A Unique Role for Kv3 Voltage-Gated Potassium Channels in Starburst Amacrine Cell Signaling in Mouse Retina

Ozaita, Andrés; Petit-Jacques, Jérôme; Völgyi, Béla; Ho, Chi Shun; Joho, Rolf H.; Bloomfield, Stewart A.; Rudy, Bernardo

doi:10.1523/jneurosci.1275-04.2004

Cited by 75 publications

(93 citation statements)

References 55 publications

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“…Similar differential localization of GABA A receptors has been described in hippocampal pyramidal cells (Nusser et al, 1996a) and cerebellar granule cells (Nusser et al, 1996b). In addition to receptors, it has recently been shown that mouse starburst amacrine cells express strongly Kv3 voltage-gated potassium channels on their cell bodies and proximal dendrites, with the intermediate and distal dendrites showing significantly lower levels of expression (Ozaita et al, 2004). Also, on rabbit starburst amacrine cells, there is evidence that chloride gradients generated by two different cation-chloride cotransporters contribute to differences in biophysical properties seen on the proximal and distal dendrites of these cells (Gavrikov et al, 2003).…”

Section: Functional Compartmentalization On Individual Neuronssupporting

confidence: 65%

Compartmental localization of γ-aminobutyric acid type B receptors in the cholinergic circuitry of the rabbit retina

Zucker¹,

Nilson²,

Ehinger³

et al. 2005

J. Comp. Neurol.

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Although many effects of gamma-aminobutyric acid (GABA) on retinal function have been attributed to GABA(A) and GABA(C) receptors, specific retinal functions have also been shown to be mediated by GABA(B) receptors, including facilitation of light-evoked acetylcholine release from the rabbit retina (Neal and Cunningham [1995] J. Physiol. 482:363-372). To explain the results of a rich set of experiments, Neal and Cunningham proposed a model for this facilitation. In this model, GABA(B) receptor-mediated inhibition of glycinergic cells would reduce their own inhibition of cholinergic cells. In turn, muscarinic input from the latter to the glycinergic cells would complete a negative-feedback circuitry. In this study, we have used immunohistochemical techniques to test elements of this model. We report that glycinergic amacrine cells are GABA(B) receptor negative. In contrast, our data reveal the localization of GABA(B) receptors on cholinergic/GABAergic starburst amacrine cells. High-resolution localization of GABA(B) receptors on starburst amacrine cells shows that they are discretely localized to a limited population of its varicosities, the majority of likely synaptic-release sites being devoid of detectable levels of GABA(B) receptors. Finally, we identify a glycinergic cell that is a potential muscarinic receptor-bearing target of GABA(B)-modulated acetylcholine release. This target is the DAPI-3 cell. We propose, based on these data, a modification of the Neal and Cunningham model in which GABA(B) receptors are on starburst, not glycinergic amacrine cells.

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Section: Functional Compartmentalization On Individual Neuronssupporting

confidence: 65%

Compartmental localization of γ-aminobutyric acid type B receptors in the cholinergic circuitry of the rabbit retina

Zucker¹,

Nilson²,

Ehinger³

et al. 2005

J. Comp. Neurol.

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“…The large TEA-induced enhancement of evoked GABA release is absent in Kv3.1/Kv3.2 double knock-out mice To obtain more direct evidence that the effect of TEA on spikeevoked GABA release is mainly attributable to blockade of presynaptic channels containing Kv3.1 and Kv3.2 proteins, we performed experiments using Kv3.1/Kv3.2 double knock-out (DKO) mice (Ozaita et al, 2004). In slices prepared from DKO mice, the large TEA-induced enhancement of eIPSCs seen in wild-type animals was absent, and TEA produced only a small increase in the eIPSC (Fig.…”

Section: Resultsmentioning

confidence: 99%

Specific Functions of Synaptically Localized Potassium Channels in Synaptic Transmission at the Neocortical GABAergic Fast-Spiking Cell Synapse

Goldberg

Watanabe²,

Chang³

et al. 2005

J. Neurosci.

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Potassium (K ϩ ) channel subunits of the Kv3 subfamily (Kv3.1-Kv3.4) display a positively shifted voltage dependence of activation and fast activation/deactivation kinetics when compared with other voltage-gated K ϩ channels, features that confer on Kv3 channels the ability to accelerate the repolarization of the action potential (AP) efficiently and specifically. In the cortex, the Kv3.1 and Kv3.2 proteins are expressed prominently in a subset of GABAergic interneurons known as fast-spiking (FS) cells and in fact are a significant determinant of the fast-spiking discharge pattern. However, in addition to expression at FS cell somata, Kv3.1 and Kv3.2 proteins also are expressed prominently at FS cell terminals, suggesting roles for Kv3 channels in neurotransmitter release. We investigated the effect of 1.0 mM tetraethylammonium (TEA; which blocks Kv3 channels) on inhibitory synaptic currents recorded in layer II/III neocortical pyramidal cells. Spike-evoked GABA release by FS cells was enhanced nearly twofold by 1.0 mM TEA, with a decrease in the paired pulse ratio (PPR), effects not reproduced by blockade of the non-Kv3 subfamily K ϩ channels also blocked by low concentrations of TEA. Moreover, in Kv3.1/Kv3.2 double knock-out (DKO) mice, the large effects of TEA were absent, spike-evoked GABA release was larger, and the PPR was lower than in wild-type mice. Together, these results suggest specific roles for Kv3 channels at FS cell terminals that are distinct from those of Kv1 and large-conductance Ca 2ϩ -activated K ϩ channels (also present at the FS cell synapse). We propose that at FS cell terminals synaptically localized Kv3 channels keep APs brief, limiting Ca 2ϩ influx and hence release probability, thereby influencing synaptic depression at a synapse designed for sustained high-frequency synaptic transmission.

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“…In neocortex, thalamus, hippocampus, and striatum, Kv3-type channels are found in GABAergic cells (mostly interneurons) that also express the calcium-binding protein parvalbumin (PV), a marker for fastspiking neurons. The genetic elimination of Kv3.1 or Kv3.3 increases AP duration, reduces high-frequency firing, and affects synaptic transmission of neurons in several brain nuclei (Lau et al, 2000;Porcello et al, 2002;Macica et al, 2003;Matsukawa et al, 2003;McMahon et al, 2004;Ozaita et al, 2004). The coexpression of Kv3.1 and Kv3.3 channel subunits in several brain regions suggests that functional redundancy among these subunits may exist.…”

Section: Introductionmentioning

confidence: 99%

Ablation of Kv3.1 and Kv3.3 Potassium Channels Disrupts Thalamocortical OscillationsIn VitroandIn Vivo

Espinosa

Torres-Vega

Marks³

et al. 2008

J. Neurosci.

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The genes Kcnc1 and Kcnc3 encode the subunits for the fast-activating/fast-deactivating, voltage-gated potassium channels Kv3.1 and Kv3.3, which are expressed in several brain regions known to be involved in the regulation of the sleep-wake cycle. When these genes are genetically eliminated, Kv3.1/Kv3.3-deficient mice display severe sleep loss as a result of unstable slow-wave sleep. Within the thalamocortical circuitry, Kv3.1 and Kv3.3 subunits are highly expressed in the thalamic reticular nucleus (TRN), which is thought to act as a pacemaker at sleep onset and to be involved in slow oscillatory activity (spindle waves) during slow-wave sleep. We showed that in cortical electroencephalographic recordings of freely moving Kv3.1/Kv3.3-deficient mice, spectral power is reduced up to 70% at frequencies Ͻ15 Hz. In addition, the number of sleep spindles in vivo as well as rhythmic rebound firing of TRN neurons in vitro is diminished in mutant mice. Kv3.1/Kv3.3-deficient TRN neurons studied in vitro show ϳ60% increase in action potential duration and a reduction in highfrequency firing after depolarizing current injections and during rebound burst firing. The results support the hypothesis that altered electrophysiological properties of TRN neurons contribute to the reduced EEG power at slow frequencies in the thalamocortical network of Kv3-deficient mice.

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A Unique Role for Kv3 Voltage-Gated Potassium Channels in Starburst Amacrine Cell Signaling in Mouse Retina

Cited by 75 publications

References 55 publications

Compartmental localization of γ-aminobutyric acid type B receptors in the cholinergic circuitry of the rabbit retina

Compartmental localization of γ-aminobutyric acid type B receptors in the cholinergic circuitry of the rabbit retina

Specific Functions of Synaptically Localized Potassium Channels in Synaptic Transmission at the Neocortical GABAergic Fast-Spiking Cell Synapse

Ablation of Kv3.1 and Kv3.3 Potassium Channels Disrupts Thalamocortical OscillationsIn VitroandIn Vivo

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