Literature DB >> 21224222

Low-voltage activated Kv1.1 subunits are crucial for the processing of sound source location in the lateral superior olive in mice.

Anita Karcz1, Matthias H Hennig, Carol A Robbins, Bruce L Tempel, Rudolf Rübsamen, Cornelia Kopp-Scheinpflug.   

Abstract

Voltage-gated potassium (Kv) channels containing Kv1.1 subunits are strongly expressed in neurons that fire temporally precise action potentials (APs). In the auditory system, AP timing is used to localize sound sources by integrating interaural differences in time (ITD) and intensity (IID) using sound arriving at both cochleae. In mammals, the first nucleus to encode IIDs is the lateral superior olive (LSO), which integrates excitation from the ipsilateral ventral cochlear nucleus and contralateral inhibition mediated via the medial nucleus of the trapezoid body. Previously we reported that neurons in this pathway show reduced firing rates, longer latencies and increased jitter in Kv1.1 knockout (Kcna1−/−) mice. Here, we investigate whether these differences have direct impact on IID processing by LSO neurons. Single-unit recordings were made from LSO neurons of wild-type (Kcna1+/+) and from Kcna1−/− mice. IID functions were measured to evaluate genotype-specific changes in integrating excitatory and inhibitory inputs. In Kcna1+/+ mice, IID sensitivity ranged from +27 dB (excitatory ear more intense) to −20 dB (inhibitory ear more intense), thus covering the physiologically relevant range of IIDs. However, the distribution of IID functions in Kcna1−/− mice was skewed towards positive IIDs, favouring ipsilateral sound positions. Our computational model revealed that the reduced performance of IID encoding in the LSO of Kcna1−/− mice is mainly caused by a decrease in temporal fidelity along the inhibitory pathway. These results imply a fundamental role for Kv1.1 in temporal integration of excitation and inhibition during sound source localization.

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Year:  2011        PMID: 21224222      PMCID: PMC3060593          DOI: 10.1113/jphysiol.2010.203331

Source DB:  PubMed          Journal:  J Physiol        ISSN: 0022-3751            Impact factor:   5.182


  49 in total

1.  Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem.

Authors:  J J Grigg; H M Brew; B L Tempel
Journal:  Hear Res       Date:  2000-02       Impact factor: 3.208

2.  Varying overall sound intensity to the two ears impacts interaural level difference discrimination thresholds by single neurons in the lateral superior olive.

Authors:  Jeffrey J Tsai; Kanthaiah Koka; Daniel J Tollin
Journal:  J Neurophysiol       Date:  2009-12-16       Impact factor: 2.714

3.  Processing of interaural intensity differences in the LSO: role of interaural threshold differences.

Authors:  T J Park; P Monsivais; G D Pollak
Journal:  J Neurophysiol       Date:  1997-06       Impact factor: 2.714

4.  Activity-dependent refinement of inhibitory connections.

Authors:  D H Sanes; C Takács
Journal:  Eur J Neurosci       Date:  1993-06-01       Impact factor: 3.386

5.  Time can be traded for intensity in the lower auditory system.

Authors:  B Grothe; T J Park
Journal:  Naturwissenschaften       Date:  1995-11

6.  Kv1.1-containing channels are critical for temporal precision during spike initiation.

Authors:  Joshua X Gittelman; Bruce L Tempel
Journal:  J Neurophysiol       Date:  2006-05-03       Impact factor: 2.714

7.  Noradrenaline increases high-frequency firing at the calyx of Held synapse during development by inhibiting glutamate release.

Authors:  Ricardo M Leão; Henrique Von Gersdorff
Journal:  J Neurophysiol       Date:  2002-05       Impact factor: 2.714

8.  Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1.1.

Authors:  Helen M Brew; Janice L Hallows; Bruce L Tempel
Journal:  J Physiol       Date:  2003-02-28       Impact factor: 5.182

9.  Kv1.1 channel subunits are not necessary for high temporal acuity in behavioral and electrophysiological gap detection.

Authors:  Paul D Allen; Nicholas Schmuck; James R Ison; Joseph P Walton
Journal:  Hear Res       Date:  2008-09-30       Impact factor: 3.208

10.  Sound pressure transformation at the pinna of Mus domesticus.

Authors:  Q C Chen; D Cain; P H Jen
Journal:  J Exp Biol       Date:  1995-09       Impact factor: 3.312

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  19 in total

1.  Cav1.3 calcium channels are required for normal development of the auditory brainstem.

Authors:  Jan J Hirtz; Michael Boesen; Nadine Braun; Joachim W Deitmer; Florian Kramer; Christian Lohr; Britta Müller; Hans Gerd Nothwang; Jörg Striessnig; Stefan Löhrke; Eckhard Friauf
Journal:  J Neurosci       Date:  2011-06-01       Impact factor: 6.167

2.  Deficits in responding to brief noise offsets in Kcna1 -/- mice reveal a contribution of this gene to precise temporal processing seen previously only for stimulus onsets.

Authors:  James R Ison; Paul D Allen
Journal:  J Assoc Res Otolaryngol       Date:  2012-06

3.  Specific synaptic input strengths determine the computational properties of excitation-inhibition integration in a sound localization circuit.

Authors:  Enida Gjoni; Friedemann Zenke; Brice Bouhours; Ralf Schneggenburger
Journal:  J Physiol       Date:  2018-08-28       Impact factor: 5.182

4.  Genetic perturbations suggest a role of the resting potential in regulating the expression of the ion channels of the KCNA and HCN families in octopus cells of the ventral cochlear nucleus.

Authors:  Xiao-Jie Cao; Donata Oertel
Journal:  Hear Res       Date:  2017-01-05       Impact factor: 3.208

5.  Kcna1 gene deletion lowers the behavioral sensitivity of mice to small changes in sound location and increases asynchronous brainstem auditory evoked potentials but does not affect hearing thresholds.

Authors:  Paul D Allen; James R Ison
Journal:  J Neurosci       Date:  2012-02-15       Impact factor: 6.167

Review 6.  Decreased temporal precision of neuronal signaling as a candidate mechanism of auditory processing disorder.

Authors:  Conny Kopp-Scheinpflug; Bruce L Tempel
Journal:  Hear Res       Date:  2015-06-25       Impact factor: 3.208

7.  Strengthening of the Efferent Olivocochlear System Leads to Synaptic Dysfunction and Tonotopy Disruption of a Central Auditory Nucleus.

Authors:  Mariano N Di Guilmi; Luis E Boero; Valeria C Castagna; Adrián Rodríguez-Contreras; Carolina Wedemeyer; María Eugenia Gómez-Casati; Ana Belén Elgoyhen
Journal:  J Neurosci       Date:  2019-06-19       Impact factor: 6.167

8.  Auditory deficits of Kcna1 deletion are similar to those of a monaural hearing impairment.

Authors:  Anita Karcz; Paul D Allen; Joseph Walton; James R Ison; Cornelia Kopp-Scheinpflug
Journal:  Hear Res       Date:  2015-01-17       Impact factor: 3.208

Review 9.  Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources.

Authors:  Donata Oertel; Xiao-Jie Cao; James R Ison; Paul D Allen
Journal:  Trends Neurosci       Date:  2017-08-31       Impact factor: 13.837

10.  Dopaminergic projections of the subparafascicular thalamic nucleus to the auditory brainstem.

Authors:  Alexander A Nevue; Richard A Felix; Christine V Portfors
Journal:  Hear Res       Date:  2016-09-10       Impact factor: 3.208

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