Adaptive intrinsic plasticity in human dentate gyrus granule cells during temporal lobe epilepsy

Cerebral Cortex

Volumn 22, Issue 9, 2012, Pages 2087-2101

  Stegen, Michael ^a   Kirchheim, Florian ^a,b   Hanuschkin, Alexander ^a   Staszewski, Ori ^a   Veh, Rüdiger W ^c   Wolfart, Jakob ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

hippocampus neurons; homeostasis; hyperpolarization activated cyclic nucleotide gated (HCN) channels h current; Kir channels; neuroprotection

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL;

ADOLESCENT; ADULT; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CHILD; DENTATE GYRUS; DISEASE SEVERITY; FEMALE; GRANULE CELL; HIPPOCAMPAL SCLEROSIS; HUMAN; HUMAN CELL; MALE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; POTASSIUM CURRENT; PRIORITY JOURNAL; TEMPORAL LOBE EPILEPSY; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; DENTATE GYRUS; EPILEPSY, TEMPORAL LOBE; HUMANS; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES;

EID: 84864958394     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr294     Document Type: Article

References (74)

1. Aponte Y, Lien CC, Reisinger E, Jonas P. 2006. Hyperpolarizationactivated cation channels in fast-spiking interneurons of rat hippocampus. J Physiol. 574:229-243. (Pubitemid 43905808)
2. Bender RA, Kirschstein T, Kretz O, Brewster AL, Richichi C, Ruschenschmidt C, Shigemoto R, Beck H, Frotscher M, Baram TZ. 2007. Localization of HCN1 channels to presynaptic compartments: novel plasticity that may contribute to hippocampal maturation. J Neurosci. 27:4697-4706. (Pubitemid 46663575)
3. Bender RA, Soleymani SV, Brewster AL, Nguyen ST, Beck H, Mathern GW, Baram TZ. 2003. Enhanced expression of a specific hyperpolarization-activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus. J Neurosci. 23:6826-6836. (Pubitemid 36951211)
4. Berger T, Larkum ME, Luscher HR. 2001. High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol. 85:855-868. (Pubitemid 32147785)
5. Brauer AU, Savaskan NE, Kole MH, Plaschke M, Monteggia LM, Nestler EJ, Simburger E, Deisz RA, Ninnemann O, Nitsch R. 2001. Molecular and functional analysis of hyperpolarization-activated pacemaker channels in the hippocampus after entorhinal cortex lesion. FASEB J. 15:2689-2701. (Pubitemid 33131095)
6. Brewster A, Bender RA, Chen Y, Dube C, Eghbal-Ahmadi M, Baram TZ. 2002. Developmental febrile seizures modulate hippocampal gene expression of hyperpolarization-activated channels in an isoformand cell-specific manner. J Neurosci. 22:4591-4599. (Pubitemid 37465675)
7. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, Farrant M. 2001. Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature. 409:88-92. (Pubitemid 32098630)
8. Campanac E, Daoudal G, Ankri N, Debanne D. 2008. Downregulation of dendritic I(h) in CA1 pyramidal neurons after LTP. J Neurosci. 28:8635-8643.
9. Cendes F, Andermann F, Gloor P, Lopes-Cendes I, Andermann E, Melanson D, Jones-Gotman M, Robitaille Y, Evans A, Peters T. 1993. Atrophy of mesial structures in patients with temporal lobe epilepsy: cause or consequence of repeated seizures? Ann Neurol. 34:795-801. (Pubitemid 23357892)
10. Chen K, Aradi I, Thon N, Eghbal-Ahmadi M, Baram TZ, Soltesz I. 2001. Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat Med. 7:331-337. (Pubitemid 32224349)
11. Chen X, Shu S, Schwartz LC, Sun C, Kapur J, Bayliss DA. 2010. Homeostatic regulation of synaptic excitability: tonic GABA(A) receptor currents replace I(h) in cortical pyramidal neurons of HCN1 knock-out mice. J Neurosci. 30:2611-2622.
12. Chevaleyre V, Castillo PE. 2002. Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci U S A. 99:9538-9543. (Pubitemid 34764648)
13. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, et al. 1999. Molecular diversity of K+ channels. Ann N Y Acad Sci. 868:233-285.
14. de Lanerolle NC, Lee TS. 2005. New facets of the neuropathology and molecular profile of human temporal lobe epilepsy. Epilepsy Behav. 7:190-203.
15. Dugladze T, Vida I, Tort AB, Gross A, Otahal J, Heinemann U, Kopell NJ, Gloveli T. 2007. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc Natl Acad Sci U S A. 104:17530-17535. (Pubitemid 350219872)
16. Dyhrfjeld-Johnsen J, Morgan RJ, Foldy C, Soltesz I. 2008. Upregulated HCurrent in hyperexcitable CA1 dendrites after febrile seizures. Front Cell Neurosci. 2:2.
17. Dyhrfjeld-Johnsen J, Morgan RJ, Soltesz I. 2009. Double trouble? Potential for hyperexcitability following both channelopathic upand downregulation of I(h) in epilepsy. Front Neurosci. 3:25-33.
18. Fan Y, Fricker D, Brager DH, Chen X, Lu HC, Chitwood RA, Johnston D. 2005. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat Neurosci. 8:1542-1551. (Pubitemid 41573669)
19. Franz O, Liss B, Neu A, Roeper J. 2000. Single-cell mRNA expression of HCN1 correlates with a fast gating phenotype of hyperpolarizationactivated cyclic nucleotide-gated ion channels (Ih) in central neurons. Eur J Neurosci. 12:2685-2693.
20. Gasparini S, DiFrancesco D. 1997. Action of the hyperpolarizationactivated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pflugers Arch. 435:99-106. (Pubitemid 28068744)
21. Hemond P, Migliore M, Ascoli GA, Jaffe DB. 2009. The membrane response of hippocampal CA3b pyramidal neurons near rest: heterogeneity of passive properties and the contribution of hyperpolarization-activated currents. Neuroscience. 160:359-370.
22. Hsu D. 2007. The dentate gyrus as a filter or gate: a look back and a look ahead. Prog Brain Res. 163:601-613. (Pubitemid 47321455)
23. Hu H, Vervaeke K, Graham LJ, Storm JF. 2009. Complementary theta resonance filtering by two spatially segregated mechanisms in CA1 hippocampal pyramidal neurons. J Neurosci. 29:14472-14483.
24. Huang CC, Hsu KS. 2003. Reexamination of the role of hyperpolarization- activated cation channels in short- and long-term plasticity at hippocampal mossy fiber synapses. Neuropharmacology. 44: 968-981.
25. Huang Z, Walker MC, Shah MM. 2009. Loss of dendritic HCN1 subunits enhances cortical excitability and epileptogenesis. J Neurosci. 29:10979-10988.
26. Huggenberger S, Vater M, Deisz RA. 2009. Interlaminar differences of intrinsic properties of pyramidal neurons in the auditory cortex of mice. Cereb Cortex. 19:1008-1018.
27. Isokawa M. 1996. Decrement of GABAA receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J Neurophysiol. 75:1901-1908.
28. Jung MW, McNaughton BL. 1993. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus. 3:165-182. (Pubitemid 23130073)
29. Jung S, Bullis JB, Lau IH, Jones TD, Warner LN, Poolos NP. 2010. Downregulation of dendritic HCN channel gating in epilepsy is mediated by altered phosphorylation signaling. J Neurosci. 30:6678-6688.
30. Jung S, Jones TD, Lugo JN Jr, Sheerin AH, Miller JW, D'Ambrosio R, Anderson AE, Poolos NP. 2007. Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J Neurosci. 27:13012-13021. (Pubitemid 350159594)
31. Krueppel R, Remy S, Beck H. 2011. Dendritic integration in hippocampal dentate granule cells. Neuron. 71:512-528.
32. Li X, Ascoli GA. 2006. Computational simulation of the input-output relationship in hippocampal pyramidal cells. J Comput Neurosci. 21:191-209.
33. Liu M, Pleasure SJ, Collins AE, Noebels JL, Naya FJ, Tsai MJ, Lowenstein DH. 2000. Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy. Proc Natl Acad Sci U S A. 97:865-870. (Pubitemid 30070401)
34. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z. 2002. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci. 5:1185-1193. (Pubitemid 35247178)
35. Magee JC. 1999. Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci. 2:508-514. (Pubitemid 30491230)
36. Marcelin B, Chauviere L, Becker A, Migliore M, Esclapez M, Bernard C. 2009. h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy. Neurobiol Dis. 33:436-447.
37. Mellor J, Nicoll RA, Schmitz D. 2002. Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science. 295:143-147. (Pubitemid 34052366)
38. Moroni A, Barbuti A, Altomare C, Viscomi C, Morgan J, Baruscotti M, DiFrancesco D. 2000. Kinetic and ionic properties of the human HCN2 pacemaker channel. Pflugers Arch. 439:618-626. (Pubitemid 30140155)
39. Narayanan R, Johnston D. 2007. Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron. 56:1061-1075. (Pubitemid 350251113)
40. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsaki G, Siegelbaum SA, Kandel ER, et al. 2004. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell. 119:719-732. (Pubitemid 39535758)
41. Notomi T, Shigemoto R. 2004. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol. 471:241-276. (Pubitemid 38292766)
42. Pape HC. 1996. Queer current and pacemaker: the hyperpolarizationactivated cation current in neurons. Annu Rev Physiol. 58:299-327.
43. Poolos NP. 2009. Genetic loss of HCN1 channels is exciting, but is it epileptic? Epilepsy Curr. 10:51-52.
44. Poolos NP, Migliore M, Johnston D. 2002. Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci. 5:767-774. (Pubitemid 34827595)
45. Powell KL, Ng C, O'Brien TJ, Xu SH, Williams DA, Foote SJ, Reid CA. 2008. Decreases inHCNmRNAexpressionin the hippocampus after kindling and status epilepticus in adult rats. Epilepsia. 49:1686-1695.
46. Pruss H, Wenzel M, Eulitz D, Thomzig A, Karschin A, Veh RW. 2003. Kir2 potassium channels in rat striatum are strategically localized to control basal ganglia function. Brain Res Mol Brain Res. 110:203-219. (Pubitemid 36184694)
47. Richichi C, Brewster AL, Bender RA, Simeone TA, Zha Q, Yin HZ, Weiss JH, Baram TZ. 2008. Mechanisms of seizure-induced 'transcriptional channelopathy' of hyperpolarization-activated cyclic nucleotide gated (HCN) channels. Neurobiol Dis. 29:297-305.
48. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL. 2008. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One. 3:e1997.
49. Santoro B, Baram TZ. 2003. The multiple personalities of h-channels. Trends Neurosci. 26:550-554. (Pubitemid 37176910)
50. Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA. 2000. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci. 20:5264-5275. (Pubitemid 30457723)
51. Santoro B, Lee JY, Englot DJ, Gildersleeve S, Piskorowski RA, Siegelbaum SA, Winawer MR, Blumenfeld H. 2010. Increased seizure severity and seizure-related death in mice lacking HCN1 channels. Epilepsia. 51:1624-1627.
52. Santoro B, Piskorowski RA, Pian P, Hu L, Liu H, Siegelbaum SA. 2009. TRIP8b splice variants form a family of auxiliary subunits that regulate gating and trafficking of HCN channels in the brain. Neuron. 62:802-813.
53. Santoro B, Tibbs GR. 1999. The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels. Ann N Y Acad Sci. 868:741-764. (Pubitemid 29281192)
54. Schmidt-Hieber C, Jonas P, Bischofberger J. 2007. Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci. 27:8430-8441. (Pubitemid 47219611)
55. Selke K, Muller A, Kukley M, Schramm J, Dietrich D. 2006. Firing pattern and calbindin-D28k content of human epileptic granule cells. Brain Res. 1120:191-201. (Pubitemid 44754964)
56. Shah MM, Anderson AE, Leung V, Lin X, Johnston D. 2004. Seizureinduced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron. 44:495-508. (Pubitemid 39423350)
57. Shin M, Brager D, Jaramillo TC, Johnston D, Chetkovich DM. 2008. Mislocalization of h channel subunits underlies h channelopathy in temporal lobe epilepsy. Neurobiol Dis. 32:26-36.
58. Spruston N, Johnston D. 1992. Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol. 67:508-529.
59. Stabel J, Ficker E, Heinemann U. 1992. Young CA1 pyramidal cells of rats, but not dentate gyrus granule cells, express a delayed inward rectifying current with properties of IQ. Neurosci Lett. 135:231-234.
60. Steephen JE, Manchanda R. 2009. Differences in biophysical properties of nucleus accumbens medium spiny neurons emerging from inactivation of inward rectifying potassium currents. J Comput Neurosci. 27:453-470.
61. Stegen M, Young CC, Haas CA, Zentner J, Wolfart J. 2009. Increased leak conductance in dentate gyrus granule cells of temporal lobe epilepsy patients with Ammon's horn sclerosis. Epilepsia. 50: 646-653.
62. Stieber J, Stockl G, Herrmann S, Hassfurth B, Hofmann F. 2005. Functional expression of the human HCN3 channel. J Biol Chem. 280:34635-34643. (Pubitemid 41504594)
63. Surges R, Brewster AL, Bender RA, Beck H, Feuerstein TJ, Baram TZ. 2006. Regulated expression of HCN channels and cAMP levels shape the properties of the h current in developing rat hippocampus. Eur J Neurosci. 24:94-104. (Pubitemid 44050670)
64. Surges R, Freiman TM, Feuerstein TJ. 2003. Gabapentin increases the hyperpolarization-activated cation current Ih in rat CA1 pyramidal cells. Epilepsia. 44:150-156. (Pubitemid 36206015)
65. Thom M, Sisodiya SM, Beckett A, Martinian L, Lin WR, Harkness W, Mitchell TN, Craig J, Duncan J, Scaravilli F. 2002. Cytoarchitectural abnormalities in hippocampal sclerosis. J Neuropathol Exp Neurol. 61:510-519. (Pubitemid 34602999)
66. van Welie I, van Hooft JA, Wadman WJ. 2004. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization- activated Ih channels. Proc Natl Acad Sci U S A. 101:5123-5128. (Pubitemid 38469213)
67. Vida I. 2009. 'Leaky' neurons in the epileptic hippocampus: should we get excited? J Physiol. 587:4127-4128.
68. Wierschke S, Lehmann TN, Dehnicke C, Horn P, Nitsch R, Deisz RA. 2010. Hyperpolarization-activated cation currents in human epileptogenic neocortex. Epilepsia. 51:404-414.
69. Williamson A, Patrylo PR. 2007. Physiological studies of human dentate granule cells. Prog Brain Res. 163:183-198.
70. Williamson A, Spencer DD, Shepherd GM. 1993. Comparison between the membrane and synaptic properties of human and rodent dentate granule cells. Brain Res. 622:194-202. (Pubitemid 23264965)
71. Williamson A, Telfeian AE, Spencer DD. 1995. Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J Neurophysiol. 74: 378-387.
72. Wuarin JP, Dudek FE. 2001. Excitatory synaptic input to granule cells increases with time after kainate treatment. J Neurophysiol. 85: 1067-1077. (Pubitemid 32209594)
73. Wyler AR, Dohan FC, Schweitzer JB, Berry AD. 1992. A grading system for hippocampal sclerosis. J Epilepsy. 5:220-225.
74. Young CC, Stegen M, Bernard R, Muller M, Bischofberger J, Veh RW, Haas CA, Wolfart J. 2009. Upregulation of inward rectifier K+ (Kir2) channels in dentate gyrus granule cells in temporal lobe epilepsy. J Physiol. 587:4213-4233.