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Functional Neuroimaging Insights into the Physiology of Human Sleep.
Open accessAbstract
Functional brain imaging has been used in humans to noninvasively investigate the neural mechanisms underlying the generation of sleep stages. On the one hand, REM sleep has been associated with the activation of the pons, thalamus, limbic areas, and temporo-occipital cortices, and the deactivation of prefrontal areas, in line with theories of REM sleep generation and dreaming properties. On the other hand, during non-REM (NREM) sleep, decreases in brain activity have been consistently found in the brainstem, thalamus, and in several cortical areas including the medial prefrontal cortex (MPFC), in agreement with a homeostatic need for brain energy recovery. Benefiting from a better temporal resolution, more recent studies have characterized the brain activations related to phasic events within specific sleep stages. In particular, they have demonstrated that NREM sleep oscillations (spindles and slow waves) are indeed associated with increases in brain activity in specific subcortical and cortical areas involved in the generation or modulation of these waves. These data highlight that, even during NREM sleep, brain activity is increased, yet regionally specific and transient. Besides refining the understanding of sleep mechanisms, functional brain imaging has also advanced the description of the functional properties of sleep. For instance, it has been shown that the sleeping brain is still able to process external information and even detect the pertinence of its content. The relationship between sleep and memory has also been refined using neuroimaging, demonstrating post-learning reactivation during sleep, as well as the reorganization of memory representation on the systems level, sometimes with long-lasting effects on subsequent memory performance. Further imaging studies should focus on clarifying the role of specific sleep patterns for the processing of external stimuli, as well as the consolidation of freshly encoded information during sleep.
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“Prospective cognition during sleep also differs from that during wake in that some brain regions supporting episodic future stimulation in wake are conspicuously deactivated during sleep, including dorsolateral prefrontal cortex and regions of the posterior parietal lobes [64–66].”
From Constructive episodic simulation in dreams (2022) · cites this paper as [65]
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Human REM sleep: influence on feeding behaviour, with clinical implications
Horne, J. A. (2015) · Sleep Medicine · doi:10.1016/j.sleep.2015.04.002 · Cited by 35
McAvoy, M. P., Larson‐Prior, L. J., Ludwikow, M., Zhang, D., Snyder, A. Z., Gusnard, D. L., Raichle, M. E., & d’Avossa, G. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00900.2011 · Cited by 34
Role of sleep in neurodegeneration: the consensus report of the 5th Think Tank World Sleep Forum
Ferini‐Strambi, L., Liguori, C., Lucey, B. P., Mander, B. A., Spira, A. P., Videnović, A., Baumann, C. R., Franco, O. H., Fernandes, M., Gnarra, O., et al. (2023) · Neurological Sciences · doi:10.1007/s10072-023-07232-7 · Cited by 34
“Neuronal metabolic activity measured by 18F-fluorode-oxyglucose PET decreases during NREM sleep [26, 27].”
Perogamvros, L., & Schwartz, S. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_271 · Cited by 29
“More specifically, activity decreases in the brainstem, thalamus, basal ganglia, basal forebrain and in several cortical areas including the medial prefrontal cortex (PFC) and precuneus (Dang-Vu et al. 2010).”
BackgroundMishra, A., Yang, P., Manuel, T. J., Newton, A. T., Phipps, M. A., Luo, H., Sigona, M. K., Reed, J. L., Gore, J. C., Grissom, W. A., et al. (2023) · Brain stimulation · doi:10.1016/j.brs.2023.09.013 · Cited by 28
“Alternatively, cingulotomy is performed for pain relief in late-stage cancer pain patients.”
The Influence of EEG References on the Analysis of Spatio-Temporal Interrelation Patterns
Ríos-Herrera, W. A., Olguín-Rodríguez, P. V., Arzate-Mena, J. D., Corsi‐Cabrera, M., Escalona, J., Marín-García, A., Ramos‐Loyo, J., Rivera, A. L., Rivera, D., Berruecos, J. F. Z., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00941 · Cited by 28
“For instance, dominant sources alter drastically during the transition from wake state to sleep (Steriade, 2003) and during sleep cycles (Pace-Schott and Hobson, 2002; Steriade, 2003; Dang-Vu et al., 2010; Brown et al., 2012; Jones, 2019).”
BackgroundCorrelations between adolescent processing speed and specific spindle frequencies
Nader, R. S., & Smith, C. T. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00030 · Cited by 26
“Dang-Vu et al. (2010) observed that the faster spindle activity was associated with more extensive cortical activation; the results from our adolescents suggest that it is the faster (or higher frequency) brain activity that is associated with some forms of intelligence.”
BackgroundThe occurrence of individual slow waves in sleep is predicted by heart rate
Mensen, A., Zhang, Z., Qi, M., & Khatami, R. (2016) · Scientific Reports · doi:10.1038/srep29671 · Cited by 25
Lassmann, Ł., Pollis, M., Żółtowska, A., & Manfredini, D. (2022) · Biomedicines · doi:10.3390/biomedicines10071528 · Cited by 26
Kong, S. D., Gordon, C. J., Hoyos, C. M., Wassing, R., D'Rozario, A. L., Mowszowski, L., Ireland, C., Palmer, J. R., Grunstein, R. R., Shine, J. M., et al. (2023) · Brain Communications · doi:10.1093/braincomms/fcad129 · Cited by 25
“prefrontal cortex, anterior cingulate cortex, and precuneus) regions.(75)”
BackgroundJakobson, A., Fitzgerald, P. B., & Conduit, R. (2012) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2011.00994.x · Cited by 23
“The general consensus from neuroimaging research is that posterior temporo–occipital association regions are activated consistently during REM sleep (Dang-Vu et al., 2010).”
Constructive episodic simulation in dreams
Wamsley, E. J. (2022) · PLOS ONE · doi:10.1371/journal.pone.0264574 · Cited by 22
Autonomic/central coupling benefits working memory in healthy young adults
Chen, P., Whitehurst, L. N., Naji, M., & Mednick, S. C. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107267 · Cited by 26
Shi, Y., Zhang, L., He, C., Yin, Y., Song, R., Chen, S., Fan, D., Zhou, D., Yuan, Y., Xie, C., et al. (2021) · Journal of Affective Disorders · doi:10.1016/j.jad.2021.08.027 · Cited by 22
Horne, J. (2013) · Sleep Medicine · doi:10.1016/j.sleep.2013.05.019 · Cited by 21
Investigating the effect of a nap following experimental trauma on analogue PTSD symptoms
Wilhelm, I., Azza, Y., Brennwald, K., Ehrt‐Schäfer, Y., Seifritz, E., & Kleim, B. (2021) · Scientific Reports · doi:10.1038/s41598-021-83838-1 · Cited by 20
Motor imagery practice benefits during arm immobilization
Debarnot, U., Perrault, A. A., Virginie Sterpenich, A., Legendre, G., Huber, C., Guillot, A., & Schwartz, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-88142-6 · Cited by 25
Building your best day for healthy brain aging—The neuroprotective effects of optimal time use
Mellow, M. L., Dumuid, D., Thacker, J. S., Dorrian, J., & Smith, A. E. (2019) · Maturitas · doi:10.1016/j.maturitas.2019.04.204 · Cited by 19
Akkol, E. K., Bardakçı, H., Yücel, Ç., Karatoprak, G. Ş., Karpuz, B., & Khan, H. Z. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/6168199 · Cited by 22
“This impairment was claimed to be located in subcortical and cortical regions and might be due to the neurons ’ overpolarized silent state during slow-wave sleep [53].”
Belinda, C. D., & Christian, M. S. (2022) · Academy of Management Journal · doi:10.5465/amj.2021.0377 · Cited by 24
Frank, E., Benabou, M., Bentzley, B. S., Bianchi, M. T., Goldstein, T. R., Konopka, G., Maywood, E. S., Pritchett, D., Sheaves, B., & Thomas, J. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12600 · Cited by 20
Memory traces of long-range coordinated oscillations in the sleeping human brain
Piantoni, G., van der Werf, Y. D., Jensen, O. B., & Someren, E. J. W. V. (2014) · Human Brain Mapping · doi:10.1002/hbm.22613 · Cited by 25
“Reactivation of distributed neuronal networks is thought to be of key importance in memory consolidation, in particular for tasks that require the integration of information from separate systems [Dang-Vu et al., 2010], such as the MT task used in this experiment [Fogel et al., 2007].”
MethodAutonomic Activity during a Daytime Nap Facilitates Working Memory Improvement
Chen, P., Whitehurst, L. N., Naji, M., & Mednick, S. C. (2020) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01588 · Cited by 20
“In addition, SWS has been linked to synaptic plasticity and cortical reorganization (Tononi and Cirelli, 2003; Takashima et al., 2006; Dang-Vu et al., 2010).”
BackgroundZempel, J. M., Politte, D. G., Kelsey, M., Verner, R., Nolan, T. S., Abbas Babajani-feremi, A., Prior, F., & Larson‐Prior, L. J. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00076 · Cited by 21
Altered brain perfusion patterns in wakefulness and slow-wave sleep in sleepwalkers
Desjardins, M.-È., Baril, A., Soucy, J., Dang‐Vu, T. T., Désautels, A., Petit, D., Montplaisir, J. Y., & Zadra, A. L. (2018) · SLEEP · doi:10.1093/sleep/zsy039 · Cited by 20
Self-citationEdwards, C. L., Malinowski, J., Rohner, S. L., Bennett, P. D., Ruby, P. M., & Blagrove, M. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00831 · Cited by 29
“…eye movement (REM) sleep, is involved in functional reorganization of the brain that subserves emotional memory consolidation (Nishida et al., 2009; Dang-Vu et al., 2010; Wamsley and Stickgold, 2011; Groch et al., 2013, 2015), emotion regulation (Walker and Van der Helm, 2009), and cognitive…”
BackgroundThe Neuroscience of Sleep and Dreams
McNamara, P. (2019) · Cambridge University Press eBooks · doi:10.1017/9781316817094 · Cited by 21
Llewellyn, S. (2016) · Consciousness and Cognition · doi:10.1016/j.concog.2016.09.018 · Cited by 17
Sleep-Dependent Consolidation of Value-Based Learning
Baran, B., Daniels, D., & Spencer, R. M. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075326 · Cited by 17
Stickgold, R., & Wamsley, E. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-24288-2.00048-9 · Cited by 17
Zhang, F., Zhong, R., Li, S., Chang, R. C., & Le, W. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1696-9 · Cited by 19
Metadata
- Authors
- Dang-Vu, T. T., Schabus, M., Desseilles, M., Sterpenich, V., Bonjean, M., & Maquet, P.
- Affiliations
- University of Liège (BE)
- University of Geneva (CH)
- Howard Hughes Medical Institute (US)
- Venue
- SLEEP
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-12
- Volume
- 33
- Issue
- 12
- Pages
- 1589-1603
- ISSN
- 0161-8105 (ISSN-L)
- 1550-9109
- PMC
- PMC2982729
- OpenAlex
- W2101059856
- Cited by
- 284
- References
- 166
- Citations by year
- 2026: 17 · 2025: 27 · 2024: 15 · 2023: 14 · 2022: 20 · 2021: 10 · 2020: 13 · 2019: 38 · 2018: 15 · 2017: 13 · 2016: 12 · 2015: 19 · 2014: 21 · 2013: 26 · 2012: 19
- FWCI
- 1.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- SLEEP (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Open Repository and Bibliography (University of Liège) (submittedVersion)
- Repository of the University of Namur (submittedVersion)
- Funders
- National Institute of Biomedical Imaging and Bioengineering (R01EB009282)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- sleep physiology, REM sleep, NREM sleep, sleep stages, dreams, sleep spindles, slow waves, sleep oscillations, brain energy homeostasis, medial prefrontal cortex, sleep and memory, memory consolidation
- MeSH terms
- Brain, Electroencephalography, Humans, Learning, Magnetic Resonance Imaging, Memory, Sleep, Wakefulness, Positron-Emission Tomography
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