Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance.
Open accessAbstract
Excessive glucocorticoid exposure during chronic stress causes synapse loss and learning impairment. Under normal physiological conditions, glucocorticoid activity oscillates in synchrony with the circadian rhythm. Whether and how endogenous glucocorticoid oscillations modulate synaptic plasticity and learning is unknown. Here we show that circadian glucocorticoid peaks promote postsynaptic dendritic spine formation in the mouse cortex after motor skill learning, whereas troughs are required for stabilizing newly formed spines that are important for long-term memory retention. Conversely, chronic and excessive exposure to glucocorticoids eliminates learning-associated new spines and disrupts previously acquired memories. Furthermore, we show that glucocorticoids promote rapid spine formation through a non-transcriptional mechanism by means of the LIM kinase-cofilin pathway and increase spine elimination through transcriptional mechanisms involving mineralocorticoid receptor activation. Together, these findings indicate that tightly regulated circadian glucocorticoid oscillations are important for learning-dependent synaptic formation and maintenance. They also delineate a new signaling mechanism underlying these effects.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Training mice at glucocorticoid peaks resulted in a higher rate of spine formation.
“Training mice at glucocorticoid peaks resulted in higher rate of spine formation, whereas glucocorticoid troughs following training was necessary for stabilization of spines formed during training and long-term memory retention (Liston et al., 2013).”
From Spatiotemporal dynamics of dendritic spines in the living brain (2014) · cites this paper as Liston et al., 2013
Glucocorticoid troughs following training were necessary for stabilization of spines formed during training and long-term memory retention.
“Training mice at glucocorticoid peaks resulted in higher rate of spine formation, whereas glucocorticoid troughs following training was necessary for stabilization of spines formed during training and long-term memory retention (Liston et al., 2013).”
From Spatiotemporal dynamics of dendritic spines in the living brain (2014) · cites this paper as Liston et al., 2013
The glucocorticoid level impacts motor learning-induced spine dynamics.
“Recently, it has also been found that the glucocorticoid level impacts motor learning-induced spine dynamics.”
From Spatiotemporal dynamics of dendritic spines in the living brain (2014) · cites this paper as Liston et al., 2013
Circadian changes in spine formation and removal are important for motor learning.
“Moreover, circadian changes in spine formation and removal are important for motor learning.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [38]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Protective and Damaging Effects of Stress Mediators
McEwen, B. S. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801153380307 · Cited by 6,733 · see citing works
Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP
Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., & Sanes, J. R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00084-2 · Cited by 3,042 · see citing works
Brain corticosteroid receptor balance in health and disease
de Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joëls, M. (1998) · Endocrine Reviews · doi:10.1210/edrv.19.3.0331 · Cited by 2,614 · see citing works
Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation
REUL, J. M. H. M., & KLOET, E. R. D. (1985) · Endocrinology · doi:10.1210/endo-117-6-2505 · Cited by 2,580 · see citing works
The Corticosteroid Receptor Hypothesis of Depression
Holsboer, F. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00159-7 · Cited by 2,181 · see citing works
Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action
Tsankova, N. M., Berton, O., Renthal, W., Kumar, A., Neve, R. L., & Nestler, E. J. (2006) · Nature Neuroscience · doi:10.1038/nn1659 · Cited by 1,780 · see citing works
Dendritic spine changes associated with hippocampal long-term synaptic plasticity
Engert, F., & Bonhoeffer, T. (1999) · Nature · doi:10.1038/19978 · Cited by 1,664 · see citing works
Cortisol levels during human aging predict hippocampal atrophy and memory deficits
Lupien, S. J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N. P. V., Thakur, M., McEwen, B. S., Hauger, R. L., & Meaney, M. J. (1998) · Nature Neuroscience · doi:10.1038/271 · Cited by 1,653 · see citing works
HDAC2 negatively regulates memory formation and synaptic plasticity
Guan, J.-S., Haggarty, S. J., Giacometti, E., Dannenberg, J.-H., Joseph, N., Gao, J., Nieland, T. J. F., Zhou, Y., Wang, X., Mazitschek, R., et al. (2009) · Nature · doi:10.1038/nature07925 · Cited by 1,644 · see citing works
The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3138 · Cited by 1,393 · see citing works
Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons
Watanabe, Y., Gould, E., & McEwen, B. S. (1992) · Brain Research · doi:10.1016/0006-8993(92)91597-8 · Cited by 1,212 · see citing works
Rapid formation and selective stabilization of synapses for enduring motor memories
Xu, T., Yu, X., Perlik, A. J., Tobin, W. F., Zweig, J. A., Tennant, K., Jones, T., & Zuo, Y. (2009) · Nature · doi:10.1038/nature08389 · Cited by 1,193 · see citing works
Stress and glucocorticoids impair retrieval of long-term spatial memory
de Quervain, D. J.-F., Roozendaal, B., & McGaugh, J. L. (1998) · Nature · doi:10.1038/29542 · Cited by 1,182 · see citing works
Stably maintained dendritic spines are associated with lifelong memories
Yang, G., Pan, F., & Gan, W.-B. (2009) · Nature · doi:10.1038/nature08577 · Cited by 1,182 · see citing works
Self-citationNongenomic actions of steroid hormones
Lösel, R., & Wehling, M. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1009 · Cited by 980 · see citing works
Liston, C., Miller, M. M., Goldwater, D. S., Radley, J. J., Rocher, A. B., Hof, P. R., Morrison, J. H., & McEwen, B. S. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1184-06.2006 · Cited by 968 · see citing works
Self-citationChronic Stress Causes Frontostriatal Reorganization and Affects Decision-Making
Dias-Ferreira, E., Sousa, J. C., Melo, I., Morgado, P., Mesquita, A. R., Cerqueira, J. J., Costa, R. M., & Sousa, N. (2009) · Science · doi:10.1126/science.1171203 · Cited by 858 · see citing works
Structural Changes Accompanying Memory Storage
Bailey, C. H., & Kandel, E. R. (1993) · Annual Review of Physiology · doi:10.1146/annurev.ph.55.030193.002145 · Cited by 856 · see citing works
Flavell, S. W., & Greenberg, M. E. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125631 · Cited by 832 · see citing works
Repeated Stress Induces Dendritic Spine Loss in the Rat Medial Prefrontal Cortex
Radley, J. J., Rocher, A. B., Miller, M., Janssen, W. G. M., Liston, C., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi104 · Cited by 820 · see citing works
Self-citationThe glucocorticoid receptor: rapid exchange with regulatory sites in living cells
McNally, J. G., Müller, W. G., Walker, D., Wolford, R., & Hager, G. L. (2000) · Science · doi:10.1126/science.287.5456.1262 · Cited by 802 · see citing works
Di, S., Malcher‐Lopes, R., Halmos, K. C., & Tasker, J. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-04850.2003 · Cited by 801 · see citing works
Karst, H., Berger, S., Turiault, M., Tronche, F., Schütz, G., & Joëls, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507572102 · Cited by 774 · see citing works
Abnormal Spine Morphology and Enhanced LTP in LIMK-1 Knockout Mice
Meng, Y., Zhang, Y., Tregoubov, V., Janus, C., Cruz, L., Jackson, M., Lu, W.-Y., MacDonald, J. F., Wang, J. Y., Falls, D. L., et al. (2002) · Neuron · doi:10.1016/s0896-6273(02)00758-4 · Cited by 688 · see citing works
Self-citationThe Dynamics of Dendritic Structure in Developing Hippocampal Slices
Dailey, M. E., & Smith, S. J. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-02983.1996 · Cited by 611 · see citing works
Histone Deacetylase 5 Epigenetically Controls Behavioral Adaptations to Chronic Emotional Stimuli
Renthal, W., Maze, I., Krishnan, V., Covington, H. E., Xiao, G., Kumar, A., Russo, S. J., Graham, A., Tsankova, N., Kippin, T. E., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.032 · Cited by 599 · see citing works
Wellman, C. L. (2001) · Journal of Neurobiology · doi:10.1002/neu.1079 · Cited by 594 · see citing works
Activity-Dependent Regulation of MEF2 Transcription Factors Suppresses Excitatory Synapse Number
Flavell, S. W., Cowan, C. W., Kim, T.-K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C., & Greenberg, M. E. (2006) · Science · doi:10.1126/science.1122511 · Cited by 573 · see citing works
Spine growth precedes synapse formation in the adult neocortex in vivo
Knott, G. W., Holtmaat, A., Wilbrecht, L., Welker, E., & Svoboda, K. (2006) · Nature Neuroscience · doi:10.1038/nn1747 · Cited by 563 · see citing works
Circadian Variation in Sports Performance
Atkinson, G., & Reilly, T. (1996) · Sports Medicine · doi:10.2165/00007256-199621040-00005 · Cited by 558 · see citing works
Roozendaal, B., Okuda, S., van der Zee, E. A., & McGaugh, J. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601874103 · Cited by 499 · see citing works
Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory
Yuen, E. Y., Liu, W., Karatsoreos, I. N., Feng, J., McEwen, B. S., & Yan, Z. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906791106 · Cited by 481 · see citing works
Thinned-skull cranial window technique for long-term imaging of the cortex in live mice
Yang, G., Pan, F., Parkhurst, C. N., Grutzendler, J., & Gan, W. (2010) · Nature Protocols · doi:10.1038/nprot.2009.222 · Cited by 438 · see citing works
Self-citationOpposite effects of fear conditioning and extinction on dendritic spine remodelling.
Lai, C. S. W., Franke, T. F., & Gan, W.-B. (2012) · Nature · doi:10.1038/nature10792 · Cited by 392 · see citing works
Self-citationQuirarte, G. L., Roozendaal, B., & McGaugh, J. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.14048 · Cited by 385 · see citing works
Ultradian hormone stimulation induces glucocorticoid receptor-mediated pulses of gene transcription
Stavreva, D. A., Wiench, M., John, S., Conway-Campbell, B. L., McKenna, M. A., Pooley, J. R., Johnson, T. A., Voss, T. C., Lightman, S. L., & Hager, G. L. (2009) · Nature Cell Biology · doi:10.1038/ncb1922 · Cited by 375 · see citing works
Hill, M. N., McLaughlin, R. J., Pan, B., Fitzgerald, M. L., Roberts, C. J., Lee, T. T. Y., Karatsoreos, I. N., Mackie, K., Viau, V., Pickel, V. M., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0496-11.2011 · Cited by 357 · see citing works
Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo
Liston, C., & Gan, W.-B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110444108 · Cited by 352 · see citing works
Self-citationBridging cognition, the brain and molecular genetics: evidence from Williams syndrome
Bellugi, U., Lichtenberger, L., Mills, D. L., Galaburda, A. M., & Korenberg, J. R. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01397-1 · Cited by 351 · see citing works
Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition
Buffelli, M., Burgess, R. W., Feng, G., Lobe, C. G., Lichtman, J. W., & Sanes, J. R. (2003) · Nature · doi:10.1038/nature01844 · Cited by 332 · see citing works
ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity
Gu, J., Lee, C. W., Fan, Y., Komlos, D., Tang, X., Sun, C., Yu, K., Hartzell, H. C., Chen, G., Bamburg, J. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2634 · Cited by 325 · see citing works
Stress-Induced Facilitation of Classical Conditioning
Shors, T. J., Weiss, C., & Thompson, R. F. (1992) · Science · doi:10.1126/science.1636089 · Cited by 310 · see citing works
High Ca2+-phosphate transfection efficiency in low-density neuronal cultures
Jiang, M., & Chen, G. (2006) · Nature Protocols · doi:10.1038/nprot.2006.86 · Cited by 304 · see citing works
Campolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., & Cuomo, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900835106 · Cited by 294 · see citing works
Circadian modulation of learning and memory in fear-conditioned mice.
Chaudhury, D., & Colwell, C. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00471-5 · Cited by 282 · see citing works
Alterations in Synaptic Strength Preceding Axon Withdrawal
Colman, H., Nabekura, J., & Lichtman, J. W. (1997) · Science · doi:10.1126/science.275.5298.356 · Cited by 261 · see citing works
Hippocampal-dependent learning requires a functional circadian system
Ruby, N. F., Hwang, C. E., Wessells, C., Fernandez, F., Zhang, P., Sapolsky, R., & Heller, H. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808259105 · Cited by 234 · see citing works
Datson, N. A., van der Perk, J., de Kloet, E. R., & Vreugdenhil, E. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01685.x · Cited by 230 · see citing works
Activation of Trk neurotrophin receptors by glucocorticoids provides a neuroprotective effect
Jeanneteau, F., Garabedian, M. J., & Chao, M. V. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709102105 · Cited by 215 · see citing works
Self-citationShort and long-term motor skill learning in an accelerated rotarod training paradigm
Buitrago, M. M. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.01.001 · Cited by 213 · see citing works
In VivoMeasurement of Brain Extracellular Space Diffusion by Cortical Surface Photobleaching
Binder, D. K., Papadopoulos, M. C., Haggie, P. M., & Verkman, A. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2294-04.2004 · Cited by 192 · see citing works
Sleep and wakefulness out of phase with internal biological time impairs learning in humans
Wright, K. P., Hull, J. T., Hughes, R. J., Ronda, J. M., & Czeisler, C. A. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.4.508 · Cited by 191 · see citing works
A Role for Local Calcium Signaling in Rapid Synaptic Partner Selection by Dendritic Filopodia
Löhmann, C., & Bonhoeffer, T. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.025 · Cited by 169 · see citing works
The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching
Jeanneteau, F. D., Deinhardt, K., Miyoshi, G., Bennett, A. M., & Chao, M. V. (2010) · Nature Neuroscience · doi:10.1038/nn.2655 · Cited by 163 · see citing works
Self-citationMorsink, M. C., Steenbergen, P. J., Vos, J. B., Karst, H., Joëls, M., De Kloet, E. R., & Datson, N. A. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01413.x · Cited by 160 · see citing works
Low Doses of Dexamethasone Can Produce a Hypocorticosteroid State in the Brain
Karssen, A. M., Meijer, O. C., Berry, A., Piñol, R. S., & de Kloet, E. R. (2005) · Endocrinology · doi:10.1210/en.2005-0501 · Cited by 105 · see citing works
Li, C., & Waters, R. S. (1991) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/s0317167100031267 · Cited by 99 · see citing works
The hippocampus is necessary for enhancements and impairments of learning following stress
Bangasser, D. A., & Shors, T. J. (2007) · Nature Neuroscience · doi:10.1038/nn1973 · Cited by 97 · see citing works
Hübener, M., & Bonhoeffer, T. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.033 · Cited by 94 · see citing works
Shattuck, N. L., Tvaryanas, A. P., & Shattuck, L. G. (2012) · SLEEP · doi:10.5665/sleep.2002 · Cited by 33 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., Lafaille, J. J., Hempstead, B. L., Littman, D. R., & Gan, W.-B. (2013) · Cell · doi:10.1016/j.cell.2013.11.030 · Cited by 2,599 · see citing works
Self-citationStress Effects on Neuronal Structure: Hippocampus, Amygdala, and Prefrontal Cortex
McEwen, B. S., Nasca, C., & Gray, J. D. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.171 · Cited by 1,574 · see citing works
Mechanisms of stress in the brain
McEwen, B. S., Bowles, N. P., Gray, J. D., Hill, M. N., Hunter, R. G., Karatsoreos, I. N., & Nasca, C. (2015) · Nature Neuroscience · doi:10.1038/nn.4086 · Cited by 1,386 · see citing works
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.012 · Cited by 1,389 · see citing works
Neurobiological and Systemic Effects of Chronic Stress
McEwen, B. S. (2017) · Chronic Stress · doi:10.1177/2470547017692328 · Cited by 1,059 · see citing works
“removal are important for motor learning.(38) Finally, glucocorticoids are able to program some of the cellular circadian clocks in brain(39) as well as in liver(40) leading to dissonance between brain regions and also contributing to obesity and metabolic syndrome that is produced by chronic glucocorticoid administra…”
BackgroundSustained rescue of prefrontal circuit dysfunction by antidepressant-induced spine formation
Moda-Sava, R. N., Murdock, M. H., Parekh, P. K., Fetcho, R. N., Huang, B. S., Huynh, T. N., Witztum, J., Shaver, D. C., Rosenthal, D. L., Alway, E. J., et al. (2019) · Science · doi:10.1126/science.aat8078 · Cited by 643 · see citing works
Self-citationUncertainty and stress: Why it causes diseases and how it is mastered by the brain
Peters, A., McEwen, B. S., & Friston, K. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.004 · Cited by 652 · see citing works
Sleep promotes branch-specific formation of dendritic spines after learning
Yang, G., Lai, C. S. W., Cichon, J., Ma, L., Li, W., & Gan, W.-B. (2014) · Science · doi:10.1126/science.1249098 · Cited by 616 · see citing works
Self-citationREM sleep selectively prunes and maintains new synapses in development and learning
Li, W., Ma, L., Yang, G., & Gan, W.-B. (2017) · Nature Neuroscience · doi:10.1038/nn.4479 · Cited by 543 · see citing works
Self-citationThe Functional and Clinical Significance of the 24-Hour Rhythm of Circulating Glucocorticoids
Oster, H., Challet, E., Ott, V., Arvat, E., de Kloet, E. R., Dijk, D.-J., Lightman, S., Vgontzas, A., & Van Cauter, E. (2017) · Endocrine Reviews · doi:10.1210/er.2015-1080 · Cited by 548 · see citing works
Toward understanding how early-life stress reprograms cognitive and emotional brain networks
Chen, Y., & Baram, T. Z. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.181 · Cited by 474 · see citing works
The microbiota regulate neuronal function and fear extinction learning
Chu, C., Murdock, M. H., Jing, D., Won, T. H., Chung, H., Kressel, A. M., Tsaava, T., Addorisio, M. E., Putzel, G. G., Zhou, L., et al. (2019) · Nature · doi:10.1038/s41586-019-1644-y · Cited by 421 · see citing works
The impact of developmental timing for stress and recovery
Gee, D. G., & Casey, B. J. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2015.02.001 · Cited by 245 · see citing works
“…impact of psychological stressors on neuroplasticity, although glucocorticoids, and their directmanipulation, canmodify the brain in anatomically selective ways (Sapolsky, 1986; Liston et al., 2013) and alter the expression of neurotrophic factors essential for neuroplasticity (Smith et al., 1995).”
BackgroundMcEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0121 · Cited by 253 · see citing works
Obesity diminishes synaptic markers, alters microglial morphology, and impairs cognitive function
Bocarsly, M. E., Fasolino, M., Kane, G. A., LaMarca, E. A., Kirschen, G. W., Karatsoreos, I. N., McEwen, B. S., & Gould, E. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511593112 · Cited by 250 · see citing works
The Relationship between PSD-95 Clustering and Spine Stability <i>In Vivo</i>
Cane, M., Maco, B., Knott, G., & Holtmaat, A. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3353-13.2014 · Cited by 216 · see citing works
Endocrine Effects of Circadian Disruption
Bedrosian, T. A., Fonken, L. K., & Nelson, R. J. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105102 · Cited by 170 · 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
Lucassen, P. J., Oomen, C. A., Naninck, E. F. G., Fitzsimons, C. P., van Dam, A.-M., Czeh, B., & Korosi, A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021303 · Cited by 166 · see citing works
Circadian rhythms and addiction: Mechanistic insights and future directions.
Logan, R. W., Williams, W. P., & McClung, C. A. (2014) · Behavioral Neuroscience · doi:10.1037/a0036268 · Cited by 142 · see citing works
Redefining neuroendocrinology: Epigenetics of brain-body communication over the life course
McEwen, B. S. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.11.001 · Cited by 129 · see citing works
Cortisol awakening response in patients with psychosis: systematic review and meta-analysis
Berger, M., Kraeuter, A. K., Romanik, D., Malouf, P., Amminger, G. P., & Sarnyai, Z. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.027 · Cited by 109 · see citing works
Synaptic Mechanisms Regulating Mood State Transitions in Depression
Parekh, P. K., Johnson, S. B., & Liston, C. (2022) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-110920-040422 · Cited by 101 · see citing works
Self-citationStress-induced remodeling of hippocampal CA3 pyramidal neurons
McEwen, B. S. (2016) · Brain Research · doi:10.1016/j.brainres.2015.12.043 · Cited by 105 · see citing works
Circadian dynamics in measures of cortical excitation and inhibition balance
Chellappa, S. L., Gaggioni, G., Ly, J. Q. M., Papachilleos, S., Borsu, C., Brzozowski, A., Rosanova, M., Sarasso, S., Luxen, A., Middleton, B., et al. (2016) · Scientific Reports · doi:10.1038/srep33661 · Cited by 84 · see citing works
Musazzi, L., Treccani, G., & Popoli, M. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00060 · Cited by 83 · see citing works
Spatiotemporal dynamics of dendritic spines in the living brain
Chen, C.-C., Lu, J., & Zuo, Y. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00028 · Cited by 88 · see citing works
Control of dendritic spine morphological and functional plasticity by small GTPases.
Woolfrey, K. M., & Srivastava, D. P. (2016) · Neural Plasticity · doi:10.1155/2016/3025948 · Cited by 76 · see citing works
Profiling DNA break sites and transcriptional changes in response to contextual fear learning
Stott, R. T., Kritsky, O., & Tsai, L.-H. (2021) · PLOS ONE · doi:10.1371/journal.pone.0249691 · Cited by 62 · see citing works
Epigenetic Interactions and the Brain-Body Communication
McEwen, B. S. (2017) · Psychotherapy and Psychosomatics · doi:10.1159/000449150 · Cited by 39 · see citing works
Unno, K., Sumiyoshi, A., Konishi, T., Hayashi, M., Taguchi, K., Muguruma, Y., Inoue, K., Iguchi, K., Nonaka, H., Kawashima, R., et al. (2020) · Nutrients · doi:10.3390/nu12010174 · Cited by 39 · see citing works
Memory corticalization triggered by REM sleep: mechanisms of cellular and systems consolidation
Almeida-Filho, D. G., Queiroz, C. M., & Ribeiro, S. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2886-9 · Cited by 38 · see citing works
Morin, E. L., Howell, B. R., Feczko, E., Earl, E., Pincus, M., Reding, K., Kovacs-Balint, Z. A., Meyer, J. S., Styner, M., Fair, D., et al. (2020) · Development and Psychopathology · doi:10.1017/s0954579420001133 · Cited by 37 · see citing works
Lightman, S., & Terry, J. R. (2014) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70182-7 · Cited by 28 · see citing works
Physiological plasticity in elephants: highly dynamic glucocorticoids in African and Asian elephants
Pokharel, S. S., & Brown, J. L. (2023) · Conservation Physiology · doi:10.1093/conphys/coad088 · Cited by 23 · see citing works
Improving outcomes in patients with adrenal insufficiency: a review of current and future treatments
Johannsson, G., Skrtic, S., Lennernäs, H., Quinkler, M., & Stewart, P. M. (2014) · Current Medical Research and Opinion · doi:10.1185/03007995.2014.925865 · Cited by 21 · see citing works
- Authors
- Liston, C., Cichon, J. M., Jeanneteau, F., Jia, Z., Chao, M. V., & Gan, W.-B.
- Affiliations
- Stanford Medicine (US)
- New York University (US)
- Centre National de la Recherche Scientifique (FR)
- Hospital for Sick Children (CA)
- Corresponding author
- Liston, Conor
- Gan, Wen-Biao
- Venue
- Nature Neuroscience
- Published
- 2013-04-28
- Volume
- 16
- Issue
- 6
- Pages
- 698-705
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3896394
- OpenAlex
- W2030933765
- Cited by
- 358
- References
- 60
- Citations by year
- 2026: 17 · 2025: 12 · 2024: 21 · 2023: 22 · 2022: 21 · 2021: 22 · 2020: 33 · 2019: 32 · 2018: 30 · 2017: 25 · 2016: 35 · 2015: 39 · 2014: 41 · 2013: 8
- FWCI
- 20.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- Weill Cornell Medical College
- National Institute of Mental Health (R01MH085324, K99MH097822, R01MH086651, R00MH097822, MH086651)
- National Institute of Neurological Disorders and Stroke (R01NS021072, R01NS047325, NS-21072, R56NS021072)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- corticosterone, dendritic spine formation, synapse maintenance, motor skill learning, long-term memory, chronic stress, LIM kinase, cofilin, cytoskeletal remodeling, mineralocorticoid receptor, synaptic plasticity, cortical synapses
- MeSH terms
- Animals, Behavior, Animal, Cerebral Cortex, Circadian Rhythm, Female, Glucocorticoids, Learning, Male, Neuronal Plasticity, Synapses, Time Factors, Signal Transduction, Mice, Knockout, Dendritic Spines, Mice
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
