Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms

Havekes, Robbert; Meerlo, Peter; Abel, Ted

doi:10.1007/7854_2015_369

Cited by 78Sleep and Wakefulness ResearchMemory and Neural MechanismsSleep and Work-Related Fatigue

Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms

Havekes, Robbert, Meerlo, Peter, Abel, Ted·2015·Current Topics in Behavioral Neurosciences

DOI 10.1007/7854_2015_369

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Abstract

Although the exact functions of sleep remain a topic of debate, several hypotheses propose that sleep benefits neuronal plasticity, which ultimately supports brain function and cognition . For over a century, researchers have applied a wide variety of behavioral, electrophysiological, biochemical, and molecular approaches to study how memory processes are promoted by sleep and perturbed by sleep loss. Interestingly, experimental studies indicate that cognitive impairments as a consequence of sleep deprivation appear to be most severe with learning and memory processes that require the hippocampus , which suggests that this brain region is particularly sensitive to the consequences of sleep loss. Moreover, recent studies in laboratory rodents indicate that sleep deprivation impairs hippocampal neuronal plasticity and memory processes by attenuating intracellular cyclic adenosine monophosphate (cAMP)-protein kinase A (PKA) signaling. Attenuated cAMP-PKA signaling can lead to a reduced activity of the transcription factor cAMP response element binding protein (CREB) and ultimately affect the expression of genes and proteins involved in neuronal plasticity and memory formation. Pharmacogenetic experiments in mice show that memory deficits following sleep deprivation can be prevented by specifically boosting cAMP signaling in excitatory neurons of the hippocampus. Given the high incidence of sleep disturbance and sleep restriction in our 24/7 society, understanding the consequences of sleep loss and unraveling the underlying molecular mechanisms is of great importance.

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Many selective synaptic pruning and refinement processes occur during sleep, and sleep is crucial for proper circuit maturation and long-term memory formation in humans and animals.
“Many of these selective synaptic pruning and refinement processes occur during sleep, and sleep is crucial for proper circuit maturation and long-term memory formation in humans and animals201–204.”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [203]

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Yang, R., Hu, S.-J., Wang, Y., Zhang, W., Luo, W., & Chen, J. (2008) · Brain Research · doi:10.1016/j.brainres.2008.07.033 · Cited by 80 · see citing works
Glucocorticoids Are Not Responsible for Paradoxical Sleep Deprivation-Induced Memory Impairments
Tiba, P. A., Oliveira, M. G. D. M., Rossi, V. C., Tufik, S., & Suchecki, D. (2008) · SLEEP · doi:10.1093/sleep/31.4.505 · Cited by 80 · see citing works
Sustained sleep fragmentation results in delayed changes in hippocampal-dependent cognitive function associated with reduced dentate gyrus neurogenesis
Sportiche, N., Suntsova, N., Methippara, M. M., Bashir, T., Mitrani, B., Szymusiak, R. S., & McGinty, D. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.06.038 · Cited by 76 · see citing works
Transgenic Inhibition of Neuronal Protein Kinase A Activity Facilitates Fear Extinction
Isiegas, C., Park, A., Kandel, E. R., Abel, T. G., & Lattal, K. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2743-06.2006 · Cited by 73 · see citing works
Self-citation
Transiently Increasing cAMP Levels Selectively in Hippocampal Excitatory Neurons during Sleep Deprivation Prevents Memory Deficits Caused by Sleep Loss
Havekes, R., Bruinenberg, V. M., Tudor, J. C., Ferri, S. L., Baumann, A., Meerlo, P., & Abel, T. G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2403-14.2014 · Cited by 73 · see citing works
Self-citation
REM restriction persistently alters strategy used to solve a spatial taskPreprint
Bjorness, T. E., Riley, B. T., Tysor, M. K., & Poe, G. R. (2005) · Learning & Memory · doi:10.1101/lm.84805 · Cited by 69 · see citing works
Antidepressant Suppression of Non-REM Sleep Spindles and REM Sleep Impairs Hippocampus-Dependent Learning While Augmenting Striatum-Dependent Learning
Watts, A., Gritton, H. J., Sweigart, J., & Poe, G. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0170-12.2012 · Cited by 68 · see citing works
Sleep deprivation impairs contextual fear conditioning and attenuates subsequent behavioural, endocrine and neuronal responses
Hagewoud, 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
Self-citation
Sleep Modulates the Neural Substrates of Both Spatial and Contextual Memory Consolidation
Rauchs, G., Orban, P., Schmidt, C., Albouy, G., Balteau, E., Degueldre, C., Schnackers, C., Virginie Sterpenich, A., Tinguely, G., Luxen, A., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002949 · Cited by 62 · see citing works
Role of the dorsal hippocampus in object memory load
Sannino, S., Russo, F., Torromino, G., Pendolino, V., Calabresi, P., & De Leonibus, E. (2012) · Learning & Memory · doi:10.1101/lm.025213.111 · Cited by 57 · see citing works
Eliminating the adrenal stress response does not affect sleep deprivation-induced acquisition deficits in the water maze
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
Spatial and reversal learning in the Morris water maze are largely resistant to six hours of REM sleep deprivation following trainingPreprint
Walsh, C. M., Booth, V., & Poe, G. R. (2011) · Learning & Memory · doi:10.1101/lm.2099011 · Cited by 53 · see citing works
A new automated method for rat sleep deprivation with minimal confounding effects on corticosterone and locomotor activity
Leenaars, C. H. C., Demattéis, M., Joosten, R. N. J. M. A., Eggels, L., Sandberg, H., Schirris, M., Feenstra, M. G. P., & Someren, E. J. W. V. (2011) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2011.01.014 · Cited by 45 · see citing works
Calcineurin contributes to spatial memory impairment induced by rapid eye movement sleep deprivation
Wang, G.-P., Huang, L., Wu, H., Zhang, L., You, Z.-D., & Zhao, Z. (2009) · Neuroreport · doi:10.1097/wnr.0b013e32832f0772 · Cited by 44 · see citing works
The effects of rapid eye movement sleep deprivation and recovery on spatial reference memory of young rats
Li, S., Tian, Y., Ding, Y., Jin, X., Yan, C., & Shen, X. (2009) · Learning & Behavior · doi:10.3758/lb.37.3.246 · Cited by 42 · see citing works
NR2A at CA1 Synapses Is Obligatory for the Susceptibility of Hippocampal Plasticity to Sleep Loss
Longordo, F., Kopp, C., Mishina, M., Luján, R., & Lüthi, A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1215-09.2009 · Cited by 42 · see citing works
Sleep deprivation impairs emotional memory retrieval in mice: Influence of sex
Fernandes‐Santos, L., Patti, C. L., Zanin, K. A., Fernandes, H. A., Tufik, S. B., Andersen, M. L., & Frussa‐Filho, R. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.03.014 · Cited by 40 · see citing works
Effect of Valproic Acid Through Regulation of NMDA Receptor–ERK Signaling in Sleep Deprivation Rats
Park, H. J., Kang, W. S., Paik, J., & Kim, J. W. (2011) · Journal of Molecular Neuroscience · doi:10.1007/s12031-011-9673-5 · Cited by 33 · see citing works
Sleep deprivation alters phosphorylated CREB levels in the amygdala: Relationship with performance in a fear conditioning task
de Pinho, N. C., Moreira, K. D. M., Hipólide, D. C., Sinigaglia‐Coimbra, R., Ferreira, T. L., Nóbrega, J. N., Tufik, S., & Oliveira, M. G. M. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.043 · Cited by 19 · see citing works
Reduced-volume cues effectively support fear conditioning despite sleep deprivation
Ruskin, D. N., & LaHoste, G. J. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.08.014 · Cited by 9 · see citing works

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Rhythms of life: circadian disruption and brain disorders across the lifespan
Logan, R. W., & McClung, C. A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0088-y · Cited by 713 · see citing works
The role of sleep in regulating structural plasticity and synaptic strength: implications for memory and cognitive function
Raven, F., Van der Zee, E. A., Meerlo, P., & Havekes, R. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.05.002 · Cited by 331 · see citing works
Self-citation
Sleep research goes wild: new methods and approaches to investigate the ecology, evolution and functions of sleep
Rattenborg, N. C., de la Iglesia, H. O., Kempenaers, B., Lesku, J. A., Meerlo, P., & Scriba, M. F. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0251 · Cited by 184 · see citing works
Self-citation
Global and local complexity of intracranial EEG decreases during NREM sleep
Schartner, M. M., Pigorini, A., Gibbs, S. A., Arnulfo, G., Sarasso, S., Barnett, L., Nobili, L., Massimini, M., Seth, A. K., & Barrett, A. B. (2017) · Neuroscience of Consciousness · doi:10.1093/nc/niw022 · Cited by 128 · see citing works
REM Sleep Is Causal to Successful Consolidation of Dangerous and Safety Stimuli and Reduces Return of Fear after Extinction
Menz, M. M., Rihm, J. S., & Büchel, C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3083-15.2016 · Cited by 99 · see citing works
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
“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…”
Self-citation
Role of Protein Kinase C in Bipolar Disorder: A Review of the Current Literature
Saxena, A., Scaini, G., Bavaresco, D. V., Leite, C., Valvassoria, S. S., Carvalho, A. F., & Quevedo, J. (2017) · Complex Psychiatry · doi:10.1159/000480349 · Cited by 85 · see citing works
Neurochemical mechanisms for memory processing during sleep: basic findings in humans and neuropsychiatric implications
Feld, G. B., & Jan Born, A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0490-9 · Cited by 79 · see citing works
The beneficial role of memory reactivation for language learning during sleep: A review
Schreiner, T., & Rasch, B. (2016) · Brain and Language · doi:10.1016/j.bandl.2016.02.005 · Cited by 72 · see citing works
REM 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
Sleep and hippocampal neurogenesis: Implications for Alzheimer’s disease
Kent, B. A., & Mistlberger, R. E. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.02.004 · Cited by 64 · see citing works
Sleep and memory: The impact of sleep deprivation on transcription, translational control, and protein synthesis in the brain
Lyons, L. C., Vanrobaeys, Y. S., & Abel, T. G. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15787 · Cited by 62 · see citing works
Self-citation
Altered 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
Self-citation
Drosophila as a Model to Study the Relationship Between Sleep, Plasticity, and Memory
Dissel, S. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00533 · Cited by 49 · 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
Self-citation
The stress of losing sleep: Sex-specific neurobiological outcomes
Wright, C. J., Milosavljevic, S., & Pocivavsek, A. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100543 · Cited by 45 · see citing works
Individual Differences in Animal Stress Models: Considering Resilience, Vulnerability, and the Amygdala in Mediating the Effects of Stress and Conditioned Fear on Sleep
Wellman, L. L., Fitzpatrick, M. E., Hallum, O. Y., Sutton, A. M., Williams, B. L., & Sanford, L. D. (2016) · SLEEP · doi:10.5665/sleep.5856 · Cited by 42 · see citing works
Impacts 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
Self-citation
Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia
Krishnan, H. C., Gandour, C. E., Ramos, J. L., Wrinkle, M. C., Sanchez-Pacheco, J. J., & Lyons, L. C. (2016) · SLEEP · doi:10.5665/sleep.6320 · Cited by 40 · see citing works
The PDE4 cAMP-Specific Phosphodiesterases: Targets for Drugs with Antidepressant and Memory-Enhancing Action
Bolger, G. B. (2017) · Advances in neurobiology · doi:10.1007/978-3-319-58811-7_4 · Cited by 36 · see citing works
Progressive increase in the complexity and translatability of rodent testing to assess space-radiation induced cognitive impairment
Britten, R. A., Wellman, L. L., & Sanford, L. D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.027 · Cited by 36 · see citing works
Alzheimer's disease pathogenesis: The role of disturbed sleep in attenuated brain plasticity and neurodegenerative processes
Havekes, R., Heckman, P. R. A., Wams, E. J., Stasiukonytė, N., Meerlo, P., & Eisel, U. L. M. (2019) · Cellular Signalling · doi:10.1016/j.cellsig.2019.109420 · Cited by 34 · see citing works
Self-citation
Recovering 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
Self-citation
A brief period of sleep deprivation negatively impacts the acquisition, consolidation, and retrieval of object-location memories
Heckman, P. R. A., Kuhn, F. R., Meerlo, P., & Havekes, R. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107326 · Cited by 32 · see citing works
Self-citation
Sleep deprivation‐induced impairment of memory consolidation is not mediated by glucocorticoid stress hormones
Raven, 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
Self-citation
Sleep deprivation impairs learning and memory by decreasing protein O ‐GlcNAcylation in the brain of adult zebrafish
Lee, Y., Park, J. W., Kim, S., Nam, K., Lee, W., Cho, H., & Han, I. (2019) · The FASEB Journal · doi:10.1096/fj.201901399rr · Cited by 28 · see citing works
The basolateral amygdala can mediate the effects of fear memory on sleep independently of fear behavior and the peripheral stress response
Wellman, L. L., Fitzpatrick, M. E., Hallum, O. Y., Sutton, A. M., Williams, B. L., & Sanford, L. D. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.11.004 · Cited by 27 · see citing works
Sleep deprivation caused a memory defects and emotional changes in a rotenone-based zebrafish model of Parkinson’s disease
Lv, D.-J., Lingxi, L., Chen, J., Wei, S., Wang, F., Hu, H., Xie, A., & Liu, C. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112031 · Cited by 27 · see citing works
Activation of brain‐derived neurotrophic factor signaling in the basal forebrain reverses acute sleep deprivation‐induced fear memory impairments
Ma, T., Zhang, H., Xu, Z., Lu, Y., Fu, Q., Wang, W., Li, G., Wang, Y., Yang, Y., & Mi, W. (2020) · Brain and Behavior · doi:10.1002/brb3.1592 · 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
Sleep-dependent engram reactivation during hippocampal memory consolidation associated with subregion-specific biosynthetic changes
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
Modeling integrated stress, sleep, fear and neuroimmune responses: Relevance for understanding trauma and stress-related disorders
Sanford, L. D., Wellman, L. L., Adkins, A. M., Guo, M., Zhang, Y., Ren, R., Yang, L., & Tang, X. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100517 · Cited by 21 · see citing works
FABP7: a glial integrator of sleep, circadian rhythms, plasticity, and metabolic function
Gerstner, J. R., Flores, C. C., Lefton, M., Rogers, B., & Davis, C. J. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1212213 · Cited by 22 · see citing works
Unraveling the Neurobiology of Sleep and Sleep Disorders Using Drosophila
Chakravarti, L. J., Moscato, E. H., & Kayser, M. S. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.07.010 · Cited by 16 · see citing works
Shift work and cognitive impairment in later life – results of a cross-sectional pilot study testing the feasibility of a large-scale epidemiologic investigation
Weinmann, T., Vetter, C., Karch, S., Nowak, D., & Radon, K. (2018) · BMC Public Health · doi:10.1186/s12889-018-6171-5 · Cited by 18 · see citing works
Biological Rhythms Advance in Depressive Disorder
Hong, W., & Zhang, Q. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-32-9271-0_6 · Cited by 18 · see citing works
Neurocognitive, mood changes, and sleepiness in patients with REM-predominant obstructive sleep apnea
BaHammam, A. S., Pirzada, A. R., & Pandi-Perumal, S. R. (2022) · Sleep And Breathing · doi:10.1007/s11325-022-02602-5 · Cited by 18 · see citing works
Antagonism of corticotropin releasing factor in the basolateral amygdala of resilient and vulnerable rats: Effects on fear-conditioned sleep, temperature and freezing
Wellman, L. L., Fitzpatrick, M. E., Sutton, A. M., Williams, B. L., Machida, M., & Sanford, L. D. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.02.013 · Cited by 17 · see citing works
Phosphodiesterase inhibitors roflumilast and vardenafil prevent sleep deprivation‐induced deficits in spatial pattern separation
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
Self-citation
A Rodent Model of Night-Shift Work Induces Short-Term and Enduring Sleep and Electroencephalographic Disturbances
Grønli, J., Meerlo, P., Pedersen, T., Pallesen, S., Skrede, S., Marti, A. R., Wisor, J. P., Murison, R. C. C., Henriksen, T. E. G., Rempe, M. J., et al. (2016) · Journal of Biological Rhythms · doi:10.1177/0748730416675460 · Cited by 18 · see citing works
Self-citation
Elucidating the role of protein synthesis in hippocampus‐dependent memory consolidation across the day and night
Raven, F., Bolsius, Y. G., van Renssen, L. V., Meijer, E. L., van der Zee, E. A., Meerlo, P., & Havekes, R. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14684 · Cited by 16 · see citing works
Self-citation
Beyond Emotional and Spatial Processes: Cognitive Dysfunction in a Depressive Phenotype Produced by Long Photoperiod Exposure
Barnes, A., Smith, S. B., & Datta, S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170032 · Cited by 16 · see citing works
Retracted
Loss of EPAC2 alters dendritic spine morphology and inhibitory synapse density
Jones, K. A., Sumiya, M., Woolfrey, K. M., Srivastava, D. P., & Penzes, P. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2019.05.001 · Cited by 15 · see citing works
Translational neurophysiological markers for activity of the metabotropic glutamate receptor (mGluR2) modulator JNJ-40411813: Sleep EEG correlates in rodents and healthy men
Ahnaou, A., de Boer, P., Lavreysen, H., Huysmans, H., Sinha, V., Raeymaekers, L., de Casteele, T. V., Cid, J. M., Nueten, L. V., Macdonald, G. J., et al. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.11.031 · Cited by 15 · see citing works
A selective review of inhibitors of protein kinase C gamma: a neuroplasticity-related common pathway for psychiatric illness
Grados, M. A., Salehi, M., Lotfi, A., Dua, S. S., & Xie, I. Y. (2024) · Frontiers in Drug Delivery · doi:10.3389/fddev.2024.1364037 · Cited by 11 · see citing works
Fear memory consolidation in sleep requires protein kinase APreprint
Cho, J., Sypniewski, K. A., Arai, S., Yamada, K., Ogawa, S., & Pavlides, C. (2018) · Learning & Memory · doi:10.1101/lm.046458.117 · Cited by 11 · see citing works
Nicotine‐prevented learning and memory impairment in REM sleep‐deprived rat is modulated by DREAM protein in the hippocampus
Rashid, N. A., Hapidin, H., Abdullah, H., Ismail, Z., & Long, I. (2017) · Brain and Behavior · doi:10.1002/brb3.704 · Cited by 10 · see citing works
Microstructural dynamics of motor learning and sleep-dependent consolidation: A diffusion imaging study
Stee, W., Legouhy, A., Guerreri, M., Villemonteix, T., Zhang, H. G., & Peigneux, P. (2023) · iScience · doi:10.1016/j.isci.2023.108426 · Cited by 8 · see citing works
Sleep and Core Body Temperature Alterations Induced by Space Radiation in Rats
Sanford, L. D., Adkins, A. M., Boden, A. F., Gotthold, J. D., Harris, R. D., Shuboni‐Mulligan, D. D., Wellman, L. L., & Britten, R. A. (2023) · Life · doi:10.3390/life13041002 · Cited by 7 · see citing works
Sleep, Synaptic Plasticity, and Memory
Golbert, D. C. F., Souza, A. C., Filho, D. A., & Ribeiro, S. T. G. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21118-8 · Cited by 5 · see citing works
Reduced Theta Coherence and P Wave Ratio Linked to Memory Deficits After Sleep Deprivation in Rat Model
Gulia, K. K., Sivadas, N., & Kumar, V. M. (2017) · Sleep and Vigilance · doi:10.1007/s41782-017-0005-x · Cited by 5 · see citing works
Sleep is necessary for experience-dependent sequence plasticity in mouse primary visual cortex
Hosamane, N. S., Didouchevski, A. M., Malci, A., Gavornik, J. P., & Sidorov, M. S. (2024) · SLEEP · doi:10.1093/sleep/zsae262 · Cited by 4 · see citing works
Restoring Serotonergic Homeostasis in the Lateral Hypothalamus Rescues Sleep Disturbances Induced by Early-Life Obesity
Gazea, M., Patchev, A. V., Anderzhanova, E. A., Leidmaa, E., Pissioti, A., Flachskamm, C., Almeida, O. F. X., & Kimura, M. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1333-17.2017 · Cited by 4 · see citing works
Sleep Fragmentation in TcMAC21 Mouse Model of Down Syndrome
Tusk, J., Canas, M. A. S., Haydar, T. F., & Dean, T. (2025) · Nature and Science of Sleep · doi:10.2147/nss.s545188 · Cited by 3 · see citing works
Phosphodiesterase Inhibitor ‘Rolipram’ Alleviates Sleep-Deprivation-Mediated Appetitive-Delay-Conditioned Memory in the Rat
Tripathi, S., Taneja, P., & Jha, S. K. (2024) · Sleep and Vigilance · doi:10.1007/s41782-024-00287-2 · Cited by 3 · see citing works
Role of Hypothalamic CRH Neurons in Regulating the Impact of Stress on Memory and Sleep
Wiest, A., Maurer, J. J., Beier, K. T., Weber, F., & Chung, S. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.2146-24.2025 · Cited by 7 · see citing works
Wakefulness rather than sleep benefits extinction of an inhibitory operant conditioning memory in Aplysia
Vorster, A. P. A., & Jan Born, A. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.07.012 · Cited by 3 · see citing works
Does Motor Memory Reactivation through Practice and Post-Learning Sleep Modulate Consolidation?
Stee, W., & Peigneux, P. (2023) · Clocks & Sleep · doi:10.3390/clockssleep5010008 · Cited by 4 · see citing works
Sleep, gut microbiota, and mind-body medicine
Das, M., Muralitharan, G., Saini, S., & Patra, S. (2025) · Brain Behavior and Immunity Integrative · doi:10.1016/j.bbii.2025.100128 · Cited by 2 · see citing works
An Interdisciplinary Investigation of Infant Sleep: How We Study It, What It Means for Other Areas of Development, and Where Methodological Creativity Can Take Us
Horger, M. N. (2021) · CUNY Academic Works (City University of New York) · Cited by 2 · see citing works
Awareness of the future: Dolphins know when they need to remember for the futurePreprint
Ortiz, S. T., Smeele, S. Q., Osvath, M., Guerrero, A. M., Sánchez, A. H., Ramirez, C. U., Almunia, J., & von Bayern, A. M. P. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.28.625857 · Cited by 2 · see citing works
Effects of 15 cGy GCRsim Space Radiation on Conditioned Fear and Stress Responses in Stress Resilient and Vulnerable Rats: Implications for Astronaut Sleep, Health and Mission Performance
Adkins, A. M., Boden, A. F., Singh, N., Luyo, Z. N. M., Britten, R. A., Wellman, L. L., & Sanford, L. D. (2026) · Radiation Research · doi:10.1667/rade-25-00092.1 · 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
Effects of Sleep Deprivation in Young and Adult Rats: An Assessment of Memory and Anxiety
Zareian, P., & Nategh, M. (2020) · Annals of Military and Health Sciences Research · doi:10.5812/amh.107817 · Cited by 1 · see citing works
A 108-h total sleep deprivation did not impair fur seal performance in delayed matching to sample task
Lyamin, O. I., Borshchenko, V. D., & Siegel, J. M. (2023) · Journal of Comparative Physiology B · doi:10.1007/s00360-023-01511-7 · Cited by 1 · see citing works
Sex as a biological variable (SABV) modulates the consequences of sleep disturbance on hippocampal memory and synaptic plasticity
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Authors: Havekes, R., Meerlo, P., & Abel, T.
Affiliations: University of Pennsylvania (US)
University of Groningen (NL)
Corresponding author: Havekes, Robbert
ORCID: Havekes, Robbert
Meerlo, Peter
Abel, Ted
Venue: Current Topics in Behavioral Neurosciences
Publisher: Springer Berlin Heidelberg
Published: 2015
Volume: 25
Pages: 183-206
ISSN: 1866-3370 (ISSN-L)
1866-3389
DOI: 10.1007/7854_2015_369
OpenAlex: W2106411985
Cited by: 78
References: 105
Citations by year: 2026: 6 · 2025: 6 · 2024: 6 · 2023: 8 · 2022: 2 · 2021: 6 · 2020: 9 · 2019: 10 · 2018: 6 · 2017: 11 · 2016: 7 · 2015: 1
FWCI: 17.48
Type: book chapter
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Current topics in behavioral neurosciences (publishedVersion)
PubMed (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
Funders: National Institute on Aging (P01AG017628)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
Keywords: sleep, memory consolidation, sleep deprivation, hippocampus, neuroplasticity, cAMP signaling, protein kinase A, CREB, gene expression, excitatory neurons, pharmacogenetics, cognitive impairment
MeSH terms: Animals, Behavior, Animal, Memory, Sleep, Sleep Deprivation, Long-Term Potentiation

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Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms

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