 4:e8081.
77. van den Heuvel M., Mandl R., Hulshoff Pol H. Normalized cut group clustering of resting-state FMRI data. PLoS One 2008, 3:e2001.
78. van Diessen E., Otte W.M., Braun K.P., Stam C.J., Jansen F.E. Improved diagnosis in children with partial epilepsy using a multivariable prediction model based on EEG network characteristics. PLoS One 2013, 8:e59764.
79. Vlooswijk M.C., Vaessen M.J., Jansen J.F., de Krom M.C., Majoie H.J., Hofman P.A., et al. Loss of network efficiency associated with cognitive decline in chronic epilepsy. Neurology 2011, 77:938-944.
80. Watts D.J., Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 1998, 393:440-442.
81. Wilke C., Worrell G., He B. Graph analysis of epileptogenic networks in human partial epilepsy. Epilepsia 2011, 52:84-93.
82. Williamson P.D., French J.A., Thadani V.M., Kim J.H., Novelly R.A., Spencer S.S., et al. Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results, and pathology. Ann Neurol 1993, 34:781-787.
83. Wright S. Correlation and causation. J Agric Res 1921, 20:557-585.
84. Wright S. The method of path coefficients. Ann Math Stat 1934, 5:161-215.
85. Zhang Z., Liao W., Chen H., Mantini D., Ding J.R., Xu Q., et al. Altered functional-structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 2011, 134:2912-2928.