The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: Dependence on the basolateral amygdala
Open accessAbstract
Previous studies have indicated that stress-activated glucocorticoid hormones induce temporary memory retrieval impairment. The present study examined whether adrenal steroid receptors in the hippocampus mediate such glucocorticoid effects on spatial memory retrieval. The specific glucocorticoid receptor (GR) agonist 11β, 17β-dihydroxy-6,21-dimethyl-17α-pregna-4,6-trien-20yn-3-one (RU 28362; 5 or 15 ng) infused into the hippocampus of male Sprague–Dawley rats 60 min before water-maze retention testing, 24 h after training, dose-dependently impaired probe-trial retention performance, as assessed both by time spent in the training quadrant and initial latency to cross the platform location. The GR agonist did not affect circulating corticosterone levels immediately after the probe trial, indicating that RU 28362 infusions did not influence retention by altering glucocorticoid feedback mechanisms. As infusions of the GR agonist into the hippocampus 60 min before training did not influence water-maze acquisition or immediate recall, the findings indicated that the GR agonist-induced retention impairment was induced selectively by an influence on information retrieval. In contrast, pretest infusions of the GR agonist administered into the basolateral complex of the amygdala (BLA; 2 or 6 ng) did not alter retention performance in the water maze. However, N -methyl- d -aspartate-induced lesions of the BLA, made 1 week before training, blocked the memory retrieval impairment induced by intrahippocampal infusions of RU 28362 given 60 min before the retention test. These findings indicate that the effects of glucocorticoids on retrieval of long-term spatial memory depend on the hippocampus and, additionally, that neuronal input from the BLA is critical in enabling hippocampal glucocorticoid effects on memory retrieval.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The great enhancement and durability of memory for the details of arousing experiences is produced in part by the rapid induction of neuroplasticity in the hippocampus in phase 1, mediated by arousal-related afferents, including the amygdala, hypothalamus, ventral tegmental area, and locus coeruleus.
“We hypothesize that the great enhancement and durability of memory for the details of arousing experiences is produced in part by the rapid induction of neuroplasticity in the hippocampus in phase 1 (Figure 3), mediated by arousal-related afferents, including the amygdala (Abe [18]; Roozendaal et al. [315]; Abe et al. [316]; Richter-Levin [20]; McGaugh [88]; Akirav and Richter-Levin [22]),”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Roozendaal et al. [315]
Cites
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
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
Self-citationHippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · see citing works
A selective role for corticosterone in contextual-fear conditioning
Pugh, C. R., Tremblay, D., Fleshner, M., & Rudy, J. W. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.3.503 · Cited by 272 · see citing works
Support for a Bimodal Role for Type II Adrenal Steroid Receptors in Spatial Memory
Conrad, C. D., Lupien, S. J., & McEwen, B. S. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3898 · Cited by 199 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
McEwen, B. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.071 · Cited by 1,864 · see citing works
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Self-citationDiamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“…in the hippocampus in phase 1 (Figure 3), mediated by arousal-related a ff erents, including the amygdala (Abe [18]; Roozendaal et al. [315]; Abe et al. [316]; Richter-Levin [20]; McGaugh [88]; Akirav and Richter-Levin [22]), hypothalamus (Nakanishi et al. [216]), ventral tegmental…”
BackgroundStress effects on memory: An update and integration
Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714 · see citing works
Self-citationThe selfish brain: Competition for energy resources
Peters, A., Schweiger, U., Pellerin, L., Hubold, C., Oltmanns, K. M., Conrad, M., Schultes, B., Born, J., & Fehm, H. L. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.03.002 · Cited by 489 · see citing works
Stress and memory in humans: twelve years of progress?
Wolf, O. T. (2009) · Brain Research · doi:10.1016/j.brainres.2009.04.013 · Cited by 456 · see citing works
Roozendaal, B., & McGaugh, J. L. (2011) · Behavioral Neuroscience · doi:10.1037/a0026187 · Cited by 445 · see citing works
Self-citationA meta-analytic review of the effects of acute cortisol administration on human memory
Het, S., Ramlow, G., & Wolf, O. T. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.005 · Cited by 414 · see citing works
Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy
Mitra, R., & Sapolsky, R. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705615105 · Cited by 409 · see citing works
Glucocorticoid effects on object recognition memory require training-associated emotional arousal
Okuda, S., Roozendaal, B., & McGaugh, J. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307803100 · Cited by 402 · see citing works
Self-citationRoozendaal, B., Okuda, S., de Quervain, D. J.-F., & McGaugh, J. L. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.049 · Cited by 382 · see citing works
Self-citationDe Quervain, D. J. ‐., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L., Berthold, T., Nitsch, R. M., Buck, A., Roozendaal, B., & Hock, C. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02542.x · Cited by 342 · see citing works
Self-citationMyers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
Roozendaal, B., Hahn, E. L., Nathan, S. V., de Quervain, D. J.-F., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2574-04.2004 · Cited by 301 · see citing works
Self-citationStress, 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
McGaugh, J. L. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-014954 · Cited by 271 · see citing works
Self-citationNeighborhood 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
Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety
Shekhar, A., Truitt, W., Rainnie, D., & Sajdyk, T. (2005) · Stress · doi:10.1080/10253890500504557 · Cited by 237 · see citing works
Brain-Derived Neurotrophic Factor Plays a Critical Role in Contextual Fear Conditioning
Liu, I. Y. C., Lyons, W. E., Mamounas, L. A., & Thompson, R. F. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1948-04.2004 · Cited by 190 · see citing works
Kim, J. J., Koo, J. W., Lee, H. J., & Han, J.-S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4623-04.2005 · Cited by 184 · see citing works
Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences
Roozendaal, B., Barsegyan, A., & Lee, S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67006-x · Cited by 154 · see citing works
Self-citationOei, N. Y. L., Elzinga, B. M., Wolf, O. T., de Ruiter, M. B., Damoiseaux, J. S., Kuijer, J. P. A., Veltman, D. J., Scheltens, P., & Rombouts, S. A. R. B. (2007) · Brain Imaging and Behavior · doi:10.1007/s11682-007-9003-2 · Cited by 146 · see citing works
Atsak, P., Hauer, D., Campolongo, P., Schelling, G., McGaugh, J. L., & Roozendaal, B. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200742109 · Cited by 140 · see citing works
Self-citationFat-induced satiety factor oleoylethanolamide enhances memory consolidation
Campolongo, P., Roozendaal, B., Trezza, V., Cuomo, V., Astarita, G., Fu, J., McGaugh, J. L., & Piomelli, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903038106 · Cited by 133 · see citing works
Self-citationCan Posttraumatic Stress Disorder Be Prevented with Glucocorticoids?
SCHELLING, G., ROOZENDAAL, B., & de QUERVAIN, D. J. ‐. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1314.013 · Cited by 130 · see citing works
Self-citationAtsak, P., Roozendaal, B., & Campolongo, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.047 · Cited by 98 · see citing works
Self-citationKomatsuzaki, Y., Murakami, G., Tsurugizawa, T., Mukai, H., Tanabe, N., Mitsuhashi, K., Kawata, M., Kimoto, T., Ooishi, Y., & Kawato, S. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.07.173 · Cited by 87 · see citing works
Elliott, A. E., & Packard, M. G. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.012 · Cited by 84 · see citing works
The role of the brain renin-angiotensin system (RAS) in mild traumatic brain injury (TBI)
Vadhan, J. D., & Speth, R. C. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107684 · Cited by 42 · see citing works
Glucocorticoid-mediated effects of systemic oxytocin upon memory retrieval
de Oliveira, L. F., Camboim, C., Diehl, F., Consiglio, A. R., & Quillfeldt, J. A. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.05.006 · Cited by 34 · see citing works
- Authors
- Roozendaal, B., Griffith, Q. K., Buranday, J., de Quervain, D. J.-F., & McGaugh, J. L.
- Affiliations
- University of Zurich (CH)
- Center for the Neurobiology of Learning and Memory and Department of Neurobiology and Behavior, University of California, Irvine, CA 92697-3800; and Division of Psychiatry Research, University of Zürich, Lenggstrasse 31, 8029 Zürich, Switzerland Europe
- ORCID
- Roozendaal, Benno
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2003-01-21
- Volume
- 100
- Issue
- 3
- Pages
- 1328-1333
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC298772
- OpenAlex
- W1971207561
- Cited by
- 291
- References
- 5
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 2 · 2023: 5 · 2022: 6 · 2021: 6 · 2020: 13 · 2019: 5 · 2018: 9 · 2017: 13 · 2016: 8 · 2015: 14 · 2014: 15 · 2013: 19 · 2012: 9
- FWCI
- 10.61
- 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)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (58420)
- National Institutes of Health (MH12526)
- U.S. Public Health Service
- National Institute of Mental Health (R01MH012526, MH12526, R56MH012526)
- National Institute of General Medical Sciences (GM-55246-03, R25GM055246)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- glucocorticoids, hippocampus, basolateral amygdala, spatial memory retrieval, glucocorticoid receptor, RU 28362, NMDA lesions, water maze, stress, corticosterone, long-term memory
- MeSH terms
- Adrenal Cortex Hormones, Amygdala, Androstanols, Animals, Dose-Response Relationship, Drug, Glucocorticoids, Hippocampus, Male, Memory, Memory Disorders, Receptors, Glucocorticoid, N-Methylaspartate, Rats, Sprague-Dawley, Maze Learning, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
