Sleep maintains excitatory synapse diversity in the cortex and hippocampus

Dimitra Koukaroudi; Zhen Qiu; Erik Fransén; Ragini Gokhale; Edita Bulovaite; Noboru H. Komiyama; Julie Seibt; Seth G.N. Grant

doi:10.1016/j.cub.2024.07.032

Sleep maintains excitatory synapse diversity in the cortex and hippocampus

Dimitra Koukaroudi
, Zhen Qiu
, Erik Fransén
, Ragini Gokhale
, Edita Bulovaite
, Noboru H. Komiyama
, Julie Seibt
, Seth G.N. Grant (Lead / Corresponding author)

Computing

Research output: Contribution to journal › Article › peer-review

11 Citations (Scopus)

91 Downloads (Pure)

Abstract

Insufficient sleep is a global problem with serious consequences for cognition and mental health. Synapses play a central role in many aspects of cognition, including the crucial function of memory consolidation during sleep. Interference with the normal expression or function of synapse proteins is a cause of cognitive, mood, and other behavioral problems in over 130 brain disorders. Sleep deprivation (SD) has also been reported to alter synapse protein composition and synapse number, although with conflicting results. In our study, we conducted synaptome mapping of excitatory synapses in 125 regions of the mouse brain and found that sleep deprivation selectively reduces synapse diversity in the cortex and in the CA1 region of the hippocampus. Sleep deprivation targeted specific types and subtypes of excitatory synapses while maintaining total synapse density (synapse number/area). Synapse subtypes with longer protein lifetimes exhibited resilience to sleep deprivation, similar to observations in aging and genetic perturbations. Moreover, the altered synaptome architecture affected the responses to neural oscillations, suggesting that sleep plays a vital role in preserving cognitive function by maintaining the brain's synaptome architecture.

Original language	English
Pages (from-to)	3836-3843
Number of pages	14
Journal	Current Biology
Volume	34
Issue number	16
DOIs	https://doi.org/10.1016/j.cub.2024.07.032
Publication status	Published - 19 Aug 2024

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

PSD-95
SAP102
protein lifetime
protein turnover
proteostasis
sleep
sleep deprivation
synapse
synapse types
synaptome
synaptome architecture

ASJC Scopus subject areas

General Biochemistry,Genetics and Molecular Biology
General Agricultural and Biological Sciences

Access to Document

10.1016/j.cub.2024.07.032Licence: CC BY

Final Published VersionFinal published version, 4.8 MBLicence: CC BY

Cite this

@article{f131e0ec40c14416a44d223c03190c93,

title = "Sleep maintains excitatory synapse diversity in the cortex and hippocampus",

abstract = "Insufficient sleep is a global problem with serious consequences for cognition and mental health. Synapses play a central role in many aspects of cognition, including the crucial function of memory consolidation during sleep. Interference with the normal expression or function of synapse proteins is a cause of cognitive, mood, and other behavioral problems in over 130 brain disorders. Sleep deprivation (SD) has also been reported to alter synapse protein composition and synapse number, although with conflicting results. In our study, we conducted synaptome mapping of excitatory synapses in 125 regions of the mouse brain and found that sleep deprivation selectively reduces synapse diversity in the cortex and in the CA1 region of the hippocampus. Sleep deprivation targeted specific types and subtypes of excitatory synapses while maintaining total synapse density (synapse number/area). Synapse subtypes with longer protein lifetimes exhibited resilience to sleep deprivation, similar to observations in aging and genetic perturbations. Moreover, the altered synaptome architecture affected the responses to neural oscillations, suggesting that sleep plays a vital role in preserving cognitive function by maintaining the brain's synaptome architecture.",

keywords = "PSD-95, SAP102, protein lifetime, protein turnover, proteostasis, sleep, sleep deprivation, synapse, synapse types, synaptome, synaptome architecture",

author = "Dimitra Koukaroudi and Zhen Qiu and Erik Frans{\'e}n and Ragini Gokhale and Edita Bulovaite and Komiyama, \{Noboru H.\} and Julie Seibt and Grant, \{Seth G.N.\}",

note = "{\textcopyright} 2024 The Author(s).",

year = "2024",

month = aug,

day = "19",

doi = "10.1016/j.cub.2024.07.032",

language = "English",

volume = "34",

pages = "3836--3843",

journal = "Current Biology",

issn = "0960-9822",

publisher = "Cell Press",

number = "16",

}

TY - JOUR

T1 - Sleep maintains excitatory synapse diversity in the cortex and hippocampus

AU - Koukaroudi, Dimitra

AU - Qiu, Zhen

AU - Fransén, Erik

AU - Gokhale, Ragini

AU - Bulovaite, Edita

AU - Komiyama, Noboru H.

AU - Seibt, Julie

AU - Grant, Seth G.N.

PY - 2024/8/19

Y1 - 2024/8/19

N2 - Insufficient sleep is a global problem with serious consequences for cognition and mental health. Synapses play a central role in many aspects of cognition, including the crucial function of memory consolidation during sleep. Interference with the normal expression or function of synapse proteins is a cause of cognitive, mood, and other behavioral problems in over 130 brain disorders. Sleep deprivation (SD) has also been reported to alter synapse protein composition and synapse number, although with conflicting results. In our study, we conducted synaptome mapping of excitatory synapses in 125 regions of the mouse brain and found that sleep deprivation selectively reduces synapse diversity in the cortex and in the CA1 region of the hippocampus. Sleep deprivation targeted specific types and subtypes of excitatory synapses while maintaining total synapse density (synapse number/area). Synapse subtypes with longer protein lifetimes exhibited resilience to sleep deprivation, similar to observations in aging and genetic perturbations. Moreover, the altered synaptome architecture affected the responses to neural oscillations, suggesting that sleep plays a vital role in preserving cognitive function by maintaining the brain's synaptome architecture.

AB - Insufficient sleep is a global problem with serious consequences for cognition and mental health. Synapses play a central role in many aspects of cognition, including the crucial function of memory consolidation during sleep. Interference with the normal expression or function of synapse proteins is a cause of cognitive, mood, and other behavioral problems in over 130 brain disorders. Sleep deprivation (SD) has also been reported to alter synapse protein composition and synapse number, although with conflicting results. In our study, we conducted synaptome mapping of excitatory synapses in 125 regions of the mouse brain and found that sleep deprivation selectively reduces synapse diversity in the cortex and in the CA1 region of the hippocampus. Sleep deprivation targeted specific types and subtypes of excitatory synapses while maintaining total synapse density (synapse number/area). Synapse subtypes with longer protein lifetimes exhibited resilience to sleep deprivation, similar to observations in aging and genetic perturbations. Moreover, the altered synaptome architecture affected the responses to neural oscillations, suggesting that sleep plays a vital role in preserving cognitive function by maintaining the brain's synaptome architecture.

KW - PSD-95

KW - SAP102

KW - protein lifetime

KW - protein turnover

KW - proteostasis

KW - sleep

KW - sleep deprivation

KW - synapse

KW - synapse types

KW - synaptome

KW - synaptome architecture

UR - https://www.scopus.com/pages/publications/85201076609

U2 - 10.1016/j.cub.2024.07.032

DO - 10.1016/j.cub.2024.07.032

M3 - Article

C2 - 39096907

SN - 0960-9822

VL - 34

SP - 3836

EP - 3843

JO - Current Biology

JF - Current Biology

IS - 16

ER -

Sleep maintains excitatory synapse diversity in the cortex and hippocampus

Abstract

UN SDGs

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Sleep maintains excitatory synapse diversity in the cortex and hippocampus

Cite this