Regulation of epileptiform discharges in rat neocortex by HCN channels

Journal of Neurophysiology

Volumn 110, Issue 8, 2013, Pages 1733-1743

  Albertson, Asher J ^a   Williams, Sidney B ^a   Hablitz, John J ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

Epilepsy; Epileptiform discharges; HCN channels; Ih; Inhibitory interneurons; Neocortex

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; BICUCULLINE; CATION CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED NONSPECIFIC CATION CHANNEL; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EPILEPTIC DISCHARGE; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOREACTIVITY; INTERNEURON; MEMBRANE DEPOLARIZATION; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; VOLTAGE CLAMP;

EPILEPSY; EPILEPTIFORM DISCHARGES; HCN CHANNELS; IH; INHIBITORY INTERNEURONS; NEOCORTEX;

ACTION POTENTIALS; ANIMALS; BICUCULLINE; CONVULSANTS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; EPILEPSY; GABAERGIC NEURONS; INTERNEURONS; MEMBRANE POTENTIALS; NEOCORTEX; PYRAMIDAL CELLS; PYRIMIDINES; RATS; SYNAPTIC TRANSMISSION;

EID: 84885644179     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00955.2012     Document Type: Article

References (116)

1. Agmon A, Wells JE. The role of the hyperpolarization-activated cationic current Ih in the timing of interictal bursts in the neonatal hippocampus. J Neurosci 23: 3658-3668, 2003.
2. Albertson AJ, Yang J, Hablitz JJ. Decreased hyperpolarization-activated currents in layer 5 pyramidal neurons enhance excitability in focal cortical dysplasia. J Neurophysiol 106: 2189-2200, 2011.
3. Alefeld M, Sutor B, Luhmann HJ. Pattern and pharmacology of propagating epileptiform discharges in mouse cerebral cortex. Exp Neurol 153: 113-122, 1998.
4. Ali AB, Deuchars J, Pawelzik H, Thomson AM. CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices. J Physiol 507: 201-217, 1998.
5. Aponte Y, Lien CC, Reisinger E, Jonas P. Hyperpolarization-activated cation channels in fast-spiking interneurons of rat hippocampus. J Physiol 574: 229-243, 2006.
6. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8: 45-56, 2007.
7. Beenhakker MP, Huguenard JR. Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 62: 612-632, 2009.
8. Berger T, Larkum ME, Lüscher HR. High Ih channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol 85: 855-868, 2001.
9. Berger TK, Silberberg G, Perin R, Markram H. Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol 8: e1000473, 2010.
10. Brewster AL, Chen Y, Bender RA, Yeh A, Shigemoto R, Baram TZ. 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 17: 702-712, 2007.
11. Cammarota M, Losi G, Chiavegato A, Zonta M, Carmignoto G. Fast spiking interneuron control of seizure propagation in a cortical slice model of focal epilepsy. J Physiol 591: 807-822, 2013.
12. Cepeda C, Andre VM, Wu N, Yamazaki I, Uzgil B, Vinters HV, Levine MS, Mathern GW. Immature neurons and GABA networks may contribute to epileptogenesis in pediatric cortical dysplasia. Epilepsia 48, Suppl 5: 79-85, 2007.
13. Chagnac-Amitai Y, Connors BW. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61: 747-758, 1989.
14. Chen K, Aradi I, Thon N, Eghbal-Ahmadi M, Baram TZ, Soltesz I. Persistently modified h-channels after complex febrile seizures convert the seizure-induced enhancement of inhibition to hyperexcitability. Nat Med 7: 331-337, 2001.
15. Chevaleyre V, Castillo PE. Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci USA 99: 9538-9543, 2002.
16. Chung WK, Shin M, Jaramillo TC, Leibel RL, LeDuc CA, Fischer SG, Tzilianos E, Gheith AA, Lewis AS, Chetkovich DM. Absence epilepsy in apathetic, a spontaneous mutant mouse lacking the h channel subunit, HCN2. Neurobiol Dis 33: 499-508, 2009.
17. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378: 75-78, 1995.
18. Cobb SR, Larkman PM, Bulters DO, Oliver L, Gill CH, Davies CH. Activation of Ih is necessary for patterning of mGluR and mAChR induced network activity in the hippocampal CA3 region. Neuropharmacology 44: 293-303, 2003.
19. Compte A, Reig R, Descalzo VF, Harvey MA, Puccini GD, Sanchez-Vives MV. Spontaneous high-frequency (10-80 Hz) oscillations during up states in the cerebral cortex in vitro. J Neurosci 28: 13828-13844, 2008.
20. Connors BW. Initiation of synchronized neuronal bursting in neocortex. Nature 310: 685-687, 1984.
21. Cossart R, Bernard C, Ben-Ari Y. Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signaling in epilepsies. Trends Neurosci 28: 108-115, 2005.
22. Dickson CT, Magistretti J, Shalinsky MH, Fransén E, Hasselmo ME, Alonso A. Properties and role of Ih in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J Neurophysiol 83: 2562-2579, 2000.
23. Do MT, Bean BP. Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39: 109-120, 2003.
24. Dyhrfjeld-Johnsen J, Morgan R, Soltesz I. Double trouble? Potential for hyperexcitability following both channelopathic up-and downregulation of Ih in epilepsy. Front Neurosci 3: 25-33, 2009.
25. Fino E, Yuste R. Dense inhibitory connectivity in neocortex. Neuron 69: 1188-1203, 2011.
26. Fujiwara-Tsukamoto Y, Isomura Y, Imanishi M, Ninomiya T, Tsukada M, Yanagawa Y, Fukai T, Takada M. Prototypic seizure activity driven by mature hippocampal fast-spiking interneurons. J Neurosci 30: 13679-13689, 2010.
27. Gabbott PL, Somogyi P. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp Brain Res 61: 323-331, 1986.
28. Galarreta M, Hestrin S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1: 587-594, 1998.
29. Galarreta M, Hestrin S. Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292: 2295-2299, 2001.
30. Gastrein P, Campanac E, Gasselin C, Cudmore RH, Bialowas A, Carlier E, Fronzaroli-Molinieres L, Ankri N, Debanne D. The role of hyperpolarization-activated cationic current in spike-time precision and intrinsic resonance in cortical neurons in vitro. J Physiol 589: 3753-3773, 2011.
31. + channels. Nat Neurosci 12: 577-584, 2009.
32. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79, 1999.
33. Griguoli M, Maul A, Nguyen C, Giorgetti A, Carloni P, Cherubini E. Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculeare interneurons. J Neurosci 30: 10773-10783, 2010.
34. Gutnick MJ, Connors BW, Prince DA. Mechanisms of neocortical epileptogenesis in vitro. J Neurophysiol 48: 1321-1335, 1982.
35. Harris NC, Constanti A. Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J Neurophysiol 74: 2366-2378, 1995.
36. Hestrin S, Armstrong WE. Morphology and physiology of cortical neurons in layer I. J Neurosci 16: 5290-5300, 1996.
37. Holmgren C, Harkany T, Svennenfors B, Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551: 139-153, 2003.
38. Hooks BM, Hires SA, Zhang YX, Huber D, Petreanu L, Svoboda K, Shepherd GM. Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol 9: e1000572, 2011.
39. Huang Z, Lujan R, Kadurin I, Uebele VN, Renger JJ, Dolphin AC, Shah MM. Presynaptic HCN1 channels regulate CaV3.2 activity and neurotransmission at select cortical synapses. Nat Neurosci 14: 478-486, 2011.
40. Huang Z, Walker MC, Shah MM. Loss of dendritic HCN1 subunits enhances cortical excitability and epileptogenesis. J Neurosci 29: 10979-10988, 2009.
41. Jung S, Jones TD, Lugo JN Jr, Sheerin AH, Miller JW, D'Ambrosio R, Anderson AE, Poolos NP. Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J Neurosci 27: 13012-13021, 2007.
42. Kanyshkova T, Pawlowski M, Meuth P, Dube C, Bender RA, Brewster AL, Baumann A, Baram TZ, Pape HC, Budde T. Postnatal expression pattern of HCN channel isoforms in thalamic neurons: relationship to maturation of thalamocortical oscillations. J Neurosci 29: 8847-8857, 2009.
43. Kanyshkova T, Meuth P, Bista P, Liu Z, Ehling P, Caputi L, Doengi M, Chetkovich DM, Pape HC, Budde T. Differential regulation of HCN channel isoform expression in thalamic neurons of epileptic and nonepileptic rat strains. Neurobiol Dis 45: 450-461, 2012.
44. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15: 2638-2655, 1995.
45. Kawaguchi Y. Distinct firing patterns of neuronal subtypes in cortical synchronized activities. J Neurosci 21: 7261-7272, 2001.
46. Kawaguchi Y, Kondo S. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31: 277-287, 2002.
47. Kawaguchi Y, Kubota Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin-and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387-396, 1993.
48. Kilb W, Luhmann HJ. Characterization of a hyperpolarization-activated inward current in Cajal-Retzius cells in rat neonatal neocortex. J Neurophysiol 84: 1681-1691, 2000.
49. Kole MH, Brauer AU, Stuart GJ. Inherited cortical HCN1 channel loss amplifies dendritic calcium electrogenesis and burst firing in a rat absence epilepsy model. J Physiol 578: 507-525, 2007.
50. Kozloski J, Hamzei-Sichani F, Yuste R. Stereotyped position of local synaptic targets in neocortex. Science 293: 868-872, 2001.
51. Lee WL, Hablitz JJ. Initiation and maintenance of epileptiform discharges by excitatory amino acid receptors in the disinhibited rat neocortex. J Neurophysiol 65: 87-95, 1991.
52. Lefort S, Tomm C, Floyd Sarria JC, Petersen CC. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61: 301-316, 2009.
53. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5: 1185-1193, 2002.
54. 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. Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22: 216-224, 2003.
55. Lujan R, Albasanz JL, Shigemoto R, Juiz JM. Preferential localization of the hyperpolarization-activated cyclic nucleotide-gated cation channel subunit HCN1 in basket cell terminals of the rat cerebellum. Eur J Neurosci 21: 2073-2082, 2005.
56. Lupica CR, Bell JA, Hoffman AF, Watson PL. Contribution of the hyperpolarization-activated current (Ih) to membrane potential and GABA release in hippocampal interneurons. J Neurophysiol 86: 261-268, 2001.
57. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26: 5069-5082, 2006.
58. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1998.
59. Magee JC. Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2: 508-514, 1999.
60. Magloczky Z, Freund TF. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci 28: 334-340, 2005.
61. Maier N, Nimmrich V, Draguhn A. Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550: 873-887, 2003.
62. Manseau F, Marinelli S, Mndez P, Schwaller B, Prince DA, Huguenard JR, Bacci A. Desynchronization of neocortical networks by asynchronous release of GABA at autaptic and synaptic contacts from fast-spiking interneurons. PLoS Biol 8: e1000492, 2010.
63. Marcelin B, Chauviére L, Becker A, Migliore M, Esclapez M, Bernard C. h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy. Neurobiol Dis 33: 436-447, 2009.
64. Marchionni I, Maccaferri G. Quantitative dynamics and spatial profile of perisomatic GABAergic input during epileptiform synchronization in the CA1 hippocampus. J Physiol 587: 5691-5708, 2009.
65. Markram H, Wang Y, Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328, 1998.
66. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
67. Matsumoto G, Ayala GF, Gumnit RJ. Neuronal behavior and triggering mechanism in cortical epileptic focus. J Neurophysiol 32: 688-703, 1969.
68. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815-823, 1996.
69. Nolan MF, Malleret G, Lee KH, Gibbs E, Dudman JT, Santoro B, Yin D, Thompson RF, Siegelbaum SA, Kandel ER, Morozov A. The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell 115: 551-564, 2003.
70. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsaki G, Siegelbaum SA, Kandel ER, Morozov A. 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, 2004.
71. Notomi T, Shigemoto R. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471: 241-276, 2004.
72. Okaty BW, Miller MN, Sugino K, Hempel CM, Nelson SB. Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons. J Neurosci 29: 7040-7052, 2009.
73. Olah S, Fule M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461: 1278-1281, 2009.
74. Packer AM, Yuste R. Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J Neurosci 31: 13260-13271, 2011.
75. Peng B, Justice JA, Zhang K, He X, Sanchez RM. Increased basal synaptic inhibition of hippocampal area CA1 pyramidal neurons by an antiepileptic drug that enhances Ih. Neuropsychopharmacology 35: 464-472, 2010.
76. Pinto DJ, Patrick SL, Huang WC, Connors BW. Initiation, propagation, and termination of epileptiform discharges in rodent neocortex in vitro involve distinct mechanisms. J Neurosci 25: 8131-8140, 2005.
77. Poolos NP, Migliore M, Johnston D. Pharmacological upregulation of hchannels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 5: 767-774, 2002.
78. Pouille F, Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293: 1159-1163, 2001.
79. Povysheva NV, Gonzalez-Burgos G, Zaitsev AV, Kroner S, Barrionuevo G, Lewis DA, Krimer LS. Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cereb Cortex 16: 541-552, 2006.
80. Powell KL, Ng C, O'Brien TJ, Xu SH, Williams DA, Foote SJ, Reid CA. Decreases in HCN mRNA expression in the hippocampus after kindling and status epilepticus in adult rats. Epilepsia 49: 1686-1695, 2008.
81. Reyes A, Sakmann B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci 19: 3827-3835, 1999.
82. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285, 1998.
83. Robinson RB, Siegelbaum SA. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65: 453-480, 2003.
84. Roopun AK, Middleton SJ, Cunningham MO, LeBeau FE, Bibbig A, Whittington MA, Traub RD. A beta2-frequency (20-30 Hz) oscillation in nonsynaptic networks of somatosensory cortex. Proc Natl Acad Sci USA 103: 15646-15650, 2006.
85. Sánchez-Alonso JL, Halliwell JV, Colino A. ZD 7288 inhibits T-type calcium current in rat hippocampal pyramidal cells. Neurosci Lett 439: 275-280, 2008.
86. Santoro B, Tibbs GR. The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels. Ann NY Acad Sci 868: 741-764, 1999.
87. Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20: 5264-5275, 2000.
88. Scharfman HE. EPSPs of dentate gyrus granule cells during epileptiform bursts of dentate hilar "mossy" cells and area CA3 pyramidal cells in disinhibited rat hippocampal slices. J Neurosci 14: 6041-6057, 1994a.
89. Scharfman HE. Synchronization of area CA3 hippocampal pyramidal cells and non-granule cells of the dentate gyrus in bicuculline-treated rat hippocampal slices. Neuroscience 59: 245-257, 1994b.
90. Schridde U, Strauss U, Brauer AU, van Luijtelaar G. Environmental manipulations early in development alter seizure activity, Ih and HCN1 protein expression later in life. Eur J Neurosci 23: 3346-3358, 2006.
91. Shin M, Brager D, Jaramillo TC, Johnston D, Chetkovich DM. Mislocalization of h channel subunits underlies h channelopathy in temporal lobe epilepsy. Neurobiol Dis 32: 26-36, 2008.
92. Silberberg G, Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53: 735-746, 2007.
93. Somogyi P, Tamas G, Lujan R, Buhl EH. Salient features of synaptic organization in the cerebral cortex. Brain Res Rev 26: 113-135, 1998.
94. Steriade M, Amzica F, Contreras D. Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci 16: 392-417, 1996.
95. Strauss U, Kole MH, Brauer AU, Pahnke J, Bajorat R, Rolfs A, Nitsch R, Deisz RA. An impaired neocortical Ih is associated with enhanced excitability and absence epilepsy. Eur J Neurosci 19: 3048-3058, 2004.
96. Sutor B, Hablitz JJ. Influence of barium on rectification in rat neocortical neurons. Neurosci Lett 157: 62-66, 1993.
97. Tanaka Y, Tanaka Y, Furuta T, Yanagawa Y, Kaneko T. The effects of cutting solutions on the viability of GABAergic interneurons in cerebral cortical slices of adult mice. J Neurosci Methods 171: 118-125, 2008.
98. Thomson AM, Bannister AP. Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 84: 669-683, 1998.
99. Thomson AM, West DC, Wang Y, Bannister AP. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labeling in vitro. Cereb Cortex 12: 936-953, 2002.
100. Traub RD, Contreras D, Cunningham MO, Murray H, LeBeau FE, Roopun A, Bibbig A, Wilent WB, Higley MJ, Whittington MA. Singlecolumn thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts. J Neurophysiol 93: 2194-2232, 2005.
101. Trevelyan AJ, Sussillo D, Yuste R. Feedforward inhibition contributes to the control of epileptiform propagation speed. J Neurosci 27: 3383-3387, 2007.
102. Tsau Y, Guan L, Wu JY. Epileptiform activity can be initiated in various neocortical layers: an optical imaging study. J Neurophysiol 82: 1965-1973, 1999.
103. Wainger BJ, DeGennaro M, Santoro B, Siegelbaum SA, Tibbs GR. Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411: 805-810, 2001.
104. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12: 395-410, 2002.
105. Wierschke S, Lehmann TN, Dehniccke C, Horn P, Nitsch R, Deisz RA. Hyperpolarization-activated cation currents in human epileptogenic neocortex. Epilepsia 51: 404-414, 2010.
106. Williams SR, Stuart GJ. Site independence of EPSP time course is mediated by dendritic Ih in neocortical pyramidal neurons. J Neurophysiol 83: 3177-3182, 2000.
107. Winer JA, Larue DT. Populations of GABAergic neurons and axons in layer I of rat auditory cortex. Neuroscience 33: 499-515, 1989.
108. Wozny C, Williams SR. Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb Cortex 21: 1818-1826, 2011.
109. Wu J, Hablitz JJ. Cooperative activation of D1 and D2 dopamine receptors enhances a hyperpolarization-activated inward current in layer I interneurons. J Neurosci 25: 6322-6328, 2005.
110. Yan H, Li Q, Fleming R, Madison RD, Wilson WA, Swartzwelder HS. Developmental sensitivity of hippocampal interneurons to ethanol: involvement of the hyperpolarization-activated current, Ih. J Neurophysiol 101: 67-83, 2009.
111. Ying SW, Jia F, Abbas SY, Hofmann F, Ludwig A, Goldstein PA. Dendritic HCN2 channels constrain glutamate-driven excitability in reticular thalamic neurons. J Neurosci 27: 8719-8732, 2007.
112. Ylinen A, Bragin A, Nadasdy Z, Jando G, Szabo I, Sik A, Buzsaki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30-46, 1995.
113. Yue BW, Huguenard JR. The role of H-current in regulating strength and frequency of thalamic network oscillations. Thalamus Relat Syst 1: 95-103, 2001.
114. Zemankovics R, Kali S, Paulsen O, Freund TF, Hajos N. Differences in subthreshold resonance of hippocampal pyramidal cells and interneurons: the role of h-current and passive membrane characteristics. J Physiol 588: 2109-2132, 2010.
115. Zhang K, Peng B, Sanchez RM. Decreased IH in hippocampal area CA1 pyramidal neurons after perinatal seizure-inducing hypoxia. Epilepsia 47: 1023-1028, 2006.
116. Zhou FM, Hablitz JJ. Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci 16: 1131-1139, 1996.