Mossy fiber sprouting interacts with sodium channel mutations to increase dentate gyrus excitability

Epilepsia

Volumn 51, Issue 1, 2010, Pages 136-145

  Thomas, Evan A ^a,b   Reid, Christopher A ^a,b   Petrou, Steven ^a,b  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Computer simulations; Gene environment interactions; Mossy fiber sprouting; Recurrent networks; Temporal lobe epilepsy

Indexed keywords

SODIUM CHANNEL;

ARTICLE; CHANNEL GATING; COMPUTER SIMULATION; DENTATE GYRUS; EPILEPSY; EPILEPTOGENESIS; GENE; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; MOSSY FIBER; NERVE CELL NETWORK; NERVE FIBER GROWTH; PARAMETER; PRIORITY JOURNAL; SCN1B GENE;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, N-TYPE; COMPUTER SIMULATION; DENTATE GYRUS; ELECTRIC STIMULATION; EPILEPSY, TEMPORAL LOBE; EXCITATORY POSTSYNAPTIC POTENTIALS; HUMANS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MOSSY FIBERS, HIPPOCAMPAL; MUTATION; NEURAL INHIBITION; NEURAL NETWORKS (COMPUTER); NEURONS; PATCH-CLAMP TECHNIQUES; PERFORANT PATHWAY; RATS; SEIZURES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SYNAPTIC TRANSMISSION;

EID: 76249104543     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2009.02202.x     Document Type: Article

References (33)

1. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF 1991) Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 42 : 351 363.
2. Chiu C, Reid CA, Tan HO, Davies PJ, Single FN, Koukoulas I, Berkovic SF, Tan SS, Sprengel R, Jones MV, Petrou S 2008) Developmental impact of a familial GABAA receptor epilepsy mutation. Ann Neurol 64 : 284 293.
3. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD 1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495 : 387 395.
4. Dudek FE, Sutula TP 2007) Epileptogenesis in the dentate gyrus: a critical perspective. Prog Brain Res 163 : 755 773.
5. Dyhrfjeld-Johnsen J, Santhakumar V, Morgan RJ, Huerta R, Tsimring L, Soltesz I 2007) Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol 97 : 1566 1587.
6. Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ 2003) Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122 : 811 829.
7. Heinemann U, Beck H, Dreier JP, Ficker E, Stabel J, Zhang CL 1992) The dentate gyrus as a regulated gate for the propagation of epileptiform activity. Epilepsy Res Suppl 7 : 273 280.
8. Hines M 1984) Efficient computation of branched nerve equations. Int J Biomed Comput 15 : 69 76.
9. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV 1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10 : 267 282.
10. Howard AL, Neu A, Morgan RJ, Echegoyen JC, Soltesz I 2007) Opposing modifications in intrinsic currents and synaptic inputs in post-traumatic mossy cells: evidence for single-cell homeostasis in a hyperexcitable network. J Neurophysiol 97 : 2394 2409.
11. Kananura C, Haug K, Sander T, Runge U, Gu W, Hallmann K, Rebstock J, Heils A, Steinlein OK 2002) A splice-site mutation in GABRG2 associated with childhood absence epilepsy and febrile convulsions. Arch Neurol 59 : 1137 1141.
12. Lothman EW, Stringer JL, Bertram EH 1992) The dentate gyrus as a control point for seizures in the hippocampus and beyond. Epilepsy Res Suppl 7 : 301 313.
13. Lytton WW 2008) Computer modelling of epilepsy. Nat Rev Neurosci 9 : 626 637.
14. Mascagni MV, Sherman AS 1998) Numerical methods for neuronal modeling. In Kock C, Segev I (Eds) Methods in neuronal modeling: from ions to networks. MIT Press, Cambridge, MA, pp. 569 606.
15. Morgan RJ, Soltesz I 2008) Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc Natl Acad Sci U S A 105 : 6179 6184.
16. Ogiwara I, Miyamoto H, Morita N, Atapour N, Mazaki E, Inoue I, Takeuchi T, Itohara S, Yanagawa Y, Obata K, Furuichi T, Hensch TK, Yamakawa K 2007) Na(v)1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J Neurosci 27 : 5903 5914.
17. Press WH, Flannery BP, Teukolsky SA, Vetterling WT 1988) Numerical recipes in C: the art of scientific computing. Cambridge University Press, Cambridge, UK.
18. Reid CA, Berkovic SF, Petrou S 2009) Mechanisms of human inherited epilepsies. Prog Neurobiol 87 : 41 57.
19. Santhakumar V, Ratzliff AD, Jeng J, Toth Z, Soltesz I 2001) Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann Neurol 50 : 708 717.
20. Santhakumar V, Aradi I, Soltesz I 2005) Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J Neurophysiol 93 : 437 453.
21. Scheffer IE, Harkin LA, Grinton BE, Dibbens LM, Turner SJ, Zielinski MA, Xu R, Jackson G, Adams J, Connellan M, Petrou S, Wellard RM, Briellmann RS, Wallace RH, Mulley JC, Berkovic SF 2007) Temporal lobe epilepsy and GEFS+ phenotypes associated with SCN1B mutations. Brain 130 : 100 109.
22. Spampanato J, Escayg A, Meisler MH, Goldin AL 2001) Functional effects of two voltage-gated sodium channel mutations that cause generalized epilepsy with febrile seizures plus type 2. J Neurosci 21 : 7481 7490.
23. Spampanato J, Aradi I, Soltesz I, Goldin AL 2004) Increased neuronal firing in computer simulations of sodium channel mutations that cause generalized epilepsy with febrile seizures plus. J Neurophysiol 91 : 2040 2050.
24. Staley KJ, Otis TS, Mody I 1992) Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and while-cell recordings. J Neurophysiol 67 : 1346 1358.
25. Stringer JL, Lothman EW 1992) Bilateral maximal dentate activation is critical for the appearance of an afterdischarge in the dentate gyrus. Neuroscience 46 : 309 314.
26. Sutula TP, Hermann B 1999) Progression in mesial temporal lobe epilepsy. Ann Neurol 45 : 553 556.
27. Tan HO, Reid CA, Single FN, Davies PJ, Chiu C, Murphy S, Clarke AL, Dibbens L, Krestel H, Mulley JC, Jones MV, Seeburg PH, Sakmann B, Berkovic SF, Sprengel R, Petrou S 2007) Reduced cortical inhibition in a mouse model of familial childhood absence epilepsy. Proc Natl Acad Sci U S A 104 : 17536 17541.
28. Thomas EA 2000) A parallel algorithm for simulation of large neural networks. J Neurosci Methods 98 : 123 134.
29. Thomas EA, Xu R, Petrou S 2007) Computational analysis of the R85C and R85H epilepsy mutations in Na+ channel beta 1 subunits. Neuroscience 147 : 1034 1046.
30. Thomas EA, Petrou S 2008) Case for realistic modeling in understanding seizures. Expert Rev Neurother 8 : 1771 1773.
31. Wallace RH, Marini C, Petrou S, Harkin LA, Bowser DN, Panchal RG, Williams DA, Sutherland GR, Mulley JC, Scheffer IE, Berkovic SF 2001) Mutant GABA(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizures. Nat Genet 28 : 49 52.
32. Xu R, Thomas EA, Gazina EV, Richards KL, Quick M, Wallace RH, Harkin LA, Heron SE, Berkovic SF, Scheffer IE, Mulley JC, Petrou S 2007) Generalized epilepsy with febrile seizures plus-associated sodium channel beta1 subunit mutations severely reduce beta subunit-mediated modulation of sodium channel function. Neuroscience 148 : 164 174.
33. Yu FH, Mantegazza M, Westenbroek RE, Robbins CA, Kalume F, Burton KA, Spain WJ, McKnight GS, Scheuer T, Catterall WA 2006) Reduced sodium current in GABAergic interneurons in a mouse model of severe myoclonic epilepsy in infancy. Nat Neurosci 9 : 1142 1149.