Kv1.1-Containing Channels Are Critical for Temporal Precision During Spike Initiation

Gittelman, Joshua X.; Tempel, Bruce L.

doi:10.1152/jn.00092.2005

Cited by 72 publications

(69 citation statements)

References 53 publications

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“…The decrement was similar at E14, and the percentage block at other depolarizing steps was similar. Previous reports of voltage-clamp studies of the medial nucleus of the trapezoid body (MNTB) describe tissue penetration problems for dendrotoxins into slices, with complete Kv1 current block occurring only after incubation in dendrotoxins for tens of minutes (Gittelman and Tempel, 2006). Our experiments were not this long lasting; thus, we expect that unaffected Kv1 channels carried a portion of the residual current.…”

Section: Development Of Kmentioning

confidence: 73%

“…In general, blockade or absence of Kv1-type channels increases membrane time constant, resulting in broader APs (Rathouz and Trussell, 1998;Brew et al, 2003). In MNTB, the all-important temporal precision of the auditory system is disrupted in mice lacking the Kv1.1 protein (Gittelman and Tempel, 2006). Mature NM neurons exposed to DTX-I fire multiple spikes in response to depolarizing current injection (Rathouz and Trussell, 1998).…”

Section: Discussionmentioning

confidence: 99%

“…Current pulse summation with either GPSP trains or voltage steps was not as great in DTX-I exposed E18 neurons as in control E14 neurons. This is in part because of dendrotoxin tissue penetration problems (Gittelman and Tempel, 2006). Complete block of Kv1 currents may not be accomplished for tens of minutes, and residual Kv1 currents are likely shunting some excitation.…”

Section: Discussionmentioning

confidence: 99%

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A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K⁺Currents

2007

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Mature nucleus magnocellularis (NM) neurons, the avian homolog of bushy cells of the mammalian anteroventral cochlear nucleus, maintain high [ClϪ ] i and depolarize in response to GABA. Depolarizing GABAergic postsynaptic potentials (GPSPs) activate both the synaptic conductance and large outward currents, which, when coupled together, inhibit spikes via shunting and spike threshold accommodation. We studied the maturation of the synaptic and voltage-dependent components of inhibition in embryonic NM neurons using whole-cell and gramicidin-perforated patch-clamp techniques to measure Cl Ϫ reversal potential, GABAergic synaptic responses, and voltage-dependent outward currents. We found that GABA enhanced excitability in immature NM neurons, undergoing a switch to inhibitory between embryonic day 14 (E14) and E18. Low-voltage-activated Kv1-type (dendrotoxin-I sensitive) K ϩ currents increased in amplitude between E14 and E18, whereas Cl Ϫ reversal potential and synaptic conductances remained relatively stable during this period. GABA was rendered inhibitory because of this increase in low-voltage activated outward currents. GPSPs summed with other inputs to increase spike probability at E14. GPSPs shunted spikes at E18, but blocking Kv1 channels transformed this inhibition to excitation, similar to E14 neurons. Subthreshold depolarizing current steps, designed to activate outward currents similar to depolarizing GPSPs, enhanced excitability at E14 but inhibited spiking in E18 neurons. Blocking Kv1 channels reversed this effect, rendering current steps excitatory. We present the novel finding that the developmental transition of GABAergic processing from increasing neuronal excitability to inhibiting spiking can depend on changes in the expression of voltage-gated channels rather than on a change in Cl Ϫ reversal potential.

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Section: Development Of Kmentioning

confidence: 73%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K⁺Currents

2007

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“…؊/؊ mice To a large extent, the AP waveform and the firing behavior of neurons are shaped by voltage-gated potassium currents (Trussell, 1999;Dodson et al, 2002;Rothman and Manis, 2003;Gittelman and Tempel, 2006). To differentiate between various types of currents and to elucidate the molecular basis of our results depicted in Figure 8 A-C, we pharmacologically isolated lowthreshold (LTK) and high-threshold potassium (HTK) currents in LSO neurons and analyzed their transient and sustained component.…”

Section: Altered Low-threshold Potassium Currents In Ca V 13mentioning

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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“…In addition, the M-cell membrane expresses low-voltage-gated potassium channels (Nakayama and Oda, 2004). Developmental increases in potassium currents, as in the auditory brainstems of higher vertebrates (Howard et al, 2007;Nakamura and Takahashi, 2007), will also help decrease the membrane time constant at the depolarizing phase before action potential generation (Fukui and Ohmori, 2004;Gittelman and Tempel, 2006).…”

Section: Reduction Of Onset Latency Associated With M-cell Developmentmentioning

confidence: 99%

Effective Sensory Modality Activating an Escape Triggering Neuron Switches during Early Development in Zebrafish

Kohashi

Nakata²,

Oda³

2012

J. Neurosci.

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Kv1.1-Containing Channels Are Critical for Temporal Precision During Spike Initiation

Abstract: doi: 10.1152/jn.00092.2005 You might find this additional info useful... This article cites 54 articles, 32 of which you can access for free at

Cited by 72 publications

References 53 publications

A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K⁺Currents

A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K⁺Currents

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

Effective Sensory Modality Activating an Escape Triggering Neuron Switches during Early Development in Zebrafish

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Kv1.1-Containing Channels Are Critical for Temporal Precision During Spike Initiation

Abstract: doi: 10.1152/jn.00092.2005 You might find this additional info useful... This article cites 54 articles, 32 of which you can access for free at

Cited by 72 publications

References 53 publications

A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K+Currents

A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K+Currents

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

Effective Sensory Modality Activating an Escape Triggering Neuron Switches during Early Development in Zebrafish

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A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K⁺Currents

A Developmental Switch to GABAergic Inhibition Dependent on Increases in Kv1-Type K⁺Currents

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