Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1

Havekes, Robbert; Park, Alan J; Tudor, Jennifer C; Luczak, Vincent G; Hansen, Rolf T; Ferri, Sarah L; Bruinenberg, Vibeke M; Poplawski, Shane G; Day, Jonathan P; Aton, Sara J; Radwańska, Kasia; Meerlo, Peter; Houslay, Miles D; Baillie, George S; Abel, Ted

doi:10.7554/elife.13424

Cited by 292Sleep and Wakefulness ResearchMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1

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Havekes, Robbert, Park, Alan J, Tudor, Jennifer C, Luczak, Vincent G, Hansen, Rolf T, Ferri, Sarah L, Bruinenberg, Vibeke M, Poplawski, Shane G +7 more·2016·eLife

DOI 10.7554/elife.13424PMC PMC4996653

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Abstract

Brief periods of sleep loss have long-lasting consequences such as impaired memory consolidation. Structural changes in synaptic connectivity have been proposed as a substrate of memory storage. Here, we examine the impact of brief periods of sleep deprivation on dendritic structure. In mice, we find that five hours of sleep deprivation decreases dendritic spine numbers selectively in hippocampal area CA1 and increased activity of the filamentous actin severing protein cofilin. Recovery sleep normalizes these structural alterations. Suppression of cofilin function prevents spine loss, deficits in hippocampal synaptic plasticity, and impairments in long-term memory caused by sleep deprivation. The elevated cofilin activity is caused by cAMP-degrading phosphodiesterase-4A5 (PDE4A5), which hampers cAMP-PKA-LIMK signaling. Attenuating PDE4A5 function prevents changes in cAMP-PKA-LIMK-cofilin signaling and cognitive deficits associated with sleep deprivation. Our work demonstrates the necessity of an intact cAMP-PDE4-PKA-LIMK-cofilin activation-signaling pathway for sleep deprivation-induced memory disruption and reduction in hippocampal spine density.

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Sleep dysfunction (including deprivation and fragmentation) is associated with changes in hippocampal morphology and neurogenesis in animal models.
“Experimental studies using animal models have shown that sleep dysfunction (including deprivation and fragmentation) is associated with changes in hippocampal morphology and neurogenesis.”
From Towards an Integrative Account of Potential Mechanisms Mediating the Path From Sleep Dysfunction to Hallucinations (2025) · cites this paper as [88]

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Dendritic spine dynamics in associative memory: A comprehensive review
Guo, H., Ali, T., Que, J., Zhou, Y., & Bai, Y. (2023) · The FASEB Journal · doi:10.1096/fj.202202166r · Cited by 24 · see citing works

The tired hippocampus: the molecular impact of sleep deprivation on hippocampal function
Havekes, R., & Abel, T. G. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.02.005 · Cited by 143 · see citing works
Sleep deprivation impairs cAMP signalling in the hippocampus
(2009) · TUScholarShare (Temple University) · doi:10.34944/dspace/6046
A brief period of sleep deprivation causes spine loss in the dentate gyrus of mice
Raven, F., Meerlo, P., Van der Zee, E. A., Abel, T., & Havekes, R. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.018 · Cited by 96 · see citing works
Sleep deprivation reduces the density of individual spine subtypes in a branch‐specific fashion in CA1 neurons
Bolsius, Y. G., Meerlo, P., Kas, M. J., Abel, T. G., & Havekes, R. (2021) · Journal of Sleep Research · doi:10.1111/jsr.13438 · Cited by 28 · see citing works
Five Hours Total Sleep Deprivation Does Not Affect CA1 Dendritic Length or Spine Density
Brodin, A., Gabulya, S., Wellfelt, K., & Karlsson, T. E. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.854160 · Cited by 5 · see citing works

Authors: Havekes, R., Park, A. J., Tudor, J. C., Luczak, V. G., Hansen, R. T., Ferri, S. L., Bruinenberg, V. M., Poplawski, S. G., Day, J. P., Aton, S. J., Radwańska, K., Meerlo, P., Houslay, M. D., Baillie, G. S., & Abel, T.
Affiliations: University of Groningen (NL)
New York State Psychiatric Institute (US)
University of Pennsylvania (US)
University of Glasgow (GB)
University of Michigan (US)
Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
King's College London (GB)
Corresponding author: Havekes, Robbert
Abel, Ted
ORCID: Havekes, Robbert
Park, Alan J
Tudor, Jennifer C
Luczak, Vincent G
Hansen, Rolf T
Ferri, Sarah L
Poplawski, Shane G
Day, Jonathan P
Aton, Sara J
Radwańska, Kasia
Meerlo, Peter
Houslay, Miles D
Baillie, George S
Abel, Ted
Venue: eLife
Publisher: eLife Sciences Publications, Ltd
Published: 2016-08-23
Volume: 5
ISSN: 2050-084X (ISSN-L)
DOI: 10.7554/elife.13424
PMC: PMC4996653
OpenAlex: W2518307403
Cited by: 292
References: 68
Citations by year: 2026: 35 · 2025: 39 · 2024: 32 · 2023: 28 · 2022: 22 · 2021: 38 · 2020: 37 · 2019: 21 · 2018: 19 · 2017: 18 · 2016: 1
FWCI: 12.39
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
creativecommons.org/licenses/by/4.0/ (am)
creativecommons.org/licenses/by/4.0/ (tdm)
Locations: eLife (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Research Portal (King's College London) (submittedVersion, cc-by)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek (postdoctoral fellowship 825.07.029)
University of Pennsylvania (UPENN rsearch foundation grant)
National Institutes of Health (postdoctoral fellowship, 5K12GM081529, postdoctoral fellowship, T32 NS077413, 1RO1MH086415, RO1AG017628)
European Commission (FP7-PEOPLE-2009-RG-Alco_CaMK)
National Science Centre (Harmonia 2013/08/m/NZ3/00861 Grant)
Medical Research Council (Grant MR/J007412/1)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: sleep deprivation, memory impairment, hippocampal CA1, dendritic spines, cofilin, cAMP signaling, LIM kinase, synaptic plasticity, long-term memory, dendritic morphology, recovery sleep
MeSH terms: Animals, Memory Disorders, Neurons, Sleep Deprivation, Dendritic Spines, Actin Depolymerizing Factors, Mice, Cyclic Nucleotide Phosphodiesterases, Type 4, CA1 Region, Hippocampal

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Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1

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