Cited by 270Memory and Neural MechanismsStress Responses and CortisolNerve injury and regeneration

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Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation

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Schaaf, M. J. M., De Kloet, E. R., Vreugdenhil, E.·2000·Stress

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Abstract

The adrenal steroid corticosterone has profound effect on the structure and function of the hippocampus. Probably as a result of that, it modulates memory formation. In this review, the question is addressed if the corticosterone effects on memory processes are mediated by alterations in the expression of the neurotrophin Brain-Derived Neurotrophic Factor (BDNF) in the hippocampus. First, studies are described investigating the effect of corticosterone on BDNF expression in the rat hippocampus. It appears that corticosterone suppresses the BDNF expression at the mRNA and protein level in a subfield-specific way. Second, a model for the mechanism of action is proposed. In this model, activated mineralocorticoid and glucocorticoid receptors repress transcriptional activity of the BDNF promoter site-specifically via interaction with other transcription factors. Third, the implications for learning and memory are discussed. Studies show that during water maze training, corticosterone levels rise significantly, but the BDNF expression is not suppressed in any hippocampal subfield. Furthermore, high BDNF expression levels in specific subfields correlate with a good memory performance. Therefore, we suggest that the resistance of the hippocampal BDNF expression to suppression by corticosterone, as seen after water maze training, may contribute to an optimal memory performance.

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Neurogenesis and Neuroenhancement in the Pathophysiology and Treatment of Bipolar Disorder
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The Omega-3 Polyunsaturated Fatty Acid Docosahexaenoic Acid (DHA) Reverses Corticosterone-Induced Changes in Cortical Neurons
Pusceddu, M. M., Nolan, Y. M., Green, H. F., Robertson, R. C., Stanton, C., Kelly, P. M., Cryan, J. F., & Dinan, T. G. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv130 · Cited by 23
“This is in agreement with several studies showing decreased BDNF levels subsequent to chronic CORT treatment both in the rat frontal cortex (Dwivedi et al., 2006) and hippocampus (Schaaf et al., 1998, 2000; Dwivedi et al., 2006).”
Corticolimbic analysis of microRNAs and protein expressions in scopolamine-induced memory loss under stress
Eivani, M., Alijanpour, S., Arefian, E., & Rezayof, A. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107065 · Cited by 22
Spatial memory deficits in maternal iron deficiency paradigms are associated with altered glucocorticoid levels
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“The effects of corticosterone on memory function are mediated by BDNF, which is encoded by one of the primary corticosteroneresponsive genes (Schaff et al., 2000).”
Morc1 knockout evokes a depression-like phenotype in mice
Schmidt, M., Brandwein, C., Luoni, A., Sandrini, P., Calzoni, T., Deuschle, M., Cirulli, F., Riva, M. A., & Gass, P. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.08.005 · Cited by 21
Concomitant docosahexaenoic acid administration ameliorates stress-induced cognitive impairment in rats
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Effects of glucocorticoids on emotion and cognitive processes in animals
Prickaerts, J., & Steckler, T. (2005) · Techniques in the behavioral and neural sciences · doi:10.1016/s0921-0709(05)80021-5 · Cited by 25
Serum brain-derived neurotrophic factor levels as a novel biological marker for the activities of psychiatric symptoms in systemic lupus erythematosus
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“Schaaf et al (2000) have investigated the effects of corticosterone on BDNF expression in the rat hippocampus.”
Background
Chemical Constituents and Antidepressant-Like Effects in Ovariectomized Mice of the Ethanol Extract of Alternanthera philoxeroides
Khamphukdee, C., Monthakantirat, O., Chulikhit, Y., Buttachon, S., Lee, M., Silva, A. M. S., Şekeroğlu, N., & Kijjoa, A. (2018) · Molecules · doi:10.3390/molecules23092202 · Cited by 20
Genetic association of the transcription of neuroplasticity‐related genes and variation in stress‐coping style
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Chronic cortisol exposure promotes the development of a GABAergic phenotype in the primate hippocampus
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A potential role for calcium / calmodulin‐dependent protein kinase‐related peptide in neuronal apoptosis: in vivo and in vitro evidence
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“Moreover, a recent study in zebrafish demonstrated that gene knockdown of DCLK (zDCLK) induced a significant increase of apoptotic cells in the central nervous system (Shimomura et al., 2007).”
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Amygdala, Medial Prefrontal Cortex and Glucocorticoid Interactions Produce Stress-Like Effects on Memory
Kim, E. J., & Kim, J. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00210 · Cited by 21
“As these strategies are experimentally tractable to both in vitro and in vivo analyses, they have generated a wealth of information putatively in relation to stress (Schaaf et al., 2000; Groc et al., 2008).”
Background
Hyperglycemia Induces the Variations of 11 β -Hydroxysteroid Dehydrogenase Type 1 and Peroxisome Proliferator-Activated Receptor- γ Expression in Hippocampus and Hypothalamus of Diabetic Rats
Qi, W.-W., Li-yong, Z., Li, X., Li, G., Liu, Z., Hu, J., & Chen, N. (2012) · Experimental Diabetes Research · doi:10.1155/2012/107130 · Cited by 18
“However, a higher local level of GC probably contributes to the cognitive impairment and the impairment of the memory form by suppressing the hippocampus BDNF expression, which is a neurotrophic factor [12].”
Sleep and Behavior in Cross-Fostering Rats: Developmental and Sex Aspects
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The effects of eticlopride on Morris water task performance in male and female rats neonatally treated with quinpirole
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“Additionally, increases in corticosterone were shown to produce changes in neurotrophic factors in the hippocampus and prefrontal cortex, and this change may also be related to cognitive deficits produced by chronic stress (Roceri et al. 2004; Schaaf et al. 2000).”
Early psilocybin intervention alleviates behavioral despair and cognitive impairment in stressed Wistar rats
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Maladaptive Neuroplasticity Under Stress: Insights into Neuronal and Synaptic Changes in the Prefrontal Cortex
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“To unravel the complex molecular mechanisms by which stress affects the synaptic plasticity and neurogenesis, brain-derived neurotrophic factor (BDNF) was discovered as a key regulating factor (reviewed in [50–52]).”
Potential Biomarkers with Plasma Cortisol, Brain-derived Neurotrophic Factor and Nitrites in Patients with Acute Ischemic Stroke
Casas, S., Perez, A., Mattiazzi, M., López, J., Folgueira, A. L., Gargiulo-Monachelli, G. M., Deniselle, M. C. G., & Nicola, A. F. D. (2018) · Current Neurovascular Research · doi:10.2174/1567202614666171005122925 · Cited by 17
Anhedonic-like behavior and BDNF dysregulation following a single injection of cocaine during adolescence
Caffino, L., Mottarlini, F., Mingardi, J., Zita, G., Barbon, A., & Fumagalli, F. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108161 · Cited by 17
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“…are known to both decrease and increase proin ﬂ ammatory cytokines, based on the experimental conditions, as well as to diminish brain-derived neurotrophic factor (BDNF) synthesis, and increase synaptic glutamate levels, all of which are implicated in the development of psychopathology [22 – 25].”
Chronic Hormonal Imbalance and Adipose Redistribution Is Associated with Hypothalamic Neuropathology following Blast Exposure
VandeVord, P. J., Sajja, V. S. S. S., Ereifej, E. S., Hermundstad, A., Mao, S., & Hadden, T. J. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3786 · Cited by 15
“studies have shown that corticosterone and ACTH play important roles in memory formation and in the regulation of neuronal regeneration via neurotrophins, such as brain derived neurotrophic factor.(21,22)”
Corticosterone induces discrete epigenetic signatures in the dorsal and ventral hippocampus that depend upon sex and genotype: focus on methylated Nr3c1 gene
Caradonna, S. G., Einhorn, N. R., Saudagar, V., Khalil, H., Petty, G. H., Lihagen, A., LeFloch, C., Lee, F. S., Akil, H., Guidotti, A., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01864-7 · Cited by 16
“Previous work showed that overexposure to CORT affects the signaling of BDNF in the hippocampus [76, 77], and that methylation changes of Nr3c1 are linked to BDNF expression [78].”
Background
Species-relevant inescapable stress differently influences memory consolidation and retrieval of mice in a spatial radial arm maze
Janitzky, K., Schwegler, H., Kröber, A., Roskoden, T., Yanagawa, Y., & Linke, R. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.12.032 · Cited by 16
Effect of acute psychosocial stress on the brain-derived neurotrophic factor in humans – a randomized cross within trial
Hermann, R. M., Schaller, A., Lay, D., Bloch, W., Albus, C., & Petrowski, K. (2020) · Stress · doi:10.1080/10253890.2020.1854218 · Cited by 15
“…cortisol-levels as in chronic stress and in a psychological disorder like depression, are in line with reduced BDNF levels (Pittenger & Duman, 2008; Schaaf et al., 2000), repeated/interrupted acute stress showed enhanced BDNF protein and mRNA in several brain regions of rats 2 h and 28 days after…”
Background
Higher Cortisol Predicts Less Improvement in Verbal Memory Performance after Cardiac Rehabilitation in Patients with Coronary Artery Disease
Saleem, M., Herrmann, N., Swardfager, W., OH, P. I., Shammi, P., Koren, G., Uum, S. H. M. V., Kiss, A., & Lanctôt, K. L. (2013) · Cardiovascular Psychiatry and Neurology · doi:10.1155/2013/340342 · Cited by 15
The Effects of High-Intensity Interval Training with Supplementation of Flaxseed Oil on BDNF mRNA Expression and Pain Feeling in Male Rats
Rahmati-Ahmadabad, S., Azarbayjani, M. A., & Nasehi, M. (2017) · Annals of Applied Sport Science · doi:10.29252/aassjournal.5.4.1 · Cited by 14
“Moreover, oestrogen is necessary to increase protein BDNF in hippocampus in rats due to exercise (63), while stress hormones reduce hippocampus BDNF (64, 65).”
Background
Vitisin A, a Resveratrol Tetramer, Improves Scopolamine-Induced Impaired Learning and Memory Functions in Amnesiac ICR Mice
Chen, L.-G., Wang, C., Lee, Y.-S., Sie, Y.-Y., Chang, C., & Hou, W. (2022) · Biomedicines · doi:10.3390/biomedicines10020273 · Cited by 15
Neuroprotection and Sex Steroid Hormones: Evidence of Estradiol- Mediated Protection in Hypertensive Encephalopathy
Nicola, A. F. D., Brocca, M. E., Pietranera, L., & García‐Segura, L. M. (2012) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/138955712802762121 · Cited by 14
Distinctive effects of unpredictable subchronic stress on memory, serum corticosterone and hippocampal BDNF levels in high and low exploratory mice
Kazlauckas, V., Kalinine, E., Leke, R., Oses, J. P., Nunes, F., Espinosa, J., Mioranzza, S., Lulhier, F., Portela, L. V., Porciúncula, L. O., et al. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.030 · Cited by 14
The immunomodulatory tellurium compound ammonium trichloro (dioxoethylene-O,O′) tellurate reduces anxiety-like behavior and corticosterone levels of submissive mice
Gross, M., Stanciu, E., Sredni, D., Sredni, B., & Pinhasov, A. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000319 · Cited by 13
Early-life Photoperiod Influences Depression-like Behavior, Prepulse Inhibition of the Acoustic Startle Response, and Hippocampal Astrogenesis in Mice
Takai, Y., Kawai, M., Ogo, T., Ichinose, T., Furuya, S., Takaki, N., Tone, Y., Udo, H., Furuse, M., & Yasuo, S. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.01.038 · Cited by 12
“Abbreviations: BDNF, brain-derived neurotrophic factor; BrdU, 5-bromo-20-deoxyuridine; CA1, cornu ammonis-1; DCX, doublecortin; DG, dentate gyrus; EPMT, elevated plus maze test; FST, forced swim test; GFAP, glial fibrillary acidic protein; GR, glucocorticoid receptor; HPA, hypothalamic-pituitary-adrenocortical; LDs, l…”
Background
Time Course of Behavioral Alteration and mRNA Levels of Neurotrophic Factor Following Stress Exposure in Mouse
Hashikawa, N., Ogawa, T., Sakamoto, Y., Ogawa, M., Matsuo, Y., Zamami, Y., & Hashikawa‐Hobara, N. (2015) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-015-0174-x · Cited by 12
“Furthermore, corticosterone treatment decreases BDNF expression (Schaaf et al. 2000; Jacobsen and Mørk 2006).”
Background
Corticosterone is correlated to mediators of neural plasticity and epigenetic potential in the hippocampus of Senegalese house sparrows (Passer domesticus)
Kilvitis, H. J., Ardia, D. R., Thiam, M., & Martin, L. B. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.09.014 · Cited by 12
Protein synthesis inhibition before or after stress exposure results in divergent endocrine and BDNF responses disassociated from behavioral responses
Kozlovsky, N., Kaplan, Z., Zohar, J., Matar, M. A., Shimon, H., & Cohen, H. (2007) · Depression and Anxiety · doi:10.1002/da.20366 · Cited by 13
“…it is well established that both acute and chronic stress elicit distinct downregulation of hippocampal BDNF mRNA expression [Murakami et al., 2005; Schaaf et al., 1998, 2000; Smith et al., 1995; Ueyama et al., 1997], and this effect has been Depression and Anxiety attributed to increased…”
Background
Investigating the Acute and Chronic Effects of Cardiovascular Exercise on Brain-Derived Neurotrophic Factor in Early Subacute Stroke
Heras, B. D. L., Rodrigues, L., Cristini, J., Yu, E., Gan‐Or, Z., Arbour, N., Thiel, A., Tang, A., Fung, J., Eng, J. J., et al. (2025) · Neurorehabilitation and neural repair · doi:10.1177/15459683251342150 · Cited by 13
“47,48 Furthermore, while long-term CE has shown to offer both anti-inflammatory and stress-reducing benefits, 49 animal studies show that a single CE session, when implemented at higher intensities, can stimulate pro-inflammatory responses and cause up to a 20-fold increase in corticosterone…”
Sex‐specific contribution of glucocorticoid receptor alpha isoforms to anxiety and depressive‐like behavior in mice
Aleksic, M., Brkic, Z., Petrovic, Z., Francija, E., Lukić, I., & Adžić, M. (2022) · Journal of Neuroscience Research · doi:10.1002/jnr.25032 · Cited by 11
“…in cytosolic and nuclear compartments, together with the expression of GR- regulated genes: FK506- binding protein 51 (FKBP51) (Fries et al., 2017), brain- derived neurotrophic factor (BDNF) (Schaaf et al., 2000), GR (Nr3c1) (Burnstein et al., 1991), and interleukin 1β (IL1β) (Maes et al., 1993).”
Background
Early Administration of the Phytocannabinoid Cannabidivarin Prevents the Neurobehavioral Abnormalities Associated with the Fmr1-KO Mouse Model of Fragile X Syndrome
Premoli, M., Fyke, W., Bellocchio, L., Lemaire, V., Woolley-Roberts, M., Bontempi, B., & Pietropaolo, S. (2023) · Cells · doi:10.3390/cells12151927 · Cited by 10
Male-specific effects of lipopolysaccharide on glucocorticoid receptor nuclear translocation in the prefrontal cortex of depressive rats
Brkic, Z., Petrovic, Z., Franic, D., Mitić, M., & Adžić, M. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4374-y · Cited by 11
“Unlike the BDNF and COX-2 gene expressions, the patterns of IL-1β expression were not associated with GR signalling in either of the sexes, which imply other mechanism involved in its regulation.”
Influential
Distinct modifications of hippocampal glucocorticoid receptor phosphorylation and FKBPs by lipopolysaccharide in depressive female and male rats
Brkic, Z., Francija, E., Petrovic, Z., Franic, D., Lukić, I., Mitić, M., & Adžić, M. (2017) · Journal of Psychopharmacology · doi:10.1177/0269881117725914 · Cited by 11
“Those GR-regulated genes include GR itself (Dong et al., 1988), COX-2 (Goppelt-Struebe, 1997), BDNF (Schaaf et al., 2000) and p11 (Zhang et al., 2008).”
Background
Antidepressant-like activity of L-701324 in mice: A behavioral and neurobiological characterization
Liu, L., Ji, C.-H., Wang, Y., Zhao, J., Liu, Y., Tang, W., Gu, J., & Jiang, B. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113038 · Cited by 10

Authors: Schaaf, M. J. M., De Kloet, E. R., & Vreugdenhil, E.
Affiliations: National Institutes of Health (US)
Corresponding author: Vreugdenhil, E.
ORCID: Schaaf, M. J. M.
Vreugdenhil, E.
Venue: Stress
Publisher: Informa UK Limited
Published: 2000-01
Volume: 3
Issue: 3
Pages: 201-208
ISSN: 1025-3890 (ISSN-L)
1607-8888
DOI: 10.3109/10253890009001124
OpenAlex: W2109158936
Semantic Scholar: 93f10485ac4eabd2252567c71e95e9ce8d112ad1
Cited by: 270
References: 59
Citations by year: 2025: 6 · 2024: 9 · 2023: 10 · 2022: 7 · 2021: 11 · 2020: 6 · 2019: 11 · 2018: 15 · 2017: 11 · 2016: 14 · 2015: 15 · 2014: 16 · 2013: 11 · 2012: 11
FWCI: 0.67
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Stress (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Keywords: corticosterone, brain-derived neurotrophic factor, hippocampus, memory formation, learning, mineralocorticoid receptor, glucocorticoid receptor, transcriptional repression, BDNF promoter, hippocampal subfields, stress hormones
MeSH terms: CRF Receptor, Type 1, Adrenalectomy, Animals, Corticosterone, Dose-Response Relationship, Drug, Hippocampus, Kainic Acid, Learning, Memory, Models, Biological, Neurons, Promoter Regions, Genetic, Receptors, Glucocorticoid, RNA, Messenger, Serotonin Antagonists, Stress, Physiological, Transcription, Genetic, Down-Regulation, Receptors, Corticotropin-Releasing Hormone, Receptors, Mineralocorticoid, Dentate Gyrus, Brain-Derived Neurotrophic Factor, Rats

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Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation

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