The hyperpolarization-activated non-specific cation current (Ih) adjusts the membrane properties, excitability, and activity pattern of the giant cells in the rat dorsal cochlear nucleus

European Journal of Neuroscience

Volumn 37, Issue 6, 2013, Pages 876-890

  Rusznák, Zoltán ^a,b   Pál, Balázs ^b   Koszeghy, Áron ^b   Fu, Yuhong ^a   Szücs, Géza ^b   Paxinos, George ^a,c  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Developing auditory system; H current; Spontaneous activity; Synaptic transmission; ZD7288

Indexed keywords

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

ACTION POTENTIAL; ADULT ANIMAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITE; DORSAL COCHLEAR NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIAL; GIANT NERVE CELL; HYPERPOLARIZATION; HYPERPOLARIZATION ACTIVATED NON SPECIFIC CATION CURRENT; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; ION CONDUCTANCE; ION CURRENT; JUVENILE ANIMAL; MEMBRANE STEADY POTENTIAL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RAT;

ANIMALS; CATIONS; CELL MEMBRANE; COCHLEAR NUCLEUS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; EXCITATORY POSTSYNAPTIC POTENTIALS; GIANT CELLS; INHIBITORY POSTSYNAPTIC POTENTIALS; ION TRANSPORT; MEMBRANE POTENTIALS; NEURONS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; PYRIMIDINES; RATS; RATS, WISTAR;

EID: 84875372588     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12116     Document Type: Article

References (101)

1. Adams, J.C. & Warr, W.B. (1976) Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J. Comp. Neurol., 170, 107-122.
2. Alibardi, L. (2000a) Cytology of large neurons in the guinea pig dorsal cochlear nucleus contacting the inferior colliculus. Eur. J. Histochem., 44, 365-375.
3. Alibardi, L. (2000b) Cytology, synaptology and immunocytochemistry of commissural neurons and their putative axonal terminals in the dorsal cochlear nucleus of the rat. Ann. Anat., 182, 207-220.
4. Aponte, Y., Lien, C.C., Reisinger, E. & Jonas, P. (2006) Hyperpolarization-activated cation channels in fast-spiking interneurons of rat hippocampus. J. Physiol., 574, 229-243.
5. Araki, T., Ito, M. & Oshima, T. (1961) Potential changes produced by application of current steps in motoneurons. Nature, 191, 1104-1105.
6. Attwell, D. & Wilson, M. (1980) Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. J. Physiol., 309, 287-315.
7. Babalian, A.L., Ryugo, D.K. & Rouiller, E.M. (2003) Discharge properties of identified cochlear nucleus neurons and auditory nerve fibers in response to repetitive electrical stimulation of the auditory nerve. Exp. Brain Res., 153, 452-460.
8. Bakondi, G., Pór, Á., Kovács, I., Szücs, G. & Rusznák, Z. (2009) Hyperpolarization-activated, cyclic nucleotide-gated, cation non-selective channel subunit expression pattern of guinea-pig spiral ganglion cells. Neuroscience, 158, 1469-1477.
9. h) in octopus cells of the mammalian cochlear nucleus. J. Neurophysiol., 84, 806-817.
10. h in neurons of the medial nucleus of the trapezoid body: Voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. J. Neurophysiol., 70, 1420-1432.
11. h channels. Nat. Neurosci., 3, 133-141.
12. h activation and actin: involvement in long-term facilitation and cAMP-induced synaptic enhancement. Neuron, 33, 601-613.
13. Bender, R.A. & Baram, T.Z. (2008) Hyperpolarization activated cyclic-nucleotide gated (HCN) channels in developing neuronal networks. Prog. Neurobiol., 86, 129-140.
14. Bender, R.A., Kirschstein, T., Kretz, O., Brewster, A.L., Richichi, C., Rüschenschmidt, C., Shigemoto, R., Beck, H., Frotscher, M. & Baram, T.Z. (2007) Localization of HCN1 channels to presynaptic compartments: novel plasticity that may contribute to hippocampal maturation. J. Neurosci., 27, 4697-4706.
15. Biel, M., Wahl-Schott, C., Michalakis, S. & Zong, X. (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol. Rev., 89, 847-885.
16. Bon-Jego, M. & Yuste, R. (2007) Persistently active, pacemaker-like neurons in neocortex. Front. Neurosci., 1, 123-129.
17. f) in guinea-pig dissociated sinoatrial node cells. Br. J. Pharmacol., 110, 343-349.
18. Brawer, J.R., Morest, D.K. & Kane, E.C. (1974) The neuronal architecture of the cochlear nucleus of the cat. J. Comp. Neurol., 155, 251-300.
19. Brown, H.F. & DiFrancesco, D. (1980) Voltage-clamp investigations of membrane currents underlying pace-maker activity in rabbit sino-atrial node. J. Physiol., 108, 331-351.
20. Brown, H.F., DiFrancesco, D. & Noble, S.J. (1979) Cardiac pacemaker oscillation and its modulation by autonomic transmitters. J. Exp. Biol., 81, 175-204.
21. Cant, N.B. & Benson, C.G. (2003) Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res. Bull., 60, 457-474.
22. Cant, N.B. & Gaston, K.C. (1982) Pathways connecting the right and left cochlear nuclei. J. Comp. Neurol., 212, 313-326.
23. Cao, X.-J. & Oertel, D. (2011) The magnitudes of hyperpolarization-activated and low-voltage-activated potassium currents co-vary in neurons of the ventral cochlear nucleus. J. Neurophysiol., 106, 630-640.
24. h) in primary auditory neurons. Hear. Res., 110, 179-190.
25. h channels in synaptic transmission and mossy fiber LTP. Proc. Natl. Acad. Sci. USA, 99, 9538-9543.
26. h) at an excitatory synaptic terminal in the rat auditory brainstem. J. Physiol., 534, 733-744.
27. Davis, K.A. & Young, E.D. (2000) Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J. Neurophysiol., 83, 926-940.
28. Fernandez, C. & Karapas, F. (1967) The course and termination of the striae of Monakow and Held in the cat. J. Comp. Neurol., 131, 371-386.
29. Fu, X.W., Brezden, B.L. & Wu, S.H. (1997) Hyperpolarization-activated inward current in neurons of the rat's dorsal nucleus of the lateral lemniscus in vitro. J. Neurophysiol., 78, 2235-2245.
30. Golding, N.L., Robertson, D. & Oertel, D. (1995) Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J. Neurosci., 15, 3138-3153.
31. Golding, N.L., Ferragamo, M.J. & Oertel, D. (1999) Role of intrinsic conductances underlying responses to transients in octopus cells of the cochlear nucleus. J. Neurosci., 19, 2897-2905.
32. Harris, N.C. & Constanti, A. (1995) Mechanism of block by ZD7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J. Neurophysiol., 74, 2366-2378.
33. Hassfurth, B., Magnusson, A.K., Grothe, B. & Koch, U. (2009) Sensory deprivation regulates the development of the hyperpolarization-activated current in auditory brainstem neurons. Eur. J. Neurosci., 30, 1227-1238.
34. Horwitz, G.C., Risner-Janiczek, J.R., Jones, S.M. & Holt, J.R. (2011) HCN channels expressed in the inner ear are necessary for normal balance function. J. Neurosci., 31, 16814-16825.
35. Ishii, T.M., Takano, M., Xie, L.H., Noma, A. & Ohmori, H. (1999) Molecular characterization of the hyperpolarization-activated cation channel in rabbit heart sinoatrial node. J. Biol. Chem., 274, 12835-12839.
36. + currents in cochlear nucleus pyramidal cells. J. Neurophysiol., 85, 523-538.
37. Kecskes, S., Ko{double acute}szeghy, Á., Szücs, G., Rusznák, Z., Matesz, C. & Birinyi, A. (2012) Three-dimensional reconstruction and quantitative morphometric analysis of pyramidal and giant neurons of the rat dorsal cochlear nucleus. Brain Struct. Funct., DOI: 10.1007/s00429-012-0457-7 [Epub ahead of print].
38. 3H]-noradrenaline release in rat neocortex slices. Naunyn Schmiedebergs Arch. Pharmacol., 367, 422-425.
39. h) in the inferior colliculus: distribution and contribution to temporal processing. J. Neurophysiol., 90, 3679-3688.
40. Kolston, J., Osen, K.K., Hackney, C.M., Ottersen, O.P. & Storm-Mathisen, J. (1992) An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat. Embryol., 186, 443-465.
41. Ko{double acute}szeghy, Á., Pál, B., Pap, P., Pocsai, K., Nagy, Zs., Szu{double acute}cs, G. & Rusznák, Z. (2009) Purkinje-like cells of the rat cochlear nucleus: a combined functional and morphological study. Brain Res., 1297, 57-69.
42. Ko{double acute}szeghy, Á., Vincze, J., Rusznák, Z., Fu, Y., Paxinos, G., Csernoch, L. & Szücs, G. (2012) Activation of muscarinic receptors increases the activity of the granule neurones of the rat dorsal cochlear nucleus - a calcium imaging study. Pflügers Arch. - Eur. J. Physiol., 463, 829-844.
43. Leao, K.E., Leao, R.N., Sun, H., Fyffe, R.E.W. & Walmsley, B. (2006) Hyperpolarization-activated currents are differentially expressed in mice brainstem auditory nuclei. J. Physiol., 576, 849-864.
44. h) currents in auditory brainstem neurons of normal and congenitally deaf mice. Eur. J. Neurosci., 22, 147-157.
45. Lorente de Nó, R. (1981) The Primary Acoustic Nuclei. Raven, New York.
46. Lörincz, A., Notomi, T., Tamás, G., Shigemoto, R. & Nusser, Z. (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat. Neurosci., 5, 1185-1193.
47. Ludwig, A., Zong, X., Jeglitsch, M., Hofmann, F. & Biel, M. (1998) A family of hyperpolarization-activated mammalian cation channels. Nature, 393, 587-591.
48. Ludwig, A., Zong, X., Stieber, J., Hullin, R., Hofmann, F. & Biel, M. (1999) Two pacemaker channels from human heart with profoundly different activation kinetics. EMBO J., 18, 2323-2329.
49. 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, K.R., Konnerth, A., Pape, H.C., Biel, M. & Hofmann, F. (2003) Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J., 22, 216-224.
50. h) to membrane potential and GABA release in hippocampal interneurons. J. Neurophysiol., 86, 261-268.
51. Maccaferri, G., Manqoni, M., Lazzari, A. & DiFrancesco, D. (1993) Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. J. Neurophysiol., 69, 2129-2136.
52. Magee, J.C. (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci., 18, 7613-7624.
53. h normalizes temporal summation in hippocampal CA1 neurons. Nat. Neurosci., 2, 508-514.
54. Magee, J.C. (2000) Dendritic integration of excitatory synaptic input. Nat. Rev. Neurosci., 1, 181-190.
55. May, B.J. (2000) Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear. Res., 148, 74-87.
56. McCormick, D.A. & Pape, H.C. (1990) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol., 431, 291-318.
57. Meuth, S.G., Kanyshkova, T., Meuth, P., Landgraf, P., Munsch, T., Ludwig, A., Hofmann, F., Pape, H.C. & Budde, T. (2006) Membrane resting potential of thalamocortical relay neurons is shaped by the interaction among TASK3 and HCN2 channels. J. Neurophysiol., 96, 1517-1529.
58. Mo, Z.L. & Davis, R.L. (1997) Heterogeneous voltage dependence of inward rectifier currents in spiral ganglion neurons. J. Neurophysiol., 78, 3019-3027.
59. Nolan, M.F., Malleret, G., Lee, K.H., Gibbs, E., Dudman, J.T., Santoro, B., Yin, D., Thompson, R.F., Siegelbaum, S.A., Kandel, E.R. & Morozov, A. (2003) The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell, 115, 551-564.
60. Nolan, M.F., Dudman, J.T., Dodson, P.D. & Santoro, B. (2007) HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J. Neurosci., 27, 12440-12451.
61. Oertel, D., Bal, R., Gardner, S.M., Smith, P.H. & Joris, P.X. (2000) Detection of synchrony in the activity of auditory nerve fibers by octopus cells of the mammalian cochlear nucleus. Proc. Natl. Acad. Sci. USA, 97, 11773-11779.
62. Oertel, D., Shatadal, S. & Cao, X.-J. (2008) In the ventral cochlear nucleus Kv1.1 and subunits of HCN1 are colocalized at surfaces of neurons that have low-voltage-activated and hyperpolarization-activated conductances. Neuroscience, 154, 77-86.
63. Osen, K.K. (1969) Cytoarchitecture of the cochlear nuclei in the cat. J. Comp. Neurol., 136, 453-484.
64. Osen, K.K. (1972) Projections of the cochlear nuclei on the inferior colliculus in the cat. J. Comp. Neurol., 144, 355-372.
65. Ostapoff, E.-M., Feng, J.J. & Morest, D.K. (1994) Physiological and structural study of neuron types in the cochlear nucleus. II. Neuron types and their structural correlation with response properties. J. Comp. Neurol., 346, 19-42.
66. Pál, B., Pór, Á., Szücs, G., Kovács, I. & Rusznák, Z. (2003) HCN channels contribute to the intrinsic activity of cochlear pyramidal cells. Cell. Mol. Life Sci., 60, 2189-2199.
67. + channel subunits expressed by the bushy cells of the rat cochlear nucleus. Hear. Res., 199, 57-70.
68. Pál, B., Ko{double acute}szeghy, Á., Pap, P., Bakondi, G., Pocsai, K., Szu{double acute}cs, G. & Rusznák, Z. (2009) Targets, receptors and effects of muscarinic neuromodulation on giant neurones of the rat dorsal cochlear nucleus. Eur. J. Neurosci., 30, 769-782.
69. Pocsai, K., Pál, B., Pap, P., Bakondi, G., Kosztka, L., Rusznák, Z. & Szücs, G. (2007) Rhodamine backfilling and confocal microscopy as a tool for the unambiguous identification of neuronal cell types: a study of the neurones of the rat cochlear nucleus. Brain Res. Bull., 71, 529-538.
70. Pór, Á., Pocsai, K., Rusznák, Z. & Szu{double acute}cs, G. (2005) Presence and distribution of three calcium binding proteins in projection neurones of the adult rat cochlear nucleus. Brain Res., 1039, 63-74.
71. Rhode, W.S. & Greenberg, S. (1992) Physiology of the cochlear nuclei. In Popper, A.N. & Fay, R.R. (Eds), The Mammalian Auditory Pathway: Neurophysiology. Springer, Berlin, pp. 94-152.
72. Robinson, R.B. & Siegelbaum, S.A. (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol., 65, 453-480.
73. Rodrigues, A.R.A. & Oertel, D. (2006) Hyperpolarization-activated currents regulate excitability in stellate cells of the mammalian ventral cochlear nucleus. J. Neurophysiol., 95, 76-87.
74. Romand, R. & Avan, P. (1997) Anatomical and functional aspects of the cochlear nucleus. In Ehret, G. & Romand, R. (Eds), The Central Auditory System. Oxford University Press, New York, pp. 97-191.
75. Rouiller, E.M. (1997) Functional organization of the auditory pathways. In Ehret, G. & Romand, R. (Eds), The Central Auditory System. Oxford University Press, New York, pp. 3-96.
76. Rusznák, Z., Bakondi, G., Pocsai, K., Pór, Á., Kosztka, L., Pál, B., Nagy, D. & Szu{double acute}cs, G. (2008) Voltage-gated potassium channel (Kv) subunits expressed in the rat cochlear nucleus. J. Histochem. Cytochem., 56, 443-465.
77. Ryugo, D.K. & Willard, F.H. (1985) The dorsal cochlear nucleus of the mouse: a light microscopic analysis of neurons that project to the inferior colliculus. J. Comp. Neurol., 242, 381-396.
78. Saint Marie, R.L., Benson, C.G., Ostapoff, E.-M. & Morest, D.K. (1991) Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus. Hear. Res., 51, 11-28.
79. Santoro, B., Grant, S.G., Bartsch, D. & Kandel, E.R. (1997) Interactive cloning with the SH3 domain of N-src identifies a new brain specific ion channel protein, with homology to eag and cyclic nucleotide-gated channels. Proc. Natl. Acad. Sci. USA, 94, 14815-14820.
80. Santoro, B., Liu, D.T., Yao, H., Bartsch, D., Kandel, E.R., Siegelbaum, S.A. & Tibbs, G.R. (1998) Identification of a gene encoding a hyperpolarization- activated pacemaker channel of brain. Cell, 93, 717-729.
81. Schofield, B.R. & Cant, N.B. (1996) Origins and targets of commissural connections between the cochlear nuclei in guinea pigs. J. Comp. Neurol., 375, 128-146.
82. Schofield, B.R. & Coomes, D.L. (2005) Projections from auditory cortex contact cells in the cochlear nucleus that project to the inferior colliculus. Hear. Res., 206, 3-11.
83. Seifert, R., Scholten, A., Gauss, R., Mincheva, A., Lichter, P. & Kaupp, U.B. (1999) Molecular characterization of a slowly gating human hyperpolarization-activated channel predominantly expressed in thalamus, heart, and testis. Proc. Natl. Acad. Sci. USA, 96, 9391-9396.
84. Shin, K.S., Rothberg, B.S. & Yellen, G. (2001) Blocker state dependence and trapping in hyperpolarization-activated cation channels: evidence for an intracellular activation gate. J. Gen. Physiol., 117, 91-101.
85. Shore, S.F., Godfrey, D.A., Helfert, R.H., Altschuler, R.A. & Bledsoe, S.C. Jr. (1992) Connections between the cochlear nuclei in guinea pig. Hear. Res., 62, 16-26.
86. Southan, A.P., Morris, N.P., Stephens, G.J. & Robertson, B. (2000) Hyperpolarization-activated currents in presynaptic terminals of mouse cerebellar basket cells. J. Physiol., 526, 91-97.
87. Sutherland, D.P., Glendenning, K.K. & Masterton, R.B. (1998a) Role of acoustic striae in hearing: discrimination of sound-source elevation. Hear. Res., 120, 86-108.
88. Sutherland, D.P., Masterton, R.B. & Glendenning, K.K. (1998b) Role of acoustic striae in hearing: reflexive responses to elevated sound-sources. Behav. Brain Res., 97, 1-12.
89. Szabó, Z.S., Harasztosi, C.S., Sziklai, I., Szücs, G. & Rusznák, Z. (2002) Ionic currents determining the membrane characteristics of type I spiral ganglion neurons of the guinea pig. Eur. J. Neurosci., 16, 1887-1895.
90. 2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron, 56, 1076-1089.
91. Weinberg, R.J. & Rustioni, A. (1987) A cuneocochlear pathway in the rat. Neuroscience, 20, 209-219.
92. h in neocortical pyramidal neurons. J. Neurophysiol., 83, 3177-3182.
93. Wouterlood, E.G. & Mugnaini, E. (1984) Cartwheel neurons of the dorsal cochlear nucleus: a Golgi-electron microscopic study in rat. J. Comp. Neurol., 227, 136-157.
94. Yamada, R., Kuba, H., Ishii, T.M. & Ohmori, H. (2005) Hyperpolarization-activated cyclic nucleotide-gated cation channels regulate auditory coincidence detection in nucleus laminaris of the chick. J. Neurosci., 25, 8867-8877.
95. Young, E.D., Spirou, G.A., Rice, J.J. & Voigt, H.F. (1992) Neural organization and responses to complex stimuli in the dorsal cochlear nucleus. Philos. Trans. R. Soc. Lond. B Biol. Sci., 336, 407-413.
96. h channels) contributes to activity-evoked neuronal secretion. Proc. Natl. Acad. Sci. USA, 101, 1051-1056.
97. f channels in rat ventricular myocytes. Am. J. Physiol. Cell Physiol., 292, C1147-C1155.
98. Zemankovics, R., Káli, S., Paulsen, O., Freund, T.F. & Hájos, N. (2010) Differences in subthreshold resonance of hippocampal pyramidal cells and interneurons: the role of h-current and passive membrane characteristics. J. Physiol., 588, 2109-2132.
99. Zhang, S. & Oertel, D. (1993) Giant cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J. Neurophysiol., 69, 1398-1408.
100. Zheng, X. & Voigt, H.F. (2006) Computational model of response maps in the dorsal cochlear nucleus. Biol. Cybern., 95, 233-242.
101. Zucker, R.S. & Regehr, W.G. (2002) Short-term synaptic plasticity. Annu. Rev. Physiol., 64, 355-405.