Trends in Neurosciences
ReviewDendritic ion channel trafficking and plasticity
Section snippets
Dendrites and plasticity
Dendrites are extensive and elaborate processes emerging from the cell body of neurons. They occupy a large surface area and receive most synaptic inputs [1]. Their predominant function is in processing and transmitting synaptic signals to the cell body and axon initial segment, where, if threshold is reached, action potentials are initiated. This is an active process because it is known that dendrites possess an abundance of ion channels that are involved in receiving, transforming and
Role of dendritic ion channels in regulating intrinsic excitability, synaptic integration and plasticity
Dendrites contain a plethora of ion channels including K+ channels. In many central neurons the densities of most voltage-gated potassium (Kv) channels appear to be uniform or lower in distal dendrites compared with those at the soma [1]. One exception appears to be the Kv4 subunit. Immunohistochemical analysis first showed a predominantly dendritic localization of Kv4 channels [16] (Table 1). The Kv4 subunits form a fast activating and inactivating current in heterologous systems, reminiscent
Plasticity-induced post-translational modifications and membrane trafficking of dendritic ion channels
Cellular neuroplasticity has been hypothesized to underlie experience-dependent behaviors such as learning and memory and drug addiction (Figure 1). Uncovering the cellular and molecular mechanisms of the acquisition, storage and recollection of memories is a major topic of basic and translational neuroscience research because alterations in these mechanisms could contribute to multiple disease pathologies, including autism, epilepsy, Alzheimer's and Parkinson's disease. For the most part,
Concluding remarks
In summary, we have discussed how the activity and expression of dendritic ion channels can be dynamically regulated by alterations in intrinsic neuronal firing and changes in synaptic activity. Whereas enormous strides have been made in understanding how several subtypes of voltage-gated ion channels are selectively targeted to dendrites and how plasticity affects the dendritic trafficking of these channels, much less is known about others. For example, dendritic Na+ and Ca2+ channel function
Acknowledgements
This work was supported by an New Investigator Award from the Medical Research Council (G0700369, M.M.S.), a Wellcome Trust project grant (WT087363MA, M.M.S.) and the Intramural Research Program of the National Institutes of Health and the National Institute of Child Health and Human Development (D.H.).
References (110)
- et al.
Active dendrites: colorful wings of the mysterious butterflies
Trends Neurosci.
(2008) - et al.
Synaptic gain control and homeostasis
Curr. Opin. Neurobiol.
(2003) - et al.
Plasticity of dendritic function
Curr. Opin. Neurobiol.
(2005) Homeostatic signaling: the positive side of negative feedback
Curr. Opin. Neurobiol.
(2007)- et al.
Synaptic AMPA receptor plasticity and behavior
Neuron
(2009) Subcellular segregation of two A-type K+ channel proteins in rat central neurons
Neuron
(1992)Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons
Neuron
(2008)Kv2.1: a voltage-gated K+ channel critical to dynamic control of neuronal excitability
Neurotoxicology
(2005)Unique roles of SK and Kv4.2 potassium channels in dendritic integration
Neuron
(2004)Pertussis-toxin-sensitive Galpha subunits selectively bind to C-terminal domain of neuronal GIRK channels: evidence for a heterotrimeric G-protein-channel complex
Mol. Cell Neurosci.
(2005)
Gαi controls the gating of the G protein-activated K+ channel
GIRK. Neuron
Common molecular pathways mediate long-term potentiation of synaptic excitation and slow synaptic inhibition
Cell
G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons
Neuron
Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons
Neuron
HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons
Neuron
A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons
Cell
Alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP–HCN channel signaling in prefrontal cortex
Cell
Ca2+ signaling in dendritic spines
Curr. Opin. Neurobiol.
Dendritic calcium spikes induce bi-directional synaptic plasticity in the lateral amygdala
Neuropharmacology
Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons
Neuron
Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons
Neuron
A role for Kif17 in transport of Kv4.2
J. Biol. Chem.
Transmembrane interaction mediates complex formation between peptidase homologues and Kv4 channels
Mol. Cell Neurosci.
KChIP4a regulates Kv4.2 channel trafficking through PKA phosphorylation
Mol. Cell Neurosci.
Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle
Science
Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study
Nat. Neurosci.
Quantitative assessment of the distributions of membrane conductances involved in action potential backpropagation along basal dendrites
J. Neurophysiol.
Synaptic plasticity: taming the beast
Nat. Neurosci.
Dendritic excitability and synaptic plasticity
Physiol. Rev.
Plasticity of dendritic excitability
J. Neurobiol.
The distribution and targeting of neuronal voltage-gated ion channels
Nat. Rev.
Dendritic mRNA: transport, translation and function
Nat. Rev.
Protein synthesis at synaptic sites on dendrites
Annu. Rev. Neurosci.
Silent synapses and the emergence of a postsynaptic mechanism for LTP
Nat. Rev.
Identification of molecular components of A-type channels activating at subthreshold potentials
J. Neurophysiol.
Regulation of backpropagating action potentials in mitral cell lateral dendrites by A-type potassium currents
J. Neurophysiol.
K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons
Nature
Regulation of synaptic timing in the olfactory bulb by an A-type potassium current
Nat. Neurosci.
Dendritic coincidence detection of EPSPs and action potentials
Nat. Neurosci.
Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons
J. Neurosci.
Compartmentalized dendritic plasticity and input feature storage in neurons
Nature
Calcium spikes in basal dendrites of layer 5 pyramidal neurons during action potential bursts
J. Neurosci.
Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones
J. Physiol.
Deletion of Kv4.2 gene eliminates dendritic A-type K+ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons
J. Neurosci.
Localization and targeting of voltage-dependent ion channels in mammalian central neurons
Physiol. Rev.
The Kv2.1 K+ channel targets to the axon initial segment of hippocampal and cortical neurons in culture and in situ
BMC Neurosci.
Frequency-dependent regulation of rat hippocampal somato-dendritic excitability by the K+ channel subunit Kv2.1
J. Physiol.
SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines
Nat. Neurosci.
SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala
Nat. Neurosci.
Dendritic control of spontaneous bursting in cerebellar Purkinje cells
J. Neurosci.
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2023, Brain Research BulletinA novel bungarotoxin binding site-tagged construct reveals MAPK-dependent Kv4.2 trafficking
2019, Molecular and Cellular NeuroscienceCitation Excerpt :More recently, a de novo mutation in the KCND2 gene has been identified in human patients with intractable, infant-onset epilepsy and autism (Lin et al., 2018) and altered translation of Kv4.2 is observed in a mouse model of fragile X syndrome (Gross et al., 2011). The physiological importance of Kv4.2 in normal neuronal function and disease calls for detailed examination of the molecular constituents and pathways involved in channel regulation and trafficking (Shah et al., 2010). One attractive method for studying the trafficking of surface-expressed Kv4.2 is fluorescence microscopy.
Hyperexcitability of hippocampal CA1 pyramidal neurons in male offspring of a rat model of autism spectrum disorder (ASD) induced by prenatal exposure to valproic acid: A possible involvement of Ih channel current
2019, Brain ResearchCitation Excerpt :Ih channels are activated by membrane hyperpolarization at voltages near to resting membrane potentials (at potentials more negative than −50 mV) and carry out a mixed Na+/K+ current and have an essential role in controlling neuronal excitability. Ih channels are widely expressed in the principal neurons in the central and peripheral nervous system (Biel et al., 2009; DiFrancesco and DiFrancesco, 2015; Robinson and Siegelbaum, 2003; Shah et al., 2010). This channel current may influence the neuronal activity in either excitatory (Deng et al., 2008) or inhibitory (Poolos et al., 2002) way, based on the cellular distribution and features of the Ih channels, the nature and location of synaptic inputs, and the intrinsic excitability of neural cell (Santoro and Baram, 2003).
Simulations predict differing phase responses to excitation vs. inhibition in theta-resonant pyramidal neurons
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