Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats

Guzmán‐Marín, Ruben; Suntsova, Natalia; Stewart, Darya R.; Gong, Hui; Szymusiak, Ronald; McGinty, Dennis

doi:10.1113/jphysiol.2003.041665

Cited by 197Neurogenesis and neuroplasticity mechanismsSleep and Wakefulness ResearchSleep and Work-Related Fatigue

Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats

Open access

Guzmán‐Marín, Ruben, Suntsova, Natalia, Stewart, Darya R., Gong, Hui, Szymusiak, Ronald, McGinty, Dennis·2003·The Journal of Physiology

DOI 10.1113/jphysiol.2003.041665PMC PMC2342950

Open this paper in CoChat — free account

Abstract

The dentate gyrus (DG) of the adult hippocampus gives rise to progenitor cells, which have the potential to differentiate into neurons. To date it is not known whether sleep or sleep loss has any effect on proliferation of cells in the DG. Male rats were implanted for polysomnographic recording, and divided into treadmill sleep-deprived (SD), treadmill control (TC) and cage control (CC) groups. SD and TC rats were kept for 96 h on a treadmill that moved either for 3 s on/12 s off (SD group) or for 15 min on/60 min off (TC group) to equate total movement but permit sustained rest periods in TC animals. To label proliferating cells the thymidine analogue 5-bromo-2'-deoxyuridine (BrdU) was injected after the first 48 h of the experimental procedure in all groups (50 mg kg-1, I.P.). The percentage of time awake per day was 93.2 % in the SD group vs. 59.6 % in the TC group and 49.9 % in the CC group (P < 0.001). Stereological analysis showed that the number of BrdU-positive cells in the DG of the dorsal hippocampus was reduced by 54 % in the SD group in comparison with the TC and by 68 % in comparison with the CC group. These results suggest that sleep deprivation reduces proliferation of cells in the DG of the dorsal hippocampus.

Integrity signals

Registry

Crossref · 10.1113/jphysiol.2003.041665

Cites

90 of 90 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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 deprivation in rats using a treadmill for 96 hours decreases proliferation of cells in the dentate gyrus of the hippocampal formation by as much as 50%.
“sleep deprivation in rats using a treadmill for 96 hours has been reported to decrease proliferation of cells in the dentate gyrus of the hippocampal formation by as much as 50%.75”
From Sleep Deprivation and Circadian Disruption (2015) · cites this paper as [75]
Sleep deprivation in rats using a treadmill for 96 hours decreases proliferation of cells in the dentate gyrus of the hippocampal formation by as much as 50%.
“Sleep deprivation in rats using a treadmill for 96 hours has been reported to decrease proliferation of cells in the dentate gyrus of the hippocampal formation by as much as 50 %.29”
From Protective and damaging effects of stress mediators: central role of the brain (2006) · cites this paper as [29]

The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Neurogenesis in the adult human hippocampus
Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.-M., Nordborg, C., Peterson, D. A., & Gage, F. H. (1998) · Nature Medicine · doi:10.1038/3305 · Cited by 6,369 · 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
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats
Altman, J., & Das, G. D. (1965) · Journal of Comparative Neurology · doi:10.1002/cne.901240303 · Cited by 3,592 · see citing works
The Neuroendocrinology of Stress: A Never Ending Story
Lightman, S. L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01711.x · Cited by 3,570 · 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
Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation
Kuhn, H., Dickinson-Anson, H., & Gage, F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02027.1996 · Cited by 3,139 · see citing works
Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus
Malberg, J. E., Eisch, A. J., Nestler, E. J., & Duman, R. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09104.2000 · Cited by 3,111 · see citing works
Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · 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
Exercise: a behavioral intervention to enhance brain health and plasticity
Cotman, C. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02143-4 · Cited by 2,739 · see citing works
Long-Distance Neuronal Migration in the Adult Mammalian Brain
Lois, C., & Álvarez-Buylla, A. (1994) · Science · doi:10.1126/science.8178174 · Cited by 2,331 · see citing works
Cellular energy utilization and molecular origin of standard metabolic rate in mammals
Rolfe, D. F., & Brown, G. C. (1997) · Physiological Reviews · doi:10.1152/physrev.1997.77.3.731 · Cited by 2,021 · 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
Hippocampal atrophy in recurrent major depression
Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., & Vannier, M. W. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.9.3908 · Cited by 1,932 · see citing works
The Nature of the Arrestin·Receptor Complex Determines the Ultimate Fate of the Internalized Receptor
Pan, L., Gurevich, E. V., & Gurevich, V. V. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m209532200 · Cited by 1,758 · see citing works
Hippocampal Volume Reduction in Major Depression
Bremner, J. D., Narayan, M., Anderson, E. R., Staib, L. H., Miller, H. L., & Charney, D. S. (2000) · American Journal of Psychiatry · doi:10.1176/ajp.157.1.115 · Cited by 1,670 · see citing works
Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson.
Gundersen, H. J. G. (1986) · PubMed · Cited by 1,659 · 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
Neurogenesis in the Dentate Gyrus of the Adult Tree Shrew Is Regulated by Psychosocial Stress and NMDA Receptor Activation
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496 · see citing works
Neurogenesis in the Adult Rat: Electron Microscopic Analysis of Light Radioautographs
Kaplan, M., & Hinds, J. W. (1977) · Science · doi:10.1126/science.887941 · Cited by 1,478 · see citing works
Stereology of arbitrary particles*
Gundersen, H. J. G. (1986) · Journal of Microscopy · doi:10.1111/j.1365-2818.1986.tb02764.x · Cited by 1,444 · see citing works
Depression Duration But Not Age Predicts Hippocampal Volume Loss in Medically Healthy Women with Recurrent Major Depression
Sheline, Y. I., Sanghavi, M., Mintun, M. A., & Gado, M. H. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-12-05034.1999 · Cited by 1,382 · cited 1× · see citing works
“Reductions in hippocampal volume have been reported in depression (Sheline et al. 1996, 1999; Shah et al. 1998; Bremner et al. 2000).”
Background
Correlates of Sleep and Waking in Drosophila melanogaster
Shaw, P. J., Cirelli, C., Greenspan, R. J., & Tononi, G. (2000) · Science · doi:10.1126/science.287.5459.1834 · Cited by 1,300 · see citing works
The Circadian Gene Period2 Plays an Important Role in Tumor Suppression and DNA Damage Response In Vivo
Fu, L., Pelicano, H., Liu, J., Huang, P., & Lee, C. C. (2002) · Cell · doi:10.1016/s0092-8674(02)00961-3 · Cited by 1,256 · see citing works
Adenosine: A Mediator of the Sleep-Inducing Effects of Prolonged Wakefulness
Porkka-Heiskanen, T., Strecker, R. E., Thakkar, M., Bjørkum, A. A., Greene, R. W., & McCarley, R. W. (1997) · Science · doi:10.1126/science.276.5316.1265 · Cited by 1,252 · see citing works
Epidermal Growth Factor and Fibroblast Growth Factor-2 Have Different Effects on Neural Progenitors in the Adult Rat Brain
Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J., & Gage, F. H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05820.1997 · Cited by 1,208 · see citing works
Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats.
Black, J. E., Isaacs, K. R., Anderson, B. J., Alcantara, A. A., & Greenough, W. T. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.14.5568 · Cited by 1,161 · see citing works
Unbiased stereological estimation of the number of neurons in the human hippocampus
West, M. J., & Gundersen, H. J. G. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902960102 · Cited by 1,153 · cited 1× · see citing works
“The stereological sampling scheme was considered adequate when CE was less than 0.10 (West & Gundersen, 1990).”
MethodInfluential
Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging
Sapolsky, R., Krey, L., & McEwen, B. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01222.1985 · Cited by 1,129 · see citing works
Rest in Drosophila is a sleep-like state
Hendricks, J. C., Finn, S. M., Panckeri, K. A., Chavkin, J., Williams, J. A., Sehgal, A., & Pack, A. I. (2000) · Neuron · doi:10.1016/s0896-6273(00)80877-6 · Cited by 1,050 · see citing works
Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus
Lemaire, V., Koehl, M., Le Moal, M., & Abrous, D. N. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.20.11032 · Cited by 1,044 · cited 3× · see citing works
“Spatial learning was shown to promote hippocampal neurogenesis, including cell proliferation (Lemaire et al. 2000) and, on the other hand, to be impaired by Jo u rn al o f P hy si ol og y sleep deprivation (Youngblood et al. 1997, 1999; Smith & Rose, 1996, 1997; Smith et al. 1998).”
Background
Adult brain neurogenesis and psychiatry: a novel theory of depression
Jacobs, B. L., van Praag, H., & Gage, F. H. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000712 · Cited by 964 · see citing works
Infusion of Brain-Derived Neurotrophic Factor into the Lateral Ventricle of the Adult Rat Leads to New Neurons in the Parenchyma of the Striatum, Septum, Thalamus, and Hypothalamus
Pencea, V., Bingaman, K. D., Wiegand, S. J., & Luskin, M. B. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06706.2001 · Cited by 928 · see citing works
Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions
Moser, E., Moser, M. ‐., & Andersen, P. N. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03916.1993 · Cited by 916 · see citing works
Reduced fear expression after lesions of the ventral hippocampus
Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152112399 · Cited by 912 · see citing works
Peripheral Infusion of IGF-I Selectively Induces Neurogenesis in the Adult Rat Hippocampus
Åberg, M. A. I., Åberg, N. D., Hedbäcker, H., Oscarsson, J., & Eriksson, P. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-08-02896.2000 · Cited by 852 · see citing works
Restoration of brain energy metabolism as the function of sleep
Benington, J. H., & Heller, H. C. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00057-o · Cited by 828 · see citing works
Continuation of neurogenesis in the hippocampus of the adult macaque monkey
Kornack, D. R., & RAKIC, P. T. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5768 · Cited by 779 · see citing works
Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity
Gómez-Pinilla, F., Ying, Z., Roy, R. R., Molteni, R., & Edgerton, V. R. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00152.2002 · Cited by 724 · see citing works
Restoring production of hippocampal neurons in old age
Cameron, H. A., & McKay, R. D. G. (1999) · Nature Neuroscience · doi:10.1038/13197 · Cited by 710 · see citing works
Neural plasticity to stress and antidepressant treatment
Duman, R. S., Malberg, J. E., & Thome, J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00177-8 · Cited by 644 · see citing works
Sleep Enhances Plasticity in the Developing Visual Cortex
Frank, M. G., Issa, N. P., & Stryker, M. P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00279-3 · Cited by 523 · see citing works
Neurogenesis in adult primate neocortex: an evaluation of the evidence
RAKIC, P. T. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn700 · Cited by 491 · see citing works
Sleep Deprivation in the Rat: X. Integration and Discussion of the Findings
Rechtschaffen, A., Bergmann, B. M., Everson, C. A., Kushida, C. A., & Gilliland, M. A. (2002) · SLEEP · doi:10.1093/sleep/25.1.68 · Cited by 490 · see citing works
Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study
Porkka‐Heiskanen, T., Strecker, R. E., & McCarley, R. W. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00220-7 · Cited by 463 · see citing works
Molecular Mechanisms of Depression: Perspectives on New Treatment Strategies
Lang, U., & Borgwardt, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350094 · Cited by 396 · see citing works
Cortical grey matter reductions associated with treatment-resistant chronic unipolar depression
Shah, P. J., Ebmeier, K. P., Glabus, M. F., & Goodwin, G. M. (1998) · The British Journal of Psychiatry · doi:10.1192/bjp.172.6.527 · Cited by 395 · see citing works
Migration of young neurons in adult avian brain
Álvarez-Buylla, A., & Nottebohm, F. (1988) · Nature · doi:10.1038/335353a0 · Cited by 352 · see citing works
Electrolytic Lesions of the Fimbria/Fornix, Dorsal Hippocampus, or Entorhinal Cortex Produce Anterograde Deficits in Contextual Fear Conditioning in Rats
Maren, S., & Fanselow, M. S. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.3752 · Cited by 324 · see citing works
Brain Glycogen Decreases with Increased Periods of Wakefulness: Implications for Homeostatic Drive to Sleep
Kong, J., Shepel, P. N., Holden, C. P., Mackiewicz, M., Pack, A. I., & Geiger, J. D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05581.2002 · Cited by 281 · see citing works
Effects of acute physical exercise on central serotonergic systems
CHAOULOFF, F. (1997) · Medicine &amp Science in Sports &amp Exercise · doi:10.1097/00005768-199701000-00009 · Cited by 275 · see citing works
Sleep and Altered States of Consciousness
Daly, D. D. (1968) · Neurology · doi:10.1212/wnl.18.9.931 · Cited by 274 · see citing works
Spatial learning and physical activity contribute to the induction of fibroblast growth factor: neural substrates for increased cognition associated with exercise
Gómez‐Pinilla, F., So, V., & Kesslak, J. P. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00576-9 · Cited by 262 · 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
Effects of Method, Duration, and Sleep Stage on Rebounds from Sleep Deprivation in the Rat
Rechtschaffen, A., Bergmann, B. M., Gilliland, M. A., & Bauer, K. (1999) · SLEEP · doi:10.1093/sleep/22.1.11 · Cited by 231 · see citing works
Differential Effects of Dorsal and Ventral Hippocampal Lesions
Hock, B. J., & Bunsey, M. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-07027.1998 · Cited by 220 · 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
Sleep function(s) and cerebral metabolism
Maquet, P. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00017-n · Cited by 187 · see citing works
Extracellular adenosine levels in neostriatum and hippocampus during rest and activity periods of rats
Huston, J. P., Haas, H. L., Boix, F., Pfister, M., Decking, U. K. M., Schrader, J., & Schwarting, R. K. W. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00021-8 · Cited by 184 · see citing works
Circadian Variation in the Expression of Cell-Cycle Proteins in Human Oral Epithelium
Bjarnason, G. A., Jordan, R. C., & Sothern, R. B. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65306-0 · Cited by 176 · see citing works
Sleep and activity: their relation to the 24-hour clock.
Cp, R. (1967) · PubMed · Cited by 170 · 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
Sleep Deprivation in the Rat: I. Conceptual Issues
Rechtschaffen, A., Bergmann, B. M., Everson, C. A., Kushida, C. A., & Carol, A. E. (1989) · SLEEP · doi:10.1093/sleep/12.1.1 · Cited by 154 · see citing works
Brief Paradoxical Sleep Deprivation Impairs Reference, but Not Working, Memory in the Radial Arm Maze Task
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
Positive Correlations Between Cerebral Protein Synthesis Rates and Deep Sleep in <i>Macaca mulatta</i>
Nakanishi, H., Sun, Y., Nakamura, R. K., Mori, K., Ito, M., Suda, S., Namba, H., Storch, F. I., Dang, T. P., Mendelson, W., et al. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01397.x · Cited by 154 · see citing works
Sleep as neuronal detoxification and restitution
Inoué, S., Honda, K., & Komoda, Y. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00014-k · Cited by 151 · see citing works
Sleep-wakefulness patterns in the helpless rat
Adrien, J., Dugovic, C., & Martin, P. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90041-l · Cited by 140 · see citing works
Stress induced by three procedures of deprivation of paradoxical sleep
Coenen, A. M. L., & VANLUIJTELAAR, E. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90130-1 · Cited by 136 · 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
ATP-dependent DNA ligases.
Martin, I. V., & MacNeill, S. A. (2002) · Genome biology · doi:10.1186/gb-2002-3-4-reviews3005 · Cited by 122 · see citing works
Differential effect of short-term REM sleep deprivation on NGF and BDNF protein levels in the rat brain
Sei, H., Saitoh, D., Yamamoto, K., Morita, K., & Morita, Y. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02708-6 · Cited by 99 · see citing works
Brain-derived neurotrophic factor enhances spontaneous sleep in rats and rabbits
Kushikata, T., Fang, J., & Krueger, J. M. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.5.r1334 · Cited by 95 · see citing works
No evidence of brain cell degeneration after long-term sleep deprivation in rats1Published on the World Wide Web on 8 July 1999.1
Cirelli, C., Shaw, P. J., Rechtschaffen, A., & Tononi, G. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01768-0 · Cited by 85 · see citing works
A clonal analysis of glial lineages in neonatal forebrain development in vitro
Vaysse, P. J. ‐., & Goldman, J. E. (1990) · Neuron · doi:10.1016/0896-6273(90)90160-h · Cited by 84 · see citing works
Sleep deprivation modulates brain mRNAs encoding genes of glycogen metabolism
Petit, J., Tobler, I., Allaman, I., Borbély, A. A., & Magistretti, P. J. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02145.x · Cited by 81 · see citing works
The effect of sleep deprivation and recovery sleep on plasma corticosterone in the rat
Tobler, I., Murison, R. C. C., Ursin, R., Ursin, H., & Borbély, A. A. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90333-6 · Cited by 79 · see citing works
Exercise‐induced changes in brain glucose and serotonin revealed by microdialysis in rat hippocampus: effect of glucose supplementation
Bequet, F., Gomez-Mérino, D., Berthelot, M., et al. (2001) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2001.00859.x · Cited by 57 · see citing works
REM Sleep Deprivation in Monocularly Occluded Kittens Reduces the Size of Cells in LGN Monocular Segment
Shaffery, J. P., Oksenberg, A., Marks, G. A., Speciale, S. G., Mihailoff, G. A., & Roffwarg, H. P. (1998) · SLEEP · doi:10.1093/sleep/21.8.837 · Cited by 57 · see citing works
Epidermal growth factor enhances spontaneous sleep in rabbits
Kushikata, T., Fang, J., Chen, Z., Wang, Y., & Krueger, J. M. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.2.r509 · Cited by 56 · see citing works
The Effects of Paradoxical Sleep Deprivation and Valine on Spatial Learning and Brain 5-HT Metabolism
Youngblood, B. D., Smagin, G. N., Elkins, P. D., Ryan, D. H., & Harris, R. B. S. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00120-1 · Cited by 54 · see citing works
A1 adenosine receptor activation inhibits neurite process formation by rho kinase-mediated pathways
Thevananther, S., Rivera, A. L., & Rivkees, S. A. (2001) · Neuroreport · doi:10.1097/00001756-200110080-00015 · Cited by 37 · see citing works
Diurnal Variations in the Expression of Radiation-Induced Apoptosis
Ruifrok, A. C. C., Weil, M. M., Thames, H. D., et al. (1998) · Radiation Research · doi:10.2307/3579698 · Cited by 36 · see citing works
Changes in sleep in response to intracerebral injection of insulin-like growth factor-1 (IFG-1) in the rat.
Obál, F., Kapás, L., Bodosi, B., & Krueger, J. M. (1998) · PubMed · Cited by 32 · see citing works
Neurodegeneration, sleep, and cerebral energy metabolism: a testable hypothesis
Mamelak, M. (1997) · Journal of Geriatric Psychiatry and Neurology · doi:10.1177/089198879701000106 · Cited by 31 · see citing works
Distinct sleep-wake stages in rats depend differentially on age
Kirov, R., & Moyanova, S. G. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00096-4 · Cited by 25 · see citing works
The Effects of Aging and Dorsal Hippocampal Lesions: Performance on Spatial and Nonspatial Comparable Versions of the Water Maze
Stoelzel, C. R. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4054 · Cited by 21 · see citing works
Effects of light physical exercise on sleep regulation in rats
Gambelunghe, C., Rossi, R., Mariucci, G., et al. (2001) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200101000-00010 · Cited by 16 · see citing works
Dorsal hippocampal lesions impair appetitive classical conditioning to localized cues
Bonardi, C. (2001) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2001.01504.x · Cited by 7 · see citing works
Untitled work
(1998) · doi:10.1002/(sici)1098-1063(1998)8:6

Flagged first, then by citations

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
Clues to the functions of mammalian sleep
Siegel, J. M. (2005) · Nature · doi:10.1038/nature04285 · Cited by 1,040 · 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
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
Self-citation
Sleep deprivation and hippocampal vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function
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
The energy allocation function of sleep: A unifying theory of sleep, torpor, and continuous wakefulness
Schmidt, M. H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.001 · Cited by 291 · see citing works
The timing of antidepressant effects: a comparison of diverse pharmacological and somatic treatments
Machado-Vieira, R., Baumann, J., Wheeler-Castillo, C., Latov, D., Henter, I. D., Salvadore, G., & Zarate, C. A. (2010) · Pharmaceuticals · doi:10.3390/ph3010019 · Cited by 263 · see citing works
Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning
Hairston, I. S., Little, M. T. M., Scanlon, M. D., Barakat, M. T., Palmer, T. D., Sapolsky, R. M., & Heller, H. C. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00218.2005 · Cited by 223 · see citing works
Suppression of hippocampal plasticity‐related gene expression by sleep deprivation in rats
Guzman‐Marin, R., Ying, Z., Suntsova, N., Methippara, M., Bashir, T., Szymusiak, R., Gomez‐Pinilla, F., & McGinty, D. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.115287 · Cited by 206 · see citing works
Self-citation
Rapid Onset of Antidepressant Action: A New Paradigm in the Research and Treatment of Major Depressive Disorder
Machado-Vieira, R., Salvadore, G., Luckenbaugh, D. A., Manji, H. K., & Zarate, C. A. (2008) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v69n0610 · Cited by 195 · 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
The lullaby of the sun: The role of vitamin D in sleep disturbance
Muscogiuri, G., Barrea, L., Scannapieco, M., Di Somma, C., Scacchi, M., Aimaretti, G., Savastano, S., Colao, A., & Marzullo, P. (2019) · Sleep Medicine · doi:10.1016/j.sleep.2018.10.033 · Cited by 102 · see citing works
Sleep restriction by forced activity reduces hippocampal cell proliferation
Roman, V., Van der Borght, K., Leemburg, S. A., Van der Zee, E. A., & Meerlo, P. (2005) · Brain Research · doi:10.1016/j.brainres.2005.10.020 · Cited by 93 · 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

Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis
Lichtenwalner, R. J., Forbes, M. E., Bennett, S. A., Lynch, C. D., Sonntag, W. E., & Riddle, D. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00378-5 · Cited by 428 · see citing works
Differential neurogenesis in the adult rat dentate gyrus: an identifiable zone that consistently lacks neurogenesis
Melvin, N. R., Spanswick, S. C., Lehmann, H., & Sutherland, R. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05363.x · Cited by 8 · see citing works
190. Neurogenesis Inhibits Stress-Responsive Cells in the Ventral Dentate Gyrus
Anacker, C., Luna, V. M., Stevens, G. S., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.02.209 · Cited by 1 · see citing works
Impact of age and caloric restriction on neurogenesis in the dentate gyrus of C57BL/6 mice
Bondolfi, L., Ermini, F., Long, J. M., Ingram, D. K., & Jucker, M. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00083-6 · Cited by 264 · see citing works
A combination of running and memantine increases neurogenesis and reduces activation of developmentally-born dentate granule neurons in rats
Cahill, S. P., Martinovic, A., Cole, J. D., Seib, D. R., & Snyder, J. S. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112005 · Cited by 8 · see citing works

Authors: Guzmán‐Marín, R., Suntsova, N., Stewart, D. R., Gong, H., Szymusiak, R., & McGinty, D.
Affiliations: Southern Federal University (RU)
University of California, Los Angeles (US)
Corresponding author: McGinty, Dennis
ORCID: Szymusiak, Ronald
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2003-06
Volume: 549
Issue: 2
Pages: 563-571
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.2003.041665
PMC: PMC2342950
OpenAlex: W2150645528
Cited by: 197
References: 90
Citations by year: 2026: 4 · 2025: 3 · 2024: 11 · 2023: 7 · 2022: 9 · 2021: 7 · 2020: 9 · 2019: 5 · 2018: 8 · 2017: 12 · 2016: 6 · 2015: 10 · 2014: 9 · 2013: 13 · 2012: 12
FWCI: 1.96
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Department of Veterans Affairs
National Institutes of Health (5p50hl060296-10)
National Heart, Lung, and Blood Institute (P50HL-060296, HL 60296)
National Institute of Mental Health (R01MH047480, MH47480)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
Keywords: sleep deprivation, dentate gyrus, hippocampus, cell proliferation, adult neurogenesis, hippocampal progenitor cells, BrdU labeling, stereology, rats
MeSH terms: Animals, Bromodeoxyuridine, Cell Division, Corticosterone, Male, Sleep Deprivation, Sleep Stages, Wakefulness, Rats, Sprague-Dawley, Dentate Gyrus, 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

Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks