In vivo evaluation of the dentate gate theory in epilepsy

Journal of Physiology

Volumn 593, Issue 10, 2015, Pages 2379-2388

  Krook Magnuson, Esther ^a   Armstrong, Caren ^a   Bui, Anh ^a   Lew, Sean ^a   Oijala, Mikko ^a   Soltesz, Ivan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HALORHODOPSIN;

ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DENTATE GYRUS; DISEASE SEVERITY; ENTORHINAL CORTEX; EPILEPSY; GABAERGIC SYSTEM; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; IN VIVO STUDY; INTERVENTION STUDY; MOUSE; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SEIZURE; TEMPORAL LOBE EPILEPSY; ANIMAL; C57BL MOUSE; DISEASE MODEL; ELECTROENCEPHALOGRAPHY; FEMALE; INBRED MOUSE STRAIN; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; FEMALE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; SEIZURES;

EID: 84929510035     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270056     Document Type: Article

References (56)

1. Acsady L, Kamondi A, Sik A, Freund T & Buzsaki G (1998). GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18, 3386-3403.
2. Ang CW, Carlson GC & Coulter DA (2006). Massive and specific dysregulation of direct cortical input to the hippocampus in temporal lobe epilepsy. J Neurosci 26, 11850-11856.
3. Armstrong C, Krook-Magnuson E, Oijala M & Soltesz I (2013). Closed-loop optogenetic intervention in mice. Nat Protoc 8, 1475-1493.
4. Armstrong C, Krook-Magnuson E & Soltesz I (2012). Neurogliaform and Ivy cells: a major family of nNOS expressing GABAergic neurons. Front Neural Circuits 6, 23.
5. Armstrong C, Szabadics J, Tamas G & Soltesz I (2011). Neurogliaform cells in the molecular layer of the dentate gyrus as feed-forward gamma-aminobutyric acidergic modulators of entorhinal-hippocampal interplay. J Comp Neurol 519, 1476-1491.
6. Berglind F, Ledri M, Sorensen AT, Nikitidou L, Melis M, Bielefeld P, Kirik D, Deisseroth K, Andersson M & Kokaia M (2014). Optogenetic inhibition of chemically induced hypersynchronized bursting in mice. Neurobiol Dis 65, 133-141.
7. Bertram EH (2014). Extratemporal lobe circuits in temporal lobe epilepsy. Epilepsy Behav.
8. Bouilleret V, Loup F, Kiener T, Marescaux C & Fritschy JM (2000). Early loss of interneurons and delayed subunit-specific changes in GABA(A)-receptor expression in a mouse model of mesial temporal lobe epilepsy. Hippocampus 10, 305-324.
9. Bragin A, Engel J, Jr., Wilson CL, Vizentin E & Mathern GW (1999). Electrophysiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia 40, 1210-1221.
10. Buckmaster PS & Lew FH (2011). Rapamycin suppresses mossy fiber sprouting but not seizure frequency in a mouse model of temporal lobe epilepsy. J Neurosci 31, 2337-2347.
11. Cavalheiro EA, Riche DA & LeGal La Salle G (1982). Long-term effects of intrahippocampal kainic acid injection in rats: a method for inducing spontaneous recurrent seizures. Electroencephalogr Clin Neurophysiol 53, 581-589.
12. Chiang CC, Ladas TP, Gonzalez-Reyes LE & Durand DM (2014). Seizure suppression by high frequency optogenetic stimulation using in vitro and in vivo animal models of epilepsy. Brain Stimul 7, 890-899.
13. Coulter DA (1999). Chronic epileptogenic cellular alterations in the limbic system after status epilepticus. Epilepsia 40(Suppl 1), S23-33; discussion S40-21.
14. Coulter DA & Carlson GC (2007). Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog Brain Res 163, 235-812.
15. Coulter DA, Yue C, Ang CW, Weissinger F, Goldberg E, Hsu FC, Carlson GC & Takano H (2011). Hippocampal microcircuit dynamics probed using optical imaging approaches. J Physiol 589, 1893-1903.
16. deAlmeida L, Idiart M & Lisman JE (2009). The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J Neurosci 29, 7504-7512.
17. Eichenbaum H & Cohen NJ (2014). Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 83, 764-770.
18. Fisher RS (2013). Deep brain stimulation for epilepsy. Handb Clin Neurol 116, 217-234.
19. Hartley T, Lever C, Burgess N & O'Keefe J (2014). Space in the brain: how the hippocampal formation supports spatial cognition. Philos Trans R Soc Lond B Biol Sci 369, 20120510.
20. Haussler U, Bielefeld L, Froriep UP, Wolfart J & Haas CA (2012). Septotemporal position in the hippocampal formation determines epileptic and neurogenic activity in temporal lobe epilepsy. Cereb Cortex 22, 26-36.
21. Heck CN, King-Stephens D, Massey AD, Nair DR, Jobst BC, Barkley GL, Salanova V, Cole AJ, Smith MC, Gwinn RP, Skidmore C, VanNess PC, Bergey GK, Park YD, Miller I, Geller E, Rutecki PA, Zimmerman R, Spencer DC, Goldman A, Edwards JC, Leiphart JW, Wharen RE, Fessler J, Fountain NB, Worrell GA, Gross RE, Eisenschenk S, Duckrow RB, Hirsch LJ, Bazil C, O'Donovan CA, Sun FT, Courtney TA, Seale CG & Morrell MJ (2014). Two-year seizure reduction in adults with medically intractable partial onset epilepsy treated with responsive neurostimulation: final results of the RNS System Pivotal trial. Epilepsia 55, 432-441.
22. 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.
23. Heinemann U, Zhang CL & Eder C (1993). Entorhinal cortex-hippocampal interactions in normal and epileptic temporal lobe. Hippocampus 3(Spec No), 89-97.
24. Henze DA, Wittner L & Buzsaki G (2002). Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5, 790-795.
25. Hester MS & Danzer SC (2013). Accumulation of abnormal adult-generated hippocampal granule cells predicts seizure frequency and severity. J Neurosci 33, 8926-8936.
26. Kobayashi M & Buckmaster PS (2003). Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23, 2440-2452.
27. Krook-Magnuson E, Armstrong C, Oijala M & Soltesz I (2013). On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat Commun 4, 1376.
28. Krook-Magnuson E, Ledri M, Soltesz I & Kokaia M (2014a). How might novel technologies such as optogenetics lead to better treatments in epilepsy? Adv Exp Med Biol 813, 319-336.
29. Krook-Magnuson E, Szabo GG, Armstrong C, Oijala M & Soltesz I (2014b). Cerebellar directed optogenetic intervention inhibits spontaneous hippocampal seizures in a mouse model of temporal lobe epilepsy. eNeruo 2014 Dec;1(1). pii: e.2014.
30. Ledri M, Madsen MG, Nikitidou L, Kirik D & Kokaia M (2014). Global optogenetic activation of inhibitory interneurons during epileptiform activity. J Neurosci 34, 3364-3377.
31. Leutgeb JK, Leutgeb S, Moser MB & Moser EI (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315, 961-966.
32. 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.
33. Luttjohann A, Fabene PF & vanLuijtelaar G (2009). A revised Racine's scale for PTZ-induced seizures in rats. Physiol Behav 98, 579-586.
34. Lysetskiy M, Foldy C & Soltesz I (2005). Long- and short-term plasticity at mossy fiber synapses on mossy cells in the rat dentate gyrus. Hippocampus 15, 691-696.
35. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, Fujisawa S, Hsu YW, Garcia AJ, 3rd, Gu X, Zanella S, Kidney J, Gu H, Mao Y, Hooks BM, Boyden ES, Buzsaki G, Ramirez JM, Jones AR, Svoboda K, Han X, Turner EE & Zeng H (2012). A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 15, 793-802.
36. Marucci G, Rubboli G & Giulioni M (2010). Role of dentate gyrus alterations in mesial temporal sclerosis. Clin Neuropathol 29, 32-35.
37. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA & Tonegawa S (2007). Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317, 94-99.
38. Mody I, Kohr G, Otis TS & Staley KJ (1992). The electrophysiology of dentate gyrus granule cells in whole-cell recordings. Epilepsy Res Suppl 7, 159-168.
39. Morgan RJ, Santhakumar V & Soltesz I (2007). Modeling the dentate gyrus progress in brain research. In The Dentate Gyrus: A Comprehensive Guide to Structure, Function, and Clinical Implications, Volume 163, ed. Scharfman HE, pp. 639-658. Elsevier, Amsterdam.
40. Nadler JV, Perry BW, Gentry C & Cotman CW (1980). Loss and reacquisition of hippocampal synapses after selective destruction of CA3-CA4 afferents with kainic acid. Brain Res 191, 387-403.
41. Pathak HR, Weissinger F, Terunuma M, Carlson GC, Hsu FC, Moss SJ & Coulter DA (2007). Disrupted dentate granule cell chloride regulation enhances synaptic excitability during development of temporal lobe epilepsy. J Neurosci 27, 14012-14022.
42. Paz JT, Bryant AS, Peng K, Fenno L, Yizhar O, Frankel WN, Deisseroth K & Huguenard JR (2011). A new mode of corticothalamic transmission revealed in the Gria4(-/-) model of absence epilepsy. Nat Neurosci 14, 1167-1173.
43. Peirce JL, Chesler EJ, Williams RW & Lu L (2003). Genetic architecture of the mouse hippocampus: identification of gene loci with selective regional effects. Genes Brain Behav 2, 238-252.
44. Pinel JP & Rovner LI (1978). Experimental epileptogenesis: kindling-induced epilepsy in rats.Exp Neurol 58, 190-202.
45. Pun RY, Rolle IJ, Lasarge CL, Hosford BE, Rosen JM, Uhl JD, Schmeltzer SN, Faulkner C, Bronson SL, Murphy BL, Richards DA, Holland KD & Danzer SC (2012). Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron 75, 1022-1034.
46. Racine R ( 1971). Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 32, 281-294.
47. Racine RJ, Burnham WM, Gartner JG & Levitan D (1973). Rates of motor seizure development in rats subjected to electrical brain stimulation: strain and inter-stimulation interval effects. Electroencephalogr Clin Neurophysiol 35, 553-556.
48. Stegen M, Kirchheim F, Hanuschkin A, Staszewski O, Veh RW & Wolfart J (2012). Adaptive intrinsic plasticity in human dentate gyrus granule cells during temporal lobe epilepsy. Cereb Cortex 22, 2087-2101.
49. Sukhotinsky I, Chan AM, Ahmed OJ, Rao VR, Gradinaru V, Ramakrishnan C, Deisseroth K, Majewska AK & Cash SS (2013). Optogenetic delay of status epilepticus onset in an in vivo rodent epilepsy model. PloS ONE 8, e62013.
50. Tonnesen J, Sorensen AT, Deisseroth K, Lundberg C & Kokaia M (2009). Optogenetic control of epileptiform activity. Proc Natl Acad Sci U S A 106, 12162-12167.
51. Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, Anderson DJ, Mayford M, Kandel ER & Tonegawa S (1996). Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87, 1317-1326.
52. vanStrien NM, Cappaert NL & Witter MP (2009). The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10, 272-282.
53. Wozny C, Gabriel S, Jandova K, Schulze K, Heinemann U & Behr J (2005). Entorhinal cortex entrains epileptiform activity in CA1 in pilocarpine-treated rats. Neurobiol Dis 19, 451-460.
54. Wykes RC, Heeroma JH, Mantoan L, Zheng K, MacDonald DC, Deisseroth K, Hashemi KS, Walker MC, Schorge S & Kullmann DM (2012). Optogenetic and potassium channel gene therapy in a rodent model of focal neocortical epilepsy. Sci Transl Med 4, 161ra152.
55. Yu EP, Dengler CG, Frausto SF, Putt ME, Yue C, Takano H & Coulter DA (2013). Protracted postnatal development of sparse, specific dentate granule cell activation in the mouse hippocampus. J Neurosci 33, 2947-2960.
56. Zhang W, Huguenard JR & Buckmaster PS (2012). Increased excitatory synaptic input to granule cells from hilar and CA3 regions in a rat model of temporal lobe epilepsy. J Neurosci 32, 1183-1196.