A prominent soma‐dendritic distribution of Kv3.3 K<sup>+</sup> channels in electrosensory and cerebellar neurons

Rashid, Asim J.; Dunn, Robert; Turner, Ray W.

doi:10.1002/cne.1409

Cited by 33 publications

(26 citation statements)

References 67 publications

(129 reference statements)

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“…The present results are suggestive of axonal K channels with similarly rapid gating kinetics. Consistent with this idea, K V 3 channels have been detected by immunolabeling in Purkinje axons of Apteronotus electric fish (Rashid et al, 2001).…”

Section: Evidence For Specializations Of Axonal Channelssupporting

confidence: 55%

Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons

2005

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In cerebellar Purkinje neurons, the reliability of propagation of high-frequency simple spikes and spikelets of complex spikes is likely to regulate inhibition of Purkinje target neurons. To test the extent to which a one-to-one correspondence exists between somatic and axonal spikes, we made dual somatic and axonal recordings from Purkinje neurons in mouse cerebellar slices. Somatic action potentials were recorded with a whole-cell pipette, and the corresponding axonal signals were recorded extracellularly with a loose-patch pipette. Propagation of spontaneous and evoked simple spikes was highly reliable. At somatic firing rates of ϳ200 spikes/sec, Ͻ10% of spikes failed to propagate, with failures becoming more frequent only at maximal somatic firing rates (ϳ260 spikes/sec). Complex spikes were elicited by climbing fiber stimulation, and their somatic waveforms were modulated by tonic current injection, as well as by paired stimulation to depress the underlying EPSCs. Across conditions, the mean number of propagating action potentials remained just above two spikes per climbing fiber stimulation, but the instantaneous frequency of the propagating spikes changed, from ϳ375 Hz during somatic hyperpolarizations that silenced spontaneous firing to ϳ150 Hz during spontaneous activity. The probability of propagation of individual spikelets could be described quantitatively as a saturating function of spikelet amplitude, rate of rise, or preceding interspike interval. The results suggest that ion channels of Purkinje axons are adapted to produce extremely short refractory periods and that brief bursts of forward-propagating action potentials generated by complex spikes may contribute transiently to inhibition of postsynaptic neurons.

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Section: Evidence For Specializations Of Axonal Channelssupporting

confidence: 55%

Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons

2005

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“…Blocking these channels would then increase the DAP and decrease the AHP. Alternatively, mAChR activation might also down-regulate high-threshold K + currents such as Kv3.3 (Rashid et al, 2001a) or SK1 channels (Ellis et al, 2008) found in pyramidal cell dendrites, and which can regulate burst firing (Noonan et al, 2003). The similarity between the effects of carbachol and those of apamin on the AHP (Figs.…”

Section: Summary and Discussionmentioning

confidence: 98%

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

Mehaffey

Ellis

Krahe

et al. 2008

Journal of Physiology-Paris

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Sensory neurons encode natural stimuli by changes in firing rate or by generating specific firing patterns, such as bursts. Many neural computations rely on the fact that neurons can be tuned to specific stimulus frequencies. It is thus important to understand the mechanisms underlying frequency tuning. In the electrosensory system of the weakly electric fish, Apteronotus leptorhynchus, the primary processing of behaviourally relevant sensory signals occurs in pyramidal neurons of the electrosensory lateral line lobe (ELL). These cells encode low frequency prey stimuli with bursts of spikes and high frequency communication signals with single spikes. We describe here how bursting in pyramidal neurons can be regulated by intrinsic conductances in a cell subtype specific fashion across the sensory maps found within the ELL, thereby regulating their frequency tuning. Further, the neuromodulatory regulation of such conductances within individual cells and the consequences to frequency tuning are highlighted. Such alterations in the tuning of the pyramidal neurons may allow weakly electric fish to preferentially select for certain stimuli under various behaviourally relevant circumstances.

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“…Moreover, the terminal sequence PXPSIL (X, aliphatic amino acid) is present in both the teleost and mammalian Kv3.3 channel proteins and is also present at the C terminus of the rodent Kv3.2b channel (Ponce et al, 1997). We suggest that PXPSIL in the rodent Kv3.3 channel is also likely to be required for dendritic targeting of Kv3.3, as shown for cerebellar Purkinje cells (Rashid et al, 2001b;Martina et al, 2003;McKay and Turner, 2004). Additional studies are needed to determine whether the C-terminal PXPSIL sequence has similar targeting functions for both Kv3.3 and Kv3.2b channels in mammalian neurons.…”

Section: Dendritic Aptkv33 Targeting Is Directed By a C-terminal Motifmentioning

confidence: 66%

“…One explanation would be to provide subtypespecific signals to direct subcellular localization or regulation by second messengers. In this regard, Kv3.3 channels are distinct in exhibiting a dendritic distribution in several cell types in the cerebellum and electrosensory lateral line lobe (ELL) of the weakly electric fish Apteronotus leptorhynchus, whereas other Kv3 subtypes distribute preferentially to somatic and axonal membranes (Moreno et al, 1995;Sekirnjak et al, 1997;Rashid et al, 2001b;Martina et al, 2003). ELL pyramidal cells provide one of the most clear functional distinctions for Kv3 channel distribution, in that AptKv3 channels in somatic and dendritic regions differentially control the threshold for burst discharge (Rashid et al, 2001a;Noonan et al, 2003).…”

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confidence: 99%

A C-Terminal Domain Directs Kv3.3 Channels to Dendrites

Deng¹,

Rashid²,

Fernandez³

et al. 2005

J. Neurosci.

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Pyramidal neurons of the electrosensory lateral line lobe (ELL) of Apteronotus leptorhynchus express Kv3-type voltage-gated potassium channels that give rise to high-threshold currents at the somatic and dendritic levels. Two members of the Kv3 channel family, AptKv3.1 and AptKv3.3, are coexpressed in these neurons. AptKv3.3 channels are expressed at uniformly high levels in each of four ELL segments, whereas AptKv3.1 channels appear to be expressed in a graded manner with higher levels of expression in segments that process high-frequency electrosensory signals. Immunohistochemical and recombinant channel expression studies show a differential distribution of these two channels in the dendrites of ELL pyramidal neurons. AptKv3.1 is concentrated in somas and proximal dendrites, whereas AptKv3.3 is distributed throughout the full extent of the large dendritic tree. Recombinant channel expression of AptKv3 channels through in vivo viral injections allowed directed retargeting of AptKv3 subtypes over the somadendritic axis, revealing that the sequence responsible for targeting channels to distal dendrites lies within the C-terminal domain of the AptKv3.3 protein. The targeting domain includes a consensus sequence predicted to bind to a PDZ (postsynaptic density-95/Discs large/zona occludens-1)-type protein-protein interaction motif. These findings reveal that different functional roles for Kv3 potassium channels at the somatic and dendritic level of a sensory neuron are attained through specific targeting that selectively distributes Kv3.3 channels to the dendritic compartment.

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A prominent soma‐dendritic distribution of Kv3.3 K⁺ channels in electrosensory and cerebellar neurons

Cited by 33 publications

References 67 publications

Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons

Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

A C-Terminal Domain Directs Kv3.3 Channels to Dendrites

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A prominent soma‐dendritic distribution of Kv3.3 K+ channels in electrosensory and cerebellar neurons

Cited by 33 publications

References 67 publications

Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons

Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

A C-Terminal Domain Directs Kv3.3 Channels to Dendrites

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A prominent soma‐dendritic distribution of Kv3.3 K⁺ channels in electrosensory and cerebellar neurons