Two nights of recovery sleep restores hippocampal connectivity but not episodic memory after total sleep deprivation.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
29 05 2020
29 05 2020
Historique:
received:
04
10
2019
accepted:
28
04
2020
entrez:
31
5
2020
pubmed:
31
5
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Sleep deprivation significantly impairs a range of cognitive and brain function, particularly episodic memory and the underlying hippocampal function. However, it remains controversial whether one or two nights of recovery sleep following sleep deprivation fully restores brain and cognitive function. In this study, we used functional magnetic resonance imaging (fMRI) and examined the effects of two consecutive nights (20-hour time-in-bed) of recovery sleep on resting-state hippocampal connectivity and episodic memory deficits following one night of total sleep deprivation (TSD) in 39 healthy adults in a controlled in-laboratory protocol. TSD significantly reduced memory performance in a scene recognition task, impaired hippocampal connectivity to multiple prefrontal and default mode network regions, and disrupted the relationships between memory performance and hippocampal connectivity. Following TSD, two nights of recovery sleep restored hippocampal connectivity to baseline levels, but did not fully restore memory performance nor its associations with hippocampal connectivity. These findings suggest that more than two nights of recovery sleep are needed to fully restore memory function and hippocampal-memory associations after one night of total sleep loss.
Identifiants
pubmed: 32472075
doi: 10.1038/s41598-020-65086-x
pii: 10.1038/s41598-020-65086-x
pmc: PMC7260173
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8774Subventions
Organisme : NCRR NIH HHS
ID : UL1 RR024134
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH107571
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL102119
Pays : United States
Organisme : NIA NIH HHS
ID : R21 AG051981
Pays : United States
Organisme : NINDS NIH HHS
ID : P30 NS045839
Pays : United States
Références
Belenky, G. et al. Patterns of performance degradation and restoration during sleep restriction and subsequent recovery: a sleep dose-response study. J. Sleep Res. 12, 1–12 (2003).
pubmed: 12603781
doi: 10.1046/j.1365-2869.2003.00337.x
Van Dongen, H. P. A., Maislin, G., Mullington, J. M. & Dinges, D. F. The Cumulative Cost of Additional Wakefulness: Dose-Response Effects on Neurobehavioral Functions and Sleep Physiology From Chronic Sleep Restriction and Total Sleep Deprivation. Sleep 26, 117–126 (2003).
pubmed: 12683469
doi: 10.1093/sleep/26.2.117
Banks, S., Van Dongen, H. P. A., Maislin, G. & Dinges, D. F. Neurobehavioral dynamics following chronic sleep restriction: Dose-response effects of one night for recovery. Sleep 33, 1013–1026 (2010).
pubmed: 20815182
pmcid: 2910531
doi: 10.1093/sleep/33.8.1013
Ford, E. S., Cunningham, T. J. & Croft, J. B. Trends in Self-Reported Sleep Duration among US Adults from 1985 to 2012. Sleep 38, 829–832 (2015).
pubmed: 25669182
pmcid: 4402659
doi: 10.5665/sleep.4684
Watson, N. F. et al. Recommended Amount of Sleep for a Healthy Adult: A Joint Consensus Statement of the American Academy of Sleep Medicine and Sleep Research Society. Sleep 38, 843–844 (2015).
pubmed: 26039963
pmcid: 4434546
doi: 10.5665/sleep.4310
Banks, S. & Dinges, D. F. Behavioral and Physiological Consequences of Sleep Restriction. J. Clin. Sleep Med. 3, 519–528 (2007).
pubmed: 17803017
pmcid: 1978335
doi: 10.5664/jcsm.26918
Lim, J. & Dinges, D. F. Sleep deprivation and vigilant attention. Ann. N. Y. Acad. Sci. 1129, 305–322 (2008).
pubmed: 18591490
doi: 10.1196/annals.1417.002
Goel, N., Rao, H., Durmer, J. S. & Dinges, D. F. Neurocognitive Consequences of Sleep Deprivation. Semin Neurol. 29, 320–339 (2009).
pubmed: 19742409
pmcid: 3564638
doi: 10.1055/s-0029-1237117
Spaeth, A. M., Dinges, D. F. & Goel, N. Effects of Experimental Sleep Restriction on Weight Gain, Caloric Intake, and Meal Timing in Healthy Adults. Sleep 36, 981–990 (2013).
pubmed: 23814334
pmcid: 3669080
doi: 10.5665/sleep.2792
Walker, M. P. & Stickgold, R. Sleep-dependent learning and memory consolidation. Neuron 44, 121–133 (2004).
pubmed: 15450165
doi: 10.1016/j.neuron.2004.08.031
Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).
pubmed: 20046194
doi: 10.1038/nrn2762
Inostroza, M. & Born, J. Sleep for Preserving and Transforming Episodic Memory. Annu. Rev. Neurosci. 36, 79–102 (2013).
pubmed: 23642099
doi: 10.1146/annurev-neuro-062012-170429
Fernandes, C. et al. Detrimental role of prolonged sleep deprivation on adult neurogenesis. Front. Cell. Neurosci. 9, 140 (2015).
pubmed: 25926773
pmcid: 4396387
doi: 10.3389/fncel.2015.00140
Sterpenich, V. et al. Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biol. 5, e282 (2007).
pubmed: 17958471
pmcid: 2039770
doi: 10.1371/journal.pbio.0050282
Yoo, S. S., Hu, P. T., Gujar, N., Jolesz, F. A. & Walker, M. P. A deficit in the ability to form new human memories without sleep. Nat. Neurosci. 10, 385–392 (2007).
pubmed: 17293859
doi: 10.1038/nn1851
Havekes, R., Vecsey, C. G. & Abel, T. The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity. Cell. Signal. 24, 1251–1260 (2012).
pubmed: 22570866
pmcid: 3622220
doi: 10.1016/j.cellsig.2012.02.010
Havekes, R. et al. Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1. Elife 5, e13424 (2016).
pubmed: 27549340
pmcid: 4996653
doi: 10.7554/eLife.13424
Abel, T., Havekes, R., Saletin, J. M. & Walker, M. P. Sleep, plasticity and memory from molecules to whole-brain networks. Curr. Biol. 23, R774–R788 (2013).
pubmed: 24028961
pmcid: 4263505
doi: 10.1016/j.cub.2013.07.025
Menz, M. M. et al. The role of sleep and sleep deprivation in consolidating fear memories. Neuroimage 75, 87–96 (2013).
pubmed: 23501052
doi: 10.1016/j.neuroimage.2013.03.001
Yeo, B. T. T., Tandi, J. & Chee, M. W. L. Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation. Neuroimage 111, 147–158 (2015).
pubmed: 25700949
doi: 10.1016/j.neuroimage.2015.02.018
Krause, A. J. et al. The sleep-deprived human brain. Nat. Rev. Neurosci. 18, 404–418 (2017).
pubmed: 28515433
pmcid: 6143346
doi: 10.1038/nrn.2017.55
Chengyang, L. et al. Short-term memory deficits correlate with hippocampal-thalamic functional connectivity alterations following acute sleep restriction. Brain Imaging Behav. 11, 954–963 (2017).
pubmed: 27444729
doi: 10.1007/s11682-016-9570-1
Zhao, R. et al. Disrupted Resting-State Functional Connectivity in Hippocampal Subregions After Sleep Deprivation. Neuroscience 398, 37–54 (2019).
pubmed: 30529694
doi: 10.1016/j.neuroscience.2018.11.049
Sirota, A., Csicsvari, J., Buhl, D. & Buzsa´ki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. 100, 2065–2069 (2003).
pubmed: 12576550
doi: 10.1073/pnas.0437938100
Ji, D. & Wilson, M. A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci. 10, 100–107 (2007).
pubmed: 17173043
doi: 10.1038/nn1825
Logothetis, N. K. et al. Hippocampal-cortical interaction during periods of subcortical silence. Nature 491, 547–553 (2012).
pubmed: 23172213
doi: 10.1038/nature11618
Van Der Werf, Y. D. et al. Sleep benefits subsequent hippocampal functioning. Nat. Neurosci. 12, 122–123 (2009).
doi: 10.1038/nn.2253
Marshall, L. & Born, J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn. Sci. 11, 442–450 (2007).
pubmed: 17905642
doi: 10.1016/j.tics.2007.09.001
Schlichting, M. L. & Preston, A. R. Memory reactivation during rest supports upcoming learning of related content. Proc. Natl. Acad. Sci. 111, 15845–15850 (2014).
pubmed: 25331890
doi: 10.1073/pnas.1404396111
Voets, N. L. et al. Aberrant Functional Connectivity in Dissociable Hippocampal Networks Is Associated with Deficits in Memory. J. Neurosci. 34, 4920–4928 (2014).
pubmed: 24695711
pmcid: 3972719
doi: 10.1523/JNEUROSCI.4281-13.2014
Cooper, R. A. et al. Reduced Hippocampal Functional Connectivity During Episodic Memory Retrieval in Autism. Cereb. cortex 27, 888–902 (2017).
pubmed: 28057726
pmcid: 5390398
Tompary, A. & Davachi, L. Consolidation Promotes the Emergence of Representational Overlap in the Hippocampus and Medial Prefrontal Cortex. Neuron 96, 228–241 (2017).
pubmed: 28957671
pmcid: 5630271
doi: 10.1016/j.neuron.2017.09.005
Vecsey, C. G. et al. Sleep deprivation impairs cAMP signalling in the hippocampus. Nature 461, 1122–1125 (2009).
pubmed: 19847264
pmcid: 2783639
doi: 10.1038/nature08488
Drummond, S. P. A., Paulus, M. P. & Tapert, S. F. Effects of two nights sleep deprivation and two nights recovery sleep on response inhibition. J. Sleep Res. 15, 261–265 (2006).
pubmed: 16911028
doi: 10.1111/j.1365-2869.2006.00535.x
Jay, S. M. et al. The characteristics of recovery sleep when recovery opportunity is restricted. Sleep 30, 353–360 (2007).
pubmed: 17425232
doi: 10.1093/sleep/30.3.353
Mander, B. A. et al. EEG measures index neural and cognitive recovery from sleep deprivation. J. Neurosci. 30, 2686–2693 (2010).
pubmed: 20164352
pmcid: 2835412
doi: 10.1523/JNEUROSCI.4010-09.2010
Tucker, A. M., Whitney, P., Belenky, G., Hinson, J. M. & Van Dongen, H. P. A. Effects of Sleep Deprivation on Dissociated Components of Executive Functioning. Sleep 33, 47–57 (2010).
pubmed: 20120620
pmcid: 2802247
doi: 10.1093/sleep/33.1.47
de Almeida, V. Z. G. et al. Free Recall of Word Lists under Total Sleep Deprivation and after Recovery Sleep. Sleep 35, 223–230 (2012).
doi: 10.5665/sleep.1626
Philip, P. et al. Acute Versus Chronic Partial Sleep Deprivation in Middle-Aged People: Differential Effect on Performance and Sleepiness. Sleep 35, 997–1002 (2012).
pubmed: 22754046
pmcid: 3369235
doi: 10.5665/sleep.1968
Elmenhorst, D. et al. Recovery sleep after extended wakefulness restores elevated A1 adenosine receptor availability in the human brain. Proc. Natl. Acad. Sci. 114, 4243–4248 (2017).
pubmed: 28373571
doi: 10.1073/pnas.1614677114
Dinges, D. F. et al. Cumulative Sleepiness, Mood Disturbance, and Psychomotor Vigilance Performance Decrements During a Week of Sleep Restricted to 4-5 Hours per Night. Sleep 20, 267–277 (1997).
pubmed: 9231952
Wu, J. C. et al. Frontal Lobe Metabolic Decreases with Sleep Deprivation not Totally Reversed by Recovery Sleep. Neuropsychopharmacology 31, 2783–2792 (2006).
pubmed: 16880772
doi: 10.1038/sj.npp.1301166
Ikegami, K. et al. Recovery of cognitive performance and fatigue after one night of sleep deprivation. J. Occup. Health 51, 412–422 (2009).
pubmed: 19602843
doi: 10.1539/joh.L8127
Pejovic, S. et al. Effects of recovery sleep after one work week of mild sleep restriction on interleukin-6 and cortisol secretion and daytime sleepiness and performance. Am. J. Physiol. Metab. 305, E890–E896 (2013).
Lo, J. C., Ong, J. L., Leong, R. L. F., Gooley, J. J. & Chee, M. W. L. Cognitive Performance, Sleepiness, and Mood in Partially Sleep Deprived Adolescents: The Need for Sleep Study. Sleep 39, 687–698 (2016).
pubmed: 26612392
pmcid: 4763363
doi: 10.5665/sleep.5552
Boardman, J. M. et al. The ability to self-monitor cognitive performance during 60 h total sleep deprivation and following 2 nights recovery sleep. J. Sleep Res. 27, 1–8 (2018).
doi: 10.1111/jsr.12633
Saletin, J. M. et al. Human Hippocampal Structure: A Novel Biomarker Predicting Mnemonic Vulnerability to, and Recovery from, Sleep Deprivation. J. Neurosci. 36, 2355–2363 (2016).
pubmed: 26911684
pmcid: 4764658
doi: 10.1523/JNEUROSCI.3466-15.2016
Hu, P., Stylos-allan, M. & Walker, M. P. Sleep faciliates consolidation of emotional declarative memory. Psychol. Sci. 17, 891–898 (2006).
pubmed: 17100790
doi: 10.1111/j.1467-9280.2006.01799.x
Chuah, L. Y. M. et al. Donepezil Improves Episodic Memory in Young Individuals Vulnerable to the Effects of Sleep Deprivation. Sleep 32, 999–1010 (2009).
pubmed: 19725251
pmcid: 2717207
doi: 10.1093/sleep/32.8.999
Drummond, S. P. A. et al. Altered brain response to verbal learning following sleep deprivation. Nature 403, 655–657 (2000).
pubmed: 10688201
doi: 10.1038/35001068
Killgore, W. D. S. Effects of sleep deprivation on cognition. Progress in Brain Research 185, (Elsevier B.V., 2010).
Gusnard, D. A., Akbudak, E., Shulman, G. L. & Raichle, M. E. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc. Natl. Acad. Sci. 98, 4259–4264 (2001).
pubmed: 11259662
doi: 10.1073/pnas.071043098
Vincent, J. L. et al. Coherent Spontaneous Activity Identifies a Hippocampal-Parietal Memory Network. J Neurophysiol 96, 3517–3531 (2006).
pubmed: 16899645
doi: 10.1152/jn.00048.2006
Buckner, R. L., Andrews-Hanna, J. R. & Schacter, D. L. The brain’s default network: Anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124, 1–38 (2008).
pubmed: 18400922
doi: 10.1196/annals.1440.011
Ranganath, C., Heller, A., Cohen, M. X., Brozinsky, C. J. & Rissman, J. Functional connectivity with the hippocampus during successful memory formation. Hippocampus 15, 997–1005 (2005).
pubmed: 16281291
doi: 10.1002/hipo.20141
Schott, B. H. et al. The relationship between level of processing and hippocampal-cortical functional connectivity during episodic memory formation in humans. Hum. Brain Mapp. 34, 407–424 (2013).
pubmed: 22042493
doi: 10.1002/hbm.21435
Greicius, M. D., Srivastava, G., Reiss, A. L. & Menon, V. Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. 101, 4637–4642 (2004).
pubmed: 15070770
doi: 10.1073/pnas.0308627101
Sperling, R. A. et al. Functional alterations in memory networks in early alzheimer’s disease. NeuroMolecular Med. 12, 27–43 (2010).
pubmed: 20069392
pmcid: 3036844
doi: 10.1007/s12017-009-8109-7
Raichle, M. E. et al. A default mode of brain function. Proc. Natl. Acad. Sci. 95, 676–682 (2001).
doi: 10.1073/pnas.98.2.676
Vincent, J. L., Kahn, I., Snyder, A. Z., Raichle, M. E. & Buckner, R. L. Evidence for a Frontoparietal Control System Revealed by Intrinsic Functional Connectivity. J. Neurophysiol. 100, 3328–3342 (2008).
pubmed: 18799601
pmcid: 2604839
doi: 10.1152/jn.90355.2008
Sämann, P. G. et al. Increased sleep pressure reduces resting state functional connectivity. Magn. Reson. Mater. Physics, Biol. Med. 23, 375–389 (2010).
doi: 10.1007/s10334-010-0213-z
Havas, J. A. D., Parimal, S., Soon, C. S. & Chee, M. W. L. Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance. Neuroimage 59, 1745–1751 (2012).
pubmed: 21872664
doi: 10.1016/j.neuroimage.2011.08.026
Bosch, O. G. et al. Sleep deprivation increases dorsal nexus connectivity to the dorsolateral prefrontal cortex in humans. Proc. Natl. Acad. Sci. 110, 19597–19602 (2013).
pubmed: 24218598
doi: 10.1073/pnas.1317010110
Lei, Y. et al. Large-Scale Brain Network Coupling Predicts Total Sleep Deprivation Effects on Cognitive Capacity. PLoS One 10, e0133959 (2015).
pubmed: 26218521
pmcid: 4517902
doi: 10.1371/journal.pone.0133959
Nilsonne, G. et al. Intrinsic brain connectivity after partial sleep deprivation in young and older adults: Results from the Stockholm Sleepy Brain study. Sci. Rep. 7, 9422 (2017).
pubmed: 28842597
pmcid: 5573389
doi: 10.1038/s41598-017-09744-7
Fox, M. D. et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. 102, 9673–9678 (2005).
pubmed: 15976020
doi: 10.1073/pnas.0504136102
Fox, M. D. & Raichle, M. E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700–711 (2007).
pubmed: 17704812
doi: 10.1038/nrn2201
Clapp, W. C., Rubens, M. T., Sabharwal, J. & Gazzaley, A. Deficit in switching between functional brain networks underlies the impact of multitasking on working memory in older adults. Proc. Natl. Acad. Sci. 108, 7212–7217 (2011).
pubmed: 21482762
doi: 10.1073/pnas.1015297108
Turner, G. R. & Spreng, R. N. Executive functions and neurocognitive aging: Dissociable patterns of brain activity. Neurobiol. Aging 33, 826.e1–826.e13 (2012).
doi: 10.1016/j.neurobiolaging.2011.06.005
Lamond, N. et al. The dynamics of neurobehavioural recovery following sleep loss. J. Sleep Res. 16, 33–41 (2007).
pubmed: 17309761
doi: 10.1111/j.1365-2869.2007.00574.x
Smith, C. Sleep states and memory processes. Behav. Brain Res. 69, 137–145 (1995).
pubmed: 7546305
doi: 10.1016/0166-4328(95)00024-N
Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 (1997).
pubmed: 23968216
doi: 10.1162/jocn.1997.9.4.534
Ficca, G. & Salzarulo, P. What in sleep is for memory. Sleep Med. 5, 225–230 (2004).
pubmed: 15165527
doi: 10.1016/j.sleep.2004.01.018
Stickgold, R. Sleep-dependent memory consolidation. Nature 437, 1272–1278 (2005).
pubmed: 16251952
doi: 10.1038/nature04286
Rasch, B. & Born, J. About Sleep’s Role in Memory. Physiol. Rev. 93, 681–766 (2013).
pubmed: 23589831
pmcid: 3768102
doi: 10.1152/physrev.00032.2012
Andrade, K. C. et al. Sleep Spindles and Hippocampal Functional Connectivity in Human NREM Sleep. J. Neurosci. 31, 10331–10339 (2011).
pubmed: 21753010
pmcid: 6623055
doi: 10.1523/JNEUROSCI.5660-10.2011
Sämann, P. G. et al. Development of the brain’s default mode network from wakefulness to slow wave sleep. Cereb. Cortex 21, 2082–2093 (2011).
pubmed: 21330468
doi: 10.1093/cercor/bhq295
Mander, B. A. et al. Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging. Nat. Neurosci. 16, 357–364 (2013).
pubmed: 23354332
pmcid: 4286370
doi: 10.1038/nn.3324
Alhola, P. & Polo-Kantola, P. Sleep deprivation: Impact on cognitive performance. Neuropsychiatr. Dis. Treat. 3, 553–567 (2007).
pubmed: 19300585
pmcid: 2656292
Basner, M., Rao, H., Goel, N. & Dinges, D. F. Sleep deprivation and neurobehavioral dynamics. Curr. Opin. Neurobiol. 23, 854–863 (2013).
pubmed: 23523374
pmcid: 3700596
doi: 10.1016/j.conb.2013.02.008
Gujar, N., Yoo, S. S., Hu, P. & Walker, M. P. The unrested resting brain: Sleep deprivation alters activity within the default-mode network. J. Cogn. Neurosci. 22, 1637–1648 (2010).
pubmed: 19702469
pmcid: 2883887
doi: 10.1162/jocn.2009.21331
Fox, M. D. & Greicius, M. Clinical applications of resting state functional connectivity. Front. Syst. Neurosci. 4, 19 (2010).
pubmed: 20592951
pmcid: 2893721
Sanchez Panchuelo, R. M., Stephenson, M. C., Francis, S. T. & Morris, P. G. Neural brain activation imaging. Biomedical Imaging: Applications and Advances, https://doi.org/10.1533/9780857097477.2.112 (2014).
doi: 10.1533/9780857097477.2.112
Kang, J.-E. et al. Amyloid-β Dynamics Are Regulated by Orexin and the Sleep-Wake Cycle. Science (80-.). 326, 1005–1008 (2009).
doi: 10.1126/science.1180962
Jack, C. R. et al. Tracking pathophysiological processes in Alzheimer’s disease: An updated hypothetical model of dynamic biomarkers. Lancet Neurol. 12, 207–216 (2013).
pubmed: 23332364
pmcid: 3622225
doi: 10.1016/S1474-4422(12)70291-0
Gouras, G. K., Olsson, T. T. & Hansson, O. β-amyloid Peptides and Amyloid Plaques in Alzheimer’s Disease. Neurotherapeutics 12, 3–11 (2015).
pubmed: 25371168
doi: 10.1007/s13311-014-0313-y
Shokri-Kojori, E. et al. β-Amyloid accumulation in the human brain after one night of sleep deprivation. Proc. Natl. Acad. Sci. 201721694, https://doi.org/10.1073/pnas.1721694115 (2018).
doi: 10.1073/pnas.1721694115
Winer, J. R. et al. Sleep as a potential biomarker of Tau and β-amyloid burdern in the human brain. J. Neurosci. 39, 6315–6324 (2019).
pubmed: 31209175
pmcid: 6687908
doi: 10.1523/JNEUROSCI.0503-19.2019
Vitiello, M. V. & Borson, S. Sleep disturbances in patients with alzheimer’s disease: Epidemiology, pathophysiology and treatment. CNS Drugs 15, 777–796 (2001).
pubmed: 11602004
doi: 10.2165/00023210-200115100-00004
Gagnon, J.-F., Petit, D., Latreille, V. & Montplaisir, J. Neurobiology of Sleep Disturbances in Neurodegenerative Disorders. Curr. Pharm. Des. 14, 3430–3445 (2008).
pubmed: 19075719
doi: 10.2174/138161208786549353
Pace-Schott, E. F. & Spencer, R. M. C. Age-related changes in the cognitive function of sleep. Progress in Brain Research 191, (Elsevier B.V., 2011).
Harand, C. et al. How aging affects sleep-dependent memory consolidation? Front. Neurol. 3, 1–6 (2012).
doi: 10.3389/fneur.2012.00008
Fang, Z. et al. Altered salience network connectivity predicts macronutrient intake after sleep deprivation. Sci. Rep. 5, 1–8 (2015).
Yang, F. N. et al. Sleep deprivation enhances inter-stimulus interval effect on vigilant attention performance. Sleep 41, 1–12 (2018).
doi: 10.1093/sleep/zsy189
Davies, J. A., Navaratnam, V. & Redfern, P. H. A 24-hour rhythm in passive-avoidance behaviour in rats. Psychopharmacologia 32, 211–214 (1973).
pubmed: 4753534
doi: 10.1007/BF00428692
Folkard, S. Time of day and level of processing. Mem. Cognit. 7, 247–252 (1979).
doi: 10.3758/BF03197596
Folkard, S. & Monk, T. H. Circadian rhythms in human memory. Br. J. Psychol. 71, 295–307 (1980).
doi: 10.1111/j.2044-8295.1980.tb01746.x
Dunne, M. P., Roche, F. & Hartley, L. R. Effects of Time of Day on Immediate Recall and Sustained Retrieval from Semantic Memory. J. Gen. Psychol. 117, 403–410 (1990).
pubmed: 28142342
doi: 10.1080/00221309.1990.9921146
Testu, F. & Clarisse, R. Time-of-day and day-of-week effects on mnemonic performance. Chronobiol. Int. 16, 491–503 (1999).
pubmed: 10442242
doi: 10.3109/07420529908998723
Gorfine, T. & Zisapel, N. Melatonin and the human hippocampus, a time dependant interplay. J. Pineal Res. 43, 80–86 (2007).
pubmed: 17614839
doi: 10.1111/j.1600-079X.2007.00446.x
Martin, B., Buffington, A. L. H. & Welsh-Bohmer, K. A. & Brandt. J. Time of day affects episodic memory in older adults. Aging, Neuropsychol. Cogn. 15, 146–164 (2008).
Wright, K. P., Lowry, C. A. & Lebourgeois, M. K. Circadian and wakefulness-sleep modulation of cognition in humans. Front. Mol. Neurosci. 5, 1–12 (2012).
Maylor, E. A. & Badham, S. P. Effects of time of day on age-related associative deficits. Psychol. Aging 33, 7–16 (2018).
pubmed: 29494174
doi: 10.1037/pag0000199
Puttaert, D., Adam, S. & Peigneux, P. Subjectively-defined optimal/non-optimal time of day modulates controlled but not automatic retrieval processes in verbal memory. J. Sleep Res. 28, e12798 (2019).
pubmed: 30485575
doi: 10.1111/jsr.12798
Lang, P. J., Bradley, M. M. & Cuthbert, B. N. International Affective Picture System (IAPS): Instruction manual and affective ratings, Technical Report A-8. Gainesv. Cent. Res. Psychophysiology, Univ. Florida. (2008).
Macmillan, N. A. & Creelman, C. D. Detection Theory A User’s Guide. Cambridge Univ Press New York. (1991).
Fair, D. A. et al. The maturing architecture of the brain’s default network. Proc. Natl. Acad. Sci. 105, 4028–4032 (2008).
pubmed: 18322013
doi: 10.1073/pnas.0800376105
Tzourio-Mazoyer, N. et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273–289 (2002).
pubmed: 11771995
doi: 10.1006/nimg.2001.0978
Diedenhofen, B. & Musch, J. cocor: A comprehensive solution for the statistical comparison of correlations. PLoS One 10, e0121945 (2015).
pubmed: 25835001
pmcid: 4383486
doi: 10.1371/journal.pone.0121945