A brief period of sleep deprivation causes spine loss in the dentate gyrus of mice
Open accessAbstract
Sleep and sleep loss have a profound impact on hippocampal function, leading to memory impairments. Modifications in the strength of synaptic connections directly influences neuronal communication, which is vital for normal brain function, as well as the processing and storage of information. In a recently published study, we found that as little as five hours of sleep deprivation impaired hippocampus-dependent memory consolidation, which was accompanied by a reduction in dendritic spine numbers in hippocampal area CA1. Surprisingly, loss of sleep did not alter the spine density of CA3 neurons. Although sleep deprivation has been reported to affect the function of the dentate gyrus, it is unclear whether a brief period of sleep deprivation impacts spine density in this region. Here, we investigated the impact of a brief period of sleep deprivation on dendritic structure in the dentate gyrus of the dorsal hippocampus. We found that five hours of sleep loss reduces spine density in the dentate gyrus with a prominent effect on branched spines. Interestingly, the inferior blade of the dentate gyrus seems to be more vulnerable in terms of spine loss than the superior blade. This decrease in spine density predominantly in the inferior blade of the dentate gyrus may contribute to the memory deficits observed after sleep loss, as structural reorganization of synaptic networks in this subregion is fundamental for cognitive processes.
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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 [89]
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RetractedLong-Term Potentiation and Memory
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“Likewise, rodent studies investigating the link between sleep and hippocampus-dependent memory consolidation showed that a brief 5–6 h period of SD disrupts the consolidation of contextual fear memories, without affecting hippocampusindependent forms of fear memories (Graves, Heller, Pack, & Abel, 2003; Hagewoud et al…”
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“…dynamics are thought to be crucial for the storage of new information and memory consolidation (De Roo et al., 2008; Lamprecht and LeDoux, 2004; Lamprecht, 2014; Raven et al., 2017) and an impairment of spine dynamics may be an important mechanism of SD-induced memory impairments (Areal,…”
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“Other studies assessing the impact of sleep loss on structural plasticity in the hippocampus found that SD affects the CA1 region (Acosta-Pena et al., 2015; Havekes et al., 2016).”
Sleep and Adult Neurogenesis: Implications for Cognition and Mood
Mueller, A. D., Meerlo, P., McGinty, D., & Mistlberger, R. E. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_251 · Cited by 69 · see citing works
Süer, C., Dolu, N., Artis, A. S., Sahin, L., Yilmaz, A., & Cetin, A. (2011) · Neuroscience Research · doi:10.1016/j.neures.2011.01.008 · Cited by 66 · cited 1× · see citing works
“Long-term REM sleep restriction for 21 days (18 h a day) using the multiple platforms method attenuates LTP in the DG (Suer et al., 2011) and such SD-induced impairments can be prevented by both chronic caffeine treatment and regular exercise (Alhaider and Alkadhi, 2015; Zagaar, Dao, Alhaider, & Alkadhi, 2016).”
MethodHagewoud, R., BULTSMA, L. J., Barf, R. P., Koolhaas, J. M., & Meerlo, P. (2010) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2010.00895.x · Cited by 65 · see citing works
Effects of sleep disruption on rat dentate granule cell LTP in vivo
Marks, C. A., & Wayner, M. J. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.03.018 · Cited by 60 · see citing works
Saletin, J., Goldstein‐Piekarski, A. N., Greer, S. M., Stark, S. M., Stark, C. E. L., & Walker, M. P. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3466-15.2016 · Cited by 59 · see citing works
Dendritic spine dynamics leading to spine elimination after repeated inductions of LTD
Hasegawa, S., Sakuragi, S., Tominaga-Yoshino, K., & Ogura, A. (2015) · Scientific Reports · doi:10.1038/srep07707 · Cited by 55 · see citing works
Ruskin, D. N., Dunn, K. E., Billiot, I., Bazan, N. G., & LaHoste, G. J. (2005) · Life Sciences · doi:10.1016/j.lfs.2005.11.003 · Cited by 53 · see citing works
Compartmentalized PDE4A5 Signaling Impairs Hippocampal Synaptic Plasticity and Long-Term Memory
Havekes, R., Park, A. J., Tolentino, R. E., Bruinenberg, V. M., Tudor, J. C., Lee, Y., Hansen, R., Guercio, L. A., Linton, E. F., Neves, S. R., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0248-16.2016 · Cited by 52 · cited 10× · see citing works
“Strikingly, such changes were absent in area CA3 of the hippocampus (Havekes et al., 2016).”
InfluentialMcPhee, I., Cochran, S. M., & Houslay, M. D. (2001) · Cellular Signalling · doi:10.1016/s0898-6568(01)00217-0 · Cited by 49 · see citing works
Noorafshan, A., Karimi, F., Kamali, A., Karbalay‐Doust, S., & Nami, M. (2017) · Life Sciences · doi:10.1016/j.lfs.2017.09.018 · Cited by 48 · see citing works
Sleep loss disrupts Arc expression in dentate gyrus neurons
Delorme, J. E., Kodoth, V., & Aton, S. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.006 · Cited by 47 · see citing works
Vecsey, C. G., Wimmer, M. E., Havekes, R., Park, A. J., Perron, I. J., Meerlo, P., & Abel, T. G. (2013) · SLEEP · doi:10.5665/sleep.2556 · Cited by 39 · cited 1× · see citing works
“All mice were handled for two minutes on five consecutive days prior to the SD experiment in order to habituate them to the experimenter without affecting synaptic plasticity (Vecsey et al., 2013).”
Zagaar, M. A., Dao, A. T., Alhaider, I. A., & Alkadhi, K. A. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9176-4 · Cited by 37 · cited 2× · see citing works
“Sleep deprivation also reduces the phosphorylation of the cAMP response element-binding protein (pCREB), which is associated with a decrease in synaptic plasticity in the hippocampus (Luo et al., 2013; Vecsey et al., 2009; Zagaar et al., 2016).”
Chapter 1 Genetic Dissection of Neural Circuits and Behavior in Mus musculus
Havekes, R., & Abel, T. G. (2009) · Advances in genetics · doi:10.1016/s0065-2660(09)65001-x · Cited by 35 · cited 1× · see citing works
“Because the DG filters information that enters the hippocampus (Havekes and Abel, 2009), it has been suggested to play a key role in learning, memory and spatial coding (Aimone, Deng, & Gage, 2011).”
Sleep loss and structural plasticity
Areal, C. C., Warby, S. C., & Mongrain, V. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.12.010 · Cited by 35 · see citing works
Chauhan, G., Ray, K., Sahu, S., Roy, K., Jain, V., Wadhwa, M., Panjwani, U., Kishore, K., & Singh, S. B. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.09.007 · Cited by 31 · cited 1× · see citing works
“For example, SD decreases levels of brain-derived neurotrophic factor (BDNF), a molecule essential for memory retrieval and long-term potentiation, in the hippocampus, and importantly, specifically in the DG (Chauhan et al., 2016; Guzman-Marin et al., 2006; Zagaar et al., 2016).”
Alhaider, I. A., & Alkadhi, K. A. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13092 · Cited by 10 · cited 1× · see citing works
“, 2011) and such SD-induced impairments can be prevented by both chronic caffeine treatment and regular exercise (Alhaider and Alkadhi, 2015; Zagaar, Dao, Alhaider, & Alkadhi, 2016).”
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An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity
Carulli, D., & Verhaagen, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052434 · Cited by 123 · see citing works
“Indeed, sleep deprivation, which is known to prevent synaptic modification that occurs in the hippocampus during sleep [177,178], precludes a WFA-PNN decrease and leads to an increase in fear memory extinction [174].”
Relations between sleep patterns early in life and brain development: A review
Lokhandwala, S., & Spencer, R. M. C. (2022) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2022.101130 · Cited by 135 · see citing works
“Sleep has also been associated with increased spine density in hippocampal CA1 and dentate gyrus in mice 2–3 months of age (Havekes et al., 2016; Raven et al., 2019).”
BackgroundCellular and Molecular Differences Between Area CA1 and the Dentate Gyrus of the Hippocampus
Alkadhi, K. A. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1541-2 · Cited by 113 · see citing works
How rhythms of the sleeping brain tune memory and synaptic plasticity
Puentes-Mestril, C., Roach, J. P., Niethard, N., Żochowski, M., & Aton, S. J. (2019) · SLEEP · doi:10.1093/sleep/zsz095 · Cited by 90 · see citing works
Spano, G. M., Banningh, S. W., Marshall, W., de Vivo, L., Bellesi, M., Loschky, S. S., Tononi, G., & Cirelli, C. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0380-19.2019 · Cited by 96 · see citing works
“, 2016) and more limited changes in the dentate gyrus (Raven et al., 2019).”
BackgroundImpact of sleep disturbances on neurodegeneration: Insight from studies in animal models
Owen, J. E., & Veasey, S. C. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104820 · Cited by 90 · see citing works
Delorme, J. E., Wang, L., Kuhn, F. R., Kodoth, V., Ma, J., Martinez, J. D., Raven, F., Toth, B. A., Balendran, V., Vega-Medina, A., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2019318118 · Cited by 77 · see citing works
“It may also contribute to other effects of SD on the dorsal hippocampal network, including disruption of long-term potentiation (4, 5), reduction of plasticity-associated gene expression (19), and decreases in dendritic spine density on pyramidal neurons (5, 48).”
Circadian Rhythms of Perineuronal Net Composition
Pantazopoulos, H., Gisabella, B., Rexrode, L., Benefield, D., Yıldız, E., Seltzer, P., Valeri, J., Chelini, G., Reich, A., Ardelt, M., et al. (2020) · eNeuro · doi:10.1523/eneuro.0034-19.2020 · Cited by 73 · see citing works
“Sleep Deprivation Prevents the Decrease of PNNs During the Day in the Mouse Hippocampus Sleep deprivation by gentle handling has been previously shown to prevent synaptic modification that occurs in the hippocampus during sleep in rodents (Havekes et al., 2016; Raven et al., 2018).”
BackgroundREM Sleep Deprivation Impairs Learning and Memory by Decreasing Brain O-GlcNAc Cycling in Mouse
Kim, S.-M., Zhang, S., Park, J., Sung, H. J., Tran, T.-D. T., Chung, C., & Han, I. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01094-7 · Cited by 69 · see citing works
“Loss of dendritic spines is a common alteration triggered by REMSD [56].”
BackgroundStahn, A. C., & Kühn, S. (2021) · Cognitive Processing · doi:10.1007/s10339-021-01050-5 · Cited by 64 · see citing works
Wong, L., Tann, J. Y., Ibáñez, C. F., & Sajikumar, S. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2876-18.2019 · Cited by 62 · see citing works
“SD has been shown to lead to the loss of dendritic spines in CA1 and dentate gyrus but not CA3 region, although the underlying mechanisms that ac- count for these region-specific changes remain to be investigated (Havekes et al., 2016b; Raven et al., 2019).”
BackgroundLyons, L. C., Vanrobaeys, Y. S., & Abel, T. G. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15787 · Cited by 62 · see citing works
“In mice, studies using Golgi staining to visualize dendritic branches and spines found that 5 h of acute sleep deprivation decreases spine number in the CA1 and dentate gyrus (Havekes et al., 2016; Raven et al., 2019; Wong et al., 2019).”
BackgroundAltered hippocampal transcriptome dynamics following sleep deprivation
Gaine, M. E., Bahl, E., Chatterjee, S., Michaelson, J. J., Abel, T. G., & Lyons, L. C. (2021) · Molecular Brain · doi:10.1186/s13041-021-00835-1 · Cited by 56 · see citing works
A brief period of sleep deprivation leads to subtle changes in mouse gut microbiota
Aidy, S. E., Bolsius, Y. G., Raven, F., & Havekes, R. (2019) · Journal of Sleep Research · doi:10.1111/jsr.12920 · Cited by 50 · see citing works
Sleep loss disrupts Arc expression in dentate gyrus neurons
Delorme, J. E., Kodoth, V., & Aton, S. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.006 · Cited by 47 · see citing works
“show that spine density in DG granule cells is reduced after 5 h of SD (Raven et al., 2018).”
Weiss, J. T., & Donlea, J. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.777799 · Cited by 47 · see citing works
“Similarly, sleep deprivation leads to decreased spine density in the dentate gyrus (Raven et al., 2019), and disrupts the formation of new spines following learning (Yang et al.”
BackgroundImpacts of Sleep Loss versus Waking Experience on Brain Plasticity: Parallel or Orthogonal?
Havekes, R., & Aton, S. J. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.03.010 · Cited by 39 · see citing works
“, [18,20]) and dentate gyrus (DG) granule cells [26] (for a review, see [27]).”
BackgroundTranslational changes induced by acute sleep deprivation uncovered by TRAP-Seq
Lyons, L. C., Chatterjee, S., Vanrobaeys, Y. S., Gaine, M. E., & Abel, T. G. (2020) · Molecular Brain · doi:10.1186/s13041-020-00702-5 · Cited by 39 · see citing works
Neurocognitive Effects of Sleep Disruption in Children and Adolescents
Spruyt, K. (2020) · Child and Adolescent Psychiatric Clinics of North America · doi:10.1016/j.chc.2020.08.003 · Cited by 39 · see citing works
Suresh, K., Raavi, V., Kumar, M. H., & Shankar, V. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107559 · Cited by 38 · see citing works
Experience and sleep-dependent synaptic plasticity: from structure to activity
Sun, L., Zhou, H., Cichon, J., & Yang, G. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0234 · Cited by 37 · see citing works
“Consistent with this, sleep has been associated with increased spine density in hippocampal CA1 and dentate gyrus in mice at two to three months of age, though no effect of sleep loss is detected in CA3 [12,13].”
BackgroundInfluentialDelorme, J. E., Wang, L., Kodoth, V., Wang, Y., Ma, J., Jiang, S., & Aton, S. J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2108534118 · Cited by 34 · see citing works
“Indeed, sleep loss seems to disrupt plasticity mechanisms within the hippocampus more dramatically than in other brain areas (41, 69).”
BackgroundRecovering object-location memories after sleep deprivation-induced amnesia
Bolsius, Y. G., Heckman, P. R. A., Paraciani, C., Wilhelm, S. A., Raven, F., Meijer, E. L., Kas, M. J., Ramirez, S., Meerlo, P., & Havekes, R. (2022) · Current Biology · doi:10.1016/j.cub.2022.12.006 · Cited by 33 · see citing works
Sleep, brain vascular health and ageing
Mahalakshmi, A. M., Ray, B., Tuladhar, S., Bhat, A., Bishir, M., Bolla, S. R., Yang, J. P., Essa, M. M., Chidambaram, S. B., Guillemin, G. J., et al. (2020) · GeroScience · doi:10.1007/s11357-020-00235-8 · Cited by 31 · see citing works
Puentes-Mestril, C., Delorme, J. E., Wang, L., Donnelly, M. J., Popke, D. S., Jiang, S., & Aton, S. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1883-20.2021 · Cited by 29 · see citing works
“In hippocampal structures such as the DG and CA1, available data suggest that both markers of neuronal activity and synaptic plasticity are disrupted after SD (Havekes et al., 2016; Tudor et al., 2016; Ognjanovski et al., 2018; Delorme et al., 2019; Raven et al., 2019).”
BackgroundRaven, F., Heckman, P. R. A., Havekes, R., & Meerlo, P. (2019) · Journal of Sleep Research · doi:10.1111/jsr.12972 · Cited by 28 · see citing works
“In both experiments, mice were sleep deprived using the gentle stimulation method (Havekes et al., 2016; Prince & Abel, 2013; Raven et al., 2019; van der Borght et al., 2006).”
MethodBolsius, 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
“Mice were sleep deprived for 5 h at the start of the lights-on period (7:00 a.m.) using the gentle handling method (Havekes & Aton, 2020; Havekes et al., 2016; Raven et al., 2019).”
InfluentialSuresh, K., Raavi, V., Kumar, M. H., & Shankar, V. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.12.002 · Cited by 27 · see citing works
“The dendritic spines of both CA1 and dentate gyrus (DG) regions of the hippocampus were reduced in 5 h sleep-deprived mice (Havekes et al., 2016; Raven et al., 2019).”
BackgroundPicard, K., Corsi, G., Decoeur, F., Castro, M. A. D., Bordeleau, M., Persillet, M., Layé, S., Limatola, C., Tremblay, M., & Nadjar, A. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.09.016 · Cited by 26 · see citing works
Effect of Electroacupuncture at GV20 on Sleep Deprivation‐Induced Depression‐Like Behavior in Mice
Xu, X., Zheng, P., Zhao, H., Song, B., & Wang, F. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/7481813 · Cited by 25 · see citing works
“48h S-Dep was associated with dramatically reduced BDNF expression in the CA1, CA3, and dentate gyrus (DG) of the hippocampus, accompanied by attenuated Ca/calmodulindependent protein kinase II (CAMKII) and the cAMP response element binding protein (CREB) expression and mitigated CREB phosphorylation [32, 33].”
BackgroundThe Engram’s Dark Horse: How Interneurons Regulate State-Dependent Memory Processing and Plasticity
Raven, F., & Aton, S. J. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.750541 · Cited by 27 · see citing works
Sleep-mediated regulation of reward circuits: implications in substance use disorders
Guo, R., Vaughan, D. T., Rojo, A. L. A., & Huang, Y. H. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01356-8 · Cited by 24 · see citing works
Post-learning micro- and macro-structural neuroplasticity changes with time and sleep
Stee, W., & Peigneux, P. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114369 · Cited by 24 · see citing works
Seidler, R. D., Stern, C., Basner, M., Stahn, A. C., Wuyts, F. L., & zu Eulenburg, P. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.876789 · Cited by 22 · see citing works
“, 2014), sleep deprivation (Raven et al., 2019), and isolation and confinement (Cinini et al.”
BackgroundStahn, A. C., Bucher, D., zu Eulenburg, P., Denise, P., Smith, N., Pagnini, F., & White, O. (2023) · npj Microgravity · doi:10.1038/s41526-023-00295-y · Cited by 22 · see citing works
Wang, L., Park, L. M., Wu, W.-S., King, D., Vega-Medina, A., Raven, F., Martinez, J. D., Ensing, A., McDonald, K., Yang, Z., et al. (2024) · iScience · doi:10.1016/j.isci.2024.109408 · Cited by 21 · see citing works
“…data, which have found disruptions in these pathways after SD, either across the hippocampus as a whole, or specifically within the DG. 12,15,47,48 Since both actin cytoskeletal remodeling and ribosomal biogenesis are critically associated with memory storage in the hippocampus, 12,15,49,50…”
BackgroundAhnaou, A., & Drinkenburg, W. H. I. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.039 · Cited by 23 · see citing works
Molecular Mechanisms of Memory Consolidation That Operate During Sleep
Reyes‐Resina, I., Samer, S., Kreutz, M. R., & Oelschlegel, A. M. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.767384 · Cited by 19 · see citing works
“Somewhat conflicting results have been described for the hippocampus (mostly focused on Cornu Ammonis 1, CA1), as some studies found a decrease in spine number after SD compared to a period of undisturbed sleep (Havekes et al., 2016; Raven et al., 2019; Wong et al., 2019), while others reported that spine number (Iked…”
BackgroundA short-term memory trace persists for days in the mouse hippocampus
Wally, M. E., Nomoto, M., Abdou, K., Murayama, E., & Inokuchi, K. (2022) · Communications Biology · doi:10.1038/s42003-022-04167-1 · Cited by 20 · see citing works
Heckman, P. R. A., Kuhn, F. R., Raven, F., Bolsius, Y. G., Prickaerts, J., Meerlo, P., & Havekes, R. (2020) · Synapse · doi:10.1002/syn.22150 · Cited by 16 · see citing works
Walsh, E. N., Shetty, M. S., Diba, K., & Abel, T. G. (2022) · eNeuro · doi:10.1523/eneuro.0380-22.2022 · Cited by 15 · see citing works
Structural synaptic plasticity across sleep and wake
Bellesi, M., & de Vivo, L. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.12.007 · Cited by 15 · see citing works
“Since then, the study of sleep-dependent structural plasticity has gained much attention and multiple research groups measured spine density and turnover across sleep, wake and sleep deprivation in the hippocampus [17–19], dentate gyrus [20,21], prefrontal cortex [18,22], somatosensory and motor cortex [23,24,25 ] fin…”
The role of calcium and CaMKII in sleep
Wang, Y., Minami, Y., Ode, K. L., & Ueda, H. R. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.1059421 · Cited by 14 · see citing works
“Also, sleep deprivation decreased dendritic spine numbers in hippocampal CA1 but not in CA3 in mice (Havekes et al., 2016; Raven et al., 2019).”
BackgroundPittner, K., Rasmussen, J. M., Lim, M. M., Gilmore, J. H., Styner, M. A., Entringer, S., Wadhwa, P. D., & Buß, C. (2023) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2023.100091 · Cited by 15 · see citing works
Zhao, H., Blokland, A., Prickaerts, J., Havekes, R., & Heckman, P. R. A. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114798 · Cited by 13 · see citing works
“Interestingly, within the hippocampus, the dentate gyrus (DG) is particularly vulnerable to the effects of SD [20].”
BackgroundGisabella, B., Babu, J., Valeri, J., Rexrode, L., & Pantazopoulos, H. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.646678 · Cited by 13 · see citing works
“Furthermore, sleep deprivation results in decreases of dendritic spines (Raven et al., 2019) as well as the number of granule cells expressing the immediate early gene Arc in the mouse dentate gyrus (Delorme et al., 2019).”
BackgroundYang, X., Cao, Z., Zhang, J., Shao, B., Song, M., Han, Y., & Li, Y. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.09.145 · Cited by 13 · see citing works
Regulation of dendritic spines in the amygdala following sleep deprivation
Rexrode, L., Tennin, M., Babu, J., Young, C., Bollavarapu, R., Lawson, L. A., Valeri, J., Pantazopoulos, H., & Gisabella, B. (2023) · Frontiers in Sleep · doi:10.3389/frsle.2023.1145203 · Cited by 12 · see citing works
“Studies from other groups also point to hippocampal subregion and branch specific changes, with evidence for upscaling of spines during sleep in the dentate gyrus and in the very distal apical branches of CA1 neurons (Raven et al., 2019; Bolsius et al., 2022).”
BackgroundYun, S., Soler, I., Tran, F. H., Haas, H. A., Shi, R., Bancroft, G. L., Suarez, M., de Santis, C. R., Reynolds, R. P., & Eisch, A. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1151877 · Cited by 6 · see citing works
“inferior blades of the DG as there are functional differences between these aspects of the DG GCL (Collins et al., 2009; Jinno, 2011; Raber et al., 2011; Alves et al., 2018; Raven et al., 2019).”
BackgroundInfluentialRaven, F., Vega-Medina, A., Schmidt, K., He, A., Vankampen, A. A., Balendran, V., & Aton, S. J. (2025) · SLEEP · doi:10.1093/sleep/zsaf064 · Cited by 11 · see citing works
Renormalizing synapses in sleep: The clock is ticking
Frank, M. G. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114533 · Cited by 10 · see citing works
Sleep deprivation and dendritic architecture: a systematic review and meta-analysis
Brodin, A., Liesecke, F., Spielbauer, J., & Karlsson, T. E. (2025) · SLEEP · doi:10.1093/sleep/zsaf146 · Cited by 8 · see citing works
“Hippocampal dendritic spine density has been found to either increase [27], decrease [28, 29], or remain unchanged [30] after SD.”
Raven, F., Vankampen, A. A., He, A., & Aton, S. J. (2026) · iScience · doi:10.1016/j.isci.2026.115067 · Cited by 5 · see citing works
“19,33 DG PV+ interneuron activation also disrupts OLM encoding.”
Coulson, R. L., Mourrain, P., & Wang, G. X. (2024) · Journal of Comparative Physiology B · doi:10.1007/s00360-023-01531-3 · Cited by 7 · see citing works
“…and gene expression, redox metabolism, DNA damage repair, dendritic spine density, and synaptic plasticity (Vecsey et al. 2009; Narwade et al. 2017; Trivedi et al. 2017; Cedernaes et al. 2018; Ämmälä et al. 2019; Cheung et al. 2019; Raven et al. 2019; Coulson et al. 2022; Vanrobaeys et al. 2023).”
BackgroundSheaves, B., Cropley, V. L., Moseley, P., Woodruff, P. W. R., Punton, G., Speth, C., Speth, J., Meerlo, P., & Brederoo, S. G. (2025) · Schizophrenia Bulletin · doi:10.1093/schbul/sbaf107 · Cited by 6 · see citing works
Moderate chronic sleep perturbation impairs glucose and lipid homeostasis in rats
Tonet, N. S., Marçal, D. F. D. S., da Silva, F. N., Brunetta, H. S., Mori, M. A., dos Santos, G. J., Moreira, E. L. G., & Rafacho, A. (2024) · SLEEP · doi:10.1093/sleep/zsae118 · Cited by 6 · see citing works
García‐Aviles, J. E., Avilez-Avilez, J. J., Sánchez-Hernández, J., Patlán-Márquez, C., Rodríguez-Alpízar, J., Becerril-Mercado, F. M., Jiménez, A., Guerrero‐Vargas, N. N., Morin, J., Rodríguez-García, M., et al. (2025) · Neurochemical Research · doi:10.1007/s11064-025-04561-1 · Cited by 6 · see citing works
Excitatory/Inhibitory imbalance as a mechanism linking autism and sleep problems
Bridi, M., & Peixoto, L. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2024.102968 · Cited by 6 · see citing works
Czarnecki, P., Lin, J. J., Aton, S. J., & Żochowski, M. (2021) · Frontiers in Network Physiology · doi:10.3389/fnetp.2021.759131 · Cited by 6 · see citing works
“In contrast, sleep deprivation was associated with the disruption of the strengthening of glutamatergic synapses, and the reduction of dendritic spines in CA1 and DG pyramidal neurons of hippocampus (Havekes et al., 2016; Raven et al., 2019).”
Optical imaging and manipulation of sleeping-brain dynamics in memory processing
Miyamoto, D. (2022) · Neuroscience Research · doi:10.1016/j.neures.2022.04.005 · Cited by 6 · 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
Chen, T., Jia, J., Gao, C., Zhong, Q., Tang, L., Sui, X., Li, S., Chen, C., & Zhang, Z. (2025) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2025.111397 · Cited by 4 · see citing works
“To address these gaps, this study investigates the effects of chronic sleep deprivation on both the transcriptome and metabolome of the hippocampus, a brain region particularly vulnerable to sleep disturbances(Raven et al., 2019).”
Picard, K., Dolhan, K., Watters, J. J., & Tremblay, M. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-55529-9_20 · Cited by 4 · see citing works
Kelly, M. P., Heckman, P. R. A., & Havekes, R. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101799 · Cited by 4 · see citing works
NLM Special Issue on Sleep and hippocampal function
Havekes, R., Aton, S. J., Tudor, J. C., & Meerlo, P. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.03.009 · Cited by 4 · see citing works
Wang, H. Y., Mao, X., Liu, S., Zhang, J., Li, E., Song, Y., Li, H., Chang, L., & Wu, Y. (2025) · Journal of Alzheimer s Disease Reports · doi:10.1177/25424823251391704 · Cited by 3 · see citing works
Zeng, S., Liu, N., Zhang, A., Duan, N., Xu, B., & Ai, C. (2025) · BMC Psychiatry · doi:10.1186/s12888-024-06395-7 · Cited by 3 · see citing works
Acute sleep loss impairs object but not spatial pattern separation in humans
Blokland, A., Jackson, M. S., Puustinen, K., Soeterboek, J., & Heckman, P. R. A. (2023) · Neuroscience Letters · doi:10.1016/j.neulet.2023.137535 · Cited by 3 · see citing works
“Similar differences in sensitivity to acute sleep loss in mice have been observed for different hippocampal subregions [19,31 – 33].”
Neurocognitive Effects of Sleep Disruption in Children and Adolescents
Spruyt, K. (2024) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2023.06.003 · Cited by 3 · see citing works
Sleep and memory: Elucidating the effects of sleep deprivation on different types of memory
Sarma, A., & Havekes, R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00048-1 · Cited by 4 · see citing works
Heckman, P. R. A., Havekes, R., & Blokland, A. (2025) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2025.108054 · Cited by 2 · see citing works
“…recent years using animal models (Giri et al., 2024; Havekes, Park, Tolentino, et al., 2016; Havekes, Park, Tudor, et al., 2016; Heckman et al., 2020; Poe & Donlea, 2023; Raven et al., 2020; Raven et al., 2018; Tudor et al., 2016; Vanrobaeys et al., 2023; Vecsey et al., 2009; Zhao et al., 2024).”
Lim, C. R., Ogawa, S., & Kumari, Y. (2024) · Archives of Pharmacal Research · doi:10.1007/s12272-024-01523-z · Cited by 2 · see citing works
“Indeed, some research suggests that sleep deprivation attenuates hippocampal dendritic spine density (Raven et al. 2019; Bolsius et al. 2022), but the overall literature appears to be inconclusive, potentially confounded by differences in sleep deprivation protocol-induced stress (Brodin et al.…”
Ochai, J., Umana, U. E., Musa, S. A., & Oladele, S. B. (2024) · Journal of Experimental and Clinical Anatomy · doi:10.4314/jeca.v21i2.15 · Cited by 1 · see citing works
“Lack of sleep has been demonstrated to significantly affect the hippocampal cell count estimation (Suntsova, 2003; Havekes et al ., 2016; Raven et al ., 2019).”
Sarma, A., Ronde, M., Smit, S., Meerlo, P., & Havekes, R. (2025) · Journal of Sleep Research · doi:10.1111/jsr.70079 · Cited by 1 · see citing works
Balendran, V., Liu, J., Wu, K., Dong, A., & Aton, S. J. (2026) · SLEEP · doi:10.1093/sleep/zsag047 · Cited by 2 · see citing works
“Because previous studies indicate a link between dendritic spine size and excitatory synapse strength [ 64, 68, 69], our f indings therefore suggest that 6 h of post-CFC SD substantially reduces the strength of individual excitatory inputs to SST + interneurons in LEC, but not MEC.”
Repeated sleep deprivation selectively reactivates hippocampal CA1 pyramidal neurons
Wang, Y., Walsh, E. N., Kasuya, J., Remedies, C. E., Resch, J. M., Lyons, L. C., & Abel, T. G. (2026) · Molecular Brain · doi:10.1186/s13041-026-01298-y · Cited by 1 · see citing works
Insomnia and Cognitive Functions: Focus on Neurobiological Mechanisms
Janjic, V., Djoković, D., Muric, M. D., Fetahović, E., Radmanović, B., Barać, S., Čolović, S., Radmanović, O., & Muric, N. N. (2026) · Psychiatry International · doi:10.3390/psychiatryint7020070 · Cited by 2 · see citing works
“…short period of SD reduced spine density in dentate granule cells, especially in the inferior blade of the dentate gyrus, suggesting that different hippocampal subregions may vary in vulnerability to sleep loss and that these structural changes may contribute to impaired memory consolidation [142].”
Baghdad, W., Brouzi, M. Y. E., Ibouzine‐Dine, L., Abouyaala, O., Arbaoui, M. E., Kessam, F. Z., Dimaoui, A., Mallouk, H., Lamtai, M., Satté, A., et al. (2026) · Neurochemical Research · doi:10.1007/s11064-026-04788-6 · Cited by 2 · see citing works
“The density of dendritic spines in the CA1 and dentate gyrus (DG) regions of the HP was reduced in mice subjected to SD for 5 h [ 21].”
Suresh, K., Raavi, V., Shankar, V., Jagadish, T. V., Kavyashree, H. M., & Sriram, N. (2026) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2026.104106 · Cited by 2 · see citing works
Dreaming reflects neural resynchronization after sleep-dependent neuroplastic adaptations.
Schulze, H. G. (2023) · Dreaming · doi:10.1037/drm0000250 · Cited by 1 · see citing works
Effect of chronic sleep restriction on ethanol preference and cortical structural plasticity
Bravo-González, F., Acosta-Hernández, M. E., Tendilla‐Beltrán, H., Flores, G., & García‐García, F. (2025) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2025.100126 · Cited by 1 · see citing works
“Similarly, the hippocampus experiences synaptic remodeling, characterized by reduced dendritic complexity and spine density, particularly in CA1 pyramidal neurons that are vital for learning and memory processes (Acosta-Pe ˜ na et al., 2015; Huang et al., 2022; Raven et al., 2019).”
Sleep and Hippocampal Memory Consolidation
Walsh, E. N., & Abel, T. G. (2025) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190069162.013.12 · Cited by 1 · see citing works
Paraciani, C., Havekes, R., Meerlo, P., & Gervais, N. J. (2025) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2025.101205 · Cited by 1 · see citing works
“Most studies show decreased density of spines following 5 – 12 h of total SD, with effects observed in the CA1 (Acosta-pe ˜ na et al., 2015; Bolsius et al., 2022; Havekes et al., 2016; Wong et al., 2019) and DG (Raven et al., 2019).”
Delorme, J. E., Wang, L., Kodoth, V., Wang, Y., Ma, J., Jiang, S., & Aton, S. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.27.221218 · Cited by 1 · see citing works
“Indeed, sleep loss seems to disrupt plasticity mechanisms within the hippocampus more dramatically than in other brain areas (Delorme et al., 2019; Raven et al., 2019).”
BackgroundDelorme, J. E., Kuhn, F. R., Wang, L., Kodoth, V., Ma, J., Jiang, S., & Aton, S. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.02.233080
“…hippocampal network, including disruption of long-term potentiation (LTP) (Havekes et al., 2016; Vecsey et al., 2009), reduction of plasticity-associated gene expression (Delorme et al., 2019), and decreases in dendritic spine density on pyramidal neurons (Havekes et al., 2016; Raven et al., 2019).”
BackgroundSleep Deprivation: Its Neural Circuits and Influence on Memory
Li, J. (2023) · Berkeley Scientific Journal · doi:10.5070/bs327262051
Latent mechanisms of plasticity are upregulated during sleep
Menarchek, B. J., & Bridi, M. (2025) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2025.103029
Activity-regulated circSamm50 modulates mitochondrial dynamics and spine structural plasticity
Chanda, K., Bapat, O., Wingfield, J. L., Avchalumov, Y., Kazantzis, M., Carter, J., Sharma, N., Davis, R. L., Yuan, J. X. ‐., Rangaraju, V., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117378
The Growth of the Brain in a Changing Environment
Biesalski, H. K. (2025) · Springer eBooks · doi:10.1007/978-3-031-99121-9_10
Additional file 1 of Altered hippocampal transcriptome dynamics following sleep deprivation
Gaine, M. E., Bahl, E., Chatterjee, S., Michaelson, J. J., Abel, T. G., & Lyons, L. C. (2021) · Figshare · doi:10.6084/m9.figshare.15161928
Additional file 1 of Translational changes induced by acute sleep deprivation uncovered by TRAP-Seq
Lyons, L. C., Chatterjee, S., Vanrobaeys, Y. S., Gaine, M. E., & Abel, T. G. (2020) · Figshare · doi:10.6084/m9.figshare.13331631
Recharge, reboot, rewire: sleep optimizes information processing in neural circuits
Aton, S. J. (2026) · SLEEP · doi:10.1093/sleep/zsag146 · Cited by 1 · see citing works
“Conversely, other studies have found that DG granule cells’ and CA1 pyramidal neurons’ dendritic spine density decreases after a few hours of gentle handling SD [ 104, 105]—a change driven by differential regulation of the actin cytoskeleton by sleep vs. SD [ 104] ( Figure 4, right ).”
Ma, J., Braun, A., Oskamp, A., Kricsfalussy-Hrabár, L., Hermes, N., Djakkani, S., Holz, U., Jakobs, S., Klein, S., Stüsgen, S., et al. (2026) · iScience · doi:10.1016/j.isci.2026.116676
Wu, J. T., Sun, J., Li, M., Wang, H., Lu, G., Guo, C., Jia, K., & Zhang, M. (2026) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2026.1857669
“Multiple studies have shown that sleep deprivation reduces the number of dendritic spines in the hippocampus and the expression of activity-dependent proteins, thereby impairing synaptic plasticity (Raven et al., 2019; Delorme et al., 2019).”
Liu, X., Lin, H., Zhong, J., Chen, X., Wang, Z., Shi, M., Shi, H., Zhang, H., Chen, P., & Ye, Z. (2026) · CNS Neuroscience & Therapeutics · doi:10.1002/cns.71134
“These findings indicate a region-specific vulnerability of hippocampal synapses to sleep deprivation, consistent with prior studies [22, 40–42].”
Ezgin, N. (2026) · Arşiv Kaynak Tarama Dergisi · doi:10.17827/aktd.1833648
- Authors
- Raven, F., Meerlo, P., Van der Zee, E. A., Abel, T., & Havekes, R.
- Affiliations
- University of Groningen (NL)
- University of Iowa (US)
- Corresponding author
- Havekes, Robbert
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2019-04
- Volume
- 160
- Pages
- 83-90
- ISSN
- 1074-7427 (ISSN-L)
- PMC
- PMC6420875
- OpenAlex
- W2794305595
- Cited by
- 96
- References
- 86
- Citations by year
- 2026: 12 · 2025: 15 · 2024: 8 · 2023: 9 · 2022: 12 · 2021: 16 · 2020: 14 · 2019: 8 · 2018: 2
- FWCI
- 5.95
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neurobiology of Learning and Memory (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by-nc-nd)
- Funders
- Human Frontiers Science Program Organization (RGY0063/2017)
- 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, dendritic spines, dentate gyrus, hippocampus, synaptic plasticity, memory consolidation, hippocampal CA1, CA3, memory impairment
- MeSH terms
- Animals, Cell Count, Male, Mice, Inbred C57BL, Sleep Deprivation, Dentate Gyrus, Dendritic Spines, Mice
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