Contribution of the Kv3.1 potassium channel to high‐frequency firing in mouse auditory neurones

1 Using a combination of patch‐clamp, in situ hybridization and computer simulation techniques, we have analysed the contribution of potassium channels to the ability of a subset of mouse auditory neurones to fire at high frequencies. 2 Voltage‐clamp recordings from the principal neurones of the medial nucleus of the trapezoid body (MNTB) revealed a low‐threshold dendrotoxin (DTX)‐sensitive current (ILT) and a high‐threshold DTX‐insensitive current (IHT). 3 I HT displayed rapid activation and deactivation kinetics, and was selectively blocked by a low concentration of tetraethylammonium (TEA; 1 mm). 4 The physiological and pharmacological properties of IHT very closely matched those of the Shaw family potassium channel Kv3.1 stably expressed in a CHO cell line. 5 An mRNA probe corresponding to the C‐terminus of the Kv3.1 channel strongly labelled MNTB neurones, suggesting that this channel is expressed in these neurones. 6 TEA did not alter the ability of MNTB neurones to follow stimulation up to 200 Hz, but specifically reduced their ability to follow higher frequency impulses. 7 A computer simulation, using a model cell in which an outward current with the kinetics and voltage dependence of the Kv3.1 channel was incorporated, also confirmed that the Kv3.1‐ like current is essential for cells to respond to a sustained train of high‐frequency stimuli. 8 We conclude that in mouse MNTB neurones the Kv3.1 channel contributes to the ability of these cells to lock their firing to high‐frequency inputs.

[1]  L. Rayleigh,et al.  XII. On our perception of sound direction , 1907 .

[2]  J. Guinan,et al.  Single Auditory Units in the Superior Olivary Complex: II: Locations of Unit Categories and Tonotopic Organization , 1972 .

[3]  W. Brownell Organization of the cat trapezoid body and the discharge characteristics of its fibers , 1975, Brain Research.

[4]  Yasuo Kawaguchi,et al.  Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin , 1987, Brain Research.

[5]  B Sakmann,et al.  Potassium channels expressed from rat brain cDNA have delayed rectifier properties , 1988, FEBS letters.

[6]  H. Wagner,et al.  Neurophysiological and anatomical substrates of sound localization in the owl , 1988 .

[7]  E. Levitan,et al.  Alternative splicing contributes to K+ channel diversity in the mammalian central nervous system. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Manis,et al.  Outward currents in isolated ventral cochlear nucleus neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  L. Kaczmarek,et al.  Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. , 1992, Journal of neurophysiology.

[10]  P. Schwartzkroin,et al.  Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons , 1993, Nature.

[11]  I. Forsythe,et al.  The binaural auditory pathway: excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  A. Brown,et al.  Stable Expression and Regulation of a Rat Brain K+ Channel , 1993, Journal of neurochemistry.

[13]  J. Kelly,et al.  Response of neurons in the lateral superior olive and medial nucleus of the trapezoid body to repetitive stimulation: Intracellular and extracellular recordings from mouse brain slice , 1993, Hearing Research.

[14]  I. Raman,et al.  Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Reyes,et al.  Membrane properties underlying the firing of neurons in the avian cochlear nucleus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  B. Rudy,et al.  Differential expression of Shaw-related K+ channels in the rat central nervous system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  G A Gutman,et al.  Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. , 1994, Molecular pharmacology.

[18]  L. Trussell,et al.  A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. , 1994, Journal of neurophysiology.

[19]  M. Vater,et al.  Parvalbumin, calbindin D‐28k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats , 1994, The Journal of comparative neurology.

[20]  O. Pongs,et al.  Inactivation properties of voltage-gated K+ channels altered by presence of β-subunit , 1994, Nature.

[21]  B. Rudy,et al.  CHAPTER 4 – Shaw-Related K+ Channels in Mammals , 1994 .

[22]  Y. Qin,et al.  GABA‐Ergic interneurons of the striatum express the shaw‐like potassium channel KvS3.1 , 1994, Synapse.

[23]  Mark Ellisman,et al.  The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  B. Walmsley,et al.  Counting quanta: Direct measurements of transmitter release at a central synapse , 1995, Neuron.

[25]  O. Pongs Regulation of the activity of voltage-gated potassium channels by β subunits , 1995 .

[26]  J. Trimmer,et al.  Association and colocalization of K+ channel alpha- and beta-subunit polypeptides in rat brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  L. Wang,et al.  Electrophysiological and pharmacological characterization of a mammalian Shaw channel expressed in NIH 3T3 fibroblasts. , 1995, Journal of neurophysiology.

[28]  I. Forsythe,et al.  Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  I. Forsythe,et al.  Pre‐ and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. , 1995, The Journal of physiology.

[30]  B. Robertson,et al.  Novel effects of dendrotoxin homologues on subtypes of mammalian Kv1 potassium channels expressed in Xenopus oocytes , 1996, FEBS letters.

[31]  B. Rudy,et al.  Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Min Li,et al.  NAB Domain Is Essential for the Subunit Assembly of both α–α and α–β Complexes of Shaker-like Potassium Channels , 1996, Neuron.

[33]  E. Guatteo,et al.  Action potentials recorded with patch-clamp amplifiers: are they genuine? , 1996, Trends in Neurosciences.

[34]  E. Friauf,et al.  Distribution of the calcium‐binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats , 1996, The Journal of comparative neurology.

[35]  O. Pongs,et al.  Kvβ1 Subunit Binding Specific for Shaker-Related Potassium Channel α Subunits , 1996, Neuron.

[36]  R. Grange,et al.  Pleiotropic effects of a disrupted K+ channel gene: reduced body weight, impaired motor skill and muscle contraction, but no seizures. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[37]  L. Kaczmarek,et al.  Localization of a high threshold potassium channel in the rat cochlear nucleus , 1997, The Journal of comparative neurology.