Regulation of the timing of MNTB neurons by short-term and long-term modulation of potassium channels

Kaczmarek, Leonard K.; Bhattacharjee, Abhishek; Desai, Rushil; Gan, Li; Song, Ping; Hehn, Christian A. A. von; Whim, Matthew D.; Yang, Bo

doi:10.1016/j.heares.2004.11.023

Cited by 61 publications

(56 citation statements)

References 68 publications

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“…The good match found here between model and LSO data suggests that membrane heterogeneity can be simplified into differences in the amplitude and dynamics of AHP. In attempting to relate this simple model to actual membrane characteristics in the LSO, it seems likely that the AHP-related response patterns studied here arise from activity of a number of ionic channels, including low-threshold potassium channels (I LTK ), hyperpolarization-actived inward currents (I h ), and inwardly rectifying potassium currents (I kir ) that have been observed in the LSO (Adam et al 2001;BarnesDavies et al 2004); calcium-dependent potassium channels (I K(Ca) ) as proposed by Zacksenhouse et al (1998); and/or sodium-activated potassium channels that have been observed in MNTB neurons (Kaczmarek et al 2005). Because the adaptation channel in our model has only two parameters, it merely simulates the time-varying shunting effect of cationic channels (most likely the potassium channels) and not their detailed biophysical properties.…”

Section: Heterogeneity In Intrinsic Properties Among Lso Cellsmentioning

confidence: 98%

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

Zhou

Colburn

2010

Journal of Neurophysiology

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Zhou Y, Colburn HS. A modeling study of the effects of membrane afterhyperpolarization on spike interval statistics and on ILD encoding in the lateral superior olive. J Neurophysiol 103: 2355-2371, 2010. First published January 27, 2010 doi:10.1152/jn.00385.2009. The lateral superior olive (LSO) is the first nucleus in the ascending auditory pathway that encodes acoustic level information from both ears, the interaural level difference (ILD). This sensitivity is believed to result from the relative strengths of ipsilateral excitation and contralateral inhibition. The study reported here simulated soundevoked responses of LSO chopper units with a focus on the role of the heterogeneity in membrane afterhyperpolarization (AHP) channels on spike interval statistics and on ILD encoding. A relatively simplified cell model was used so that the effects of interest could be isolated. Specifically, the amplitude and time constant of the AHP conductance within a leaky integrate-and-fire (LIF) cell model were studied. This extends the work of others who used a more physiologically detailed model. Results show that differences in these two parameters lead to both the distinctive chopper response patterns and to the leveldependent interval statistics as observed in vivo. In general, diverse AHP characteristics enable an enhanced contrast across population responses with respect to rate gain and temporal correlations. This membrane heterogeneity provides an internal, cell-specific dimension for the neural representation of stimulus information, allowing sensitivity to ILDs of dynamic stimuli.

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Section: Heterogeneity In Intrinsic Properties Among Lso Cellsmentioning

confidence: 98%

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

Zhou

Colburn

2010

Journal of Neurophysiology

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“…Therefore, Ca v 1.3 Ϫ/Ϫ LSO neurons appear to be structurally and functionally integrated into the brainstem circuitry. However, currents through ␣-DTX-sensitive potassium channels contribute to short EPSPs and high reliability and temporal fidelity of synaptic transmission (Brew and Forsythe, 1995;Kaczmarek et al, 2005). They also determine the rate and timing of APs (Dodson et al, 2002) and thus preserve (and possibly enhance) phase-locking behavior.…”

Section: Possible Causes Of the Impaired Developmentmentioning

confidence: 99%

Ca_v1.3 Calcium Channels Are Required for Normal Development of the Auditory Brainstem

Hirtz

Boesen²,

Braun³

et al. 2011

J. Neurosci.

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Within the Ca v 1 family of voltage-gated calcium channels, Ca v 1.2 and Ca v 1.3 channels are the predominant subtypes in the brain. Whereas specific functions for each subtype were described in the adult brain, their role in brain development is poorly understood. Here we assess the role of Ca v 1.3 subunits in the activity-dependent development of the auditory brainstem. We used Ca v 1.3-deficient (Ca v 1.3 Ϫ/Ϫ ) mice because these mice lack cochlea-driven activity that deprives the auditory centers from peripheral input. We found a drastically reduced volume in all auditory brainstem centers (range 25-59%, total 35%), which was manifest before hearing onset. A reduction was not obvious outside the auditory system. The lateral superior olive (LSO) was strikingly malformed in Ca v 1.3 Ϫ/Ϫ mice and had fewer neurons (1/3 less). The remaining LSO neurons displayed normal dendritic trees and received functional glutamatergic input, yet they fired action potentials predominantly with a multiple pattern upon depolarization, in contrast to the single firing pattern prevalent in controls. The latter finding appears to be due to a reduction of dendrototoxin-sensitive potassium conductances, presumably mediated through the K v 1.2 subtype. Fura2 imaging provided evidence for functional Ca v 1.3 channels in the LSO of wild-type mice. Our results imply that Ca v 1.3 channels are indispensable for the development of the central auditory system. We propose that the unique LSO phenotype in Ca v 1.3 Ϫ/Ϫ mice, which hitherto was not described in other hereditary deafness models, is caused by the synergistic contribution of two factors: on-site loss of Ca v 1.3 channels in the neurons plus lack of peripheral input.

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“…Changes in auditory nerve activity following deafness have been shown to induce changes in excitability and response properties in the cochlear nucleus (Francis and Manis, 2000;Kaltenbach and Afman, 2000;Kanold and Manis, 2005;Wang and Manis, 2005) and inferior colliculus (Bledsoe et al, 1995(Bledsoe et al, , 1997Mossop et al, 2000;Salvi et al, 2000;Syka and Rybalko, 2000;Vale and Sanes, 2002;Vale et al, 2004) (for reviews Moller, 2005;Syka, 2002). While the acoustic environment has been shown to influence auditory brain stem responses through modulation of voltage-gated potassium channels, this is achieved largely through phosphorylation rather than chronic alterations in gene expression (Chambard and Ashmore, 2005;Kaczmarek et al, 2005;Macica et al, 2003;Song et al, 2005). Studies in the avian cochlear nucleus (nucleus magnocellularis) have shown large deafness-related changes in Kv1.1 and Kv3.1 expression following cochlear ablation (Lu et al, 2004;von Hehn et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Deafness associated changes in expression of two-pore domain potassium channels in the rat cochlear nucleus

et al. 2006

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Two-pore domain potassium channels ( ) play an important role in setting resting membrane potential by regulating background leakage of potassium ions, which in turn controls neuronal excitability. To determine whether these channels contribute to activity-dependent plasticity following deafness, we used quantitative real-time PCR to examine the expression of 10 subunits in the rat cochlear nucleus at 3 days, 3 weeks and 3 months after bilateral cochlear ablation. There was a large sustained decrease in the expression of TASK-5, a subunit that is predominantly expressed in auditory brain stem neurons, and in the TASK-1 subunit which is highly expressed in several types of cochlear nucleus neurons. TWIK-1 and THIK-2 also showed significant decreases in expression that were maintained across all time points. TWIK-2, TREK-1 and TREK-2 showed no significant change in expression at 3 days but showed large decreases at 3 weeks and 3 months following deafness. TRAAK and TASK-3 subunits showed significant decreases at 3 days and 3 weeks following deafness, but these differences were no longer significant at 3 months. Dramatic changes in expression of subunits suggest these channels may play a role in deafness-associated changes in the excitability of cochlear nucleus neurons.

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Regulation of the timing of MNTB neurons by short-term and long-term modulation of potassium channels

Cited by 61 publications

References 68 publications

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

Ca_v1.3 Calcium Channels Are Required for Normal Development of the Auditory Brainstem

Deafness associated changes in expression of two-pore domain potassium channels in the rat cochlear nucleus

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Regulation of the timing of MNTB neurons by short-term and long-term modulation of potassium channels

Cited by 61 publications

References 68 publications

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

A Modeling Study of the Effects of Membrane Afterhyperpolarization on Spike Interval Statistics and on ILD Encoding in the Lateral Superior Olive

Cav1.3 Calcium Channels Are Required for Normal Development of the Auditory Brainstem

Deafness associated changes in expression of two-pore domain potassium channels in the rat cochlear nucleus

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Ca_v1.3 Calcium Channels Are Required for Normal Development of the Auditory Brainstem