An open hypothesis: Is epilepsy learned, and can it be unlearned?

Epilepsy and Behavior

Volumn 13, Issue 3, 2008, Pages 511-522

  Hsu, David ^a   Chen, Wei ^b   Hsu, Murielle ^a   Beggs, John M ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Critical connectivity; Epileptogenesis; Hebbian learning; Homeostasis; Neuroplasticity; Neurostimulation; Post traumatic epilepsy; Postictal state

Indexed keywords

ARTICLE; BRAIN FUNCTION; BRAIN NERVE CELL; EPILEPSY; EPILEPTIC STATE; EPILEPTOGENESIS; HOMEOSTASIS; HUMAN; HYPOTHESIS; LEARNING; LEARNING ALGORITHM; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN;

ANIMALS; ANIMALS, NEWBORN; BRAIN; COMPUTER SIMULATION; ELECTRIC STIMULATION; EPILEPSY; HUMANS; LEARNING; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; STOCHASTIC PROCESSES; TIME FACTORS;

EID: 50849122338     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2008.05.007     Document Type: Article

References (83)

1. Scharfman H.E. Epilepsy as an example of neural plasticity. Neuroscientist 8 (2002) 154-173
2. Williams P.A., Hellier J.L., White A.M., et al. Development of spontaneous seizures after experimental status epilepticus: implications for understanding epileptogenesis. Epilepsia 48 Suppl. 5 (2007) 157-163
3. Bender R.A., and Baram T.Z. Epileptogenesis in the developing brain: what can we learn from animal models?. Epilepsia 48 Suppl. 5 (2007) 2-6
4. Dube C.M., Brewster A.L., Richichi C., et al. Fever, febrile seizures and epilepsy. Trends Neurosci 30 (2007) 490-496
5. Chen J.W., Naylor D.E., and Wasterlain C.G. Advances in the pathophysiology of status epilepticus. Acta Neurol Scand Suppl 186 (2007) 7-15
6. Scharfman H.E. The neurobiology of epilepsy. Curr Neurol Neurosci Rep 7 (2007) 348-354
7. Crino P.B. Gene expression, genetics, and genomics in epilepsy: some answers, more questions. Epilepsia 48 Suppl. 2 (2007) 42-50
8. Pitkanen A., Kharatishvili I., Karhunen H., et al. Epileptogenesis in experimental models. Epilepsia 48 Suppl. 2 (2007) 13-20
9. Traub R.D., Contreras D., and Whittington M.A. Combined experimental/simulation studies of cellular and network mechanisms of epileptogenesis in vitro and in vivo. J Clin Neurophysiol 22 (2005) 330-342
10. Prinz A.A., Bucher D., and Marder E. Similar network activity from disparate circuit parameters. Nat Neurosci 7 (2004) 1345-1352
11. Hebb D. The organization of behavior: a neuropsychological theory (1949), Wiley, New York
12. Miller K.D. Synaptic economics: competition and cooperation in synaptic plasticity. Neuron 17 (1996) 371-374
13. Marder E., and Prinz A.A. Modeling stability in neuron and network function: the role of activity in homeostasis. Bioessays 24 (2002) 1145-1154
14. Abbott L.F., and Nelson S.B. Synaptic plasticity: taming the beast. Nat Neurosci 3 Suppl. (2000) 1178-1183
15. Turrigiano G.G. Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22 (1999) 221-227
16. Wirth C., and Luscher H.R. Spatiotemporal evolution of excitation and inhibition in the rat barrel cortex investigated with multielectrode arrays. J Neurophysiol 91 (2004) 1635-1647
17. Gholmieh G., Soussou W., Courellis S., et al. A biosensor for detecting changes in cognitive processing based on nonlinear systems analysis. Biosens Bioelectron 16 (2001) 491-501
18. Beggs J.M., and Plenz D. Neuronal avalanches in neocortical circuits. J Neurosci 23 (2003) 11167-11177
19. Beggs J.M., and Plenz D. Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures. J Neurosci 24 (2004) 5216-5229
20. Tang A., Jackson D., Hobbs J., et al. A maximum entropy model applied to spatial and temporal correlations from cortical networks in vitro. J Neurosci 28 (2008) 505-518
21. Hsu D., Tang A., Hsu M., et al. Simple spontaneously active Hebbian learning model: homeostasis of activity and connectivity, and consequences for learning and epileptogenesis. Phys Rev E 76 4, Pt. 1 (2007) 041909
22. Bak P., Tang C., and Wiesenfeld K. Self-organized criticality: an explanation of the 1/f noise. Phys Rev Lett 59 (1987) 381-384
23. Paczuski M., Maslov S., and Bak P. Avalanche dynamics in evolution, growth, and depinning models. Phys Rev E 53 (1996) 414-443
24. Priesemann V, Wibral M, Munk MHJ. Detection of neuronal avalanches under incomplete sampling conditions in models of self- organized criticality and the macaque brain. In: Society for Neuroscience annual meeting; San Diego, CA; 2007.
25. Hahn G, Havenith MN, Yu S, et al. Neuronal avalanches in vivo and in spiking activity. In: Society for Neuroscience annual meeting; San Diego, CA; 2007.
26. Mazzoni A., Broccard F.D., Garcia-Perez E., et al. On the dynamics of the spontaneous activity in neuronal networks. PLoS ONE 2 5 (2007) e439
27. Beggs J.M. The criticality hypothesis: how local cortical networks might optimize information processing. Philos Transact A Math Phys Eng Sci 366 (2008) 329-343
28. Plenz D., and Thiagarajan T.C. The organizing principles of neuronal avalanches: cell assemblies in the cortex?. Trends Neurosci 30 (2007) 101-110
29. Beggs JM. Neuronal avalanche. In: Scholarpedia 2007. Available at: www.scholarpedia.org/article/Neuronal_Avalanche.
30. Haldeman C., and Beggs J.M. Critical branching captures activity in living neural networks and maximizes the number of metastable States. Phys Rev Lett 94 (2005) 058101
31. Hsu D., and Beggs J.M. Neuronal avalanches and criticality: a dynamical model for homeostasis. Neurocomputing 69 (2006) 1134-1136
32. Levina A., Herrmann J.M., and Geisel T. Dynamical synapses causing self-organizing criticality in neural networks. Nat Phys 3 (2007) 857-860
33. Abbott L.F., and Rohrkemper R. A simple growth model constructs critical avalanche networks. Prog Brain Res 165 (2007) 13-19
34. Beggs J.M. How to build a critical mind. Nat Phys 3 (2007) 834-835
35. De Arcangelis L., Perrone-Capano C., and Herrmann H.J. Self-organized criticality model for brain plasticity. Phys Rev Lett 96 (2006) 028107
36. Chialvo D.R. Psychophysics: are our senses critical?. Nat Phys 2 (2006) 301-302
37. Kinouchi O., and Copelli M. Optimal dynamical range of excitable networks at criticality. Nat Phys 2 (2006) 348-352
38. Juanico D.E., Monterola C., and Saloma C. Dissipative self-organized branching in a dynamic population. Phys Rev E 75 4, Pt. 2 (2007) 045105
39. Teramae J., and Fukai T. Local cortical circuit model inferred from power-law distributed neuronal avalanches. J Comput Neurosci 22 (2007) 301-312
40. Lee K.E., and Lee J.W. Avalanche dynamics of idealized neuron function in the brain on an uncorrelated random scale-free network. Eur Phys J B 50 (2006) 271-275
41. Petermann T, Lebedev M, Nicolelis M, et al. Neuronal avalanches in vivo. In: Society for Neuroscience annual meeting; 2006.
42. Stewart C.V., and Plenz D. Homeostasis of neuronal avalanches during postnatal cortex development in vitro. J Neurosci Methods 169 (2008) 405-416
43. Bertschinger N., and Natschlager T. Real-time computation at the edge of chaos in recurrent neural networks. Neural Comput 16 (2004) 1413-1436
44. Turrigiano G.G., and Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5 (2004) 97-107
45. Turrigiano G.G., and Nelson S.B. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10 (2000) 358-364
46. Wierenga C.J., Ibata K., and Turrigiano G.G. Postsynaptic expression of homeostatic plasticity at neocortical synapses. J Neurosci 25 (2005) 2895-2905
47. Royer S., and Pare D. Conservation of total synaptic weight through balanced synaptic depression and potentiation. Nature 422 (2003) 518-522
48. Jacobs K.M., and Prince D.A. Excitatory and inhibitory postsynaptic currents in a rat model of epileptogenic microgyria. J Neurophysiol 93 (2005) 687-696
49. Li H., and Prince D.A. Synaptic activity in chronically injured, epileptogenic sensory-motor neocortex. J Neurophysiol 88 (2002) 2-12
50. Jacobs K.M., Graber K.D., Kharazia V.N., et al. Postlesional epilepsy: the ultimate brain plasticity. Epilepsia 41 Suppl. 6 (2000) S153-S161
51. Salin P., Tseng G.F., Hoffman S., et al. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 15 (1995) 8234-8245
52. Graber K.D., and Prince D.A. A critical period for prevention of posttraumatic neocortical hyperexcitability in rats. Ann Neurol 55 (2004) 860-870
53. Graber K.D., and Prince D.A. Tetrodotoxin prevents posttraumatic epileptogenesis in rats. Ann Neurol 46 (1999) 234-242
54. Houweling A.R., Bazhenov M., Timofeev I., et al. Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb Cortex 15 (2005) 834-845
55. Frohlich F., Bazhenov M., and Sejnowski T.J. Pathological effect of homeostatic synaptic scaling on network dynamics in diseases of the cortex. J Neurosci 28 (2008) 1709-1720
56. Johnston D., Christie B.R., Frick A., et al. Active dendrites, potassium channels and synaptic plasticity. Philos Trans R Soc Lond B 358 (2003) 667-674
57. Stuart G., Spruston N., Sakmann B., et al. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20 (1997) 125-131
58. Waters J., Schaefer A., and Sakmann B. Backpropagating action potentials in neurones: measurement, mechanisms and potential functions. Prog Biophys Mol Biol 87 (2005) 145-170
59. Schevon C, Emerson R. Microphysiology of human epileptogenic cortex. In: American Epilepsy Society annual meeting; Philadelphia, PA; 2007.
60. Worrell G. The spatial scale of ictogenesis. In: American Epilepsy Society annual meeting; Philadelphia, PA; 2007.
61. Levy W.B., Hocking A.B., and Wu X. Interpreting hippocampal function as recoding and forecasting. Neural Netw 18 (2005) 1242-1264
62. Madhavan R., Chao Z.C., and Potter S.M. Plasticity of recurring spatiotemporal activity patterns in cortical networks. Phys Biol 4 (2007) 181-193
63. Rolston J.D., Wagenaar D.A., and Potter S.M. Precisely timed spatiotemporal patterns of neural activity in dissociated cortical cultures. Neuroscience 148 (2007) 294-303
64. Lisman J. The theta/gamma discrete phase code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15 (2005) 913-922
65. Buzsaki G. Rhythms of the brain (2006), Oxford Univ. Press, New York
66. Buzsaki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15 (2005) 827-840
67. Skaggs W.E., McNaughton B.L., Wilson M.A., et al. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6 (1996) 149-172
68. Maurer A.P., Cowen S.L., Burke S.N., et al. Organization of hippocampal cell assemblies based on theta phase precession. Hippocampus 16 (2006) 785-794
69. Albensi B.C., Oliver D.R., Toupin J., et al. Electrical stimulation protocols for hippocampal synaptic plasticity and neuronal hyper-excitability: are they effective or relevant?. Exp Neurol 204 (2007) 1-13
70. Morrell M. Brain stimulation for epilepsy: can scheduled or responsive neurostimulation stop seizures?. Curr Opin Neurol 19 (2006) 164-168
71. Theodore W.H., and Fisher R. Brain stimulation for epilepsy. Acta Neurochir Suppl 97 Pt. 2 (2007) 261-272
72. Andrade D.M., Zumsteg D., Hamani C., et al. Long-term follow-up of patients with thalamic deep brain stimulation for epilepsy. Neurology 66 (2006) 1571-1573
73. Boon P., Vonck K., De Herdt V., et al. Deep brain stimulation in patients with refractory temporal lobe epilepsy. Epilepsia 48 (2007) 1551-1560
74. Velasco A.L., Velasco F., Velasco M., et al. Electrical stimulation of the hippocampal epileptic foci for seizure control: a double-blind, long-term follow-up study. Epilepsia 48 (2007) 1895-1903
75. Benifla M., Rutka J.T., Logan W., et al. Vagal nerve stimulation for refractory epilepsy in children: indications and experience at The Hospital for Sick Children. Childs Nerv Syst 22 (2006) 1018-1026
76. Crumrine P.K. Vagal nerve stimulation in children. Semin Pediatr Neurol 7 (2000) 216-223
77. Murphy J.V., Torkelson R., Dowler I., et al. Vagal nerve stimulation in refractory epilepsy: the first 100 patients receiving vagal nerve stimulation at a pediatric epilepsy center. Arch Pediatr Adolesc Med 157 (2003) 560-564
78. Bedard C., Krogen H., and Destexhe A. Does the 1/f frequency scaling of brain signals reflect self-organized critical states?. Phys Rev Lett 97 (2006) 118102
79. McQuarrie D.A. Statistical mechanics (2000), Univ. Science Books, Sausalito, CA
80. Theodorakis S., and Koutroumbas K. Pattern recognition. 2nd ed. (2003), Academic Press, Amsterdam
81. Montgomery Jr. E.B., Huang H., and Assadi A. Unsupervised clustering algorithm for N -dimensional data. J Neurosci Methods 144 (2005) 19-24
82. Schiff S.J., Jerger K., Duong D.H., et al. Controlling chaos in the brain. Nature 370 (1994) 615-620
83. Wu J.Y., Guan L., and Tsau Y. Propagating activation during oscillations and evoked responses in neocortical slices. J Neurosci 19 (1999) 5005-5015