Kv3 potassium channels control the duration of different arousal states by distinct stochastic and clock-like mechanisms

Rolf H. Joho, Gerald A. Marks, Felipe Espinosa

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

Sleep-wake behavior is tightly controlled in many animal species, suggesting genetically encoded, homeostatic control mechanisms that determine arousal-state dynamics. We reported that two voltage-gated potassium channels, Kv3.1 and Kv3.3, control sleep in wild-type and Kv3-mutant mice. Compared with wild-type (WT), homozygous double mutants (DKO) that lack these channels sleep 40% less in the light and 22% less in the dark. To understand how the lack of these channels affects sleep, we analysed arousal-state changes during the light period where the differences are greatest between WT and DKO. We determined the kinetic complexity of each arousal state from the episode durations of wakefulness, slow-wave sleep and rapid eye movement sleep (REMS). Based on the number of exponential components in episode-duration histograms, WT and DKO mice have several kinetically distinct states of wakefulness, and these states are longer in duration in DKO. For slow-wave sleep, WT mice have a single slow-wave sleep (SWS) state in contrast to DKO mice, which show two distinct SWS states, one that is 60% shorter than that in WT and a second that is similar in duration. Both WT and DKO mice have two kinetically distinct REMS states. DKO mice show an 84% reduction in the frequency of short REMS episodes (< 45 s) without any change in the occurrence of long REMS episodes (> 60 s). In contrast to the stochastic control of episode durations of wakefulness and SWS, the durations of both REMS states are normally distributed, indicating that the underlying control processes are fundamentally different.

Original languageEnglish (US)
Pages (from-to)1567-1574
Number of pages8
JournalEuropean Journal of Neuroscience
Volume23
Issue number6
DOIs
StatePublished - Mar 2006

Fingerprint

Shaw Potassium Channels
Arousal
Sleep
REM Sleep
Wakefulness
Voltage-Gated Potassium Channels
Light

Keywords

  • Knockout mice
  • Mutation
  • Short and long REM sleep
  • Sleep architecture

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Kv3 potassium channels control the duration of different arousal states by distinct stochastic and clock-like mechanisms. / Joho, Rolf H.; Marks, Gerald A.; Espinosa, Felipe.

In: European Journal of Neuroscience, Vol. 23, No. 6, 03.2006, p. 1567-1574.

Research output: Contribution to journalArticle

@article{cc5b3436ce144907834d0aaaf1b260fc,
title = "Kv3 potassium channels control the duration of different arousal states by distinct stochastic and clock-like mechanisms",
abstract = "Sleep-wake behavior is tightly controlled in many animal species, suggesting genetically encoded, homeostatic control mechanisms that determine arousal-state dynamics. We reported that two voltage-gated potassium channels, Kv3.1 and Kv3.3, control sleep in wild-type and Kv3-mutant mice. Compared with wild-type (WT), homozygous double mutants (DKO) that lack these channels sleep 40{\%} less in the light and 22{\%} less in the dark. To understand how the lack of these channels affects sleep, we analysed arousal-state changes during the light period where the differences are greatest between WT and DKO. We determined the kinetic complexity of each arousal state from the episode durations of wakefulness, slow-wave sleep and rapid eye movement sleep (REMS). Based on the number of exponential components in episode-duration histograms, WT and DKO mice have several kinetically distinct states of wakefulness, and these states are longer in duration in DKO. For slow-wave sleep, WT mice have a single slow-wave sleep (SWS) state in contrast to DKO mice, which show two distinct SWS states, one that is 60{\%} shorter than that in WT and a second that is similar in duration. Both WT and DKO mice have two kinetically distinct REMS states. DKO mice show an 84{\%} reduction in the frequency of short REMS episodes (< 45 s) without any change in the occurrence of long REMS episodes (> 60 s). In contrast to the stochastic control of episode durations of wakefulness and SWS, the durations of both REMS states are normally distributed, indicating that the underlying control processes are fundamentally different.",
keywords = "Knockout mice, Mutation, Short and long REM sleep, Sleep architecture",
author = "Joho, {Rolf H.} and Marks, {Gerald A.} and Felipe Espinosa",
year = "2006",
month = "3",
doi = "10.1111/j.1460-9568.2006.04672.x",
language = "English (US)",
volume = "23",
pages = "1567--1574",
journal = "European Journal of Neuroscience",
issn = "0953-816X",
publisher = "Wiley-Blackwell",
number = "6",

}

TY - JOUR

T1 - Kv3 potassium channels control the duration of different arousal states by distinct stochastic and clock-like mechanisms

AU - Joho, Rolf H.

AU - Marks, Gerald A.

AU - Espinosa, Felipe

PY - 2006/3

Y1 - 2006/3

N2 - Sleep-wake behavior is tightly controlled in many animal species, suggesting genetically encoded, homeostatic control mechanisms that determine arousal-state dynamics. We reported that two voltage-gated potassium channels, Kv3.1 and Kv3.3, control sleep in wild-type and Kv3-mutant mice. Compared with wild-type (WT), homozygous double mutants (DKO) that lack these channels sleep 40% less in the light and 22% less in the dark. To understand how the lack of these channels affects sleep, we analysed arousal-state changes during the light period where the differences are greatest between WT and DKO. We determined the kinetic complexity of each arousal state from the episode durations of wakefulness, slow-wave sleep and rapid eye movement sleep (REMS). Based on the number of exponential components in episode-duration histograms, WT and DKO mice have several kinetically distinct states of wakefulness, and these states are longer in duration in DKO. For slow-wave sleep, WT mice have a single slow-wave sleep (SWS) state in contrast to DKO mice, which show two distinct SWS states, one that is 60% shorter than that in WT and a second that is similar in duration. Both WT and DKO mice have two kinetically distinct REMS states. DKO mice show an 84% reduction in the frequency of short REMS episodes (< 45 s) without any change in the occurrence of long REMS episodes (> 60 s). In contrast to the stochastic control of episode durations of wakefulness and SWS, the durations of both REMS states are normally distributed, indicating that the underlying control processes are fundamentally different.

AB - Sleep-wake behavior is tightly controlled in many animal species, suggesting genetically encoded, homeostatic control mechanisms that determine arousal-state dynamics. We reported that two voltage-gated potassium channels, Kv3.1 and Kv3.3, control sleep in wild-type and Kv3-mutant mice. Compared with wild-type (WT), homozygous double mutants (DKO) that lack these channels sleep 40% less in the light and 22% less in the dark. To understand how the lack of these channels affects sleep, we analysed arousal-state changes during the light period where the differences are greatest between WT and DKO. We determined the kinetic complexity of each arousal state from the episode durations of wakefulness, slow-wave sleep and rapid eye movement sleep (REMS). Based on the number of exponential components in episode-duration histograms, WT and DKO mice have several kinetically distinct states of wakefulness, and these states are longer in duration in DKO. For slow-wave sleep, WT mice have a single slow-wave sleep (SWS) state in contrast to DKO mice, which show two distinct SWS states, one that is 60% shorter than that in WT and a second that is similar in duration. Both WT and DKO mice have two kinetically distinct REMS states. DKO mice show an 84% reduction in the frequency of short REMS episodes (< 45 s) without any change in the occurrence of long REMS episodes (> 60 s). In contrast to the stochastic control of episode durations of wakefulness and SWS, the durations of both REMS states are normally distributed, indicating that the underlying control processes are fundamentally different.

KW - Knockout mice

KW - Mutation

KW - Short and long REM sleep

KW - Sleep architecture

UR - http://www.scopus.com/inward/record.url?scp=33645108005&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33645108005&partnerID=8YFLogxK

U2 - 10.1111/j.1460-9568.2006.04672.x

DO - 10.1111/j.1460-9568.2006.04672.x

M3 - Article

C2 - 16553620

AN - SCOPUS:33645108005

VL - 23

SP - 1567

EP - 1574

JO - European Journal of Neuroscience

JF - European Journal of Neuroscience

SN - 0953-816X

IS - 6

ER -