Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling

Chen, Yuncai; Rex, Christopher S.; Rice, Courtney J.; Dubé, Céline M.; Gall, Christine M.; Lynch, Gary; Baram, Tallie Z.

doi:10.1073/pnas.1003825107

Cited by 256Stress Responses and CortisolMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling

Open access

Chen, Yuncai, Rex, Christopher S., Rice, Courtney J., Dubé, Céline M., Gall, Christine M., Lynch, Gary, Baram, Tallie Z.·2010·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1003825107PMC PMC2919915

Open this paper in CoChat — free account

Abstract

Stress affects the hippocampus, a brain region crucial for memory. In rodents, acute stress may reduce density of dendritic spines, the location of postsynaptic elements of excitatory synapses, and impair long-term potentiation and memory. Steroid stress hormones and neurotransmitters have been implicated in the underlying mechanisms, but the role of corticotropin-releasing hormone (CRH), a hypothalamic hormone also released during stress within hippocampus, has not been elucidated. In addition, the causal relationship of spine loss and memory defects after acute stress is unclear. We used transgenic mice that expressed YFP in hippocampal neurons and found that a 5-h stress resulted in profound loss of learning and memory. This deficit was associated with selective disruption of long-term potentiation and of dendritic spine integrity in commissural/associational pathways of hippocampal area CA3. The degree of memory deficit in individual mice correlated significantly with the reduced density of area CA3 apical dendritic spines in the same mice. Moreover, administration of the CRH receptor type 1 (CRFR 1 ) blocker NBI 30775 directly into the brain prevented the stress-induced spine loss and restored the stress-impaired cognitive functions. We conclude that acute, hours-long stress impairs learning and memory via mechanisms that disrupt the integrity of hippocampal dendritic spines. In addition, establishing the contribution of hippocampal CRH–CRFR 1 signaling to these processes highlights the complexity of the orchestrated mechanisms by which stress impacts hippocampal structure and function.

Integrity signals

Registry

Crossref · 10.1073/pnas.1003825107

Cites

91 of 91 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?

Stress can influence the number of excitatory synapses on dendritic spines already within hours in brain regions including the hippocampus.
“Stress has been shown to influence the number of excitatory synapses on dendritic spines already within hours26,40 in brain regions including the hippocampus.34,41,42”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [26]
Neurotransmitters including norepinephrine, serotonin and glutamate, as well as stress-induced release of neuropeptides and steroids, can influence synapse number and function.
“Neurotransmitters, including norepinephrine,76, 77, 78 serotonin79, 80, 81 and glutamate,82,83 as well as stress-induced release of neuropeptides26,34,84,85 and steroids,86, 87, 88 can influence synapse number and function.”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [26]

A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256 · see citing works
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 · cited 1× · see citing works
“Focusing on the effects of stress on the hippocampus, a large body of work has uncovered effects of chronic and short-term stress on learning and memory (17, 19, 22, 23).”
Background
Stress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621 · see citing works
Neural regulation of endocrine and autonomic stress responses
Ulrich-Lai, Y. M., & Herman, J. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2647 · Cited by 3,318 · see citing works
Synaptic Plasticity and Memory: An Evaluation of the Hypothesis
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.649 · Cited by 2,794 · 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 Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · see citing works
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543 · see citing works
The neuro-symphony of stress
Joëls, M., & Baram, T. Z. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2632 · Cited by 1,521 · see citing works
Self-citation
Synaptic plasticity, memory and the hippocampus: a neural network approach to causality
Neves, G., Cooke, S. F., & Bliss, T. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2303 · Cited by 1,207 · 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
Recognition memory and the medial temporal lobe: a new perspective
Squire, L. R., Wixted, J. T., & Clark, R. E. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2154 · Cited by 1,013 · see citing works
Dentritic spines : structure, dynamics and regulation
Hering, H., & Sheng, M. (2001) · Nature Reviews Neuroscience · doi:10.1038/35104061 · Cited by 961 · see citing works
Chronic Psychosocial Stress Causes Apical Dendritic Atrophy of Hippocampal CA3 Pyramidal Neurons in Subordinate Tree Shrews
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864 · see citing works
Repeated stress causes reversible impairments of spatial memory performance.
Luine, V., Villegas, M., Martinez, C., & McEwen, B. (1994) · Brain Research · doi:10.1016/0006-8993(94)91778-7 · Cited by 813 · see citing works
Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment.
Conrad, C. D., Galea, L. A. M., Kuroda, Y., & McEwen, B. S. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.6.1321 · Cited by 784 · see citing works
Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement
Sousa, N., Lukoyanov, N. V., Madeira, M. D., Almeida, O. F. X., & Paula-Barbosa, M. M. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00050-6 · Cited by 758 · see citing works
Hippocampal LTP Is Accompanied by Enhanced F-Actin Content within the Dendritic Spine that Is Essential for Late LTP Maintenance In Vivo
Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., & Inokuchi, K. (2003) · Neuron · doi:10.1016/s0896-6273(03)00206-x · Cited by 695 · see citing works
Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.902 · Cited by 664 · see citing works
Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy.
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.902 · Cited by 663 · see citing works
Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events
Larson, J., & Lynch, G. (1986) · Science · doi:10.1126/science.3704635 · Cited by 597 · see citing works
Self-citation
Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Comparison of stressors
Magarin˜os, A. M., & McEwen, B. S. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00256-i · Cited by 571 · see citing works
Object recognition memory and the rodent hippocampus
Broadbent, N. J., Gaskin, S., Squire, L. R., & Clark, R. E. (2010) · Learning & Memory · doi:10.1101/lm.1650110 · Cited by 568 · see citing works
Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval
Winters, B. D., Saksida, L. M., & Bussey, T. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.004 · Cited by 568 · see citing works
A Novel Mouse Model for Acute and Long-Lasting Consequences of Early Life Stress
Rice, C. J., Sandman, C. A., Lenjavi, M. R., & Baram, T. Z. (2008) · Endocrinology · doi:10.1210/en.2008-0633 · Cited by 521 · see citing works
Self-citation
Vasopressin: Behavioral roles of an “original” neuropeptide
Caldwell, H. K., Lee, H.-J., Macbeth, A. H., & Young, W. S. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.10.007 · Cited by 504 · see citing works
Sex Differences and Opposite Effects of Stress on Dendritic Spine Density in the Male Versus Female Hippocampus
Shors, T. J., Chua, C., & Falduto, J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06292.2001 · Cited by 496 · see citing works
Glucocorticoids and the regulation of memory in health and disease
de Quervain, D. J. ‐., Aerni, A., Schelling, G., & Roozendaal, B. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.002 · Cited by 496 · see citing works
Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes
Park, M., Salgado, J. M., Ostroff, L., Helton, T. D., Robinson, C. G., Harris, K. M., & Ehlers, M. D. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.040 · Cited by 493 · see citing works
Dendritic spines and long-term plasticity
Segal, M. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1649 · Cited by 489 · see citing works
The coming out of the brain mineralocorticoid receptor
Joëls, M., Karst, H., DeRijk, R., & de Kloet, E. R. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2007.10.005 · Cited by 481 · see citing works
Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 480 · see citing works
Mechanisms of late-onset cognitive decline after early-life stress
Brunson, K. L., Kramár, E., Lin, B., Chen, Y., Colgin, L. L., Yanagihara, T. K., Lynch, G., & Baram, T. Z. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2281-05.2005 · Cited by 479 · see citing works
Self-citation
Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation.
Kim, J. J., Foy, M. R., & Thompson, R. F. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4750 · Cited by 435 · see citing works
Structural and functional plasticity of the human brain in posttraumatic stress disorder
Bremner, J. D., Elzinga, B. M., Schmahl, C. G., & Vermetten, E. H. G. J. M. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)67012-5 · Cited by 368 · see citing works
Yeast and apoptosis
Jin, C., & Reed, J. C. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm832 · Cited by 340 · see citing works
A critical review of chronic stress effects on spatial learning and memory
Conrad, C. D. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.11.003 · Cited by 335 · see citing works
Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery
Goldwater, D. S., Pavlides, C., Hunter, R. G., Bloss, E. B., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.053 · Cited by 333 · see citing works
Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress
Magariños, A. M., Deslandes, A., & McEwen, B. S. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00163-6 · Cited by 330 · see citing works
Effects of Chronic Stress on Structure and Cell Function in Rat Hippocampus and Hypothalamus
Joëls, M., Karst, H., Alfarez, D., Heine, V. M., Qin, Y., Riel, E. V., Verkuyl, M., Lucassen, P. J., & Krugers, H. J. (2004) · Stress · doi:10.1080/10253890500070005 · Cited by 330 · see citing works
Effects of chronic stress on hippocampal long‐term potentiation
Pavlides, C., Nivón, L. G., & McEwen, B. S. (2002) · Hippocampus · doi:10.1002/hipo.1116 · Cited by 316 · see citing works
Changes in Synaptic Morphology Accompany Actin Signaling during LTP
Chen, L. Y., Rex, C. S., Casale, M. S., Gall, C. M., & Lynch, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0164-07.2007 · Cited by 296 · see citing works
Self-citation
Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone
Chen, Y., Dubé, C. M., Rice, C. J., & Baram, T. Z. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0225-08.2008 · Cited by 276 · see citing works
Self-citation
Chronic distress and incidence of mild cognitive impairment
Wilson, R. S., Schneider, J. A., Boyle, P. A., Arnold, S. E., Tang, Y., & Bennett, D. A. (2007) · Neurology · doi:10.1212/01.wnl.0000264930.97061.82 · Cited by 267 · see citing works
Chronic unpredictable stress impairs long‐term potentiation in rat hippocampal CA1 area and dentate gyrus <i>in vitro</i>
Alfarez, D. N., Joëls, M., & Krugers, H. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02622.x · Cited by 258 · see citing works
Stress effects in the hippocampus: Synaptic plasticity and memory
Kim, J. J., Song, E. Y., Kim, J. J., Song, E. Y., & Kosten, T. A. (2006) · Stress · doi:10.1080/10253890600678004 · Cited by 255 · see citing works
Sex Differences in Chronic Stress Effects on Memory in Rats
Luine, V. (2002) · Stress · doi:10.1080/1025389021000010549 · Cited by 250 · see citing works
Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress.
Xu, L., Hölscher, C., Anwyl, R., & Rowan, M. (1998) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.95.6.3204 · Cited by 248 · see citing works
Laminating the hippocampus
Förster, E., Zhao, S., & Frotscher, M. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1882 · Cited by 242 · see citing works
Brain-Derived Neurotrophic Factor Rescues Synaptic Plasticity in a Mouse Model of Fragile X Syndrome
Lauterborn, J. C., Rex, C. S., Kramár, E. A., Chen, L. Y., Pandyarajan, V., LYNCH, G. S., & Gall, C. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2624-07.2007 · Cited by 241 · see citing works
Self-citation
Chapter 8 Synaptic plasticity in learning and memory: Stress effects in the hippocampus
Howland, J. G., & Wang, Y. T. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00008-8 · Cited by 238 · see citing works
Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress
Hains, A. B., Vu, M. A. T., Maciejewski, P. K., van Dyck, C. H., Gottron, M., & Arnsten, A. F. T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908563106 · Cited by 234 · see citing works
Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus
Pawlak, R., Rao, B. S. S., Melchor, J. P., Chattarji, S., McEwen, B., & Strickland, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509232102 · Cited by 223 · see citing works
Hippocampal neuroplasticity induced by early-life stress: Functional and molecular aspects
Fenoglio, K. A., Brunson, K. L., & Baram, T. (2006) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2006.02.001 · Cited by 215 · see citing works
Self-citation
Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis
Diamond, D. M., Campbell, A. M., Park, C. R., Woodson, J. C., Conrad, C. D., Bachstetter, A. D., & Mervis, R. F. (2006) · Hippocampus · doi:10.1002/hipo.20188 · Cited by 213 · see citing works
Priming of Long-Term Potentiation in Mouse Hippocampus by Corticotropin-Releasing Factor and Acute Stress: Implications for Hippocampus-Dependent Learning
Blank, T., Nijholt, I. M., Eckart, K., & Spiess, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03788.2002 · Cited by 210 · see citing works
Stress-induced structural remodeling in hippocampus: Prevention by lithium treatment
Wood, G. E., Young, L. T., Reagan, L. P., Chen, B., & McEwen, B. S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400208101 · Cited by 197 · see citing works
Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: A three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities
Stewart, M. G., Davies, H. A., Sandi, C., Kraev, I. V., Rogachevsky, V. V., Peddie, C. J., Rodriguez, J. J., Cordero, M. I., Donohue, H. S., Gabbott, P. L. A., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.10.031 · Cited by 197 · see citing works
Stress Impairs LTP and Hippocampal‐Dependent Memorya
Diamond, D. M., & ROSE, G. M. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39271.x · Cited by 195 · see citing works
Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress
Chen, Y., Brunson, K. L., Adelmann, G., Bender, R. A., Frotscher, M., & Baram, T. Z. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.03.036 · Cited by 179 · see citing works
Self-citation
Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats
Park, C. R., Campbell, A. M., & Diamond, D. M. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01255-0 · Cited by 166 · see citing works
Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus
Chen, Y., Bender, R. A., Brunson, K. L., Pomper, J. K., Grigoriadis, D. E., Wurst, W., & Baram, T. Z. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403975101 · Cited by 166 · see citing works
Self-citation
Morphological changes in the hippocampal CA3 region induced by non-invasive glucocorticoid administration: a paradox
Magariños, A. M., Orchinik, M., & McEwen, B. S. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00882-8 · Cited by 163 · see citing works
Stimuli and consequences of dendritic release of oxytocin within the brain
Neumann, I. D. (2007) · Biochemical Society Transactions · doi:10.1042/bst0351252 · Cited by 161 · see citing works
Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: A stereological and three-dimensional ultrastructural study
Donohue, H. S., Gabbott, P. L. A., Davies, H. A., Rodríguez, J. J., Cordero, M. I., Sandi, C., Medvedev, N. I., Popov, V. I., Colyer, F. M., Peddie, C. J., et al. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.072 · Cited by 139 · see citing works
Novel and Transient Populations of Corticotropin-Releasing Hormone-Expressing Neurons in Developing Hippocampus Suggest Unique Functional Roles: A Quantitative Spatiotemporal Analysis
Chen, Y., Bender, R. A., Frotscher, M., & Baram, T. Z. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07171.2001 · Cited by 137 · see citing works
Self-citation
Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex
Sandi, C., Woodson, J. C., Haynes, V. F., Park, C. R., Touyarot, K., Lopez-Fernandez, M. A., Venero, C., & Diamond, D. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.034 · Cited by 122 · see citing works
Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone
Brunson, K. L., Avishai-Eliner, S., Hatalski, C. G., & Baram, T. Z. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000942 · Cited by 112 · see citing works
Self-citation
The opposite effects of stress on dendritic spines in male vs. female rats are NMDA receptor‐dependent
Shors, T. J., Falduto, J., & Leuner, B. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.03065.x · Cited by 105 · see citing works
The substrates of memory: Defects, treatments, and enhancement
LYNCH, G. S., Rex, C. S., Chen, L. Y., & Gall, C. M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.082 · Cited by 102 · see citing works
Self-citation
Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent
Chen, Y., Fenoglio, K. A., Dubé, C. M., Grigoriadis, D. E., & Baram, T. Z. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001863 · Cited by 98 · see citing works
Self-citation
Bidirectional shift in the cornu ammonis 3 pyramidal dendritic organization following brief stress
Kole, M. H. P., Costoli, T., Koolhaas, J. M., & Fuchs, E. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.02.014 · Cited by 96 · see citing works
Mossy fiber potentiation and long‐term potentiation involve different expression mechanisms
Staubli, U. V., Larson, J., & LYNCH, G. S. (1990) · Synapse · doi:10.1002/syn.890050410 · Cited by 95 · see citing works
Self-citation
Corticosterone shifts different forms of synaptic potentiation in opposite directions
Krugers, H. J., Alfarez, D. N., Karst, H., Parashkouhi, K., van Gemert, N., & Joëls, M. (2005) · Hippocampus · doi:10.1002/hipo.20092 · Cited by 88 · see citing works
Activity-stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats
Lambert, K. G., Buckelew, S. K., Staffiso-Sandoz, G., Gaffga, S., Carpenter, W., Fisher, J. M., & Kinsley, C. H. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00114-0 · Cited by 87 · see citing works
Corticosterone reduces dendritic complexity in developing hippocampal CA1 neurons
Alfarez, D. N., Simoni, A. D., Velzing, E. H., Bracey, E. F., Joëls, M., Edwards, F. A., & Krugers, H. J. (2009) · Hippocampus · doi:10.1002/hipo.20566 · Cited by 81 · see citing works
Peptide-induced infant status epilepticus causes neuronal death and synaptic reorganization
Baram, T. Z., & Ribak, C. E. (1995) · Neuroreport · doi:10.1097/00001756-199501000-00013 · Cited by 74 · see citing works
Self-citation
The antidepressant agomelatine blocks the adverse effects of stress on memory and enables spatial learning to rapidly increase neural cell adhesion molecule (NCAM) expression in the hippocampus of rats
Conboy, L., Tanrıkut, C., Zoladz, P. R., Campbell, A. M., Park, C. R., Gabriel, C., Mocaër, E., Sandi, C., & Diamond, D. M. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009255 · Cited by 66 · see citing works
Glucocorticoid Receptor mRNA Ontogeny in the Fetal and Postnatal Rat Forebrain
Yi, S., Masters, J. N., & Baram, T. Z. (1994) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1994.1048 · Cited by 63 · see citing works
Self-citation
Chronic restraint stress impairs acquisition and retention of spatial memory task in rats
Sunanda, Rao, B. S. S., & Raju, T. R. (2000) · Cited by 62 · see citing works
Acute stress disrupts paired pulse facilitation and long‐term potentiation in rat dorsal hippocampus through activation of glucocorticoid receptors
Cazakoff, B. N., & Howland, J. G. (2009) · Hippocampus · doi:10.1002/hipo.20738 · Cited by 58 · see citing works
Site and time dependent effects of acute stress on hippocampal long-term potentiation in freely behaving rats
Yamada, K., McEwen, B. S., & Pavlides, C. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1519-0 · Cited by 57 · see citing works
Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females
Dalla, C., Whetstone, A. S., Hodes, G. E., & Shors, T. J. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2008.10.051 · Cited by 56 · see citing works
6.3 Co-localization of brain corticosteroid receptors in the rat hippocampus
Eekelen, J. A. M. V., & de Kloet, E. R. (1992) · Progress in Histochemistry and Cytochemistry · doi:10.1016/s0079-6336(11)80102-6 · Cited by 51 · see citing works
Tianeptine: An Antidepressant with Memory-Protective Properties
Zoladz, P. R., Park, C. R., Muñoz, C., Fleshner, M., & Diamond, D. M. (2008) · Current Neuropharmacology · doi:10.2174/157015908787386096 · Cited by 42 · see citing works
Opposite effects of glucocorticoid receptor activation on hippocampal CA1 dendritic complexity in chronically stressed and handled animals
Alfarez, D. N., Karst, H., Velzing, E. H., Joëls, M., & Krugers, H. J. (2007) · Hippocampus · doi:10.1002/hipo.20360 · Cited by 39 · see citing works
Cellular correlates to spatial learning in the rat hippocampus
Andersen, P. N., Moser, E. I., Moser, M., et al. (1996) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(97)87917-x · Cited by 22 · see citing works
Effects of NADH on dopamine release in rat striatum
Pearl, S. M., Antion, M. D., Stanwood, G. D., Jaumotte, J. D., Kapatos, G., & Zigmond, M. J. (2000) · Synapse · doi:10.1002/(sici)1098-2396(200005)36:2 · Cited by 9 · see citing works
Untitled work
(1997) · doi:10.1002/(sici)1098-1063(1997)7:4

Flagged first, then by citations

Sorted by citations

Sustained 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
Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors
Ivy, A. S., Rex, C. S., Chen, Y., Dubé, C., Maras, P. M., Grigoriadis, D. E., Gall, C. M., Lynch, G., & Baram, T. Z. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1784-10.2010 · Cited by 402 · see citing works
Self-citation
A systematic review and meta-analysis of magnetic resonance imaging measurement of structural volumes in posttraumatic stress disorder
O'Doherty, D. C. M., Chitty, K. M., Saddiqui, S., Bennett, M. R., & Lagopoulos, J. (2015) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2015.01.002 · Cited by 375 · 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
The role of sleep in regulating structural plasticity and synaptic strength: implications for memory and cognitive function
Raven, F., Van der Zee, E. A., Meerlo, P., & Havekes, R. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.05.002 · Cited by 331 · see citing works
Stress, anxiety, and dendritic spines: What are the connections?
Leuner, B., & Shors, T. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.021 · Cited by 284 · see citing works
Neighborhood matters: divergent patterns of stress-induced plasticity across the brain
Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4115 · Cited by 248 · see citing works
The stressed synapse 2.0: pathophysiological mechanisms in stress-related neuropsychiatric disorders
Sanacora, G., Yan, Z., & Popoli, M. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00540-x · Cited by 197 · see citing works
The molecular physiology of CRH neurons
Aguilera, G., & Liu, Y. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.08.002 · Cited by 198 · see citing works
Chronic Stress-Associated Depressive Disorders: The Impact of HPA Axis Dysregulation and Neuroinflammation on the Hippocampus—A Mini Review
Lei, A. A., Phang, V. W. X., Lee, Y. Z., Kow, A. S. F., Tham, C. L., Ho, Y.-C., & Lee, M. T. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26072940 · Cited by 207 · see citing works
“Furthermore, intrahippocampal CRFR1 antagonists (e.g., NBI 30775) inhibit spine degeneration and ameliorate memory impairments generated by stress, confirming CRH as a crucial mediator of acute stress effects [100].”
Neuropeptide receptor ligands as drugs for psychiatric diseases: the end of the beginning?
Griebel, G., & Holsboer, F. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3702 · Cited by 194 · see citing works
Impairment of synaptic plasticity by the stress mediator CRH involves selective destruction of thin dendritic spines via RhoA signaling
Chen, Y., Kramár, E. A., Chen, L. Y., Babayan, A. H., Andres, A. L., Gall, C. M., Lynch, G., & Baram, T. Z. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.17 · Cited by 115 · see citing works
Self-citation
Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress
Maras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · see citing works
Self-citation
Preventing the Stress-Induced Shift from Goal-Directed to Habit Action with a β-Adrenergic Antagonist
Schwabe, L., Höffken, O., Tegenthoff, M., & Wolf, O. T. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3304-11.2011 · Cited by 97 · see citing works
Synergistic effects of amyloid-beta and wild-type human tau on dendritic spine loss in a floxed double transgenic model of Alzheimer's disease
Chabrier, M. A., Cheng, D., Castello, N. A., Green, K. N., & LaFerla, F. M. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.01.007 · Cited by 97 · see citing works
Caregiver maltreatment causes altered neuronal DNA methylation in female rodents
Blaze, J., & Roth, T. L. (2017) · Development and Psychopathology · doi:10.1017/s0954579417000128 · Cited by 48 · see citing works
Ethanol withdrawal-induced adaptations in prefrontal corticotropin releasing factor receptor 1-expressing neurons regulate anxiety and conditioned rewarding effects of ethanol
Patel, R. R., Wolfe, S. A., Borgonetti, V., Gandhi, P. J., Rodriguez, L., Snyder, A. E., D’Ambrosio, S., Bajo, M., Domissy, A., Head, S., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01642-3 · Cited by 33 · see citing works

Long-term potentiation and 4-aminopyridine
Haas, H. L., & Greene, R. W. (1985) · Cellular and Molecular Neurobiology · doi:10.1007/bf00711014 · Cited by 9 · see citing works
Pentobarbital modulates transmitter effects on mouse spinal neurones grown in tissue culture
Ransom, B. R., & Barker, J. L. (1975) · Nature · doi:10.1038/254703a0 · Cited by 92 · see citing works
Inhibitory postsynaptic density from the lens of phase separation
Bai, G., & Zhang, M. (2022) · Oxford Open Neuroscience · doi:10.1093/oons/kvac003 · Cited by 7 · see citing works
Development of Synaptic Responses and Plasticity at the SC-CA1 and MF-CA3 Synapses in Rat Hippocampus
Hussain, R. J., & Carpenter, D. O. (2001) · Cellular and Molecular Neurobiology · doi:10.1023/a:1012602105208 · Cited by 25 · see citing works
Postsynaptic Levels of [Ca2+]i Needed to Trigger LTD and LTP
Neveu, D., & Zucker, R. S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80081-1 · Cited by 198 · see citing works

Authors: Chen, Y., Rex, C. S., Rice, C. J., Dubé, C. M., Gall, C. M., Lynch, G., & Baram, T. Z.
Affiliations: Pediatrics and Genetics (US)
University of California, Irvine (US)
Departments of aPediatrics and
ORCID: Chen, Yuncai
Gall, Christine M.
Lynch, Gary
Baram, Tallie Z.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2010-07-06
Volume: 107
Issue: 29
Pages: 13123-13128
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1003825107
PMC: PMC2919915
OpenAlex: W2162743207
Cited by: 256
References: 91
Citations by year: 2026: 3 · 2025: 5 · 2024: 10 · 2023: 16 · 2022: 25 · 2021: 13 · 2020: 17 · 2019: 12 · 2018: 18 · 2017: 27 · 2016: 21 · 2015: 26 · 2014: 13 · 2013: 10 · 2012: 20
FWCI: 6.77
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders: George E. Hewitt Foundation for Medical Research
Fondation pour la Recherche Médicale
National Institutes of Health
National Institute of Mental Health (MH73136, R01MH073136)
National Institute of Neurological Disorders and Stroke (P01NS045260, NS 28912, NS45540, NS 37799, R01NS028912, NS-45260, R01NS037799, T32NS045540)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: acute stress, hippocampus, dendritic spine loss, corticotropin-releasing factor, CRH receptor type 1, learning and memory impairment, long-term potentiation, CA3
MeSH terms: Animals, Cognition, Corticotropin-Releasing Hormone, Hippocampus, Male, Memory, Stress, Psychological, Synapses, Time Factors, Signal Transduction, Long-Term Potentiation, 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

Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks