The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
Glucocorticoids interact with the hippocampal endocannabinoid system in impairing retrieval of contextual fear memory
Open accessAbstract
There is extensive evidence that glucocorticoid hormones impair the retrieval of memory of emotionally arousing experiences. Although it is known that glucocorticoid effects on memory retrieval impairment depend on rapid interactions with arousal-induced noradrenergic activity, the exact mechanism underlying this presumably nongenomically mediated glucocorticoid action remains to be elucidated. Here, we show that the hippocampal endocannabinoid system, a rapidly activated retrograde messenger system, is involved in mediating glucocorticoid effects on retrieval of contextual fear memory. Systemic administration of corticosterone (0.3-3 mg/kg) to male Sprague-Dawley rats 1 h before retention testing impaired the retrieval of contextual fear memory without impairing the retrieval of auditory fear memory or directly affecting the expression of freezing behavior. Importantly, a blockade of hippocampal CB1 receptors with AM251 prevented the impairing effect of corticosterone on retrieval of contextual fear memory, whereas the same impairing dose of corticosterone increased hippocampal levels of the endocannabinoid 2-arachidonoylglycerol. We also found that antagonism of hippocampal β-adrenoceptor activity with local infusions of propranolol blocked the memory retrieval impairment induced by the CB receptor agonist WIN55,212-2. Thus, these findings strongly suggest that the endocannabinoid system plays an intermediary role in regulating rapid glucocorticoid effects on noradrenergic activity in impairing memory retrieval of emotionally arousing experiences.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“As part of this protective role under aversive conditions, elevated EC signaling during stress has been shown to dampen the development of anxiety [12] and to regulate the encoding [13], retrieval [14] and extinction [15] of traumatic memories.”
From Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder (2013) · cites this paper as [14]
Citations
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
THE AMYGDALA MODULATES THE CONSOLIDATION OF MEMORIES OF EMOTIONALLY AROUSING EXPERIENCES
McGaugh, J. L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144157 · Cited by 2,296
Self-citationStress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760
Self-citationRole of Endogenous Cannabinoids in Synaptic Signaling
Freund, T. F., Katona, I., & Piomelli, D. (2003) · Physiological Reviews · doi:10.1152/physrev.00004.2003 · Cited by 1,616
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,595
Stress and cognition: are corticosteroids good or bad guys?
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01438-1 · Cited by 1,258
Katona, I., Sperlágh, B., Sı́k, A., Käfalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04544.1999 · Cited by 1,218
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 · cited 2×
“CORT doses were based on previous findings (6, 38).”
MethodSelf-citationRole of adrenal stress hormones in forming lasting memories in the brain
McGaugh, J. L., & Roozendaal, B. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00306-9 · Cited by 818
Self-citation
Cited by
Sorted by citations
Items 101–138 of 138
Kwee, C., van der Flier, F. E., Duits, P., van Balkom, A. J. L. M., Cath, D. C., & Baas, J. M. P. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06512-6 · Cited by 7
The Hippocampal Endocannabinoid System in Different Memory Phases: Unveiling the CA1 Circuitry
Quillfeldt, J. A., & Alvares, L. D. O. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_3 · Cited by 7
What Is the Role of Glucocorticoids in the Effects of Stress on the Brain?
Benarroch, E. E. (2025) · Neurology · doi:10.1212/wnl.0000000000213874 · Cited by 4
Impaired Aversive Memory Formation in GPR37L1KO Mice
Veenit, V., Zhang, X., Pasławski, W., Mantas, I., & Svenningsson, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232214290 · Cited by 4
Dragon, J., & Obuchowicz, E. (2024) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-023-02938-z · Cited by 4
Omoumi, S., Rashidy‐Pour, A., Seyedinia, S. A., Tarahomi, P., Sedaghat, K., Vafaei, A. A., & Raise‐Abdullahi, P. (2024) · Brain and Behavior · doi:10.1002/brb3.70043 · Cited by 4
Acute stress modulates hippocampal to entorhinal cortex communication
Nasretdinov, A., Jappy, D., Vazetdinova, A., Valiullina, F., & Rozov, A. V. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1327909 · Cited by 3
Nightmares and the Cannabinoids
Mamelak, M. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200114142321 · Cited by 4
Ganzel, B. L., & Morris, P. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy215 · Cited by 3
Dialectics of perisomatic inhibition—The unity and conflict of opposites
Rozov, A. V., Jappy, D., Maltseva, K., Vazetdinova, A., & Valiullina, F. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1494300 · Cited by 2
Cesare, B. D., Mancini, G. F., Lisiola, J. M., Pisaneschi, A., Sikora, V., Morena, M., Caraci, F., Riva, M. A., Schiavone, S., & Campolongo, P. (2025) · Biochemical Pharmacology · doi:10.1016/j.bcp.2025.117413 · Cited by 3
Self-citationAdrenal Stress Hormone Effects on Memory
Roozendaal, B., & Hermans, E. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00015-8 · Cited by 2
Self-citationFornari, R. V., Aerni, A., de Quervain, D. J. ‐., & Roozendaal, B. (2019) · Springer eBooks · doi:10.1007/978-3-030-16996-1_7 · Cited by 2
Self-citationEndocannabinoid signaling and stress resilience
Hill, M. N., & Patel, S. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00022-7 · Cited by 1
Corrêa, M. D. S., Fornari, R. V., Stern, C. A. J., Bertoglio, L. J., & Gazarini, L. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90877-1.00019-x · Cited by 1
Alteration of brain endocannabinoids on restraint stress-induced anxiety-like behaviors in mice
Fukumori, R., Ueo, K., Nakashima, R., & Yamaguchi, T. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115201 · Cited by 1
Brunello, C. A., Ortiz, M. G., Muñoz, P. P., Araújo, J. P., Pajuelo, J. E. C., Marti, J. C. A., Lyytikäinen, E., Hansen, M., Tonelli, S., Didio, G., et al. (2026) · Journal of Biological Chemistry · doi:10.64898/2026.04.08.717148 · Cited by 1
Atsak, P., Roozendaal, B., & Campolongo, P. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1056-4_5 · Cited by 1
Self-citationFornari, R. V., Aerni, A., Roozendaal, B., & de Quervain, D. J. ‐. (2011) · Springer eBooks · doi:10.1007/978-3-642-22272-6_5 · Cited by 1
Self-citationMcGaugh, J. L., & Roozendaal, B. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21092-4 · Cited by 1
Self-citationImpact of CBG deficiency on emotional and cognitive processes
de Medeiros, G. F. (2016) · theses.fr (ABES) · doi:10.70675/5068781bzb1fez4551z99eez04f240a93ed0 · Cited by 1
Endocannabinoid Modulation of Memory for Emotionally Arousing Experiences
Morena, M., Mariani, F., Papagianni, E., & Campolongo, P. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_1
Self-citationApoptosis and inflammation regulation after injury to the developing brain
Han, W. (2015) · Figshare
Reis, F. M. (2016) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.59.2016.tde-06122015-142707
PROGRAMA DE PÓS-GRADUAÇÃO EM MEDICINA E CIÊNCIAS DA SAÚDE ÁREA DE CONCENTRAÇÃO: NEUROCIÊNCIAS
Medicina, F. D., & Schmidt, S. D. (2012)
Volkova, E. P., Nadareishvili, G. G., & Bolshakov, A. P. (2017) · S S Korsakov Journal of Neurology and Psychiatry · doi:10.17116/jnevro20171171136-42
Volkova, E. P., Nadareishvili, G. G., & Bolshakov, A. P. (2018) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-018-0581-9
Delcellier, K. (2015) · Carleton University's Institutional Repository (MacOdrum Library, Carleton University) · doi:10.22215/etd/2015-11094
Rosa, J. (2020) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2020.tde-17072019-094546
Schwabe, L. (2024) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190917982.013.66
Central Nervous System: Pain, Movement, and Memory
Dedam, J.-P. H., Fogel, M., & Fogel, E. (2025) · Springer eBooks · doi:10.1007/978-3-031-87484-0_11
Mancini, G. F., Morena, M., & Campolongo, P. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-13908-6.00020-7
Self-citationEndocannabinoids and the neurobiology of emotional states
Petrie, G. N., Lunge, A. R., Mayo, L. M., & Hill, M. N. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-13908-6.00021-9
Chemogenetic manipulation of the hippocampus alleviates obesogenic diet-induced memory deficits
Bakoyiannis, I. (2021) · theses.fr (ABES) · doi:10.70675/f5ac23cezc829z4dc0zaf4az467fb1eb75a9
Quillfeldt, J. A., & Alvares, L. D. O. (2026) · Springer eBooks · doi:10.1007/978-3-032-12239-1_3
Mizuno, I., Matsuda, S., & Mizutani, A. (2026) · Neuropharmacology · doi:10.1016/j.neuropharm.2026.111153
Thomas, E. M. (2014) · Papyrus : Institutional Repository (Université de Montréal) · doi:10.71781/18315
Metadata
- Authors
- Atsak, P., Hauer, D., Campolongo, P., Schelling, G., McGaugh, J. L., & Roozendaal, B.
- Affiliations
- University Medical Center Groningen (NL)
- Sapienza University of Rome (IT)
- Ludwig-Maximilians-Universität München (DE)
- University of California, Irvine (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-02-13
- Volume
- 109
- Issue
- 9
- Pages
- 3504-3509
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3295257
- OpenAlex
- W2147317037
- Cited by
- 140
- References
- 64
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 8 · 2023: 11 · 2022: 8 · 2021: 7 · 2020: 7 · 2019: 9 · 2018: 9 · 2017: 13 · 2016: 12 · 2015: 16 · 2014: 14 · 2013: 11 · 2012: 5
- FWCI
- 7.54
- 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)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- glucocorticoids, endocannabinoid system, hippocampus, contextual fear memory, corticosterone, CB1 receptor, 2-arachidonoylglycerol, noradrenergic activity, propranolol, beta-adrenoceptor antagonism, WIN 55,212-2, emotional arousal, retrograde signaling
- MeSH terms
- Acoustic Stimulation, Adrenergic beta-Antagonists, Animals, Arachidonic Acids, Arousal, Conditioning, Classical, Corticosterone, Electroshock, Emotions, Fear, Glucocorticoids, Glycerides, Hippocampus, Male, Memory, Morpholines, Naphthalenes, Piperidines, Propranolol, Pyrazoles, Receptors, Glucocorticoid, Rats, Sprague-Dawley, Receptor, Cannabinoid, CB1, Freezing Reaction, Cataleptic, Benzoxazines, Rats, Cannabinoid Receptor Modulators, Endocannabinoids
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
