scholarly journals Dendritic Voltage-Gated Ion Channels Regulate the Action Potential Firing Mode of Hippocampal CA1 Pyramidal Neurons

1999 ◽  
Vol 82 (4) ◽  
pp. 1895-1901 ◽  
Author(s):  
Jeffrey C. Magee ◽  
Michael Carruth
Keyword(s):  
Ion Channels ◽  
Action Potential ◽  
Large Amplitude ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Burst Firing ◽  
Voltage Gated ◽  
Ca1 Pyramidal Neurons ◽  
Firing Mode ◽  
Voltage Gated Ion Channels

The role of dendritic voltage-gated ion channels in the generation of action potential bursting was investigated using whole cell patch-clamp recordings from the soma and dendrites of CA1 pyramidal neurons located in hippocampal slices of adult rats. Under control conditions somatic current injections evoked single action potentials that were associated with an afterhyperpolarization (AHP). After localized application of 4-aminopyridine (4-AP) to the distal apical dendritic arborization, the same current injections resulted in the generation of an afterdepolarization (ADP) and multiple action potentials. This burst firing was not observed after localized application of 4-AP to the soma/proximal dendrites. The dendritic 4-AP application allowed large-amplitude Na+-dependent action potentials, which were prolonged in duration, to backpropagate into the distal apical dendrites. No change in action potential backpropagation was seen with proximal 4-AP application. Both the ADP and action potential bursting could be inhibited by the bath application of nonspecific concentrations of divalent Ca2+ channel blockers (NiCl and CdCl). Ca2+ channel blockade also reduced the dendritic action potential duration without significantly affecting spike amplitude. Low concentrations of TTX (10–50 nM) also reduced the ability of the CA1 neurons to fire in the busting mode. This effect was found to be the result of an inhibition of backpropagating dendritic action potentials and could be overcome through the coordinated injection of transient, large-amplitude depolarizing current into the dendrite. Dendritic current injections were able to restore the burst firing mode (represented as a large ADP) even in the presence of high concentrations of TTX (300–500 μM). These data suggest the role of dendritic Na+ channels in bursting is to allow somatic/axonal action potentials to backpropagate into the dendrites where they then activate dendritic Ca2+ channels. Although it appears that most Ca2+ channel subtypes are important in burst generation, blockade of T- and R-type Ca2+ channels by NiCl (75 μM) inhibited action potential bursting to a greater extent than L-channel (10 μM nimodipine) or N-, P/Q-type (1 μM ω-conotoxin MVIIC) Ca2+ channel blockade. This suggest that the Ni-sensitive voltage-gated Ca2+ channels have the most important role in action potential burst generation. In summary, these data suggest that the activation of dendritic voltage-gated Ca2+ channels, by large-amplitude backpropagating spikes, provides a prolonged inward current that is capable of generating an ADP and burst of multiple action potentials in the soma of CA1 pyramidal neurons. Dendritic voltage-gated ion channels profoundly regulate the processing and storage of incoming information in CA1 pyramidal neurons by modulating the action potential firing mode from single spiking to burst firing.

scholarly journals Dampening of Hyperexcitability in CA1 Pyramidal Neurons by Polyunsaturated Fatty Acids Acting on Voltage-Gated Ion Channels

PLoS ONE ◽  
2012 ◽  
Vol 7 (9) ◽  
pp. e44388 ◽  
Author(s):  
Jenny Tigerholm ◽  
Sara I. Börjesson ◽  
Linnea Lundberg ◽  
Fredrik Elinder ◽  
Erik Fransén
Keyword(s):  
Fatty Acids ◽  
Ion Channels ◽  
Polyunsaturated Fatty Acids ◽  
Pyramidal Neurons ◽  
Voltage Gated ◽  
Ca1 Pyramidal Neurons ◽  
Voltage Gated Ion Channels ◽  
Gated Ion Channels

Dichotomy of Action-Potential Backpropagation in CA1 Pyramidal Neuron Dendrites

2001 ◽  
Vol 86 (6) ◽  
pp. 2998-3010 ◽  
Author(s):  
Nace L. Golding ◽  
William L. Kath ◽  
Nelson Spruston
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Synaptic Activity ◽  
Resting Potential ◽  
Model Parameters ◽  
Voltage Sensitivity ◽  
Whole Cell ◽  
Ca1 Pyramidal Neurons ◽  
Whole Cell Recordings

In hippocampal CA1 pyramidal neurons, action potentials are typically initiated in the axon and backpropagate into the dendrites, shaping the integration of synaptic activity and influencing the induction of synaptic plasticity. Despite previous reports describing action-potential propagation in the proximal apical dendrites, the extent to which action potentials invade the distal dendrites of CA1 pyramidal neurons remains controversial. Using paired somatic and dendritic whole cell recordings, we find that in the dendrites proximal to 280 μm from the soma, single backpropagating action potentials exhibit <50% attenuation from their amplitude in the soma. However, in dendritic recordings distal to 300 μm from the soma, action potentials in most cells backpropagated either strongly (26–42% attenuation; n = 9/20) or weakly (71–87% attenuation; n = 10/20) with only one cell exhibiting an intermediate value (45% attenuation). In experiments combining dual somatic and dendritic whole cell recordings with calcium imaging, the amount of calcium influx triggered by backpropagating action potentials was correlated with the extent of action-potential invasion of the distal dendrites. Quantitative morphometric analyses revealed that the dichotomy in action-potential backpropagation occurred in the presence of only subtle differences in either the diameter of the primary apical dendrite or branching pattern. In addition, action-potential backpropagation was not dependent on a number of electrophysiological parameters (input resistance, resting potential, voltage sensitivity of dendritic spike amplitude). There was, however, a striking correlation of the shape of the action potential at the soma with its amplitude in the dendrite; larger, faster-rising, and narrower somatic action potentials exhibited more attenuation in the distal dendrites (300–410 μm from the soma). Simple compartmental models of CA1 pyramidal neurons revealed that a dichotomy in action-potential backpropagation could be generated in response to subtle manipulations of the distribution of either sodium or potassium channels in the dendrites. Backpropagation efficacy could also be influenced by local alterations in dendritic side branches, but these effects were highly sensitive to model parameters. Based on these findings, we hypothesize that the observed dichotomy in dendritic action-potential amplitude is conferred primarily by differences in the distribution, density, or modulatory state of voltage-gated channels along the somatodendritic axis.

Resting and Active Properties of Pyramidal Neurons in Subiculum and CA1 of Rat Hippocampus

2000 ◽  
Vol 84 (5) ◽  
pp. 2398-2408 ◽  
Author(s):  
Nathan P. Staff ◽  
Hae-Yoon Jung ◽  
Tara Thiagarajan ◽  
Michael Yao ◽  
Nelson Spruston
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Current Injection ◽  
Synaptic Integration ◽  
Membrane Properties ◽  
Neuronal Membrane ◽  
Similar Action ◽  
Ca1 Neurons ◽  
Ca1 Pyramidal Neurons

Action potentials are the end product of synaptic integration, a process influenced by resting and active neuronal membrane properties. Diversity in these properties contributes to specialized mechanisms of synaptic integration and action potential firing, which are likely to be of functional significance within neural circuits. In the hippocampus, the majority of subicular pyramidal neurons fire high-frequency bursts of action potentials, whereas CA1 pyramidal neurons exhibit regular spiking behavior when subjected to direct somatic current injection. Using patch-clamp recordings from morphologically identified neurons in hippocampal slices, we analyzed and compared the resting and active membrane properties of pyramidal neurons in the subiculum and CA1 regions of the hippocampus. In response to direct somatic current injection, three subicular firing types were identified (regular spiking, weak bursting, and strong bursting), while all CA1 neurons were regular spiking. Within subiculum strong bursting neurons were found preferentially further away from the CA1 subregion. Input resistance ( R N), membrane time constant (τm), and depolarizing “sag” in response to hyperpolarizing current pulses were similar in all subicular neurons, while R N and τm were significantly larger in CA1 neurons. The first spike of all subicular neurons exhibited similar action potential properties; CA1 action potentials exhibited faster rising rates, greater amplitudes, and wider half-widths than subicular action potentials. Therefore both the resting and active properties of CA1 pyramidal neurons are distinct from those of subicular neurons, which form a related class of neurons, differing in their propensity to burst. We also found that both regular spiking subicular and CA1 neurons could be transformed into a burst firing mode by application of a low concentration of 4-aminopyridine, suggesting that in both hippocampal subfields, firing properties are regulated by a slowly inactivating, D-type potassium current. The ability of all subicular pyramidal neurons to burst strengthens the notion that they form a single neuronal class, sharing a burst generating mechanism that is stronger in some cells than others.

scholarly journals Large Neurohypophysial Varicosities Amplify Action Potentials: Results from Numerical Simulations

Endocrinology ◽  
2009 ◽  
Vol 150 (6) ◽  
pp. 2829-2836 ◽  
Author(s):  
C. Brad Bennett ◽  
Martin Muschol
Keyword(s):  
Ion Channels ◽  
Numerical Simulations ◽  
Action Potentials ◽  
Calcium Influx ◽  
Physiological Role ◽  
Nonlinear Dependence ◽  
Voltage Gated ◽  
Herring Bodies ◽  
Voltage Gated Ion Channels ◽  
Gated Ion Channels

Axons in the neurohypophysis are known for their “beads on a string” morphology, with numerous in-line secretory swellings lined up along the axon cable. A significant fraction of these secretory swellings, called Herring bodies, is large enough to serve as an identifying feature of the neural lobe in histological sections. Little is known about the physiological role such large axonal swellings might play in neuroendocrine physiology. Using numerical simulations, we have investigated whether large in-line varicosities affect the waveform and propagation of action potentials (APs) along neurohypophysial axons. Due to the strong nonlinear dependence of calcium influx on AP waveforms, such modulation would inevitably affect neuroendocrine release. The parameters for our numerical simulations were matched to established properties of voltage-gated ion channels in neurohypophysial swellings. We find that even a single in-line varicosity can severely depress AP waveforms far upstream in the axonal cable. In contrast, AP depolarization within varicosities becomes amplified. Amplification within varicosities varies in a nontrivial manner with varicosity dimensions, and is most pronounced for diameters close to those of Herring bodies. Overall, we find that large axonal varicosities significantly modulate AP waveforms and their propagation, and do so over large distances. Varicosity size is the main determinant for the observed AP amplification, with the kinetics of voltage-gated ion channels playing a noticeable but secondary role. Our results imply that large varicosities are sites of enhanced hormone release, suggesting that small and large varicosities target different neurohypophysial structures.

scholarly journals Luciferase shRNA Presents off-Target Effects on Voltage-Gated Ion Channels in Mouse Hippocampal Pyramidal Neurons

eNeuro ◽  
2017 ◽  
Vol 4 (5) ◽  
pp. ENEURO.0186-17.2017 ◽  
Author(s):  
Yuto Hasegawa ◽  
Wenjie Mao ◽  
Sucharita Saha ◽  
Georgia Gunner ◽  
Jenya Kolpakova ◽  
...  
Keyword(s):  
Ion Channels ◽  
Pyramidal Neurons ◽  
Hippocampal Pyramidal Neurons ◽  
Voltage Gated ◽  
Voltage Gated Ion Channels ◽  
Target Effects ◽  
Gated Ion Channels

scholarly journals Small-conductance Ca2+-activated K+ channels modulate action potential-induced Ca2+ transients in hippocampal neurons

2013 ◽  
Vol 109 (6) ◽  
pp. 1514-1524 ◽  
Author(s):  
Raffaella Tonini ◽  
Teresa Ferraro ◽  
Marisol Sampedro-Castañeda ◽  
Anna Cavaccini ◽  
Martin Stocker ◽  
...  
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Hippocampal Neurons ◽  
Pyramidal Neurons ◽  
Apical Dendrite ◽  
Channel Blockers ◽  
Sk Channels ◽  
Hippocampal Pyramidal Neurons ◽  
Voltage Gated ◽  
Small Conductance

In hippocampal pyramidal neurons, voltage-gated Ca2+ channels open in response to action potentials. This results in elevations in the intracellular concentration of Ca2+ that are maximal in the proximal apical dendrites and decrease rapidly with distance from the soma. The control of these action potential-evoked Ca2+ elevations is critical for the regulation of hippocampal neuronal activity. As part of Ca2+ signaling microdomains, small-conductance Ca2+-activated K+ (SK) channels have been shown to modulate the amplitude and duration of intracellular Ca2+ signals by feedback regulation of synaptically activated Ca2+ sources in small distal dendrites and dendritic spines, thus affecting synaptic plasticity in the hippocampus. In this study, we investigated the effect of the activation of SK channels on Ca2+ transients specifically induced by action potentials in the proximal processes of hippocampal pyramidal neurons. Our results, obtained by using selective SK channel blockers and enhancers, show that SK channels act in a feedback loop, in which their activation by Ca2+ entering mainly through L-type voltage-gated Ca2+ channels leads to a reduction in the subsequent dendritic influx of Ca2+. This underscores a new role of SK channels in the proximal apical dendrite of hippocampal pyramidal neurons.

scholarly journals Polyunsaturated fatty acid analogues differentially affect cardiac NaV, CaV, and KV channels through unique mechanisms

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Briana M Bohannon ◽  
Alicia de la Cruz ◽  
Xiaoan Wu ◽  
Jessica J Jowais ◽  
Marta E Perez ◽  
...  
Keyword(s):  
Ion Channels ◽  
Action Potential ◽  
Induced Pluripotent Stem Cell ◽  
Voltage Gated ◽  
Kv Channels ◽  
Cardiac Ion Channels ◽  
Induced Pluripotent ◽  
Voltage Gated Ion Channels ◽  
Ventricular Action Potential ◽  
Gated Ion Channels

The cardiac ventricular action potential depends on several voltage-gated ion channels, including NaV, CaV, and KV channels. Mutations in these channels can cause Long QT Syndrome (LQTS) which increases the risk for ventricular fibrillation and sudden cardiac death. Polyunsaturated fatty acids (PUFAs) have emerged as potential therapeutics for LQTS because they are modulators of voltage-gated ion channels. Here we demonstrate that PUFA analogues vary in their selectivity for human voltage-gated ion channels involved in the ventricular action potential. The effects of specific PUFA analogues range from selective for a specific ion channel to broadly modulating cardiac ion channels from all three families (NaV, CaV, and KV). In addition, a PUFA analogue selective for the cardiac IKs channel (Kv7.1/KCNE1) is effective in shortening the cardiac action potential in human-induced pluripotent stem cell-derived cardiomyocytes. Our data suggest that PUFA analogues could potentially be developed as therapeutics for LQTS and cardiac arrhythmia.

Biologically inspired reversible osmotic actuation through voltage-gated ion channels

2012 ◽  
Vol 23 (12) ◽  
pp. 1395-1403 ◽  
Author(s):  
Eric Freeman ◽  
Lisa Weiland
Keyword(s):  
Ion Channels ◽  
Action Potentials ◽  
High Energy ◽  
High Energy Density ◽  
Proof Of Concept ◽  
Biologically Inspired ◽  
Voltage Gated ◽  
Motor Cells ◽  
Voltage Gated Ion Channels ◽  
Gated Ion Channels

This study focuses on the development of a novel high-energy density actuator based on biomimicry principles. The system proposed here draws inspiration from plant motor cells and provides proof of concept for a highly configurable reversible osmotic actuator through the application of voltage-gated ion channels and action potentials. Computational methods are employed to measure the effectiveness of the proposed system in comparison to similar novel actuators.

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