Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning
Abstract
Sleep deprivation impairs hippocampal-dependent learning, which, in turn, is associated with increased survival of newborn cells in the hippocampus. We tested whether the deleterious effects of sleep restriction on hippocampus-dependent memory were associated with reduced cell survival in the hippocampus. We show that sleep restriction impaired hippocampus-dependent learning and abolished learning-induced neurogenesis. Animals were trained in a water maze on either a spatial learning (hippocampus-dependent) task or a nonspatial (hippocampus-independent) task for 4 days. Sleep-restricted animals were kept awake for one-half of their rest phase on each of the training days. Consistent with previous reports, animals trained on the hippocampus-dependent task expressed increased survival of newborn cells in comparison with animals trained on the hippocampus-independent task. This increase was abolished by sleep restriction that caused overall reduced cell survival in all animals. Sleep restriction also selectively impaired spatial learning while performance in the nonspatial task was, surprisingly, improved. Further analysis showed that in both training groups fully rested animals applied a spatial strategy irrespective of task requirements; this strategy interfered with performance in the nonspatial task. Conversely, in sleep-restricted animals, this preferred spatial strategy was eliminated, favoring the use of nonspatial information, and hence improving performance in the nonspatial task. These findings suggest that sleep loss altered behavioral strategies to those that do not depend on the hippocampus, concomitantly reversing the neurogenic effects of hippocampus-dependent learning.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Sleep restriction by novelty exposure prevents the increased survival of new dentate gyrus neurons promoted by spatial training in a Morris water maze.
“Nevertheless, sleep restriction by novelty exposure, a more subtle method, prevented the increased survival of new dentate gyrus neurons promoted by spatial training in a Morris water maze.77”
From Sleep Deprivation and Circadian Disruption (2015) · cites this paper as [77]
Sleep restriction by novelty exposure prevents the increased survival of new dentate gyrus neurons promoted by spatial training in a Morris water maze.
“Nevertheless, sleep restriction by novelty exposure, a more subtle method, prevented the increased survival of new dentate gyrus neurons promoted by spatial training in a Morris water maze.31”
From Protective and damaging effects of stress mediators: central role of the brain (2006) · cites this paper as [31]
Cites
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · see citing works
Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus
van Praag, H., Kempermann, G., & Gage, F. H. (1999) · Nature Neuroscience · doi:10.1038/6368 · Cited by 3,880 · see citing works
More hippocampal neurons in adult mice living in an enriched environment
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997) · Nature · doi:10.1038/386493a0 · Cited by 3,513 · see citing works
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Running enhances neurogenesis, learning, and long-term potentiation in mice
van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13427 · Cited by 2,904 · see citing works
Gratzner, H. G. (1982) · Science · doi:10.1126/science.7123245 · Cited by 2,653 · see citing works
Learning enhances adult neurogenesis in the hippocampal formation
Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999) · Nature Neuroscience · doi:10.1038/6365 · Cited by 2,157 · see citing works
Neurogenesis in the adult is involved in the formation of trace memories
Shors, T. J., Miesegaes, G. R., Beylin, A. V., Zhao, M., Rydel, T. A., & Gould, E. (2001) · Nature · doi:10.1038/35066584 · Cited by 2,014 · see citing works
Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854 · see citing works
Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus
Cameron, H. A., & Mckay, R. D. G. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1040 · Cited by 1,585 · see citing works
Memory of sequential experience in the hippocampus during slow wave sleep
Lee, A. K., & Wilson, M. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)01096-6 · Cited by 1,296 · see citing works
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148 · see citing works
Effects of early and late nocturnal sleep on declarative and procedural memory
Plihal, W., & Born, J. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.4.534 · Cited by 1,026 · see citing works
Dependence on REM Sleep of Overnight Improvement of a Perceptual Skill
Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. M., & Sagi, D. (1994) · Science · doi:10.1126/science.8036518 · Cited by 1,002 · see citing works
Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B. T., Vinet, M. C., Friocourt, G., McDonnell, N., Reiner, O., Kahn, A., et al. (1999) · Neuron · doi:10.1016/s0896-6273(00)80777-1 · Cited by 1,000 · see citing works
Doublecortin expression levels in adult brain reflect neurogenesis
Couillard‐Després, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., Bogdahn, U., Winkler, J., Kuhn, H. G., & Aigner, L. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03813.x · Cited by 967 · see citing works
Spatial memory and hippocampal function
Olton, D. S., & Paras, B. C. (1979) · Neuropsychologia · doi:10.1016/0028-3932(79)90042-3 · Cited by 927 · see citing works
Palmer, T. D., Markakis, E. A., Willhoite, A. R., Safar, F., & Gage, F. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-19-08487.1999 · Cited by 909 · see citing works
Self-citationMultiple Parallel Memory Systems in the Brain of the Rat
White, N. M., & McDonald, R. J. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4008 · Cited by 888 · see citing works
A role for adult neurogenesis in spatial long-term memory
Snyder, J. S., Hong, N. S., McDonald, R. J., & Wojtowicz, J. M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.10.009 · Cited by 854 · see citing works
Neurogenesis may relate to some but not all types of hippocampal‐dependent learning
Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., & Gould, E. (2002) · Hippocampus · doi:10.1002/hipo.10103 · Cited by 853 · see citing works
Stress and hippocampal neurogenesis
Gould, E., & Tanapat, P. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00247-4 · Cited by 805 · see citing works
Are spatial memories strengthened in the human hippocampus during slow wave sleep?
Peigneux, P., Laureys, S., Fuchs, S., Collette, F., Perrin, F., Reggers, J., Phillips, C., Degueldre, C., Del Fiore, G., Aerts, J., et al. (2004) · Neuron · doi:10.1016/j.neuron.2004.10.007 · Cited by 766 · see citing works
Adrenal hormones suppress cell division in the adult rat dentate gyrus
Gould, E., Cameron, H. A., Daniels, D., Woolley, C. S., & McEwen, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03642.1992 · Cited by 652 · see citing works
Sleep-dependent learning: A nap is as good as a night
Mednick, S., Nakayama, K., & Stickgold, R. (2003) · Nature Neuroscience · doi:10.1038/nn1078 · Cited by 594 · see citing works
Early sleep triggers memory for early visual discrimination skills
Gais, S., Plihal, W., Wagner, U., & Born, J. (2000) · Nature Neuroscience · doi:10.1038/81881 · Cited by 558 · see citing works
Kempermann, G., Brandon, E. P., & Gage, F. H. (1998) · Current Biology · doi:10.1016/s0960-9822(07)00377-6 · Cited by 385 · see citing works
Effects of early and late nocturnal sleep on priming and spatial memory
Plihal, W., & Born, J. (1999) · Psychophysiology · doi:10.1111/1469-8986.3650571 · Cited by 364 · see citing works
Leuner, B., Mendolia‐Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E., & Shors, T. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0204-04.2004 · Cited by 289 · see citing works
The relationships between memory systems and sleep stages
Rauchs, G., Desgranges, B., Foret, J., & Eustache, F. (2005) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2005.00450.x · Cited by 279 · see citing works
Ribeiro, S., Gervasoni, D., Soares, E. S., Zhou, Y., Lin, S.-C., Pantoja, J., Lavine, M., & Nicolelis, M. A. L. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020024 · Cited by 272 · see citing works
Sleep restriction alters the hypothalamic-pituitary-adrenal response to stress
Meerlo, P., Koehl, M., Van Der Borght, K., & Turek, F. W. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00790.x · Cited by 250 · see citing works
Sleep states, memory processes and synaptic plasticity
Smith, C. T. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00218-9 · Cited by 230 · see citing works
Sleep and memory: a molecular perspective
Graves, L. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01744-6 · Cited by 216 · see citing works
Evidence for a paradoxical sleep window for place learning in the Morris water maze
Smith, C., & Rose, G. M. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02054-3 · Cited by 211 · see citing works
Garcia, A. D. R., Steiner, B., Kronenberg, G., Bick‐Sander, A., & Kempermann, G. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00130.x · Cited by 209 · see citing works
Guan, Z., Peng, X., & Fang, J. (2004) · Brain Research · doi:10.1016/j.brainres.2004.05.032 · Cited by 208 · see citing works
Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats
Guzmán‐Marín, R., Suntsova, N., Stewart, D. R., Gong, H., Szymusiak, R., & McGinty, D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.041665 · Cited by 197 · see citing works
Sleep deprivation by the “flower pot” technique and spatial reference memory
Youngblood, B. D., Zhou, J., Smagin, G. N., Ryan, D. H., & Harris, R. B. S. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00363-0 · Cited by 167 · see citing works
Benington, J. H., Kodali, S., & Heller, H. C. (1994) · SLEEP · doi:10.1093/sleep/17.1.28 · Cited by 166 · see citing works
Self-citationWalicke, P. A., & Baird, A. (1988) · Developmental Brain Research · doi:10.1016/0165-3806(88)90009-0 · Cited by 155 · see citing works
Smith, C. T., Conway, J. M., & Rose, G. M. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3809 · Cited by 154 · see citing works
Posttraining paradoxical sleep in rats is increased after spatial learning in the Morris water maze.
Smith, C., & Rose, G. M. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.6.1197 · Cited by 127 · see citing works
Davis, C. J., Harding, J. W., & Wright, J. W. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02508-3 · Cited by 115 · see citing works
Ruskin, D. N., Liu, C., Dunn, K. E., Bazan, N. G., & LaHoste, G. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03426.x · Cited by 107 · see citing works
Cirelli, C. (2002) · Journal of Applied Physiology · doi:10.1152/jappl.2002.92.1.394 · Cited by 96 · see citing works
Gender and Strain Influence on Neurogenesis in Dentate Gyrus of Young Rats
Perfilieva, E., Risedal, A., Nyberg, J., Johansson, B. B., & Eriksson, P. S. (2001) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200103000-00004 · Cited by 85 · see citing works
Hairston, I. S., Peyron, C., Denning, D. P., Ruby, N. F., Flores, J., Sapolsky, R. M., Heller, H. C., & O’Hara, B. F. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00894.2003 · Cited by 79 · see citing works
Self-citationParadoxical sleep increases predict successful learning in a complex operant task.
Smith, C. T., & Wong, P. T. P. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.2.282 · Cited by 74 · see citing works
Paradoxical sleep increases predict successful learning in a complex operant task.
Smith, C., & Wong, P. T. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.2.282 · Cited by 74 · see citing works
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
Schaaf, M. J. M., Sibug, R. M., Duurland, R., Fluttert, M., Oitzl, M. S., de Kloet, E. R., & Vreugdenhil, E. (1999) · Stress · doi:10.3109/10253899909001121 · Cited by 51 · see citing works
Sleep deprivation elevates plasma corticosterone levels in neonatal rats
Hairston, I. S., Ruby, N. F., Brooke, S. M., Peyron, C., Denning, D. P., Heller, H. C., & Sapolsky, R. M. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)02309-6 · Cited by 49 · see citing works
Self-citationAwareness in memory: being explicit about the role of sleep
Jan Born, A., & Wagner, U. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.04.010 · Cited by 38 · see citing works
Miserendino, M. J. D., Haile, C. N., & Kosten, T. A. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1411-4 · Cited by 22 · see citing works
Jacobson, L., Brooke, S., & Sapolsky, R. (1993) · Brain Research · doi:10.1016/0006-8993(93)90140-i · Cited by 16 · see citing works
Self-citationNilsson (1999) · doi:10.1002/(sici)1097-4695(19990615)39:4
Flagged first, then by citations
Cited by
Sorted by citations
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
Control of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477 · see citing works
Protective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/bmcewen · Cited by 1,220 · see citing works
Neurogenesis may relate to some but not all types of hippocampal‐dependent learning
Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., & Gould, E. (2002) · Hippocampus · doi:10.1002/hipo.10103 · Cited by 853 · see citing works
Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load
McEwen, B. S. (2006) · Metabolism · doi:10.1016/j.metabol.2006.07.008 · Cited by 624 · see citing works
Spatial Relational Memory Requires Hippocampal Adult Neurogenesis
Dupret, D., Revest, J., Koehl, M., Ichas, F., Giorgi, F. D., Costet, P., Abrous, D. N., & Piazza, P. V. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001959 · Cited by 595 · see citing works
Is there a link between adult neurogenesis and learning?
Leuner, B., Gould, E., & Shors, T. J. (2006) · Hippocampus · doi:10.1002/hipo.20153 · Cited by 530 · see citing works
Environmental enrichment, new neurons and the neurobiology of individuality
Kempermann, G. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0120-x · Cited by 479 · see citing works
Structural Plasticity and Hippocampal Function
Leuner, B., & Gould, E. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100359 · Cited by 452 · see citing works
Lucassen, P. J., Meerlo, P., Naylor, A. S., van Dam, A. M., Dayer, A. G., Fuchs, E., Oomen, C. A., & Czéh, B. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.08.003 · Cited by 449 · see citing works
Beebe, D. W. (2006) · Sleep · doi:10.1093/sleep/29.9.1115 · Cited by 446 · see citing works
Fabel, K. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.22.002.2009 · Cited by 429 · see citing works
Spatial Learning Depends on Both the Addition and Removal of New Hippocampal Neurons
Dupret, D., Fabre, A., Döbrössy, M. D., Panatier, A., Rodriguez, J. J., Lamarque, S., Lemaire, V., Oliet, S. H. R., Piazza, P., & Abrous, D. N. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050214 · Cited by 387 · see citing works
Plümpe, T., Ehninger, D., Steiner, B., Klempin, F., Jessberger, S., Brandt, M., Römer, B., Rodriguez, G. R., Kronenberg, G., & Kempermann, G. (2006) · BMC Neuroscience · doi:10.1186/1471-2202-7-77 · Cited by 388 · see citing works
Sleep Deprivation and Circadian Disruption
McEwen, B. S., & Karatsoreos, I. N. (2015) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2014.11.007 · Cited by 338 · see citing works
New neurons in the adult brain: the role of sleep and consequences of sleep loss
Meerlo, P., Mistlberger, R. E., Jacobs, B. L., Craig Heller, H., & McGinty, D. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.07.004 · Cited by 318 · see citing works
Kreutzmann, J. C., Havekes, R., Abel, T., & Meerlo, P. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.053 · Cited by 309 · see citing works
Banks, S., Van Dongen, H. P. A., Maislin, G., & Dinges, D. F. (2010) · Sleep · doi:10.1093/sleep/33.8.1013 · Cited by 295 · see citing works
Schmidt, M. H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.001 · Cited by 291 · see citing works
The cognitive cost of sleep lost
McCoy, J. G., & Strecker, R. E. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.07.004 · Cited by 284 · see citing works
Adult Hippocampal Neurogenesis, Synaptic Plasticity and Memory: Facts and Hypotheses
Bruel‐Jungerman, E., Rampon, C., & Laroche, S. (2007) · Reviews in the Neurosciences · doi:10.1515/revneuro.2007.18.2.93 · Cited by 281 · see citing works
Chronic Insomnia and MRI-Measured Hippocampal Volumes: A Pilot Study
Riemann, D. W., Voderholzer, U., Spiegelhalder, K., Hornyak, M., Buysse, D. J., Nissen, C., Hennig, J., Perlis, M. L., van Elst, L. T., & Feige, B. (2007) · SLEEP · doi:10.1093/sleep/30.8.955 · Cited by 256 · see citing works
Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids
Mirescu, C., Peters, J. D., Noiman, L., & Gould, E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608644103 · Cited by 233 · see citing works
Total sleep deprivation, chronic sleep restriction and sleep disruption
Reynolds, A. C., & Banks, S. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53702-7.00006-3 · Cited by 209 · see citing works
Wadhwa, M., Prabhakar, A., Ray, K., Roy, K., Kumari, P., Jha, P. K., Kishore, K., Kumar, S., & Panjwani, U. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0998-z · Cited by 206 · see citing works
RetractedJoo, E. Y., Kim, H., Suh, S. A., & Hong, S. B. (2014) · SLEEP · doi:10.5665/sleep.3836 · Cited by 199 · see citing works
Sisti, H. M., Glass, A. L., & Shors, T. J. (2007) · Learning & Memory · doi:10.1101/lm.488707 · Cited by 188 · see citing works
Inflammatory cytokine-associated depression
Lotrich, F. E. (2015) · Brain Research · doi:10.1016/j.brainres.2014.06.032 · Cited by 183 · see citing works
Epp, J. R., Spritzer, M. D., & Galea, L. A. M. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.046 · Cited by 176 · see citing works
Rothman, S. M., Herdener, N., Frankola, K. A., Mughal, M. R., & Mattson, M. P. (2013) · Brain Research · doi:10.1016/j.brainres.2013.07.010 · Cited by 172 · see citing works
Cognitive neuroscience of sleep
Poe, G. R., Walsh, C. M., & Bjorness, T. E. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53702-7.00001-4 · Cited by 174 · see citing works
A time to remember: The role of circadian clocks in learning and memory.
Smarr, B. L., Jennings, K. J., Driscoll, J. R., & Kriegsfeld, L. J. (2014) · Behavioral Neuroscience · doi:10.1037/a0035963 · Cited by 166 · see citing works
Effects of sleep deprivation on neural functioning: an integrative review
Boonstra, T. W., Stins, J. F., Daffertshofer, A., & Beek, P. J. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6457-8 · Cited by 166 · see citing works
Cellular consequences of sleep deprivation in the brain☆
Cirelli, C. (2006) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2006.04.001 · Cited by 164 · see citing works
The Role of Sleep in Memory Consolidation and Brain Plasticity: Dream or Reality?
Frank, M. G., & Benington, J. H. (2006) · The Neuroscientist · doi:10.1177/1073858406293552 · Cited by 143 · see citing works
Experimental sleep deprivation as a tool to test memory deficits in rodents
Colavito, V., Fabene, P. F., Grassi-Zucconi, G., Pifferi, F., Lamberty, Y., Bentivoglio, M., & Bertini, G. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2013.00106 · Cited by 142 · see citing works
Hippocampal neurogenesis is reduced by sleep fragmentation in the adult rat
Guzmán-Marı́n, R., Bashir, T., Suntsova, N., Szymusiak, R. S., & McGinty, D. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.05.030 · Cited by 139 · see citing works
Blunden, S. L., & Beebe, D. W. (2006) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2005.11.003 · Cited by 128 · see citing works
Kim, Y., Laposky, A. D., Bergmann, B. M., & Turek, F. W. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610351104 · Cited by 128 · see citing works
Guzmán-Marı́n, R., Suntsova, N., Bashir, T., Nienhuis, R., Szymusiak, R. S., & McGinty, D. (2008) · SLEEP · doi:10.1093/sleep/31.2.167 · Cited by 125 · see citing works
Galea, L. A. M., Uban, K. A., Epp, J. R., Brummelte, S., Barha, C. K., Wilson, W. L., Lieblich, S. E., & Pawluski, J. L. (2008) · Canadian Journal of Experimental Psychology/Revue canadienne de psychologie expérimentale · doi:10.1037/a0014501 · Cited by 122 · see citing works
Sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones
Mueller, A. D., Pollock, M. S., Lieblich, S. E., Epp, J. R., Galea, L. A. M., & Mistlberger, R. E. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00858.2007 · Cited by 122 · see citing works
Neural plasticity and stress coping in teleost fishes
Sørensen, C., Johansen, I. B., & Øverli, Ø. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.12.003 · Cited by 120 · see citing works
Neurobiological Consequences of Sleep Deprivation
Alkadhi, K. A., Zagaar, M. A., Alhaider, I. A., Salim, S., & Aleisa, A. M. (2013) · Current Neuropharmacology · doi:10.2174/1570159x11311030001 · Cited by 121 · see citing works
Learning-Induced Survival of New Neurons Depends on the Cognitive Status of Aged Rats
Drapeau, E., Montaron, M., Aguerre, S., & Abrous, D. N. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1031-07.2007 · Cited by 119 · see citing works
Activity Dependency and Aging in the Regulation of Adult NeurogenesisPreprint
Kempermann, G. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018929 · Cited by 113 · see citing works
Frank, M. G., & Heller, H. C. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_140 · Cited by 109 · see citing works
Self-citationEffects of Sleep Deprivation on Memory in Mice: Role of State-Dependent Learning
Patti, C. L., Zanin, K. A., Sanday, L., Kameda, S. R., Fernandes‐Santos, L., Fernandes, H. A., Andersen, M. L., Tufik, S., & Frussa‐Filho, R. (2010) · SLEEP · doi:10.1093/sleep/33.12.1669 · Cited by 100 · see citing works
Hagewoud, R., Whitcomb, S. N., Heeringa, A. N., Havekes, R., Koolhaas, J. M., & Meerlo, P. (2010) · Sleep · doi:10.1093/sleep/33.10.1315 · Cited by 99 · see citing works
Chapter 5 Development of Neural Circuits in the Adult Hippocampus
Li, Y., Mu, Y., & Gage, F. H. (2009) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)01205-8 · Cited by 99 · see citing works
Adult Neurogenesis and Hippocampal Memory Function: New Cells, More Plasticity, New Memories?
Kitabatake, Y., Sailor, K. A., Ming, G., & Song, H. (2007) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2006.10.008 · Cited by 96 · see citing works
Fox, H. C., Jackson, E. D., & Sinha, R. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.03.007 · Cited by 99 · see citing works
Hippocampus-dependent learning influences hippocampal neurogenesis
Epp, J. R., Chow, C., & Galea, L. A. M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00057 · Cited by 95 · see citing works
Neuroimaging findings in primary insomnia
O’Byrne, J., Rosa, M. B., Gouin, J.-P., & Dang‐Vu, T. T. (2014) · Pathologie Biologie · doi:10.1016/j.patbio.2014.05.013 · Cited by 92 · see citing works
Coping with Sleep Deprivation: Shifts in Regional Brain Activity and Learning Strategy
Hagewoud, R., Havekes, R., Tiba, P. A., Novati, A., Hogenelst, K., Weinreder, P., van der Zee, E. A., & Meerlo, P. (2010) · SLEEP · doi:10.1093/sleep/33.11.1465 · Cited by 92 · see citing works
Impact 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
‘One night’ sleep deprivation stimulates hippocampal neurogenesis
Grassi Zucconi, G., Cipriani, S., Balgkouranidou, I., & Scattoni, R. (2006) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.01.009 · Cited by 86 · see citing works
Wadhwa, M., Prabhakar, A., Anand, J. P., Ray, K., Prasad, D. N., Kumar, B., & Panjwani, U. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.08.004 · Cited by 82 · see citing works
RetractedDaurat, A., Foret, J., Bret-Dibat, J. L., Fureix, C., & Tiberge, M. (2007) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390701236116 · Cited by 80 · see citing works
Beyond refueling: Investigating the diversity of functions of migratory stopover events
Linscott, J. A., & Senner, N. R. (2021) · Ornithological Applications · doi:10.1093/ornithapp/duaa074 · Cited by 80 · see citing works
Animal Studies on the Role of Sleep in Memory: From Behavioral Performance to Molecular Mechanisms
Havekes, R., Meerlo, P., & Abel, T. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_369 · Cited by 78 · see citing works
Ecologically relevant spatial memory use modulates hippocampal neurogenesis
LaDage, L. D., Roth, T. C., Fox, R. A., & Витальевич, П. В. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.1769 · Cited by 78 · see citing works
The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation
Roth, T. C., Rattenborg, N. C., & Витальевич, П. В. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0209 · Cited by 79 · see citing works
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
Neurogenesis in the aged and neurodegenerative brain
Shruster, A., Melamed, E., & Offen, D. (2010) · APOPTOSIS · doi:10.1007/s10495-010-0491-y · Cited by 74 · see citing works
Sleep, dreaming, and mental health: A review of historical and neurobiological perspectives
Palagini, L., & Rosenlicht, N. Z. (2010) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2010.07.003 · Cited by 74 · see citing works
Microbiota-Gut-Brain Axis Regulation of Adult Hippocampal Neurogenesis
Guzzetta, K. E., Cryan, J. F., & O’Leary, O. F. (2022) · Brain Plasticity · doi:10.3233/bpl-220141 · Cited by 74 · see citing works
Dalla, C., Bangasser, D. A., Edgecomb, C., & Shors, T. J. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.02.003 · Cited by 70 · see citing works
Shors, T. J., Olson, R. L., Bates, M. E., Selby, E. A., & Alderman, B. L. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.08.012 · Cited by 69 · see citing works
Sleep Deprivation and Circadian Disruption Stress, Allostasis, and Allostatic Load
McEwen, B. S., & Karatsoreos, I. N. (2022) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2022.03.005 · Cited by 70 · see citing works
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
Li, M., Wang, R., Zhao, M., Zhai, J., Liu, B., Yu, D., & Yuan, K. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9932-y · Cited by 65 · see citing works
Sahu, S., Kauser, H., Ray, K., Kishore, K., Kumar, S., & Panjwani, U. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.07.021 · Cited by 66 · see citing works
Ward, C. P., McCoy, J. G., McKenna, J. T., Connolly, N. P., McCarley, R. W., & Strecker, R. E. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.064 · Cited by 66 · see citing works
Tosini, G., Ye, K., & Iuvone, P. M. (2012) · The Neuroscientist · doi:10.1177/1073858412446634 · Cited by 65 · 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
Leuner, B., Waddell, J., Gould, E., & Shors, T. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2781-06.2006 · Cited by 60 · see citing works
Sleep Extension before Sleep Loss
Arnal, P. J., Lapole, T., Erblang, M., Guillard, M., Bourrilhon, C., Léger, D., Chennaoui, M., & Millet, G. Y. (2016) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000925 · Cited by 59 · see citing works
Neural Consequences of Chronic Short Sleep: Reversible or Lasting?
Zhao, Z., Zhao, X., & Veasey, S. C. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00235 · Cited by 58 · see citing works
Sleep Characteristics and Temperament in Preterm Children at Two Years of Age
Caravale, B., Sette, S., Cannoni, E., Marano, A., Riolo, E., Devescovi, A., Curtis, M. D., & Bruni, O. (2017) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.6728 · Cited by 57 · see citing works
Daulatzai, M. A. (2013) · Neurotoxicity Research · doi:10.1007/s12640-013-9407-2 · Cited by 55 · see citing works
Task difficulty in the Morris water task influences the survival of new neurons in the dentate gyrus
Epp, J. R., Haack, A. K., & Galea, L. A. M. (2009) · Hippocampus · doi:10.1002/hipo.20692 · Cited by 55 · see citing works
Mueller, A. D., Mear, R. J., & Mistlberger, R. E. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.019 · Cited by 54 · see citing works
Detrimental role of prolonged sleep deprivation on adult neurogenesis
Fernandes, C., Rocha, N., Rocha, S., Herrera-Solís, A., Salas-Pacheco, J. M., García‐García, F., Murillo‐Rodríguez, E., Yuan, T., Machado, S. E. D. C., & Arias-Carrión, Ó. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00140 · Cited by 54 · see citing works
Trauma exposure and sleep: using a rodent model to understand sleep function in PTSD
Vanderheyden, W. M., Poe, G. R., & Liberzon, I. (2014) · Experimental Brain Research · doi:10.1007/s00221-014-3890-4 · Cited by 54 · see citing works
LaDage, L. D., Roth, T. C., & Витальевич, П. В. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.0861 · Cited by 52 · see citing works
Ettore, É., Bakardjian, H., Sole, M., Lévy, M., Habert, M., Gabelle, A., Dubois, B., Robert, P. H., & David, R. (2019) · SLEEP · doi:10.1093/sleep/zsz137 · Cited by 52 · see citing works
Epp, J. R., Haack, A. K., & Galea, L. A. M. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.01.001 · Cited by 51 · see citing works
5‐HT7, NEUROGENESIS AND ANTIDEPRESSANTS: A PROMISING THERAPEUTIC AXIS FOR TREATING DEPRESSION
Nandam, L. S., Jhaveri, D. J., & Bartlett, P. F. (2007) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2007.04608.x · Cited by 50 · see citing works
Olonode, E. T., Aderibigbe, A. O., Adeoluwa, O. A., Eduviere, A. T., & Ben‐Azu, B. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.024 · Cited by 49 · see citing works
Zielinski, M. R., Davis, J. M., Fadel, J. R., & Youngstedt, S. D. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.038 · Cited by 49 · see citing works
Leung, J. W.-H., Cheung, K., Ngai, S. P. C., Tsang, H. W. H., & Lau, B. W.-M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165645 · Cited by 48 · see citing works
Mohlenhoff, B. S., O’Donovan, A., Weiner, M. W., & Neylan, T. C. (2017) · Current Psychiatry Reports · doi:10.1007/s11920-017-0835-1 · Cited by 47 · see citing works
The pharmacology of wakefulness
Miller, D. B., & O'Callaghan, J. P. (2006) · Metabolism · doi:10.1016/j.metabol.2006.07.007 · Cited by 46 · see citing works
Soto-Rodríguez, S., López-Armas, G. D. C., Luquı́n, S., Ramos-Zúñiga, R., Jáuregui-Huerta, F., González-Pérez, Ó., & González-Castañeda, R. E. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00132 · Cited by 46 · see citing works
Zhang, P., Tan, C.-W., Chen, G.-H., Ge, Y.-J., Xu, J., Xia, L., Wang, F., Li, X., & Kong, X.-Y. (2018) · Sleep Medicine · doi:10.1016/j.sleep.2017.12.012 · Cited by 46 · see citing works
Short-term sleep deprivation may alter the dynamics of hippocampal cell proliferation in adult rats
Junek, A., Rusak, B., & Semba, K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.018 · Cited by 42 · see citing works
Epp, J. R., Scott, N. A., & Galea, L. A. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.025 · Cited by 44 · see citing works
Yang, S.-R., Sun, H., Huang, Z., Yao, M., & Qu, W. (2012) · SLEEP · doi:10.5665/sleep.1888 · Cited by 44 · see citing works
The Functional Impact of Sleep Deprivation, Sleep Restriction, and Sleep Fragmentation
Short, M. A., & Banks, S. (2013) · Springer eBooks · doi:10.1007/978-1-4614-9087-6_2 · Cited by 42 · see citing works
- Authors
- Hairston, I. S., Little, M. T. M., Scanlon, M. D., Barakat, M. T., Palmer, T. D., Sapolsky, R. M., & Heller, H. C.
- Affiliations
- University of California, Berkeley (US)
- ORCID
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2005-12
- Volume
- 94
- Issue
- 6
- Pages
- 4224-4233
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2096232633
- Cited by
- 223
- References
- 57
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 6 · 2023: 2 · 2022: 5 · 2021: 4 · 2020: 11 · 2019: 11 · 2018: 6 · 2017: 13 · 2016: 9 · 2015: 20 · 2014: 11 · 2013: 17 · 2012: 10
- FWCI
- 7.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01hd037315-05)
- National Institute of Mental Health (F31-MH-65168-01, F31MH065168)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD37315)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- sleep restriction, sleep deprivation, hippocampus-dependent learning, spatial learning, hippocampal neurogenesis, water maze, behavioral strategies, memory consolidation
- MeSH terms
- Doublecortin Domain Proteins, Animals, Behavior, Animal, Bromodeoxyuridine, Cell Count, Cell Survival, Corticosterone, Cues, Hippocampus, Immunohistochemistry, Learning, Microtubule-Associated Proteins, Neurons, Neuropeptides, Radioimmunoassay, Reaction Time, Sleep Deprivation, Spatial Behavior, Time Factors, Chi-Square Distribution, Polysomnography, Maze Learning, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review