Preictal activity of subicular, CA1, And dentate gyrus principal neurons in the dorsal hippocampus before spontaneous seizures in a rat model of temporal lobe epilepsy

Journal of Neuroscience

Volumn 34, Issue 50, 2014, Pages 16671-16687

  Fujita, Satoshi ^a,c   Toyoda, Izumi ^a   Thamattoor, Ajoy K ^c   Buckmaster, Paul S ^a,b  

^a Departments of Comparative Medicine Stanford   (United States)

^b STANFORD UNIVERSITY   (United States)

^c NIHON UNIVERSITY   (Japan)

Author keywords

Hippocampus; Subiculum; Unit recording

Indexed keywords

ATROPINE METHYL BROMIDE; DIAZEPAM; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH RECORDING; BRAIN ELECTROPHYSIOLOGY; CELL COUNTING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENTATE GYRUS; ELECTROSTIMULATION; EPILEPTIC STATE; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS THETA RHYTHM; LOCAL FIELD POTENTIAL; MALE; NERVE CELL NETWORK; NERVE POTENTIAL; NISSL STAINING; NONHUMAN; RAT; REM SLEEP DEPRIVATION; SEIZURE; SPIKE WAVE; SUBICULUM; SURGERY; TEMPORAL LOBE EPILEPSY; ACTION POTENTIAL; ANIMAL; DISEASE MODEL; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; DENTATE GYRUS; DISEASE MODELS, ANIMAL; EPILEPSY, TEMPORAL LOBE; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES;

EID: 84916607115     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0584-14.2014     Document Type: Article

References (92)

1. Alme CB, Buzzetti RA, Marrone DF, Leutgeb JK, Chawla MK, Schaner MJ, Bohanick JD, Khoboko T, Leutgeb S, Moser EI, Moser MB, McNaughton BL, Barnes CA (2010) Hippocampal granule cells opt for early retire-ment. Hippocampus 20:1109-1123. CrossRef Medline
2. Alonso-Nanclares L, Kastanauskaite A, Rodriguez JR, Gonzalez-Soriano J, Defelipe J (2011) A stereological study of synapse number in the epileptic human hippocampus. Front Neuroanat 5:8. CrossRef Medline
3. Anderson MI, O’Mara SM (2003) Analysis of recordings of single-unit firing and population activity in the dorsal subiculum of unrestrained, freely moving rats. J Neurophysiol 90:655-665. CrossRef Medline
4. Avoli M, Barbarosie M, Lucke A, Nagao T, Lopantsev V, Köhling R (1996) Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J Neurosci 16:3912-3924.Medline
5. Babb TL, Crandall PH (1976) Epileptogenesis of human limbic neurons in psychomotor epileptics. Electroencephalogr Clin Neurophysiol 40:225-243. CrossRef Medline
6. Babb TL, Wilson CL, Isokawa-Akesson M (1987) Firing patterns of human limbic neurons during stereoencephalography (SEEG) and clinical temporal lobe seizures. Electroencephalogr Clin Neurophysiol 66:467-482. CrossRef Medline
7. Bartolomei F, Khalil M, Wendling F, Sontheimer A, Régis J, Ranjeva JP, Guye M, Chauvel P (2005) Entorhinal cortex involvement in human mesial temporal lobe epilepsy: an electrophysiologic and volumetric study. Epi-lepsia 46:677-687. CrossRef Medline
8. Bartolomei F, Chauvel P, Wendling F (2008) Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 131:1818-1830. CrossRef Medline
9. Bertram EH (1997) Functional anatomy of spontaneous seizures in a rat model of limbic epilepsy. Epilepsia 38:95-105. CrossRef Medline
10. Bertram EH, Mangan PS, Zhang D, Scott CA, Williamson JM (2001) The midline thalamus: alterations and a potential role in limbic epilepsy. Epi-lepsia 42:967-978. CrossRef Medline
11. Bikson M, Fox JE, Jefferys JGR (2003) Neuronal aggregate formation un-derlies spatiotemporal dynamics of nonsynaptic seizure initiation. J Neurophysiol 89:2330-2333. CrossRef Medline
12. Bland BH, Konopacki J, Dyck R (2005) Heterogeneity among hippocampal pyramidal neurons revealed by their relation to theta-band oscillation and synchrony. Exp Neurol 195:458-474. CrossRef Medline
13. Bower MR, Buckmaster PS (2008) Changes in granule cell firing rates pre-cede locally recorded spontaneous seizures by minutes in an animal model of temporal lobe epilepsy. J Neurophysiol 99:2431-2442. CrossRef Medline
14. Bower MR, Stead M, Meyer FB, Marsh WR, Worrell GA (2012) Spatiotem-poral neuronal correlates of seizure generation in focal epilepsy. Epilepsia 53:807-816. CrossRef Medline
15. Bragin A, Engel J Jr, Wilson CL, Vizentin E, Mathern GW (1999) Electro-physiologic analysis of a chronic seizure model after unilateral hippocampal KA injection. Epilepsia 40:1210-1221. CrossRef Medline
16. Bragin A, Wilson CL, Engel J Jr (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clus-ters: a hypothesis. Epilepsia 41 [Suppl 6]:S144-S152.
17. Arecep-tors in the medial septal region induces epileptiform activity in the hippocampus. Neurosci Lett 434:133-138. CrossRef Medline
18. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.Medline
19. Chauvière L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C (2009) Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci 29:5402-5410. CrossRef Medline
20. Chen S, Su H, Yue C, Remy S, Royeck M, Sochivko D, Opitz T, Beck H, Yaari Y (2011) An increase in persistent sodium current contributes to intrinsic neuronal bursting after status epilepticus. J Neurophysiol 105:117-129. CrossRef Medline
21. Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421. CrossRef Medline
22. Colom LV, García-Hernández A, Castañeda MT, Perez-Cordova MG, Garrido-Sanabria ER (2006) Septo-hippocampal networks in chronically epileptic rats: potential antiepileptic effects of theta rhythm genera-tion. J Neurophysiol 95:3645-3653. CrossRef Medline
23. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274-287.Medline
24. Cymerblit-Sabba A, Schiller Y (2012) Development of hypersynchrony in the cortical network during chemoconvulsant-induced epileptic seizures in vivo. J Neurophysiol 107:1718-1730. CrossRef Medline
25. Engel J Jr, Williamson PD, Wieser HG (1997) Mesial temporal lobe epilepsy. In: Epilepsy: a comprehensive textbook (Engel J Jr, Pedley TA, eds), pp 2417-2426. Philadelphia: Lippincott-Raven.
26. Fabó D, Maglóczky Z, Wittner L, Pék A, Eross L, Czirják S, Vajda J, Sólyom A, Rásonyi G, Szucs A, Kelemen A, Juhos V, Grand L, Dombovári B, Halász P, Freund TF, Halgren E, Karmos G, Ulbert I (2008) Properties of in vivo interictal spike generation in the human subiculum. Brain 131:485-499. CrossRef Medline
27. Feldt Muldoon SF, Soltesz I, Cossart R (2013) Spatially clustered neuronal assemblies comprise the microstructure of synchrony in chronically epileptic networks. Proc Natl Acad Sci U S A 110:3567-3572. CrossRef Medline
28. Fox SE, Ranck JB Jr (1975) Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats. Exp Neurol 49:299-313. CrossRef Medline
29. Gnatkovsky V, Librizzi L, Trombin F, de Curtis M (2008) Fast activity at seizure onset is mediated by inhibitory circuits in the entorhinal cortex in vitro. Ann Neurol 64:674-686. CrossRef Medline
30. Grasse DW, Karunakaran S, Moxon KA (2013) Neuronal synchrony and the transition to spontaneous seizures. Exp Neurol 248:72-84. CrossRef Medline
31. Harris KD, Henze DA, Csicsvari J, Hirase H, Buzsáki G (2000) Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J Neurophysiol 84:401-414.Medline
32. He de F, Ma DL, Tang YC, Engel J Jr, Bragin A, Tang FR (2010) Morphophysiologic characteristics of dorsal subicular network in mice after pilocarpine-induced status epilepticus. Brain Pathol 20:80-95. CrossRef Medline
33. Hellier JL, Dudek FE (1999) Spontaneous motor seizures of rats with kainate-induced epilepsy: effect of time of day and activity state. Epilepsy Res 35:47-57. CrossRef Medline
34. Henze DA, Borhegyi Z, Csicsvari J, Mamiya A, Harris KD, Buzsáki G (2000) Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J Neurophysiol 84:390-400. Medline
35. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R, Rivera C (2007) Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27:9866-9873. CrossRef Medline
36. Huberfeld G, de la Prida ML, Pallud J, Cohen I, Le Van Quyen M, Adam C, Clemenceau S, Baulac M, Miles R (2011) Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy. Nat Neurosci 14:627-634. CrossRef Medline
37. Inostroza M, Brotons-Mas JR, Laurent F, Cid E, de la Prida LM (2013) Spe-cific impairment of “what-where-when” episodic-like memory in experimental models of temporal lobe epilepsy. J Neurosci 33:17749-17762. CrossRef Medline
38. Jefferys JGR, Hass HL (1982) Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission. Nature 300:448-450. CrossRef Medline
39. Jensen MS, Yaari Y (1997) Role of intrinsic burst firing, potassium accumu-lation, and electrical coupling in the elevated potassium model of hippocampal epilepsy. J Neurophysiol 77:1224-1233. Medline
40. Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165-182. CrossRef Medline
41. Kandel ER, Spencer WA (1961) Excitation and inhibition of single pyramidal cells during hippocampal seizure. Exp Neurol 4:162-179. CrossRef Medline
42. Keller CJ, Truccolo W, Gale JT, Eskandar E, Thesen T, Carlson C, Devinsky O, Kuzniecky R, Doyle WK, Madsen JR, Schomer DL, Mehta AD, Brown EN, Hochberg LR, Ulbert I, Halgren E, Cash SS (2010) Heterogeneous neu-ronal firing patterns during interictal epileptiform discharges in the hu-man cortex. Brain 133:1668-1681. CrossRef Medline
43. Kitchigina VF, Butuzova MV (2009) Theta activity of septal neurons during different epileptic phases: the same frequency but different significance? Exp Neurol 216:449-458. CrossRef Medline
44. Klausberger T, Magill PJ, Márton LF, Roberts JDB, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state-and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848. CrossRef Medline
45. Knopp A, Kivi A, Wozny C, Heinemann U, Behr J (2005) Cellular and network properties of the subiculum in the pilocarpine model of temporal lobe epilepsy. J Comp Neurol 483:476-488. CrossRef Medline
46. Knopp A, Frahm C, Fidzinski P, Witte OW, Behr J (2008) Loss of GABAergic neurons in the subiculum and its functional implications in temporal lobe epilepsy. Brain 131:1516-1527. CrossRef Medline
47. Lehmann TN, Gabriel S, Eilers A, Njunting M, Kovacs R, Schulze K, Lanksch WR, Heinemann U (2001) Fluorescent tracer in pilocarpine-treated rats shows widespread aberrant hippocampal neuronal connectivity. Eur J Neurosci 14:83-95. CrossRef Medline
48. Lenck-Santini PP, Holmes GL (2008) Altered phase precession and com-pression of temporal sequences by place cells in epileptic rats. J Neurosci 28:5053-5062. CrossRef Medline
49. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966. CrossRef Medline
50. Lévesque M, Salami P, Gotman J, Avoli M (2012) Two seizure-onset types reveal specific patterns of high-frequency oscillations in a model of temporal lobe epilepsy. J Neurosci 32:13264-13272. CrossRef Medline
51. Lieb JP, Walsh GO, Babb TL, Walter RD, Crandall PH (1976) A comparison of EEG seizure patterns recorded with surface and depth electrodes in patients with temporal lobe epilepsy. Epilepsia 17:137-160. CrossRef Medline
52. Lin H, Hangya B, Fox SE, Muller RU (2012) Repetitive convulsant-induced seizures reduce the number but not precision of hippocampal place cells. J Neurosci 32:4163-4178. CrossRef Medline
53. Margerison JH, Corsellis JA (1966) Epilepsy and the temporal lobes. Brain 89:499-530. CrossRef Medline
54. Matsumoto H, Ajmone Marsan C (1964) Cortical cellular phenomena in experimental epilepsy: ictal manifestations. Exp Neurol 9:305-326. CrossRef Medline
55. Mello LE, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM (1993) Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34:985-995. CrossRef Medline
56. Miller JW, Turner GM, Gray BC (1994) Anticonvulsant effects of the exper-imental induction of hippocampal theta activity. Epilepsy Res 18:195-204. CrossRef Medline
57. Mitchell SJ, Ranck JB Jr (1980) Generation of theta rhythm in medial ento-rhinal cortex of freely moving rats. Brain Res 189:49-66. CrossRef Medline
58. Mody I, Lambert JDC, Heinemann U (1987) Low extracellular magnesium induces epileptiform activity and spreading depression in rat hippocampal slices. J Neurophysiol 57:869-888. Medline
59. Neunuebel JP, Knierim JJ (2012) Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J Neurosci 32:3848-3858. CrossRef Medline
60. Paxinos G, Watson C (2009) The rat brain in stereotaxic coordinates, Ed 6. Burlington, MA: Elsevier/Academic.
61. Popova IY, Sinelnikova VV, Kitchigina VF (2008) Disturbance of the corre-lation between hippocampal and septal EEGs during epileptogenesis. Neurosci Lett 442:228-233. CrossRef Medline
62. Prince DA, Wilder BJ (1967) Control mechanisms in cortical epileptogenic foci. Arch Neurol 16:194-202. CrossRef Medline
63. Quesney LF (1986) Clinical and EEG features of complex partial seizures of temporal lobe origin. Epilepsia 27 [Suppl 2]:S27-S45.
64. Racine RJ (1972) Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294. CrossRef Medline
65. Rafiq A, DeLorenzo RJ, Coulter DA (1993) Generation and propagation of epileptiform discharges in a combined entorhinal cortex/hippocampal slice. J Neurophysiol 70:1962-1974. Medline
66. Ranck JB Jr (1973) Studies on single neurons in dorsal hippocampal forma-tion and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41:461-531. Medline
67. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsáki G (2012) Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15:769-775. CrossRef Medline
68. 2-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J Physiol 532:205-216. CrossRef Medline
69. Schevon CA, Weiss SA, McKhann G Jr, Goodman RR, Yuste R, Emerson RG, Trevelyan AJ (2012) Evidence of an inhibitory restraint of seizure activity in humans. Nat Commun 3:1060. CrossRef Medline
70. Sedigh-Sarvestani M, Thuku GI, Sunderam S, Parkar A, Weinstein SL, Schiff SJ, Gluckman BJ (2014) Rapid eye movement sleep and hippocampal theta oscillations precede seizure onset in the tetanus toxin model of temporal lobe epilepsy. J Neurosci 34:1105-1114. CrossRef Medline
71. Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339-2356. Medline
72. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683-697. CrossRef Medline
73. Spencer SS (1998) Substrates of localization-related epilepsies: biologic implications of localizing findings in humans. Epilepsia 39:114-123. CrossRef Medline
74. Spencer SS (2002) Neural networks in human epilepsy: evidence of and im-plications for treatment. Epilepsia 43:219-227. CrossRef Medline
75. Spencer SS, Spencer DD (1994) Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia 35:721-727. CrossRef Medline
76. Spencer SS, Williamson PD, Spencer DD, Mattson RH (1987) Human hippocampal seizure spread studied by depth and subdural recording: the hippocampal commissure. Epilepsia 28:479-489. CrossRef Medline
77. Spencer SS, Spencer DD, Williamson PD, Mattson R (1990) Combined depth and subdural electrode investigation in uncontrolled epilepsy. Neurology 40:74-79. CrossRef Medline
78. Spencer SS, Guimaraes P, Katz A, Kim J, Spencer D (1992) Morphological patterns of seizures recorded intracranially. Epilepsia 33:537-545. CrossRef Medline
79. Sperling MR, O’Connor MJ (1989) Comparison of depth and subdural elec-trodes in recording temporal lobe seizures. Neurology 39:1497-1504. CrossRef Medline
80. Sypert GW, Ward AA (1967) The hyperexcitable neuron: microelectrode studies of the chronic epileptic focus in the intact, awake monkey. Exp Neurol 19:107-114. Medline
81. Takano H, McCartney M, Ortinski PI, Yue C, Putt ME, Coulter DA (2012) Deterministic and stochastic neuronal contributions to distinct synchronous CA3 network bursts. J Neurosci 32:4743-4754. CrossRef Medline
82. Toyoda I, Bower MR, Leyva F, Buckmaster PS (2013) Early activation of ventral hippocampus and subiculum during spontaneous seizures in a rat model of temporal lobe epilepsy. J Neurosci 33:11100-11115. CrossRef Medline
83. Traynelis SF, Dingledine R (1988) Potassium-induced spontaneous electro-graphic seizures in the rat hippocampal slice. J Neurophysiol 59:259-276. Medline
84. Truccolo W, Donoghue JA, Hochberg LR, Eskandar EN, Madsen JR, Ander-son WS, Brown EN, Halgren E, Cash SS (2011) Single-neuron dynamics in human focal epilepsy. Nat Neurosci 14:635-641. CrossRef Medline
85. Tyler AL, Mahoney JM, Richard GR, Holmes GL, Lenck-Santini PP, Scott RC (2012) Functional network changes in hippocampal CA1 after status epi-lepticus predict spatial memory deficits in rats. J Neurosci 32:11365-11376. CrossRef Medline
86. Verzeano M, Crandall PH, Dymond A (1971) Neuronal activity of the amygdala in patients with psychomotor epilepsy. Neuropsychologia 9:331-344. CrossRef Medline
87. Viskontas IV, Ekstrom AD, Wilson CL, Fried I (2007) Characterizing in-terneuron and pyramidal cells in the human medial temporal lobe in vivo using extracellular recordings. Hippocampus 17:49-57. CrossRef Medline
88. Walker WG, Dovey VJ (1944) Electro-encephalography in cases of sub-cortical tumour. J Neurol Neurosurg Psych 7:57-65. CrossRef
89. Wellmer J, Su H, Beck H, Yaari Y (2002) Long-lasting modification of intrinsic discharge properties in subicular neurons following status epilep-ticus. Eur J Neurosci 16:259-266. CrossRef
90. Wennberg R, Arruda F, Quesney LF, Olivier A (2002) Preeminence of ex-trahippocampal structures in the generation of mesial temporal seizures: evidence from human depth electrode recordings. Epilepsia 43:716-726. CrossRef Medline
91. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological esti-mation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497. CrossRef Medline
92. Ziburkus J, Cressman JR, Barreto E, Schiff SJ (2006) Interneuron and pyra-midal cell interplay during in vitro seizure-like events. J Neurophysiol 95:3948-3954. CrossRef Medline