Voltage Gated Potassium Channels: Structure and Function of Kv1 to Kv9 Subfamilies

Rudy, Bernardo; Maffie, Jon K.; Amarillo, Yimy; Clark, Brian; Goldberg, Ethan M.; Jeong, Hwan Jeong; Kruglikov, Illya; Kwon, Elaine; Nadal, Marcela S.; Zagha, Edward

doi:10.1016/b978-008045046-9.01630-2

Cited by 27 publications

(23 citation statements)

References 24 publications

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“…We found that layer 5 CC-Parv neurons are characterized by a delayed AP response near-threshold, as well as a lower firing rate and instantaneous frequency compared to the layer 5 Parv neurons. Bath application of either of the Kv1-specific blocker DTX-I or the Kv1.1 (for review see, Pongs, 2007 ; Rudy et al, 2009 ; Jan and Jan, 2012 ) subunit-specific blocker DTX-K abolished the characteristic delayed-response of the first AP observed near threshold current injections, converting the firing pattern to a more continuous discharge pattern as was observed for the layer 5 Parv neurons. By blocking this current, a large reduction in both the threshold current injection and the voltage threshold for the generation of the AP was observed that ultimately increased the instantaneous frequency in the layer 5 CC-Parv neurons.…”

Section: Discussionmentioning

confidence: 92%

“…The finding that layer 5 CC-Parv neurons are characterized by a strong AHP and delayed firing suggested the possibility that the slow inactivation of K + current can be responsible for controlling the near-threshold excitability of CC-Parv neurons (Figure 4 ). The kinetic and voltage-dependent properties of Kv1 K + channels are heterogeneous (Rudy et al, 2009 ); those known to be activated near-threshold potentials are characterized by subunits of the Kv1 sub-family that display differences in inactivation as a function of the precise subunit composition (Coetzee et al, 1999 ). For this reason, we considered Kv1 channels to be strong candidates to explain the mechanism in question.…”

Section: Resultsmentioning

confidence: 99%

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Layer 5 Callosal Parvalbumin-Expressing Neurons: A Distinct Functional Group of GABAergic Neurons

Zurita

Feyen

Apicella

2018

Front. Cell. Neurosci.

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Previous studies have shown that parvalbumin-expressing neurons (CC-Parv neurons) connect the two hemispheres of motor and sensory areas via the corpus callosum, and are a functional part of the cortical circuit. Here we test the hypothesis that layer 5 CC-Parv neurons possess anatomical and molecular mechanisms which dampen excitability and modulate the gating of interhemispheric inhibition. In order to investigate this hypothesis we use viral tracing to determine the anatomical and electrophysiological properties of layer 5 CC-Parv and parvalbumin-expressing (Parv) neurons of the mouse auditory cortex (AC). Here we show that layer 5 CC-Parv neurons had larger dendritic fields characterized by longer dendrites that branched farther from the soma, whereas layer 5 Parv neurons had smaller dendritic fields characterized by shorter dendrites that branched nearer to the soma. The layer 5 CC-Parv neurons are characterized by delayed action potential (AP) responses to threshold currents, lower firing rates, and lower instantaneous frequencies compared to the layer 5 Parv neurons. Kv1.1 containing K+ channels are the main source of the AP repolarization of the layer 5 CC-Parv and have a major role in determining both the spike delayed response, firing rate and instantaneous frequency of these neurons.

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Section: Discussionmentioning

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Layer 5 Callosal Parvalbumin-Expressing Neurons: A Distinct Functional Group of GABAergic Neurons

Zurita

Feyen

Apicella

2018

Front. Cell. Neurosci.

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“…In general, Kv1 channels are expressed predominantly in axons, including synaptic terminals, although some neurons have been shown to express Kv1 proteins in somatic and dendritic compartments as well (reviewed in Lai and Jan 2006; Vacher and others 2008; Rudy and others 2009). …”

Section: Molecular Organization Of the Aismentioning

confidence: 99%

“…They were initially discovered as the currents mediating muscarinic excitation of neuronal activity, and hence called M-currents (Brown and Adams 1980). This subfamily of K + channels is of great interest because four of its five members have been associated with human disease (reviewed in Rudy and others 2009). …”

Section: Molecular Organization Of the Aismentioning

confidence: 99%

Electrogenic Tuning of the Axon Initial Segment

2009

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Action potentials (APs) provide the primary means of rapid information transfer in the nervous system. Where exactly these signals are initiated in neurons has been a basic question in neurobiology and the subject of extensive study. Converging lines of evidence indicate that APs are initiated in a discrete and highly specialized portion of the axon-the axon initial segment (AIS). The authors review key aspects of the organization and function of the AIS and focus on recent work that has provided important insights into its electrical signaling properties. In addition to its main role in AP initiation, the new findings suggest that the AIS is also a site of complex AP modulation by specific types of ion channels localized to this axonal domain. Keywordsaction potential initiation; neocortical neurons; GABA; fast-spiking interneurons; axon initial segment (AIS); Kv1 potassium channels One of the remarkable specializations of neurons is their exquisite morphology and highly polarized nature. The axon is the main output structure of neurons that allows the activity of single cells to be rapidly conveyed to large numbers of post-synaptic targets. The axon initial segment (AIS) is the proximal portion of the axon beginning at the emergence of the axon from the soma (the axon hillock) and ending at the onset of the myelin sheath. This, of course, is a general definition that must be modified in specific cases (such as for unmyelinated axons and cells in which the axon emerges from a dendrite).Multiple lines of evidence point to the AIS as the site of initiation of the action potential (AP), the basic unit of information transfer in the nervous system. AP initiation occurs at the AIS because the threshold for AP generation is lowest at this site. This in turn is due to the presence of a high density-and perhaps unique properties-of voltage-gated sodium (Na + ) channels at the AIS. Cellular and molecular studies show that the AIS is a highly organized subcellular compartment, or domain, that possesses a number of ultrastructural and biochemical specializations. Moreover, in the cortex, the AIS is the specific and only target of a unique subtype of GABAergic interneuron, the chandelier cell. Finally, the AIS expresses a number of functionally important and disease-related molecules that appear to provide "electrogenic" tuning of neuronal excitability.

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“…The molecular identification and biophysical characterization of ion channels in vertebrates has revealed a large diversity of molecular mechanisms potentially involved in controlling the membrane behavior at subthreshold potentials (Hille 2001;Yu and Catterall 2004). Members of many different families of potassium channels display biophysical properties consistent with activation at subthreshold potentials (Coetzee et al 1999;Rudy et al 2009). Similarly, hyperpolarization-activated cationic channels (HCN) (Biel et al 2009), low-threshold calcium channels (Perez-Reyes 2003), persistent sodium currents (Waxman et al 2002), and leak sodium channels (Ren 2011) also operate at subthreshold potentials.…”

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confidence: 99%

The interplay of seven subthreshold conductances controls the resting membrane potential and the oscillatory behavior of thalamocortical neurons

Amarillo

Zagha

Mato

et al. 2014

Journal of Neurophysiology

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Amarillo Y, Zagha E, Mato G, Rudy B, Nadal MS. The interplay of seven subthreshold conductances controls the resting membrane potential and the oscillatory behavior of thalamocortical neurons. J Neurophysiol 112: 393-410, 2014. First published April 23, 2014 doi:10.1152/jn.00647.2013.-The signaling properties of thalamocortical (TC) neurons depend on the diversity of ion conductance mechanisms that underlie their rich membrane behavior at subthreshold potentials. Using patch-clamp recordings of TC neurons in brain slices from mice and a realistic conductance-based computational model, we characterized seven subthreshold ion currents of TC neurons and quantified their individual contributions to the total steady-state conductance at levels below tonic firing threshold. We then used the TC neuron model to show that the resting membrane potential results from the interplay of several inward and outward currents over a background provided by the potassium and sodium leak currents. The steady-state conductances of depolarizing I h (hyperpolarization-activated cationic current), I T (low-threshold calcium current), and I NaP (persistent sodium current) move the membrane potential away from the reversal potential of the leak conductances. This depolarization is counteracted in turn by the hyperpolarizing steady-state current of I A (fast transient A-type potassium current) and I Kir (inwardly rectifying potassium current). Using the computational model, we have shown that single parameter variations compatible with physiological or pathological modulation promote burst firing periodicity. The balance between three amplifying variables (activation of I T , activation of I NaP , and activation of I Kir ) and three recovering variables (inactivation of I T , activation of I A , and activation of I h ) determines the propensity, or lack thereof, of repetitive burst firing of TC neurons. We also have determined the specific roles that each of these variables have during the intrinsic oscillation. thalamocortical neuron; subthreshold conductances; resting membrane potential; repetitive burst firing THE RESTING MEMBRANE PERMEABILITY of neurons defines the resting membrane potential (RMP) and determines neuronal excitability. This resting membrane permeability is determined by ion channels that are active at levels below the threshold for action potential firing. The molecular identification and biophysical characterization of ion channels in vertebrates has revealed a large diversity of molecular mechanisms potentially involved in controlling the membrane behavior at subthreshold potentials (Hille 2001;Yu and Catterall 2004). Members of many different families of potassium channels display biophysical properties consistent with activation at subthreshold potentials (Coetzee et al. 1999;Rudy et al. 2009). Similarly, hyperpolarization-activated cationic channels (HCN) (Biel et al. 2009), low-threshold calcium channels (Perez-Reyes 2003), persistent sodium currents (Waxman et al. 2002), and leak sodium channels (Ren 2011) also ...

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Voltage Gated Potassium Channels: Structure and Function of Kv1 to Kv9 Subfamilies

Cited by 27 publications

References 24 publications

Layer 5 Callosal Parvalbumin-Expressing Neurons: A Distinct Functional Group of GABAergic Neurons

Layer 5 Callosal Parvalbumin-Expressing Neurons: A Distinct Functional Group of GABAergic Neurons

Electrogenic Tuning of the Axon Initial Segment

The interplay of seven subthreshold conductances controls the resting membrane potential and the oscillatory behavior of thalamocortical neurons

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