Inherited cortical HCN1 channel loss amplifies dendritic calcium electrogenesis and burst firing in a rat absence epilepsy model

Journal of Physiology

Volumn 578, Issue 2, 2007, Pages 507-525

  Kole, Maarten H P ^a   Bräuer, Anja U ^b   Stuart, Greg J ^a  

^a Biology and Environment   (Australia)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL 1; ION CHANNEL; UNCLASSIFIED DRUG; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL 2; ISOPROTEIN;

ABSENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; COMPARTMENT MODEL; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DENDRITE; ELECTROCORTICOGRAPHY; EPILEPTOGENESIS; FREQUENCY MODULATION; IDIOPATHIC DISEASE; MALE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; RECORDING; SIMULATION; SPIKE WAVE; THALAMUS; ABSENCE EPILEPSY; CELLULAR DISTRIBUTION; FIRING RATE; GENERALIZED EPILEPSY; NERVE CELL CHARACTERISTICS AND FUNCTIONS; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; PROTEIN EXPRESSION; SPIKE WAVE DISCHARGE; WHOLE CELL PATCH CLAMP;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; DENDRITES; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; EPILEPSY, ABSENCE; EXCITATORY POSTSYNAPTIC POTENTIALS; ION CHANNELS; MALE; MEMBRANE POTENTIALS; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, INBRED STRAINS; RATS, WISTAR; SOMATOSENSORY CORTEX;

EID: 33846200737     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2006.122028     Document Type: Article

References (59)

1. Avoli M, Gloor P, Kostopoulos G & Gotman J (1983). An analysis of penicillin-induced generalized spike and wave discharges using simultaneous recordings of cortical and thalamic single neurons. J Neurophysiol 50, 819-837
2. Berger T, Senn W & Luscher HR (2003). Hyperpolarization-activated current Ih disconnects somatic and dendritic spike initiation zones in layer V pyramidal neurons. J Neurophysiol 90, 2428-2437.
3. Bräuer AU, Savaskan NE, Kole MHP, 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.
4. Brewster AL, Bernard JA, Gall CM & Baram TZ (2005). Formation of heteromeric hyperpolarization-activated cyclic nucleotide-gated (HCN) channels in the hippocampus is regulated by developmental seizures. Neurobiol Dis 19, 200-207.
5. Brewster AL, Chen Y, Bender RA, Yeh A, Shigemoto R & Baram TZ (2006). Quantitative analysis and subcellular distribution of mRNA and protein expression of the hyperpolarization-activated cyclic nucleotide-gated channels throughout development in rat hippocampus. Cereb Cortex.
6. Budde T, Caputi L, Kanyshkova T, Staak R, Abrahamczik C, Munsch T & Pape HC (2005). Impaired regulation of thalamic pacemaker channels through an imbalance of subunit expression in absence epilepsy. J Neurosci 25, 9871-9882.
7. Carnevale NT & Johnston D (1982). Electrophysiological characterization of remote chemical synapses. J Neurophysiol 47, 606-621.
8. Chagnac-Amitai Y, Luhmann HJ & Prince DA (1990). Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J Comp Neurol 296, 598-613.
9. 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.
10. Coenen AM & van Luijtelaar EL (1987). The WAG/Rij rat model for absence epilepsy: Age and sex factors. Epilepsy Res 1, 297-301.
11. Coenen AM & van Luijtelaar EL (2003). Genetic animal models for absence epilepsy: A review of the WAG/Rij strain of rats. Behav Genet 33, 635-655.
12. Crunelli V & Leresche N (2002). Childhood absence epilepsy: Genes, channels, neurons and networks. Nat Rev Neurosci 3, 371-382.
13. D'Antuono M, Inaba Y, Biagini G, D'Arcangelo G, Tancredi V & Avoli M (2006). Synaptic hyperexcitability of deep layer neocortical cells in a genetic model of absence seizures. Genes Brain Behav 5, 73-84.
14. Di Pasquale E, Keegan KD & Noebels JL (1997). Increased excitability and inward rectification in layer V cortical pyramidal neurons in the epileptic mutant mouse Stargazer. J Neurophysiol 77, 621-631.
15. + channels in hippocampal mossy fiber boutons. Neuron 45, 405-417.
16. Fanselow EE, Sameshima K, Baccala LA & Nicolelis MA (2001). Thalamic bursting in rats during different awake behavioral states. Proc Natl Acad Sci U S A 98, 15330-15335.
17. Gauguier D, van Luijtelaar G, Bihoreau MT, Wilder SP, Godfrey RF, Vossen J, Coenen A & Cox RD (2004). Chromosomal mapping of genetic loci controlling absence epilepsy phenotypes in the WAG/Rij rat. Epilepsia 45, 908-915.
18. Gomora JC, Daud AN, Weiergraber M & Perez-Reyes E (2001). Block of cloned human T-type calcium channels by succinimide antiepileptic drugs. Mol Pharmacol 60, 1121-1132.
19. Helmchen F, Svoboda K, Denk W & Tank DW (1999). In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci 2, 989-996.
20. Hines ML & Carnevale NT (1997). The NEURON simulation environment. Neural Comput 9, 1179-1209.
21. Holmes MD, Brown M & Tucker DM (2004). Are 'generalized'seizures truly generalized? Evidence of localized mesial frontal and frontopolar discharges in absence. Epilepsia 45, 1568-1579.
22. Kandel A & Buzsaki G (1997). Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat. J Neurosci 17, 6783-6797.
23. Karpova AV, Bikbaev AF, Coenen AM & van Luijtelaar G (2005). Morphometric Golgi study of cortical locations in WAG/Rij rats: The cortical focus theory. Neurosci Res 51, 119-128.
24. Klein JP, Khera DS, Nersesyan H, Kimchi EY, Waxman SG & Blumenfeld H (2004). Dysregulation of sodium channel expression in cortical neurons in a rodent model of absence epilepsy. Brain Res 1000, 102-109.
25. h channels in pyramidal neuron dendrites: Properties, distribution, and impact on action potential output. J Neurosci 26, 1677-1687.
26. Kuisle M, Wanaverbecq N, Brewster AL, Frere SG, Pinault D, Baram TZ & Luthi A (2006). Functional stabilization of weakened thalamic pacemaker channel regulation in rat absence epilepsy. J Physiol 575, 83-100.
27. Larkum ME, Kaiser KM & Sakmann B (1999). Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc Natl Acad Sci U S A 96, 14600-14604.
28. 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.
29. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, Feil S, Feil R, Lancel M, Chien KR, Konnerth A, Pape HC, Biel M & Hofmann F (2003). Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22, 216-224.
30. Mainen ZF & Sejnowski TJ (1996). Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363-366.
31. Manning JP, Richards DA, Leresche N, Crunelli V & Bowery NG (2004). Cortical-area specific block of genetically determined absence seizures by ethosuximide. Neuroscience 123, 5-9.
32. Meeren HK, Pijn JP, van Luijtelaar EL, Coenen AM & Lopes da Silva FH (2002). Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J Neurosci 22, 1480-1495.
33. Midzyanovskaya IS, Salonin DV, Bosnyakova DY, Kuznetsova GD & van Luijtelaar EL (2004). The multiple effects of ketamine on electroencephalographic activity and behavior in WAG/Rij rats. Pharmacol Biochem Behav 79, 83-91.
34. Mulley JC, Scheffer IE, Petrou S & Berkovic SF (2003). Channelopathies as a genetic cause of epilepsy. Curr Opin Neurol 16, 171-176.
35. Nicolelis MA & Fanselow EE (2002). Thalamocortical optimization of tactile processing according to behavioral state. Nat Neurosci 5, 517-523.
36. h channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471, 241-276.
37. Peeters BW, Kerbusch JM, Coenen AM, Vossen JM & van Luijtelaar EL (1992). Genetics of spike-wave discharges in the electroencephalogram (EEG) of the WAG/Rij inbred rat strain: A classical Mendelian crossbreeding study. Behav Genet 22, 361-368.
38. Pinault D (2003). Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5-9 Hz oscillations. J Physiol 552, 881-905.
39. Pinault D, Slezia A & Acsady L (2006). Corticothalamic 5-9 Hz oscillations are more pro-epileptogenic than sleep spindles in rats. J Physiol 574, 209-227.
40. Poolos NP (2004). The yin and yang of the H-channel and its role in epilepsy. Epilepsy Curr 4, 3-6.
41. Poolos NP, Migliore M & Johnston D (2002). Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 5, 767-774.
42. Reichova I & Sherman SM (2004). Somatosensory corticothalamic projections: Distinguishing drivers from modulators. J Neurophysiol 92, 2185-2197.
43. Santoro B, Wainger BJ & Siegelbaum SA (2004). Regulation of HCN channel surface expression by a novel c-terminal protein-protein interaction. J Neurosci 24, 10750-10762.
44. h and HCN1 protein expression later in life. Eur J Neurosci 23, 3346-3358.
45. Schubert D, Staiger JF, Cho N, Kotter R, Zilles K & Luhmann HJ (2001). Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J Neurosci 21, 3580-3592.
46. Seidenbecher T, Staak R & Pape HC (1998). Relations between cortical and thalamic cellular activities during absence seizures in rats. Eur J Neurosci 10, 1103-1112.
47. Shah MM, Anderson AE, Leung V, Lin X & Johnston D (2004). Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44, 495-508.
48. Steriade M & Amzica F (2003). Sleep oscillations developing into seizures in corticothalamic systems. Epilepsia 44 (Suppl. 12), 9-20.
49. h is associated with enhanced excitability and absence epilepsy. Eur J Neurosci 19, 3048-3058.
50. Stuart G, Schiller J & Sakmann B (1997). Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol 505, 617-632.
51. Stuart G & Spruston N (1998). Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18, 3501-3510.
52. Timofeev I, Bazhenov M, Sejnowski T & Steriade M (2002). Cortical hyperpolarization-activated depolarizing current takes part in the generation of focal paroxysmal activities. Proc Natl Acad Sci U S A 99, 9533-9537.
53. van Luijtelaar G & Sitnikova E (2006). Global and focal aspects of absence epilepsy: The contribution of genetic models. Neurosci Biobehav Rev 30, 983-1003.
54. Vergnes M, Marescaux C, Depaulis A, Micheletti G & Warter JM (1986). Ontogeny of spontaneous petit mal-like seizures in Wistar rats. Brain Res 395, 85-87.
55. Vergnes M, Marescaux C, Micheletti G, Reis J, Depaulis A, Rumbach L & Warter JM (1982). Spontaneous paroxysmal electroclinical patterns in rat: A model of generalized non-convulsive epilepsy. Neurosci Lett 33, 97-101.
56. Wiest MC, Bentley N & Nicolelis MA (2005). Heterogeneous integration of bilateral whisker signals by neurons in primary somatosensory cortex of awake rats. J Neurophysiol 93, 2966-2973.
57. Williams SR & Stuart GJ (1999). Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol 521, 467-482.
58. h in neocortical pyramidal neurons. J Neurophysiol 83, 3177-3182.
59. Williams SR & Stuart GJ (2003). Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23, 7358-7367.