Sex Differences in the Effects of Acute and Chronic Stress and Recovery after Long-Term Stress on Stress-Related Brain Regions of Rats
Open accessAbstract
Studies show that sex plays a role in stress-related depression, with women experiencing a higher vulnerability to its effect. Two major targets of antidepressants are brain-derived neurotrophic factor (BDNF) and cyclic adenosine monophosphate response element-binding protein (CREB). The aim of this study was to investigate the levels of CREB, phosphorylation of CREB (pCREB), and BDNF in stress-related brain regions of male and female rats after stress and recovery. CREB and pCREB levels were examined in CA1, CA2, CA3, paraventricular nucleus of the thalamus (PVT), amygdala, anterior cingulate area, dorsal part (ACAd), and infralimbic area of prefrontal cortex (PFC), whereas dentate gyrus (DG) and prelimbic area (PL) of PFC were examined for BDNF levels. Our results demonstrate that levels of CREB and pCREB in male CA1, CA2 and CA3, PVT, amygdala, and ACAd were reduced by stress, whereas the same brain regions of female rats exhibited no change. BDNF levels were decreased by chronic stress in female PL but were increased by acute stress in female DG. BDNF levels in male DG and PL were found not to undergo change in response to stress. Abnormalities in morphology occurred after chronic stress in males but not in females. In all cases, the levels of CREB, pCREB, and BDNF in recovery animals were comparable to the levels of these proteins in control animals. These findings demonstrate a sexual dimorphism in the molecular response to stress and suggest that these differences may have important implications for potential therapeutic treatment of depression.
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Chronic glucocorticoid exposure reduces brain-derived neurotrophic factor levels in the PFC, as does chronic stress, but it is not yet known whether this contributes to the observed dendritic changes.
“Chronic glucocorticoid exposure also reduces brain-derived neurotrophic factor levels in the PFC119, as does chronic stress120, but it is not yet known whether this contributes to the observed dendritic changes.”
From Stress signalling pathways that impair prefrontal cortex structure and function (2009) · cites this paper as [120]
Citation 120 attaches to the chronic-stress portion of the sentence, not the glucocorticoid-exposure claim. The Results section (“BDNF Levels in Male and Female PL and DG”; page not available in our copy) reports reduced BDNF in the prelimbic PFC after chronic stress in female rats, but no significant change in male rats. The unqualified claim omits that sex-specific limit. (LLM, conf=0.90)
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Cites
A Neurotrophic Model for Stress-Related Mood Disorders
Duman, R. S., & Monteggia, L. M. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.02.013 · Cited by 3,375 · see citing works
Kessler, R. (1993) · Journal of Affective Disorders · doi:10.1016/0165-0327(93)90026-g · Cited by 2,207 · see citing works
Function and regulation of CREB family transcription factors in the nervous system
Lonze, B. E., & Ginty, D. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)00828-0 · Cited by 2,127 · see citing works
Simerly, R. B., Swanson, L. W., Chang, C., & Muramatsu, M. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902940107 · Cited by 2,118 · see citing works
Nibuya, M., Morinobu, S., & Duman, R. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07539.1995 · Cited by 2,109 · see citing works
Glucocorticoids and Hippocampal Atrophy in Neuropsychiatric Disorders
Sapolsky, R. M. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.10.925 · Cited by 2,016 · see citing works
Epidemiology of women and depression
Kessler, R. (2003) · Journal of Affective Disorders · doi:10.1016/s0165-0327(02)00426-3 · Cited by 2,006 · see citing works
Brain Maps: Structure of the Rat Brain
Swanson, L. W. (1992) · Medical Entomology and Zoology · Cited by 1,851 · see citing works
New approaches to antidepressant drug discovery: beyond monoamines
Berton, O., & Nestler, E. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1846 · Cited by 1,589 · see citing works
Smith, M., Makino, S., Květňanský, R., & Post, R. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01768.1995 · Cited by 1,429 · see citing works
Carlezon, W. A., Duman, R. S., & Nestler, E. J. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.06.005 · Cited by 1,351 · see citing works
Drevets, W. C. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00203-8 · Cited by 1,146 · see citing works
Plasticity of the Hippocampus: Adaptation to Chronic Stress and Allostatic Load
McEwen, B. S. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05830.x · Cited by 875 · see citing works
Multiple promoters direct tissue-specific expression of the rat BDNF gene
Timmusk, T., Palm, K., Metsis, M., Reintam, T., Paalme, V., Saarma, M., & Persson, H. (1993) · Neuron · doi:10.1016/0896-6273(93)90335-o · Cited by 858 · see citing works
Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells
Rajkowska, G. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00950-1 · Cited by 822 · see citing works
Efferent projections of the infralimbic cortex of the rat
Hurley, K. M., Herbert, H., Moga, M. M., & Saper, C. B. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903080210 · Cited by 777 · see citing works
Cotter, D., Mackay, D., Landau, S., Kerwin, R., & Everall, I. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.6.545 · Cited by 766 · see citing works
Identification of a Signaling Pathway Involved in Calcium Regulation of BDNF Expression
Shieh, P. B., Hu, S.-C., Bobb, K., Timmusk, T., & Ghosh, A. (1998) · Neuron · doi:10.1016/s0896-6273(00)81011-9 · Cited by 693 · see citing works
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
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
Neuroimaging studies of mood disorder effects on the brain
Sheline, Y. I. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00347-0 · Cited by 660 · see citing works
Effects of adverse experiences for brain structure and function
McEwen, B. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00964-1 · Cited by 639 · see citing works
Conkright, M. D., Canettieri, G., Screaton, R. A., Guzmán, E., Miraglia, L. J., Hogenesch, J. B., & Montminy, M. (2003) · Molecular Cell · doi:10.1016/j.molcel.2003.08.013 · Cited by 602 · see citing works
Galea, L. A. M., McEwen, B. S., Tanapat, P., Deak, T., Spencer, R. L., & Dhabhar, F. S. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00233-9 · Cited by 540 · see citing works
Antidepressants and neuroplasticity
D'Sa, C. M., & Duman, R. S. (2002) · Bipolar Disorders · doi:10.1034/j.1399-5618.2002.01203.x · Cited by 516 · see citing works
Barrot, M., Olivier, J. D. A., Perrotti, L. I., DiLeone, R. J., Berton, O., Eisch, A. J., Impey, S., Storm, D. R., Neve, R. L., Yin, J. C., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172091899 · Cited by 508 · see citing works
cAMP Response Element-Mediated Gene Transcription Is Upregulated by Chronic Antidepressant Treatment
Thome, J., Sakai, N., Shin, K.-H., Steffen, C., Zhang, Y.-J., Impey, S., Storm, D. R., & Duman, R. S. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04030.2000 · Cited by 507 · see citing works
Monteggia, L. M., Luikart, B., Barrot, M., Theobold, D., Malkovska, I., Nef, S., Parada, L. F., & Nestler, E. J. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.021 · Cited by 502 · see citing works
Vogt, B. A., & Laureys, S. (2005) · Progress in brain research · doi:10.1016/s0079-6123(05)50015-3 · Cited by 497 · see citing works
Protein phosphatase 1 is a molecular constraint on learning and memory
Genoux, D., Haditsch, U., Knobloch, M., Michalon, A., Storm, D., & Mansuy, I. M. (2002) · Nature · doi:10.1038/nature00928 · Cited by 472 · see citing works
Adachi, M., Barrot, M., Autry, A. E., Theobald, D., & Monteggia, L. M. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.09.019 · Cited by 380 · see citing works
Graef, I. A., Wang, F., Charron, F., Chen, L., Neilson, J., Tessier-Lavigne, M., & Crabtree, G. R. (2003) · Cell · doi:10.1016/s0092-8674(03)00390-8 · Cited by 379 · see citing works
The Role of CREB in Depression and Antidepressant Treatment
Blendy, J. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.11.003 · Cited by 365 · see citing works
Iourgenko, V., Zhang, W., Mickanin, C., Daly, I., Jiang, C., Hexham, J. M., Orth, A. P., Miraglia, L. J., Meltzer, J., Garza, D., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1932773100 · Cited by 362 · see citing works
BEBBINGTON, P. E., DUNN, G., JENKINS, R., LEWIS, G., BRUGHA, T., FARRELL, M., & MELTZER, H. (1998) · Psychological Medicine · doi:10.1017/s0033291797006077 · Cited by 330 · see citing works
Li, S., Wang, C., Wang, M., Murakami, Y., & Matsumoto, K. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.01.004 · Cited by 329 · see citing works
Conti, A. C., Cryan, J. F., Dalvi, A., Lucki, I., & Blendy, J. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-08-03262.2002 · Cited by 328 · see citing works
Calcium regulation of gene expression in neuronal cells
Ghosh, A., Ginty, D. D., Bading, H., & Greenberg, M. E. (1994) · Journal of Neurobiology · doi:10.1002/neu.480250309 · Cited by 326 · see citing works
Chen, A. C. H., Shirayama, Y., Shin, K.-H., Neve, R. L., & Duman, R. S. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01114-8 · Cited by 314 · see citing works
Estrogen Receptor Gene Expression in Relation to Neuropsychiatric Disorders
Östlund, H., Keller, É., & Hurd, Y. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1286.006 · Cited by 287 · see citing works
The Role of Functional Neuroimaging in the Neuropsychology of Depression
Liotti, M., & Mayberg, H. S. (2001) · Journal of Clinical and Experimental Neuropsychology · doi:10.1076/jcen.23.1.121.1223 · Cited by 277 · see citing works
Puberty and the emergence of gender differences in psychopathology
Hayward, C., & Sanborn, K. (2002) · Journal of Adolescent Health · doi:10.1016/s1054-139x(02)00336-1 · Cited by 270 · see citing works
Rasmusson, A. M. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00286-5 · Cited by 259 · see citing works
Stress sensitivity and the development of affective disorders
Bale, T. L. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.033 · Cited by 245 · see citing works
Repeated stress increases catalytic TrkB mRNA in rat hippocampus
Nibuya, M., Takahashi, M., Russell, D., & Duman, R. S. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00335-3 · Cited by 236 · see citing works
Functional actions of corticosteroids in the hippocampus
Joëls, M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.064 · Cited by 209 · see citing works
Sairanen, M., O’Leary, O. F., Knuuttila, J. E., & Castrén, E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.069 · Cited by 206 · see citing works
Stress induces neuronal death in the hippocampus of castrated rats
Mizoguchi, K., Kunishita, T., Chui, D., & Tabira, T. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90495-s · Cited by 206 · see citing works
Estrogen mediates sex differences in stress-induced prefrontal cortex dysfunction
Shansky, R. M., Glavis-Bloom, C., Lerman, D., McRae, P., Benson, C., Miller, K., Cosand, L., Horvath, T. L., & Arnsten, A. F. T. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001435 · Cited by 200 · cited 1× · see citing works
“Hippocampus and PFC are implicated as the key sites of neuropathology in depression (Rajkowska 2000; McEwen 2001; Shansky et al. 2004).”
BackgroundAcute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice
Pizarro, J. M., Lumley, L. A., Medina, W., Robison, C. L., Chang, W. E., Alagappan, A., Bah, M. J., Dawood, M. Y., Shah, J. D., Mark, B., et al. (2004) · Brain Research · doi:10.1016/j.brainres.2004.06.085 · Cited by 196 · see citing works
Falconer, E. M., & Galea, L. A. M. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02542-3 · Cited by 192 · see citing works
BDNF impairment in the hippocampus is related to enhanced despair behavior in CB1 knockout mice
Aso, E., Ozaita, A., Valdizán, E. M., Ledent, C. A., Pazos, Á., Maldonado, R. J., & Valverde, O. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.05149.x · Cited by 189 · see citing works
Alteration in the Hypothalamic-Pituitary-Ovarian Axis in Depressed Women
Young, E. A., MIDGLEY, A. R., Carlson, N. E., & Brown, M. B. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.12.1157 · Cited by 187 · see citing works
Stanciu, M., Radulović, J., & Spiess, J. (2001) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00174-7 · Cited by 178 · see citing works
Placing gender at the centre of health programming: challenges and limitations
Vlassoff, C., & Moreno, C. G. (2002) · Social Science & Medicine · doi:10.1016/s0277-9536(01)00339-2 · Cited by 172 · see citing works
Pandey, S. C., Roy, A., & Zhang, H. (2003) · Alcoholism: Clinical and Experimental Research · doi:10.1097/01.alc.0000056616.81971.49 · Cited by 168 · see citing works
Nikulina, E. M., Covington, H. E., Ganschow, L., Hammer, R. P., & Miczek, K. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.10.029 · Cited by 158 · see citing works
Neurogenesis and Helplessness Are Mediated by Controllability in Males But Not in Females
Shors, T. J., Mathew, J., Sisti, H. M., Edgecomb, C., Beckoff, S., & Dalla, C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.033 · Cited by 140 · see citing works
Modulation of synaptic plasticity by stress and antidepressants
Popoli, M., Gennarelli, M., & Racagni, G. (2002) · Bipolar Disorders · doi:10.1034/j.1399-5618.2002.01159.x · Cited by 139 · see citing works
Elevated Concentrations of CRF in the Locus Coeruleus of Depressed Subjects
Bissette, G., Klimek, V., Pan, J., Stockmeier, C., & Ordway, G. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300191 · Cited by 136 · see citing works
Franklin, T. B., & Perrot-Sinal, T. S. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.05.008 · Cited by 134 · see citing works
Hagihara, K., Hirata, S., Osada, T., Hirai, M., & Kato, J. (1992) · Molecular Brain Research · doi:10.1016/0169-328x(92)90179-f · Cited by 134 · see citing works
Wallace, T. L., Stellitano, K. E., Neve, R. L., & Duman, R. S. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.04.010 · Cited by 133 · see citing works
Bilang‐Bleuel, A., Rech, J., Carli, S. D., Holsboer, F., & Reul, J. M. H. M. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01934.x · Cited by 130 · see citing works
Modulation of Anxiety-Like Behavior and Morphine Dependence in CREB-Deficient Mice
Valverde, O., Mantamadiotis, T., Torrecilla, M., Ugedo, L., Pineda, J., Bleckmann, S. C., Gass, P., Kretz, O., Mitchell, J., Schütz, G., et al. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300416 · Cited by 118 · see citing works
Depression: What We can Learn from Postmortem Studies
Rajkowska, G. (2003) · The Neuroscientist · doi:10.1177/1073858403252773 · Cited by 114 · see citing works
Quetiapine reverses the suppression of hippocampal neurogenesis caused by repeated restraint stress
Luo, C., Xu, H., & Li, X. (2005) · Brain Research · doi:10.1016/j.brainres.2005.09.043 · Cited by 114 · see citing works
Self-citationLaifenfeld, D., Karry, R., Grauer, E., Klein, E., & Ben-Shachar, D. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.03.023 · Cited by 103 · see citing works
Gender-specific effects of social housing in rats after chronic mild stress exposure
Westenbroek, C. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(02)00310-x · Cited by 102 · see citing works
Self-citationBurton, C. L., Chatterjee, D., Chatterjee‐Chakraborty, M., Lovic, V., Grella, S. L., Steiner, M. S., & Fleming, A. S. (2007) · Brain Research · doi:10.1016/j.brainres.2007.05.003 · Cited by 89 · see citing works
Gender-specific effects of social housing on chronic stress-induced limbic FOS expression
Westenbroek, C., den Boer, J. A., & Horst, G. J. T. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00367-1 · Cited by 73 · see citing works
Self-citationCognitive deficits, schizophrenia, and the anterior cingulate cortex
Sanders, G. S., Gallup, G. G., Heinsen, H., Hof, P. R., & Schmitz, C. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)01892-2 · Cited by 66 · see citing works
Pardon, M., Roberts, R. E., Marsden, C. A., Bianchi, M., Latif, M. L., Duxon, M. S., & Kendall, D. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.033 · Cited by 60 · see citing works
Beck, C. H. M., & Fibiger, H. C. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)00391-u · Cited by 60 · see citing works
The When and Where of BDNF and the Antidepressant Response
Wang, J., Dranovsky, A., & Hen, R. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.01.008 · Cited by 55 · see citing works
Sun, M., & Alkon, D. L. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.093948 · Cited by 53 · see citing works
Miyata, K., Omori, N., Uchino, H., Yamaguchi, T., Isshiki, A., & Shibasaki, F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00225-1 · Cited by 51 · see citing works
The roots of depression in adolescent girls: Is menarche the key?
Born, L., Shea, A. K., & Steiner, M. S. (2002) · Current Psychiatry Reports · doi:10.1007/s11920-002-0073-y · Cited by 50 · see citing works
Rantamäki, T., Knuuttila, J. E. A., Hokkanen, M., & Ċastrén, E. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.10.001 · Cited by 50 · see citing works
Nanda, S. A., & Mack, K. J. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00054-1 · Cited by 49 · see citing works
Lin, Y., Westenbroek, C., Bakker, P. L., Termeer, J., Liu, A., Li, X., & Horst, G. J. T. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn035 · Cited by 48 · see citing works
Self-citationStress disorders and gender: implications for theory and research.
Carter-Snell, C., & Hegadoren, K. (2003) · PubMed · Cited by 43 · see citing works
Some assessments of the amygdala role in suprahypothalamic neuroendocrine regulation: a minireview.
Talarovičová, A., Kršková, L., & Kiss, A. (2007) · PubMed · Cited by 29 · see citing works
Shors, T. J. (1999) · Neuroreport · doi:10.1097/00001756-199909090-00021 · Cited by 27 · see citing works
Hebda‐Bauer, E. K., Watson, S. J., & Akil, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03487.x · Cited by 22 · see citing works
Yang, C., Huang, C., & Hsu, K. (2008) · Hippocampus · doi:10.1002/hipo.20414 · Cited by 17 · see citing works
Bubser, M., & Deutch, A. Y. (1999) · Synapse · doi:10.1002/(sici)1098-2396(199904)32:1
Flagged first, then by citations
Research works printed but not linked: 1
- Conkright MD Canettieri G Screaton R Guzman E Miraglia L Hogenesch JB Montminy M TORCs: transducers of regulated CREB activity Mol Cell 2003 12 413 423 14536081
Cited by
Sorted by citations
Stress signalling pathways that impair prefrontal cortex structure and function
Arnsten, A. F. T. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2648 · Cited by 3,299 · see citing works
Lucassen, P. J., Pruessner, J. C., Sousa, N., Almeida, O. F. X., Dam, A. M. V., Rajkowska, G., Swaab, D. F., & Czéh, B. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1223-5 · Cited by 449 · see citing works
James, K. A., Stromin, J., Steenkamp, N., & Combrinck, M. I. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1085950 · Cited by 461 · see citing works
Synaptic plasticity in depression: molecular, cellular and functional correlates.
Marsden, W. N. (2013) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.12.012 · Cited by 321 · see citing works
Sandman, C. A., Davis, E. P., Buß, C., & Glynn, L. M. (2011) · Neuroendocrinology · doi:10.1159/000327017 · Cited by 293 · see citing works
Fear extinction and BDNF: translating animal models of PTSD to the clinic
Andero, R., & Ressler, K. J. (2012) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2012.00801.x · Cited by 275 · see citing works
Stress effects on BDNF expression: Effects of age, sex, and form of stress
Bath, K. G., Schilit, A., & Lee, F. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.01.074 · Cited by 197 · see citing works
Male or Female? Brains are Intersex
Joel, D. (2011) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00057 · Cited by 191 · see citing works
Perry, J. L., Joseph, J. E., Jiang, Y., Zimmerman, R. S., Kelly, T. H., Darna, M., Huettl, P., Dwoskin, L. P., & Bardo, M. T. (2011) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.09.001 · Cited by 180 · see citing works
The Relationships Between Stress, Mental Disorders, and Epigenetic Regulation of BDNF
Miao, Z., Wang, Y., & Sun, Z. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041375 · Cited by 178 · see citing works
Beyond sex differences: new approaches for thinking about variation in brain structure and function
Joel, D., & Fausto‐Sterling, A. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0451 · Cited by 147 · see citing works
Transcriptional Control of Monocyte Gene Expression in Post-Traumatic Stress Disorder
O’Donovan, A., Sun, B., Cole, S., Rempel, H., Lenoci, M., Pulliam, L., & Neylan, T. (2011) · Disease Markers · doi:10.1155/2011/560572 · Cited by 141 · see citing works
Simpson, J., & Kelly, J. P. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.12.036 · Cited by 135 · see citing works
Realini, N., Viganò, D., Guidali, C., Zamberletti, E., Rubino, T., & Parolaro, D. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.09.003 · Cited by 130 · see citing works
Neighborhood disadvantage and adolescent stress reactivity
Hackman, D. A., Betancourt, L. M., Brodsky, N. L., Hurt, H., & Farah, M. J. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00277 · Cited by 124 · see citing works
Love is more than just a kiss: a neurobiological perspective on love and affection
de Boer, A., van Buel, E. M., & Ter Horst, G. J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.017 · Cited by 123 · see citing works
Joel, D. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-27 · Cited by 103 · see citing works
Neurobehavioral risk is associated with gestational exposure to stress hormones
Sandman, C. A., & Davis, E. P. (2012) · Expert Review of Endocrinology & Metabolism · doi:10.1586/eem.12.33 · Cited by 90 · see citing works
Lenglos, C., Mitra, A., Guèvremont, G., & Timofeeva, E. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12028 · Cited by 82 · see citing works
Perrino, C., Ferdinandy, P., Bøtker, H. E., Brundel, B. J. J. M., Collins, P. D., Davidson, S. M., den Ruijter, H. M., Engel, F. B., Gerdts, E., Girão, H., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa155 · Cited by 84 · see citing works
Shiers, S. I., Pradhan, G., Mwirigi, J. M., Mejia, G., Ahmad, A., Kroener, S., & Price, T. J. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0713-18.2018 · Cited by 79 · see citing works
Sex differences in cerebral ischemia: Possible molecular mechanisms
Siegel, C. S., Turtzo, L. C., & McCullough, L. D. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22406 · Cited by 74 · see citing works
Blume, S. R., Padival, M., Urban, J. H., & Rosenkranz, J. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-48683-3 · Cited by 71 · see citing works
Lee, T. T. Y., & Hill, M. N. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.017 · Cited by 67 · see citing works
Melcangi, R. C., & García‐Segura, L. M. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.06.001 · Cited by 63 · see citing works
Shin, S., Lay, J. E. L., Everett, L. J., Gupta, R. K., Rafiq, K., & Kaestner, K. H. (2014) · Molecular Metabolism · doi:10.1016/j.molmet.2014.08.001 · Cited by 63 · see citing works
Venezia, A. C., Pitchford, L. M., Sapp, R. M., Spangenburg, E. E., & Roth, S. M. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.12.026 · Cited by 57 · see citing works
The Neurotrophic Hypothesis of Depression Revisited: New Insights and Therapeutic Implications
Jaggar, M., Fanibunda, S. E., Ghosh, S. K., Duman, R. S., & Vaidya, V. A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813333-0.00006-8 · Cited by 58 · see citing works
Wellman, C. L., Bollinger, J. L., & Moench, K. M. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.11.007 · Cited by 53 · see citing works
Barfield, E. T., & Gourley, S. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.10.015 · Cited by 53 · see citing works
Behavioral and neural sequelae of stressor exposure are not modulated by controllability in females
Baratta, M., Leslie, N. R., Fallon, I. P., Dolzani, S. D., Chun, L., Tamalunas, A., Watkins, L., & Maier, S. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13833 · Cited by 49 · see citing works
Preez, A. D., Eum, J., Eiben, I., Eiben, P., Zunszain, P. A., Pariante, C. M., Thuret, S., & Fernandes, C. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2020.100896 · Cited by 46 · see citing works
Rasia‐Filho, A. A., Dalpian, F., Menezes, I. C., Brusco, J., Moreira, J. E., & Cohen, R. S. (2012) · PubMed · doi:10.14670/hh-27.985 · Cited by 45 · see citing works
Mitić, M., Simic, I., Djordjevic, J., Radojcic, M. B., & Adžić, M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.12.012 · Cited by 45 · see citing works
Sikandaner, H., Park, S. Y., Kim, M. J., Park, S. N., & Yang, D. W. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.10.046 · Cited by 45 · see citing works
Olave, F. A., Aguayo, F. I., Román-Albasini, L., Corrales, W. A., Silva, J. P., González, P. I., Lagos, S., García-Pérez, M. A., Alarcón-Mardones, M., Rojas, P. S., et al. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100440 · Cited by 41 · see citing works
Sex differences and estrous cycle effects on foreground contextual fear conditioning
Cossio, R., Carreira, M. B., Vásquez, C. E., & Britton, G. B. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.026 · Cited by 41 · see citing works
Moench, K. M., & Wellman, C. L. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.12.035 · Cited by 41 · see citing works
Chronic social defeat up-regulates expression of norepinephrine transporter in rat brains
Chen, P., Fan, Y., Li, Y., Sun, Z., Bissette, G., & Zhu, M. (2011) · Neurochemistry International · doi:10.1016/j.neuint.2011.11.003 · Cited by 41 · see citing works
Effect of Cold Stress on Neurobehavioral and Physiological Parameters in Rats
Elmarzouki, H., Aboussaleh, Y., Najimi, M., Chigr, F., & Ahami, A. O. T. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.660124 · Cited by 38 · see citing works
Sex-based differences in gene expression in hippocampus following postnatal lead exposure
Schneider, J. S., Anderson, D. W., Sonnenahalli, H., & Vadigepalli, R. (2011) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2011.08.008 · Cited by 38 · see citing works
Hudson, S. P., Jacobson‐Pick, S., & Anisman, H. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.007 · Cited by 35 · see citing works
Immune status influences fear and anxiety responses in mice after acute stress exposure
Clark, S. M., Sand, J., Francis, T. C., Nagaraju, A., Michael, K. C., Keegan, A. D., Kusnecov, A. W., Gould, T. D., & Tonelli, L. H. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.02.001 · Cited by 33 · see citing works
Saland, S. K., Duclot, F., & Kabbaj, M. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.11.002 · Cited by 33 · see citing works
The sex-dependent response to psychosocial stress and ischaemic heart disease
Helman, T. J., Headrick, J. P., Stapelberg, N. J. C., & Braidy, N. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1072042 · Cited by 34 · see citing works
Boxelaere, M. V., Clements, J., Callaerts, P., D’Hooge, R., & Callaerts‐Vegh, Z. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188537 · Cited by 31 · see citing works
Wellman, C. L., & Moench, K. M. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5023-4 · Cited by 31 · see citing works
Sierksma, A. S. R., Vanmierlo, T., Vry, J. D., Raijmakers, M., Steinbusch, H. W. M., van den Hove, D., & Prickaerts, J. (2012) · Neurochemistry International · doi:10.1016/j.neuint.2012.06.022 · Cited by 29 · see citing works
Gouweleeuw, L., Hovens, I. B., Liu, H., Naudé, P. J. W., & Schoemaker, R. G. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.04.040 · Cited by 29 · see citing works
Reconceptualizing sex, brain and psychopathology: interaction, interaction, interaction
Joel, D., & Yankelevitch-Yahav, R. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12732 · Cited by 28 · see citing works
Gestational stress influences cognition and behavior
Sandman, C. A., & Davis, E. P. (2010) · Future Neurology · doi:10.2217/fnl.10.35 · Cited by 27 · see citing works
Homiack, D., O’Cinneide, E. M., Hajmurad, S., Barrileaux, B., Stanley, M., Kreutz, M. R., & Schrader, L. A. (2017) · Hippocampus · doi:10.1002/hipo.22749 · Cited by 26 · see citing works
Hansson, A. C., Rimondini, R., Heilig, M. A., Mathé, A. A., & Sommer, W. H. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881110393049 · Cited by 28 · see citing works
Uridine treatment prevents REM sleep deprivation-induced learning and memory impairment
Öcalan, B., Çakır, A., Koç, C., Süyen, G. G., & Kahveci, N. (2019) · Neuroscience Research · doi:10.1016/j.neures.2019.01.003 · Cited by 26 · see citing works
Infrared Thermography Reveals Sex-Specific Responses to Stress in Mice
Faraji, J., & Metz, G. A. S. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00079 · Cited by 25 · see citing works
Developmental changes in hippocampal shape among preadolescent children
Lin, M., Fwu, P. T., Buß, C., Davis, E. P., Head, K., Muftuler, L. T., Sandman, C. A., & Su, M. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.06.001 · Cited by 24 · see citing works
Sex differences in the delayed impact of acute stress on the amygdala
Gupta, K., & Chattarji, S. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100292 · Cited by 25 · see citing works
Rosinger, Z. J., Guzman, R. M. D., Jacobskind, J. S., Saglimbeni, B., Malone, M., Fico, D., Justice, N. J., Forni, P. E., & Zuloaga, D. G. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112847 · Cited by 24 · see citing works
Hippocampal signaling pathways are involved in stress-induced impairment of memory formation in rats
Sardari, M., Rezayof, A., & Khodagholi, F. (2015) · Brain Research · doi:10.1016/j.brainres.2015.08.015 · Cited by 24 · see citing works
Zhang, C., Liu, B., Pawluski, J. L., Steinbusch, H. W. M., Kunikullaya, K. U., & Song, C. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114220 · Cited by 22 · see citing works
Balkaya, M., Seidel, J. L., Sadeghian, H., Qin, T., Chung, D. Y., Eikermann‐Haerter, K., van den Maagdenberg, A. M. J. M., Ferrari, M. D., & Ayata, C. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.006 · Cited by 21 · see citing works
Yaskin, V. A. (2013) · Russian Journal of Ecology · doi:10.1134/s1067413613030156 · Cited by 19 · see citing works
Mirjalili, R., Shokouh, E., Dehkordi, N. S., Afsari, R., Shafia, S., & Rashidy‐Pour, A. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.113864 · Cited by 20 · see citing works
Salama, O., Attia, M. M., & Abdel-Razek, M. A. S. (2019) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2019.01.014 · Cited by 18 · see citing works
Curtis, G. R., Gargiulo, A. T., Carpenter, B. A., Pirino, B. E., Hawks, A., Coleman, S. A., Syed, N., Gupta, A., & Barson, J. R. (2022) · Addiction Neuroscience · doi:10.1016/j.addicn.2022.100058 · Cited by 16 · see citing works
Poggini, S., Bon, G. M., Golia, M. T., Albanese, N. C., Viglione, A., Poleggi, A., Limatola, C., Maggi, L., & Branchi, I. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113256 · Cited by 16 · see citing works
Sexual dimorphism in pre-clinical studies of depression
Alshammari, T. K. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110120 · Cited by 14 · see citing works
Derks, N. M., Gaszner, B., Bernhardt, K., Roubos, E. W., & Kozicz, T. (2009) · Peptides · doi:10.1016/j.peptides.2009.09.009 · Cited by 14 · see citing works
Saad, N., Raviv, D., Zer‐Aviv, T. M., & Akirav, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015492 · Cited by 13 · see citing works
Zhong, Q., Lai, S., He, J., Zhong, S., Song, X., Wang, Y., Zhang, Y., Chen, G., Yan, S., & Jia, Y. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.05.039 · Cited by 12 · see citing works
Brain‐Derived Neurotrophic Factor ( BDNF ) and Sex Differences in Metabolic Regulation
Zanesco, A. M., & Velloso, L. A. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70245 · Cited by 9 · see citing works
Shamabadi, A., Karimi, H., Fallahzadeh, M. A., Vaseghi, S., Bahri, R. A., Fallahpour, B., Abdolghaffari, A. H., & Akhondzadeh, S. (2024) · International Clinical Psychopharmacology · doi:10.1097/yic.0000000000000550 · Cited by 8 · see citing works
Homiack, D., O’Cinneide, E. M., Hajmurad, S., Dohanich, G. P., & Schrader, L. A. (2018) · Stress · doi:10.1080/10253890.2018.1484099 · Cited by 8 · see citing works
Neves, L. D. S., de Mattos, G. V. R. M., Oliveira-Nazareth, Y., da Silva, R. S., & Campello-Costa, P. (2025) · Translational Psychiatry · doi:10.1038/s41398-025-03668-x · Cited by 9 · see citing works
Wei, F., Zhang, L., Ma, B., Li, W., Deng, X. Y., Zheng, T., Wang, X., & Jing, Y. (2021) · Peptides · doi:10.1016/j.peptides.2021.170659 · Cited by 6 · see citing works
Parekh, S. V., Adams, L. O., Barkell, G. A., & Lysle, D. T. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06310-0 · Cited by 6 · see citing works
Seo, M., Pyeon, S. Y., & Kim, M. S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26157611 · Cited by 5 · see citing works
Mujinya, R., Kalange, M., Ochieng, J. J., Ninsiima, H. I., Eze, E. D., Afodun, A. M., Nabirumbi, R., Sulaiman, S. O., Kairania, E., Echoru, I., et al. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.551508 · Cited by 4 · see citing works
Mazza, M., Lisci, F. M., Brisi, C., Traversi, G., Gaetani, E., Pola, R., & Marano, G. (2024) · Future Pharmacology · doi:10.3390/futurepharmacol4030030 · Cited by 4 · see citing works
Neuroprotective roles of neurotrophic growth factors in mood disorders
Jiang, C., & Salton, S. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814037-6.00010-0 · Cited by 5 · see citing works
Chronic Stress Effects on Corticolimbic Morphology
Wellman, C. L. (2011) · doi:10.1002/9781118083222.ch10 · Cited by 4 · see citing works
Gauthier, M., Hebert, L.-P., Dugast, E., Lardeux, V., Letort, K., Thiriet, N., Belnoue, L., Balado, É., Solinas, M., & Belujon, P. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111335 · Cited by 3 · see citing works
Aykaç, A., Öncül, Ş., & Onur, R. (2018) · Marmara Pharmaceutical Journal · doi:10.12991/mpj.2018.56 · Cited by 2 · see citing works
“Epidemiological studies indicate that women are more susceptible to stress-induced psychopathologies than men and depression occur twice as frequently in women [19-21].”
BackgroundEscribano-Cadena, Y., Tendilla‐Beltrán, H., & Flores, G. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.07.041 · Cited by 2 · see citing works
Khlebnikova, N. N., Krupina, N. A., Kushnareva, E. Y., & Орлова, И. Н. (2015) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-015-2956-z · Cited by 2 · see citing works
Chronic Stress and Sex Differences on Cognition
Luine, V. N. (2011) · doi:10.1002/9781118083222.ch26 · Cited by 1 · see citing works
Simpson, J. (2011) · ARAN (University of Galway Research Repository) (Ollscoil na Gaillimhe – University of Galway) · doi:10.13025/17838 · Cited by 1 · see citing works
The effects of early diet on cognition and the brain
Isaacs, E., & Lucas, A. (2011) · Elsevier eBooks · doi:10.1533/9780857092922.1.3
Les enképhalines et dynorphines dans la résilience au stress chronique
Bérubé, P. (2013) · Corpus Université Laval (Université Laval)
Zhang, C., Liu, B., Pawluski, J. L., Steinbusch, H. W. M., Kunikullaya, K. U., & Song, C. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4145422
Sex differences in social synchronization of conditioned fearPreprint
Ito, W., & Morozov, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.10.10.511569
Zhang, C. (2023) · doi:10.26481/dis.20230705cz
McEwen, B. S., & Chattarji, S. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0017
Social stress, cortisol awakening response and sex: association with hippocampus and amygdala volume
Wang, R., Noack, H., Kuhn, L., Nieratschker, V., Habel, U., Derntl, B., & Kogler, L. (2025) · Biology of Sex Differences · doi:10.1186/s13293-025-00801-9
Bahí, A., & Dreyer, J. (2026) · Psychopharmacology · doi:10.1007/s00213-026-07091-y
- Authors
- Lin, Y., Ter Horst, G. J., Wichmann, R., Bakker, P., Liu, A., Li, X., & Westenbroek, C.
- Affiliations
- University Medical Center Groningen (NL)
- Peking University (CN)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-12-10
- Volume
- 19
- Issue
- 9
- Pages
- 1978-1989
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC2722422
- OpenAlex
- W2145152438
- Cited by
- 100
- References
- 86
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 3 · 2023: 6 · 2022: 8 · 2021: 4 · 2020: 7 · 2019: 7 · 2018: 6 · 2017: 2 · 2016: 6 · 2015: 2 · 2014: 6 · 2013: 7 · 2012: 10
- FWCI
- 2.71
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Cerebral Cortex (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- Rijksuniversiteit Groningen
- Universitair Medisch Centrum Groningen
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- sex differences, chronic stress, acute stress, stress recovery, depression, CREB, CREB phosphorylation, brain-derived neurotrophic factor, hippocampus, paraventricular thalamus, amygdala, anterior cingulate cortex, prefrontal cortex, dentate gyrus, prelimbic cortex, sexual dimorphism, antidepressant targets
- MeSH terms
- Acute Disease, Animals, Brain, Female, Male, Neuronal Plasticity, Sex Factors, Stress, Psychological, Tissue Distribution, Rats, Wistar, Cyclic AMP Response Element-Binding Protein, Brain-Derived Neurotrophic Factor, Recovery of Function, CREB-Binding Protein, Rats
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