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A small fraction of strongly cooperative sodium channels boosts neuronal encoding of high frequencies.

Huang M, Volgushev M, Wolf F - PLoS ONE (2012)

Bottom Line: Models with a small fraction, [Formula: see text], of strongly cooperative channels generate APs with the most rapid onset dynamics.In this regime APs are triggered by simultaneous opening of the cooperative channel fraction and exhibit a pronounced biphasic waveform often observed in cortical neurons.We conclude that presence of a small fraction of strongly coupled sodium channels can explain characteristic features of cortical APs and has a functional impact of enhancing the spike encoding of rapidly varying signals.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Dynamics and Self-Organization, Bernstein Center for Computational Neuroscience, and Faculty of Physics, Georg August University School of Science, Göttingen, Germany.

ABSTRACT
Generation of action potentials (APs) is a crucial step in neuronal information processing. Existing biophysical models for AP generation almost universally assume that individual voltage-gated sodium channels operate statistically independently, and their avalanche-like opening that underlies AP generation is coordinated only through the transmembrane potential. However, biological ion channels of various types can exhibit strongly cooperative gating when clustered. Cooperative gating of sodium channels has been suggested to explain rapid onset dynamics and large threshold variability of APs in cortical neurons. It remains however unknown whether these characteristic properties of cortical APs can be reproduced if only a fraction of channels express cooperativity, and whether the presence of cooperative channels has an impact on encoding properties of neuronal populations. To address these questions we have constructed a conductance-based neuron model in which we continuously varied the size of a fraction [Formula: see text] of sodium channels expressing cooperativity and the strength of coupling between cooperative channels [Formula: see text]. We show that starting at a critical value of the coupling strength [Formula: see text], the activation curve of sodium channels develops a discontinuity at which opening of all coupled channels becomes an all-or-none event, leading to very rapid AP onsets. Models with a small fraction, [Formula: see text], of strongly cooperative channels generate APs with the most rapid onset dynamics. In this regime APs are triggered by simultaneous opening of the cooperative channel fraction and exhibit a pronounced biphasic waveform often observed in cortical neurons. We further show that presence of a small fraction of cooperative Na+ channels significantly improves the ability of neuronal populations to phase-lock their firing to high frequency input fluctuation. We conclude that presence of a small fraction of strongly coupled sodium channels can explain characteristic features of cortical APs and has a functional impact of enhancing the spike encoding of rapidly varying signals.

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Channel activation and AP dynamics in models with cooperative sodium channels.(A,B) Activation curves of sodium channels and (C.D) AP phase plots for the models with a small () and a large () fraction of cooperative channels, and a weak coupling (, blue traces) or strong coupling (, red traces).
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pone-0037629-g003: Channel activation and AP dynamics in models with cooperative sodium channels.(A,B) Activation curves of sodium channels and (C.D) AP phase plots for the models with a small () and a large () fraction of cooperative channels, and a weak coupling (, blue traces) or strong coupling (, red traces).

Mentions: In the cooperative WB model, AP waveform and onset dynamics assessed using vs. phase plots were very sensitive to the fraction of cooperative channels and the coupling strength (Fig. 3). The AP onset was essentially determined by the activation of the cooperative channel fraction, and its rapidness increased with coupling strength. For a small fraction of strongly cooperative channels the AP waveform was typically biphasic (Fig. 3C). For a large fraction of cooperative channels the AP was monophasic with rapid onset (Fig. 3D). APs were considered biphasic if had 3 zero crossings during the AP upstroke, as opposed to 1 zero-crossing for monophasic APs.


A small fraction of strongly cooperative sodium channels boosts neuronal encoding of high frequencies.

Huang M, Volgushev M, Wolf F - PLoS ONE (2012)

Channel activation and AP dynamics in models with cooperative sodium channels.(A,B) Activation curves of sodium channels and (C.D) AP phase plots for the models with a small () and a large () fraction of cooperative channels, and a weak coupling (, blue traces) or strong coupling (, red traces).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3362627&req=5

pone-0037629-g003: Channel activation and AP dynamics in models with cooperative sodium channels.(A,B) Activation curves of sodium channels and (C.D) AP phase plots for the models with a small () and a large () fraction of cooperative channels, and a weak coupling (, blue traces) or strong coupling (, red traces).
Mentions: In the cooperative WB model, AP waveform and onset dynamics assessed using vs. phase plots were very sensitive to the fraction of cooperative channels and the coupling strength (Fig. 3). The AP onset was essentially determined by the activation of the cooperative channel fraction, and its rapidness increased with coupling strength. For a small fraction of strongly cooperative channels the AP waveform was typically biphasic (Fig. 3C). For a large fraction of cooperative channels the AP was monophasic with rapid onset (Fig. 3D). APs were considered biphasic if had 3 zero crossings during the AP upstroke, as opposed to 1 zero-crossing for monophasic APs.

Bottom Line: Models with a small fraction, [Formula: see text], of strongly cooperative channels generate APs with the most rapid onset dynamics.In this regime APs are triggered by simultaneous opening of the cooperative channel fraction and exhibit a pronounced biphasic waveform often observed in cortical neurons.We conclude that presence of a small fraction of strongly coupled sodium channels can explain characteristic features of cortical APs and has a functional impact of enhancing the spike encoding of rapidly varying signals.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Dynamics and Self-Organization, Bernstein Center for Computational Neuroscience, and Faculty of Physics, Georg August University School of Science, Göttingen, Germany.

ABSTRACT
Generation of action potentials (APs) is a crucial step in neuronal information processing. Existing biophysical models for AP generation almost universally assume that individual voltage-gated sodium channels operate statistically independently, and their avalanche-like opening that underlies AP generation is coordinated only through the transmembrane potential. However, biological ion channels of various types can exhibit strongly cooperative gating when clustered. Cooperative gating of sodium channels has been suggested to explain rapid onset dynamics and large threshold variability of APs in cortical neurons. It remains however unknown whether these characteristic properties of cortical APs can be reproduced if only a fraction of channels express cooperativity, and whether the presence of cooperative channels has an impact on encoding properties of neuronal populations. To address these questions we have constructed a conductance-based neuron model in which we continuously varied the size of a fraction [Formula: see text] of sodium channels expressing cooperativity and the strength of coupling between cooperative channels [Formula: see text]. We show that starting at a critical value of the coupling strength [Formula: see text], the activation curve of sodium channels develops a discontinuity at which opening of all coupled channels becomes an all-or-none event, leading to very rapid AP onsets. Models with a small fraction, [Formula: see text], of strongly cooperative channels generate APs with the most rapid onset dynamics. In this regime APs are triggered by simultaneous opening of the cooperative channel fraction and exhibit a pronounced biphasic waveform often observed in cortical neurons. We further show that presence of a small fraction of cooperative Na+ channels significantly improves the ability of neuronal populations to phase-lock their firing to high frequency input fluctuation. We conclude that presence of a small fraction of strongly coupled sodium channels can explain characteristic features of cortical APs and has a functional impact of enhancing the spike encoding of rapidly varying signals.

Show MeSH
Related in: MedlinePlus