Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling

René Wilbers; Verjinia D Metodieva; Sarah Duverdin; Djai B Heyer; Anna A Galakhova; Eline J Mertens; Tamara D Versluis; Johannes C Baayen; Sander Idema; David P Noske; Niels Verburg; Ronald B Willemse; Philip C de Witt Hamer; Maarten H P Kole; Christiaan P J de Kock; Huibert D Mansvelder; Natalia A Goriounova

doi:10.1126/sciadv.ade3300

Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling

René Wilbers, Verjinia D Metodieva, Sarah Duverdin, Djai B Heyer, Anna A Galakhova, Eline J Mertens, Tamara D Versluis, Johannes C Baayen, Sander Idema, David P Noske, Niels Verburg, Ronald B Willemse, Philip C de Witt Hamer, Maarten H P Kole, Christiaan P J de Kock, Huibert D Mansvelder, Natalia A Goriounova

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Abstract

Human cortical pyramidal neurons are large, have extensive dendritic trees, and yet have unexpectedly fast input-output properties: Rapid subthreshold synaptic membrane potential changes are reliably encoded in timing of action potentials (APs). Here, we tested whether biophysical properties of voltage-gated sodium (Na+) and potassium (K+) currents in human pyramidal neurons can explain their fast input-output properties. Human Na+ and K+ currents exhibited more depolarized voltage dependence, slower inactivation, and faster recovery from inactivation compared with their mouse counterparts. Computational modeling showed that despite lower Na+ channel densities in human neurons, the biophysical properties of Na+ channels resulted in higher channel availability and contributed to fast AP kinetics stability. Last, human Na+ channel properties also resulted in a larger dynamic range for encoding of subthreshold membrane potential changes. Thus, biophysical adaptations of voltage-gated Na+ and K+ channels enable fast input-output properties of large human pyramidal neurons.

Original language	English
Pages (from-to)	eade3300
Journal	Science advances
Volume	9
Issue number	41
DOIs	https://doi.org/10.1126/sciadv.ade3300
Publication status	Published - 13 Oct 2023

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Wilbers, R., Metodieva, V. D., Duverdin, S., Heyer, D. B., Galakhova, A. A., Mertens, E. J., Versluis, T. D., Baayen, J. C., Idema, S., Noske, D. P., Verburg, N., Willemse, R. B., de Witt Hamer, P. C., Kole, M. H. P., de Kock, C. P. J., Mansvelder, H. D., & Goriounova, N. A. (2023). Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling. Science advances, 9(41), eade3300. https://doi.org/10.1126/sciadv.ade3300

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title = "Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling",

abstract = "Human cortical pyramidal neurons are large, have extensive dendritic trees, and yet have unexpectedly fast input-output properties: Rapid subthreshold synaptic membrane potential changes are reliably encoded in timing of action potentials (APs). Here, we tested whether biophysical properties of voltage-gated sodium (Na+) and potassium (K+) currents in human pyramidal neurons can explain their fast input-output properties. Human Na+ and K+ currents exhibited more depolarized voltage dependence, slower inactivation, and faster recovery from inactivation compared with their mouse counterparts. Computational modeling showed that despite lower Na+ channel densities in human neurons, the biophysical properties of Na+ channels resulted in higher channel availability and contributed to fast AP kinetics stability. Last, human Na+ channel properties also resulted in a larger dynamic range for encoding of subthreshold membrane potential changes. Thus, biophysical adaptations of voltage-gated Na+ and K+ channels enable fast input-output properties of large human pyramidal neurons.",

author = "Ren{\'e} Wilbers and Metodieva, {Verjinia D} and Sarah Duverdin and Heyer, {Djai B} and Galakhova, {Anna A} and Mertens, {Eline J} and Versluis, {Tamara D} and Baayen, {Johannes C} and Sander Idema and Noske, {David P} and Niels Verburg and Willemse, {Ronald B} and {de Witt Hamer}, {Philip C} and Kole, {Maarten H P} and {de Kock}, {Christiaan P J} and Mansvelder, {Huibert D} and Goriounova, {Natalia A}",

year = "2023",

month = oct,

day = "13",

doi = "10.1126/sciadv.ade3300",

language = "English",

volume = "9",

pages = "eade3300",

journal = "Science advances",

issn = "2375-2548",

publisher = "American Association for the Advancement of Science (AAAS)",

number = "41",

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Wilbers, R, Metodieva, VD, Duverdin, S, Heyer, DB, Galakhova, AA, Mertens, EJ, Versluis, TD, Baayen, JC, Idema, S, Noske, DP, Verburg, N, Willemse, RB, de Witt Hamer, PC, Kole, MHP, de Kock, CPJ, Mansvelder, HD & Goriounova, NA 2023, 'Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling', Science advances, vol. 9, no. 41, pp. eade3300. https://doi.org/10.1126/sciadv.ade3300

TY - JOUR

T1 - Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling

AU - Wilbers, René

AU - Metodieva, Verjinia D

AU - Duverdin, Sarah

AU - Heyer, Djai B

AU - Galakhova, Anna A

AU - Mertens, Eline J

AU - Versluis, Tamara D

AU - Baayen, Johannes C

AU - Idema, Sander

AU - Noske, David P

AU - Verburg, Niels

AU - Willemse, Ronald B

AU - de Witt Hamer, Philip C

AU - Kole, Maarten H P

AU - de Kock, Christiaan P J

AU - Mansvelder, Huibert D

AU - Goriounova, Natalia A

PY - 2023/10/13

Y1 - 2023/10/13

N2 - Human cortical pyramidal neurons are large, have extensive dendritic trees, and yet have unexpectedly fast input-output properties: Rapid subthreshold synaptic membrane potential changes are reliably encoded in timing of action potentials (APs). Here, we tested whether biophysical properties of voltage-gated sodium (Na+) and potassium (K+) currents in human pyramidal neurons can explain their fast input-output properties. Human Na+ and K+ currents exhibited more depolarized voltage dependence, slower inactivation, and faster recovery from inactivation compared with their mouse counterparts. Computational modeling showed that despite lower Na+ channel densities in human neurons, the biophysical properties of Na+ channels resulted in higher channel availability and contributed to fast AP kinetics stability. Last, human Na+ channel properties also resulted in a larger dynamic range for encoding of subthreshold membrane potential changes. Thus, biophysical adaptations of voltage-gated Na+ and K+ channels enable fast input-output properties of large human pyramidal neurons.

AB - Human cortical pyramidal neurons are large, have extensive dendritic trees, and yet have unexpectedly fast input-output properties: Rapid subthreshold synaptic membrane potential changes are reliably encoded in timing of action potentials (APs). Here, we tested whether biophysical properties of voltage-gated sodium (Na+) and potassium (K+) currents in human pyramidal neurons can explain their fast input-output properties. Human Na+ and K+ currents exhibited more depolarized voltage dependence, slower inactivation, and faster recovery from inactivation compared with their mouse counterparts. Computational modeling showed that despite lower Na+ channel densities in human neurons, the biophysical properties of Na+ channels resulted in higher channel availability and contributed to fast AP kinetics stability. Last, human Na+ channel properties also resulted in a larger dynamic range for encoding of subthreshold membrane potential changes. Thus, biophysical adaptations of voltage-gated Na+ and K+ channels enable fast input-output properties of large human pyramidal neurons.

U2 - 10.1126/sciadv.ade3300

DO - 10.1126/sciadv.ade3300

M3 - Article

C2 - 37824607

SN - 2375-2548

VL - 9

SP - eade3300

JO - Science advances

JF - Science advances

IS - 41

ER -

Human voltage-gated Na+ and K+ channel properties underlie sustained fast AP signaling

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