Reemerging role of cable properties in action potential initiation

Ma, Yunyong; Huguenard, John R.

doi:10.1073/pnas.1300520110

Cited by 7 publications

(8 citation statements)

References 20 publications

(14 reference statements)

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“…To understand the underlying mechanism, we asked how the somatic depolarization affects spike initiation in the initial axonal segment. It was recently reported that even small plastic changes in the availability or distribution of Na + channels in this segment may have a profound effect on cell excitation 16 21 .…”

Section: Discussionmentioning

confidence: 99%

“…Nonetheless, a very recent study in cortical cells, which combined dual-patch soma–axon recordings with axonal Na + imaging, predicted that minor changes in the Na + channel distribution in the proximal axon could have a strong effect on neuronal excitability 16 . This basic phenomenon was not intuitively understood in the past and may have fundamental implications of our understanding of cell excitability 21 .…”

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confidence: 99%

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Neuronal adaptation involves rapid expansion of the action potential initiation site

et al. 2014

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Action potential (AP) generation is the key to information-processing in the brain. Although APs are normally initiated in the axonal initial segment, developmental adaptation or prolonged network activity may alter the initiation site geometry thus affecting cell excitability. Here we find that hippocampal dentate granule cells adapt their spiking threshold to the kinetics of the ongoing dendrosomatic excitatory input by expanding the AP-initiation area away from the soma while also decelerating local axonal spikes. Dual-patch soma–axon recordings combined with axonal Na+ and Ca2+ imaging and biophysical modelling show that the underlying mechanism involves distance-dependent inactivation of axonal Na+ channels due to somatic depolarization propagating into the axon. Thus, the ensuing changes in the AP-initiation zone and local AP propagation could provide activity-dependent control of cell excitability and spiking on a relatively rapid timescale.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Neuronal adaptation involves rapid expansion of the action potential initiation site

et al. 2014

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“…In resting cardiac myocytes, the ion leakage occurs mainly through Kir2 K + channels, which maintain the negative V rest (Hibino et al, 2010). If the leakage is large, a large inward current flow is needed to bring the membrane potential to V th , because a greater part of the inward current is short-circuited by the leak (Ma and Huguenard, 2013). The second passive membrane property introduced above, membrane capacitance (C m ; see Glossary), is directly related to the surface area of the cell membrane, and it…”

Section: Passive Membrane Responsesmentioning

confidence: 99%

“…The electrical excitation of a cell requires that an inward current flows into the cell and depolarizes the resting membrane potential (V rest ; see Glossary) to V th (Spector, 2013;Ma and Huguenard, 2013;Varghese, 2016). In multicellular tissue, the current flow occurs between electrically coupled cells.…”

Section: Introductionmentioning

confidence: 99%

Feeling the heat: source–sink mismatch as a mechanism underlying the failure of thermal tolerance

Vornanen

2020

Journal of Experimental Biology

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A mechanistic explanation for the tolerance limits of animals at high temperatures is still missing, but one potential target for thermal failure is the electrical signaling off cells and tissues. With this in mind, here I review the effects of high temperature on the electrical excitability of heart, muscle and nerves, and refine a hypothesis regarding high temperature-induced failure of electrical excitation and signal transfer [the temperature-dependent deterioration of electrical excitability (TDEE) hypothesis]. A central tenet of the hypothesis is temperature-dependent mismatch between the depolarizing ion current (i.e. source) of the signaling cell and the repolarizing ion current (i.e. sink) of the receiving cell, which prevents the generation of action potentials (APs) in the latter. A source–sink mismatch can develop in heart, muscles and nerves at high temperatures owing to opposite effects of temperature on source and sink currents. AP propagation is more likely to fail at the sites of structural discontinuities, including electrically coupled cells, synapses and branching points of nerves and muscle, which impose an increased demand of inward current. At these sites, temperature-induced source–sink mismatch can reduce AP frequency, resulting in low-pass filtering or a complete block of signal transmission. In principle, this hypothesis can explain a number of heat-induced effects, including reduced heart rate, reduced synaptic transmission between neurons and reduced impulse transfer from neurons to muscles. The hypothesis is equally valid for ectothermic and endothermic animals, and for both aquatic and terrestrial species. Importantly, the hypothesis is strictly mechanistic and lends itself to experimental falsification.

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“…Although the variety of processes involved in translation of synaptic conductances at the dendrites into changes of the membrane potential at the site of action potential initiation is beyond the scope of this review, few points are worth mentioning. Of clear relevance for encoding is the shortening of the effective time constant, either by decreasing membrane resistance in high conductance state (Destexhe and others 2003), or by decreasing local capacitance at the spike initiation zone by shifting it into the axon, which results in partial isolation of the initiation zone from the large capacitance of the soma (Baranauskas and others 2013; Ma and Huguenard 2013). The isolation from the soma might be especially strong when the axon originates from a dendrite (Hausser and others 1995; Martina and others 2000; Thome and others 2014).…”

Section: Cellular and Network Mechanisms That Affect The Speed Of Neumentioning

confidence: 99%

Cortical Specializations Underlying Fast Computations

Volgushev

2015

Neuroscientist

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The time course of behaviorally relevant environmental events sets temporal constraints on neuronal processing. How does the mammalian brain make use of the increasingly complex networks of the neocortex, while making decisions and executing behavioral reactions within a reasonable time? The key parameter determining the speed of computations in neuronal networks is a time interval that neuronal ensembles need to process changes at their input and communicate results of this processing to downstream neurons. Theoretical analysis identified basic requirements for fast processing: use of neuronal populations for encoding, background activity, and fast onset dynamics of action potentials in neurons. Experimental evidence shows that populations of neocortical neurons fulfil these requirements. Indeed, they can change firing rate in response to input perturbations very quickly, within 1 to 3 ms, and encode high-frequency components of the input by phase-locking their spiking to frequencies up to 300 to 1000 Hz. This implies that time unit of computations by cortical ensembles is only few, 1 to 3 ms, which is considerably faster than the membrane time constant of individual neurons. The ability of cortical neuronal ensembles to communicate on a millisecond time scale allows for complex, multiple-step processing and precise coordination of neuronal activity in parallel processing streams, while keeping the speed of behavioral reactions within environmentally set temporal constraints.

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Reemerging role of cable properties in action potential initiation

Cited by 7 publications

References 20 publications

Neuronal adaptation involves rapid expansion of the action potential initiation site

Neuronal adaptation involves rapid expansion of the action potential initiation site

Feeling the heat: source–sink mismatch as a mechanism underlying the failure of thermal tolerance

Cortical Specializations Underlying Fast Computations

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