Effects of early-life stress on cognitive function and hippocampal structure in female rodents.
Open accessAbstract
We tested the effect of early-life stress (ELS) - 24h maternal deprivation (MD) at postnatal day (PND) 3 - on cognitive performance and hippocampal structure in 12-17-week-old female rats. Behavioral performance was examined in: the Elevated Plus Maze, as an index for general anxiety; the rodent Iowa gambling test, probing reward-based decision making; and the object recognition and object-in-location task, to assess non-stressful contextual memory performance. We further determined hippocampal dentate gyrus (DG) volume and cell density as well as adult proliferation and neurogenesis rates. Half of the rats was treated with the glucocorticoid receptor antagonist mifepristone during a critical pre-pubertal developmental window (PNDs 26-28), in an attempt to ameliorate the potentially adverse behavioral consequences of ELS. Neither MD nor treatment with the glucocorticoid antagonist affected behavioral performance of the females in any of the tasks. Also, DG structure, proliferation and neurogenesis were not different between the groups. Lack of structural differences and a behavioral phenotype in non-stressful hippocampus dependent learning tasks fits with the lack of phenotype generally reported after ELS in female but less so in male rodents. As evident from an extensive literature review, female and male animals appear to respond more similarly to early-life adversity when tested in anxiety-related tasks. This agrees with recent findings in humans suggesting that females may be relatively resilient to the structural/hippocampal effects of childhood maltreatment, but not to the anxiety and mood-related psychopathology for which childhood maltreatment is considered a risk factor.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Males are more affected than females in a broad range of behavioral domains following early postnatal manipulations of maternal care in rodents.
“Focusing on early postnatal manipulations of maternal care in rodents as a model for ELS, it seems that males are more affected than females in a broad range of behavioral domains (Loi et al., 2017; Schroeder et al., 2018).”
From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Loi et al., 2017
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
The global prevalence of common mental disorders: a systematic review and meta-analysis 1980–2013
Steel, Z., Marnane, C., Iranpour, C., Chey, T., Jackson, J. W., Patel, V., & Silove, D. (2014) · International Journal of Epidemiology · doi:10.1093/ije/dyu038 · Cited by 2,846 · see citing works
Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys
Kessler, R. C., McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., Aguilar-Gaxiola, S., Alhamzawi, A. O., Alonso, J., Angermeyer, M., et al. (2010) · British Journal of Psychiatry · doi:10.1192/bjp.bp.110.080499 · Cited by 2,640 · see citing works
A Genome-Wide Association Search for Type 2 Diabetes Genes in African Americans
Palmer, N. D., McDonough, C. W., Hicks, P. J., Roh, B. H., Wing, M. R., An, S. S., Hester, J. M., Bailey, J. N. C., Bostrom, M. A., Rudock, M. E., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029202 · Cited by 1,805 · see citing works
A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., et al. (2009) · Science · doi:10.1126/science.1173215 · Cited by 1,642 · see citing works
Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011) · Nature · doi:10.1038/nature09817 · Cited by 1,567 · see citing works
Bevins, R. A., & Besheer, J. (2006) · Nature Protocols · doi:10.1038/nprot.2006.205 · Cited by 1,278 · see citing works
Anxiety, defence and the elevated plus-maze.
Rodgers, R., & Dalvi, A. (1997) · Neuroscience and Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00058-9 · Cited by 1,028 · see citing works
Saxe, M. D., Battaglia, F., Wang, J.-W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D. R., Sofroniew, M. V., Kandel, E. R., Santarelli, L., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607207103 · Cited by 1,020 · see citing works
Do rats have a prefrontal cortex?
Uylings, H. B. M., Groenewegen, H. J., & Kolb, B. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.028 · Cited by 1,013 · see citing works
Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy
Mueller, B. R., & Bale, T. L. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1424-08.2008 · Cited by 988 · see citing works
When Is the Hippocampus Involved in Recognition Memory?
Barker, G. R. I., & Warburton, E. C. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6413-10.2011 · Cited by 818 · see citing works
Differential Control of Learning and Anxiety along the Dorsoventral Axis of the Dentate Gyrus
Kheirbek, M. A., Drew, L. J., Burghardt, N. S., Costantini, D. O., Tannenholz, L., Ahmari, S. E., Zeng, H., Fenton, A. A., & Hen, R. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.038 · Cited by 713 · see citing works
One-trial object recognition in rats and mice: Methodological and theoretical issues
Ennaceur, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.036 · Cited by 676 · see citing works
Aimone, J. B., Deng, W., & Gage, F. H. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.010 · Cited by 663 · see citing works
Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health
Meaney, M. J., Moshe Szyf, A., & Seckl, J. R. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.05.003 · Cited by 660 · see citing works
Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings
Leppänen, J. M. (2006) · Current Opinion in Psychiatry · doi:10.1097/01.yco.0000191500.46411.00 · Cited by 632 · see citing works
Running enhances spatial pattern separation in mice
Creer, D. J., Romberg, C., Saksida, L. M., van Praag, H., & Bussey, T. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911725107 · Cited by 553 · see citing works
A role for adult TLX-positive neural stem cells in learning and behaviour
Zhang, C., Zou, Y., He, W., Gage, F. H., & Evans, R. M. (2008) · Nature · doi:10.1038/nature06562 · Cited by 523 · see citing works
Pattern separation: a common function for new neurons in hippocampus and olfactory bulb
Sahay, A., Wilson, D. A., & Hen, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.012 · Cited by 514 · see citing works
Adult Neurogenesis Modulates the Hippocampus-Dependent Period of Associative Fear Memory
北村, 貴., Saitoh, Y., Takashima, N., Murayama, A., Niibori, Y., Ageta, H., Sekiguchi, M., Sugiyama, H., & Inokuchi, K. (2009) · Cell · doi:10.1016/j.cell.2009.10.020 · Cited by 489 · see citing works
Kalinichev, M., Easterling, K. W., Plotsky, P. M., & Holtzman, S. G. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00781-5 · Cited by 484 · see citing works
Lucassen, P. J., Meerlo, P., Naylor, A. S., van Dam, A. M., Dayer, A. G., Fuchs, E., Oomen, C. A., & Czéh, B. (2010) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.08.003 · Cited by 449 · see citing works
Self-citationWigger, A., & Neumann, I. D. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00300-x · Cited by 443 · see citing works
Proof of Concept Trial of Dronabinol in Obstructive Sleep Apnea
Prasad, B., Radulovacki, M. G., & Carley, D. W. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00001 · Cited by 424 · see citing works
Pryce, C. R., Rüedi‐Bettschen, D., Dettling, A. C., Weston, A. A., Russig, H. D., Ferger, B., & Feldon, J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.011 · Cited by 414 · see citing works
Reynolds, K., Pietrzak, R. H., El-Gabalawy, R. M., Mackenzie, C. S., & Sareen, J. (2015) · World Psychiatry · doi:10.1002/wps.20193 · Cited by 411 · see citing works
Oomen, C. A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F. N., Manders, E. M. M., Joëls, M., Lucassen, P. J., & Krugers, H. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0247-10.2010 · Cited by 352 · see citing works
Self-citationMetabolic rate in the right amygdala predicts negative affect in depressed patients
Abercrombie, H., Schaefer, S., Larson, C., Oakes, T., Lindgren, K. A., Holden, J., Perlman, S. B., Turski, P., Krahn, D., Benca, R., et al. (1998) · NeuroReport · doi:10.1097/00001756-199810050-00028 · Cited by 345 · see citing works
Heine, V. M., Maslam, S., Joëls, M., & Lucassen, P. J. (2004) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00090-3 · Cited by 318 · see citing works
Self-citationChronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats
Brummelte, S., & Galea, L. A. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.023 · Cited by 309 · see citing works
Neural circuitry for rat recognition memory
Warburton, E. C., & Brown, M. W. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.050 · Cited by 307 · see citing works
Pawluski, J. L., Brummelte, S., Barha, C. K., Crozier, T. M., & Galea, L. A. M. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.007 · Cited by 306 · see citing works
Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala
Vyas, A., Jadhav, S., & Chattarji, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.003 · Cited by 299 · see citing works
Romeo, R. D., Mueller, A., Sisti, H. M., Ogawa, S., McEwen, B. S., & Brake, W. G. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00063-1 · Cited by 285 · see citing works
Naninck, E. F. G., Hoeijmakers, L., Kakava-Georgiadou, N., Meesters, A., Lazic, S. E., Lucassen, P. J., & Kőrösi, A. (2014) · Hippocampus · doi:10.1002/hipo.22374 · Cited by 281 · see citing works
Self-citationVeenema, A. H., Bredewold, R., & Neumann, I. D. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.008 · Cited by 263 · see citing works
The Maternal Separation Paradigm and Adult Emotionality and Cognition in Male and Female Wistar Rats
Lehmann, J., Pryce, C. R., Bettschen, D., & Feldon, J. (1999) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00150-1 · Cited by 260 · see citing works
McIntosh, J. F., Anisman, H., & Merali, Z. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00005-x · Cited by 255 · see citing works
Szuran, T. F., Pliška, V., Pokorny, J., & Welzl, H. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00351-6 · Cited by 253 · see citing works
Macrı̀, S., Mason, G. J., & Würbel, H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03541.x · Cited by 237 · see citing works
Oomen, C. A., Mayer, J. L., de Kloet, E. R., Joëls, M., & Lucassen, P. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05972.x · Cited by 231 · see citing works
Self-citationLehmann, J., Stöhr, T., & Feldon, J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00122-9 · Cited by 217 · see citing works
Bowman, R. E., MacLusky, N. J., Sarmiento, Y., Frankfurt, M., Gordon, M., & Luine, V. N. (2004) · Endocrinology · doi:10.1210/en.2003-1759 · Cited by 216 · see citing works
Natural variation and genetic covariance in adult hippocampal neurogenesis
Kempermann, G., Chesler, E. J., Lu, L., Williams, R. W., & Gage, F. H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510291103 · Cited by 205 · see citing works
Ennaceur, A., Michalíková, S., Bradford, A., & Ahmed, S. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.11.006 · Cited by 195 · see citing works
Opposite effects of early maternal deprivation on neurogenesis in male versus female rats
Oomen, C. A., Girardi, C. E. N., Cahyadi, R., Verbeek, E. C., Krugers, H., Joëls, M., & Lucassen, P. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0003675 · Cited by 190 · see citing works
Self-citationMayer, J. L., Klumpers, L. E., Maslam, S., de Kloet, E. R., Joëls, M., & Lucassen, P. J. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01455.x · Cited by 181 · see citing works
Self-citationSlotten, H. A., Kalinichev, M., Hagan, J. J., Marsden, C. A., & Fone, K. C. F. (2006) · Brain Research · doi:10.1016/j.brainres.2006.04.066 · Cited by 179 · see citing works
Maternal deprivation increases cell death in the infant rat brain
Li, Z., Levine, S. D., Dent, G. W., Zhan, Y., Xing, G., Okimoto, D. K., Gordon, M. K., Post, R. M., & Smith, M. A. (2002) · Developmental Brain Research · doi:10.1016/s0926-6410(01)00118-5 · Cited by 174 · see citing works
Lucassen, P. J., Naninck, E. F. G., van Goudoever, J. B., Fitzsimons, C. P., Joëls, M., & Kőrösi, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.08.002 · Cited by 173 · see citing works
Self-citationKundaković, M., Lim, S. C., Gudsnuk, K. M., & Champagne, F. A. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00078 · Cited by 172 · see citing works
Early life stress impairs fear conditioning in adult male and female rats
Kosten, T. A., Lee, H. J., & Kim, J. J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.009 · Cited by 170 · see citing works
A Facilitative Role for Corticosterone in the Acquisition of a Spatial Task Under Moderate StressPreprint
Akirav, I., Kozenicky, M., Tal, D., Sandi, C., Venero, C., & Richter‐Levin, G. (2004) · Learning & Memory · doi:10.1101/lm.61704 · Cited by 170 · see citing works
Barha, C. K., Brummelte, S., Lieblich, S. E., & Galea, L. A. M. (2010) · Hippocampus · doi:10.1002/hipo.20829 · Cited by 164 · see citing works
Complete maternal deprivation affects social, but not spatial, learning in adult rats
Lévy, F., Melo, Á. I., Galef, B. G., Madden, M., & Fleming, A. S. (2003) · Developmental Psychobiology · doi:10.1002/dev.10131 · Cited by 161 · see citing works
Early Postnatal Stress Confers Enduring Vulnerability to Limbic Epileptogenesis
Salzberg, M. R., Kumar, G., Supit, L., Jones, N. C., Morris, M. J., Rees, S. M., & O'Brien, T. J. (2007) · Epilepsia · doi:10.1111/j.1528-1167.2007.01246.x · Cited by 143 · see citing works
Oomen, C. A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F. N., Manders, E. M. M., Joëls, M., Krugers, H. J., & Lucassen, P. J. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1922-8 · Cited by 133 · see citing works
Self-citationTsoory, M., & Richter‐Levin, G. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705006255 · Cited by 132 · see citing works
The maternal deprivation animal model revisited.
Marco, E. M., Llorente, R., López-Gallardo, M., Mela, V., Llorente-Berzal, Á., Prada, C., & Viveros, M.-P. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.015 · Cited by 132 · see citing works
Samplin, E., Ikuta, T., Malhotra, A. K., Szeszko, P. R., & DeRosse, P. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.05.008 · Cited by 128 · see citing works
Holland, F. H., Ganguly, P., Potter, D. N., Chartoff, E. H., & Brenhouse, H. C. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.02.023 · Cited by 125 · see citing works
Marco, E. M., Valero, M., de la Serna, O., Aisa, B., Borcel, É., Ramírez, M. J., & Viveros, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.014 · Cited by 120 · see citing works
Object recognition testing: Statistical considerations
Akkerman, S., Prickaerts, J., Steinbusch, H. W. M., & Blokland, A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.03.024 · Cited by 114 · see citing works
Nishio, H., Kasuga, S., Ushijima, M., & Harada, Y. (2001) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(00)00070-8 · Cited by 113 · see citing works
Korevaar, D. A., Hooft, L., & ter Riet, G. (2011) · Laboratory Animals · doi:10.1258/la.2011.010121 · Cited by 110 · see citing works
Zamberletti, E., Prini, P., Speziali, S., Gabaglio, M., Solinas, M., Parolaro, D., & Rubino, T. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.038 · Cited by 107 · see citing works
Muhammad, A., & Kolb, B. E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.015 · Cited by 105 · see citing works
Llorente, R., Miguel-Blanco, C., Aisa, B., Lachize, S., Borcel, É., Meijer, O. C., Ramírez, M. J., de Kloet, E. R., & Viveros, M. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02109.x · Cited by 101 · see citing works
Llorente, R., López‐Gallardo, M., Llorente‐Berzal, A., Prada, C., García‐Segura, L. M., & Viveros, M. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.01.002 · Cited by 101 · see citing works
Marmendal, M., Roman, E., Eriksson, C. J. P., Nylander, I., & Fahlke, C. (2004) · Developmental Psychobiology · doi:10.1002/dev.20027 · Cited by 95 · see citing works
Adult hippocampal neurogenesis and its role in cognition.
Oomen, C. A., Bekinschtein, P., Kent, B. A., Saksida, L. M., & Bussey, T. J. (2014) · WIREs Cognitive Science · doi:10.1002/wcs.1304 · Cited by 93 · see citing works
Maternal care affects male and female offspring working memory and stress reactivity
Barha, C. K., Pawluski, J. L., & Galea, L. A. M. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.06.022 · Cited by 91 · see citing works
Llorente, R., Arranz, L., Marco, E. M., Moreno, E., Puerto, M., Guaza, C., la Fuente, M. D., & Viveros, M. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.002 · Cited by 90 · see citing works
van den Bos, R., Jolles, J. W., van der Knaap, L. J., Baars, A. M., & de Visser, L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.07.015 · Cited by 90 · see citing works
Llorente‐Berzal, A., Fuentes, S., Gagliano, H., López‐Gallardo, M., Armario, A., Viveros, M., & Nadal, R. A. (2011) · Addiction Biology · doi:10.1111/j.1369-1600.2011.00318.x · Cited by 88 · see citing works
Tsuda, M. C., & Ogawa, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033028 · Cited by 86 · see citing works
Strain-specific cognitive deficits in adult mice exposed to early life stress.
Mehta, M., & Schmauss, C. (2011) · Behavioral Neuroscience · doi:10.1037/a0021952 · Cited by 84 · see citing works
Diehl, L. A., Silveira, P. P., Leite, M. C., Crema, L. M., Portella, A. K., Billodre, M. N., Nunes, E., Henriques, T. P., Fidelix-da-Silva, L. B., Heis, M. D., et al. (2007) · Brain Research · doi:10.1016/j.brainres.2007.01.084 · Cited by 83 · see citing works
Barna, I., Bálint, E., Baranyi, J., Bakos, N., Makara, G. B., & Haller, J. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(03)00216-8 · Cited by 76 · see citing works
Neonatal handling alters learning in adult male and female rats in a task-specific manner
Kosten, T. A., Lee, H. J., & Kim, J. J. (2007) · Brain Research · doi:10.1016/j.brainres.2007.03.081 · Cited by 75 · see citing works
Infant maternal separation impairs adult cognitive performance in BALB/cJ mice
Wang, L., Jiao, J., & Dulawa, S. C. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2209-4 · Cited by 73 · see citing works
Machado, T. D., Molle, R. D., Laureano, D. P., Portella, A. K., Werlang, I. C. R., Benetti, C. D. S., Noschang, C. G., & Silveira, P. P. (2013) · Stress · doi:10.3109/10253890.2013.816841 · Cited by 72 · see citing works
Rees, S. L., Steiner, M. S., & Fleming, A. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.013 · Cited by 71 · see citing works
James, M. H., Campbell, E. J., Walker, F. R., Smith, D. W., Richardson, H. N., Hodgson, D. M., & Dayas, C. V. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00244 · Cited by 70 · see citing works
Neto, J. B. B., Tiba, P. A., Faturi, C. D. B., de Castro-Neto, E. F., Naffah‐Mazzacoratti, M. D. G., Mari, J. D. J., Mello, M. F., & Suchecki, D. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.09.011 · Cited by 65 · see citing works
Klomp, A., Václavů, L., Meerhoff, G. F., Reneman, L., & Lucassen, P. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097603 · Cited by 65 · see citing works
Self-citationPark, H., Chae, Y., Jang, J., Shim, I., Lee, H., & Lim, S. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2004.11.097 · Cited by 64 · see citing works
Chocyk, A., Przyborowska, A., Makuch, W., Majcher‐Maślanka, I., Dudys, D., & Wędzony, K. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.040 · Cited by 63 · see citing works
de Visser, L. (2011) · Frontiers in Neuroscience · doi:10.3389/fnins.2011.00102 · Cited by 63 · see citing works
Prusator, D. K., & Meerveld, B. G. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12472 · Cited by 62 · see citing works
Effects of early weaning on anxiety and autonomic responses to stress in rats
Ito, A., Kikusui, T., Takeuchi, Y., & Mori, Y. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.03.023 · Cited by 62 · see citing works
Eklund, M. B., & Arborelius, L. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.015 · Cited by 61 · see citing works
A rodent version of the Iowa Gambling Task: 7 years of progress
van den Bos, R., Koot, S., & de Visser, L. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00203 · Cited by 59 · see citing works
Hu, P., Oomen, C. A., van Dam, A., Wester, J., Zhou, J., Joëls, M., & Lucassen, P. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046224 · Cited by 58 · see citing works
Self-citationSex differences in rats: Effects of chronic stress on sympathetic system and anxiety
Renard, G. M., Suárez, M. M., Levin, G. M., & Rivarola, M. A. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.05.003 · Cited by 56 · see citing works
Rodríguez, D. A. L., & Dueñas, Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068010 · Cited by 56 · see citing works
Maternal deprivation induces depressive-like behaviours only in female rats
Mourlon, V., Baudin, A., Blanc, O., Lauber, A. H., Giros, B., Naudon, L., & Daugé, V. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.017 · Cited by 56 · see citing works
Effects of early life trauma are dependent on genetic predisposition: a rat study
Sterley, T.-L., Howells, F. M., & Russell, V. A. (2011) · Behavioral and Brain Functions · doi:10.1186/1744-9081-7-11 · Cited by 52 · see citing works
Spivey, J. M., Shumake, J., Colorado, R. A., Conejo, N. M., González‐Pardo, H., & Gonzalez-Lima, F. (2009) · Developmental Psychobiology · doi:10.1002/dev.20362 · Cited by 50 · see citing works
van Hasselt, F. N., de Visser, L., Tieskens, J. M., Cornelisse, S., Baars, A. M., Lavrijsen, M., Krugers, H. J., van den Bos, R., & Joëls, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037820 · Cited by 49 · see citing works
Self-citationFreund, N., Thompson, B. S., DeNormandie, J., Vaccarro, K., & Andersen, S. L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.066 · Cited by 47 · see citing works
Grissom, E. M., Hawley, W. R., Bromley-Dulfano, S. S., Marino, S. E., Stathopoulos, N. G., & Dohanich, G. P. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.06.001 · Cited by 44 · see citing works
Zimmerberg, B., & Kajunski, E. W. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.03.021 · Cited by 43 · see citing works
Effects of early rearing conditions on cognitive performance in prepubescent male and female rats
Frankola, K. A., Flora, A. L., Torres, A. K., Grissom, E. M., Overstreet, S., & Dohanich, G. P. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.04.005 · Cited by 43 · see citing works
Maternal separation modulates short-term behavioral and physiological indices of the stress response
Litvin, Y., Tovote, P., Pentkowski, N. S., Zeyda, T., King, L. B., Vasconcellos, A., Dunlap, C., Spiess, J., Blanchard, D. C., & Blanchard, R. J. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.010 · Cited by 43 · see citing works
Xiong, G.-J., Yang, Y., Wang, L.-P., Xu, L., & Mao, R.-R. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.015 · Cited by 43 · see citing works
Takase, K., Yamamoto, Y., & Yagami, T. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.016 · Cited by 40 · see citing works
Contextual Fear Conditioning in Maternal Separated Rats: The Amygdala as a Site for Alterations
Diehl, L. A., Pereira, N. D. S. C., Laureano, D. P., Benitz, A. N. D., Noschang, C. G., Ferreira, A. G. K., Scherer, E. B. D. S., Machado, F. R., Henriques, T. P., Wyse, Â. T. D. S., et al. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1230-x · Cited by 38 · see citing works
Stiller, A., Drugan, R. C., Hazi, A., & Kent, S. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.012 · Cited by 38 · see citing works
Postnatal handling reverses social anxiety in serotonin receptor 1A knockout mice
Zanettini, C., Carola, V., Iacono, L. L., Moles, A., Gross, C. T., & D'Amato, F. R. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00531.x · Cited by 33 · see citing works
Sun, X.-M., Tu, W.-Q., Shi, Y., Li, X., & Zhao, H. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.03.022 · Cited by 31 · see citing works
Mother–infant separation leads to hypoactive behavior in adolescent Holtzman rats
Spivey, J. M., Barrett, D. W., Padilla‐Tolentino, E., & Gonzalez-Lima, F. (2008) · Behavioural Processes · doi:10.1016/j.beproc.2008.05.002 · Cited by 29 · see citing works
Maternal deprivation and dendritic complexity in the basolateral amygdala
Krugers, H. J., Oomen, C. A., Gumbs, M. C. R., Li, M., Velzing, E. H., Joëls, M., & Lucassen, P. J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.09.022 · Cited by 29 · see citing works
Self-citationKao, G.-S., Cheng, L.-Y., Chen, L.-H., Tzeng, W.-Y., Cherng, C. G., Su, C.-C., Wang, C.-Y., & Yu, L. (2012) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2012.09.040 · Cited by 28 · see citing works
Veenema, A. H., de Kloet, E. R., de Wilde, M. C., Roelofs, A. J., Kawata, M., Buwalda, B., Neumann, I., Koolhaas, J. M., & Lucassen, P. J. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01555.x · Cited by 26 · see citing works
Self-citationZhang, J., Abdallah, C. G., Chen, Y., Huang, T., Huang, Q., Chong-tao, X., Xiao, Y., Liu, Y., Ding, Y., & Wu, R. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.04.035 · Cited by 24 · see citing works
Koehnle, T. J., & Rinaman, L. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.02.006 · Cited by 19 · see citing works
Juvenile male rats display lower cortical metabolic capacity than females
Spivey, J. M., Colorado, R. A., Conejo, N. M., González‐Pardo, H., & Gonzalez-Lima, F. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.05.104 · Cited by 10 · see citing works
The effect of childhood trauma on spatial cognition in adults: a possible role of sex
Syal, S., Ipser, J., Phillips, N. J., Thomas, K. G. F., van Honk, J., & Stein, D. J. (2014) · Metabolic Brain Disease · doi:10.1007/s11011-014-9497-4 · Cited by 10 · see citing works
A cross-cultural comparison study of depression assessments conducted in Japan
Targum, S. D., Nakagawa, A., & Sato, Y. (2013) · Annals of General Psychiatry · doi:10.1186/1744-859x-12-9 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 562 · see citing works
Walker, C., Bath, K. G., Joëls, M., Kőrösi, A., Larauche, M. H., Lucassen, P. J., Morris, M. J., Raineki, C., Roth, T. L., Sullivan, R. M., et al. (2017) · Stress · doi:10.1080/10253890.2017.1343296 · Cited by 402 · see citing works
Self-citationSex differences in hippocampal cognition and neurogenesis
Yagi, S., & Galea, L. A. M. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0208-4 · Cited by 340 · see citing works
Let’s call the whole thing off: evaluating gender and sex differences in executive function
Grissom, N. M., & Reyes, T. M. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-018-0179-5 · Cited by 306 · see citing works
Stress, hypothalamic–pituitary–adrenal axis, hypothalamic–pituitary–gonadal axis, and aggression.
Mbiydzenyuy, N. E., & Qulu, L.-A. (2024) · Metabolic Brain Disease · doi:10.1007/s11011-024-01393-w · Cited by 255 · see citing works
Goodwill, H. L., Manzano-Nieves, G., Gallo, M. E., Lee, H.-I., Oyerinde, E., Serre, T., & Bath, K. G. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0195-5 · Cited by 233 · see citing works
Early life stress perturbs the maturation of microglia in the developing hippocampus
Delpech, J.-C., Wei, L., Hao, J., Yu, X., Madore, C., Butovsky, O., & Kaffman, A. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.06.006 · Cited by 193 · see citing works
The stressed brain of humans and rodents
Joëls, M., Karst, H., & Sarabdjitsingh, R. A. (2018) · Acta Physiologica · doi:10.1111/apha.13066 · Cited by 189 · see citing works
Self-citationEarly-life adversity and neurological disease: age-old questions and novel answers
Short, A. K., & Baram, T. Z. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0246-5 · Cited by 180 · see citing works
Wang, D., Levine, J. L. S., Avila-Quintero, V. J., Bloch, M. H., & Kaffman, A. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0856-0 · Cited by 142 · see citing works
Early life adversity: Lasting consequences for emotional learning
Krugers, H. J., Arp, J. M., Xiong, H., Kanatsou, S., Lesuis, S. L., Kőrösi, A., Joëls, M., & Lucassen, P. J. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.11.005 · Cited by 132 · see citing works
Self-citationJohnson, F. K., & Kaffman, A. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.06.008 · Cited by 124 · see citing works
Synthesizing Views to Understand Sex Differences in Response to Early Life Adversity
Bath, K. G. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.02.004 · Cited by 124 · see citing works
Amygdala hyper-connectivity in a mouse model of unpredictable early life stress
Johnson, F. K., Delpech, J.-C., Thompson, G. J., Wei, L., Jin, H., Hermán, P., Hyder, F., & Kaffman, A. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0092-z · Cited by 115 · see citing works
Guadagno, A., Wong, T. P., & Walker, C. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.09.025 · Cited by 107 · see citing works
Kokras, N., Hodes, G. E., Bangasser, D. A., & Dalla, C. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14710 · Cited by 94 · see citing works
Adult neurogenesis, human after all (again): Classic, optimized, and future approaches
Lucassen, P. J., Fitzsimons, C. P., Salta, E., & Maletić‐Savatić, M. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112458 · Cited by 93 · see citing works
Self-citationThe behavioral phenotype of early life adversity: A 3-level meta-analysis of rodent studies
Bonapersona, V., Kentrop, J., Lissa, C. J. V., van der Veen, R., Joëls, M., & Sarabdjitsingh, R. A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.04.021 · Cited by 91 · see citing works
Self-citationEarly life adversity as a risk factor for cognitive impairment and Alzheimer’s disease
Huang, Z., Jordan, J. D., & Zhang, Q. (2023) · Translational Neurodegeneration · doi:10.1186/s40035-023-00355-z · Cited by 92 · see citing works
Yam, K. Y., Naninck, E. F. G., Abbink, M. R., la Fleur, S. E., Schipper, L., van den Beukel, J. C., Grefhorst, A., Oosting, A., van der Beek, E. M., Lucassen, P. J., et al. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.12.012 · Cited by 78 · see citing works
Self-citationInvolvement in Sports, Hippocampal Volume, and Depressive Symptoms in Children
Gorham, L. S., Jernigan, T. L., Hudziak, J. J., & Barch, D. M. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.01.011 · Cited by 76 · see citing works
White, J. D., & Kaffman, A. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01082 · Cited by 73 · see citing works
The evolving neurobiology of early-life stress
Birnie, M. T., & Baram, T. Z. (2025) · Neuron · doi:10.1016/j.neuron.2025.02.016 · Cited by 65 · see citing works
Rocha, M., Wang, D., Avila-Quintero, V. J., Bloch, M. H., & Kaffman, A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01352-4 · Cited by 56 · see citing works
The Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models
Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 52 · see citing works
Loi, M., Sarabdjitsingh, R. A., Tsouli, A., Trinh, S., Arp, M., Krugers, H. J., Karst, H., van den Bos, R., & Joëls, M. (2017) · eNeuro · doi:10.1523/eneuro.0253-17.2017 · Cited by 54 · see citing works
Self-citationHu, P., Maita, I., Phan, M. L., Gu, E., Kwok, C., Dieterich, A., Gergues, M. M., Yohn, C. N., Wang, Y., Zhou, J.-N., et al. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01070-3 · Cited by 49 · see citing works
Self-citationNerve Growth Factor, Stress and Diseases
Ceci, F. M., Ferraguti, G., Petrella, C., Greco, A., Tirassa, P., Iannitelli, A., Ralli, M., Vitali, M., Ceccanti, M., Chaldakov, G. N., et al. (2020) · Current Medicinal Chemistry · doi:10.2174/0929867327999200818111654 · Cited by 51 · see citing works
Klinger, K., Gomes, F. V., Rincón‐Cortés, M., & Grace, A. A. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2019.07.134 · Cited by 46 · see citing works
A novel mouse model for vulnerability to alcohol dependence induced by early-life adversity
Okhuarobo, A., Bolton, J. L., Igbe, I., Zorrilla, E. P., Baram, T. Z., & Contet, C. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100269 · Cited by 45 · see citing works
The Problem of Malnutrition Associated with Major Depressive Disorder from a Sex-Gender Perspective
Montero, C. G., Ortega, M. A., Álvarez-Mon, M. Á., Fraile‐Μartinez, O., Romero-Bazán, A., Lahera, G., Montes, J. M. G., Molina-Ruiz, R. M., Mora, F., Rodríguez–Jiménez, R., et al. (2022) · Nutrients · doi:10.3390/nu14051107 · Cited by 46 · see citing works
Pattwell, S. S., & Bath, K. G. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.04.014 · Cited by 46 · see citing works
Kentrop, J., Smid, C. R., Achterberg, E. J. M., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., Joëls, M., & van der Veen, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00193 · Cited by 41 · see citing works
Self-citationLesuis, S. L., Kaplick, P. M., Lucassen, P. J., & Krugers, H. J. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.02.023 · Cited by 40 · see citing works
Self-citationMalcon, L. M. C., Wearick‐Silva, L. E., Zaparte, A., Orso, R., Luft, C., Tractenberg, S. G., Donadio, M. V. F., de Oliveira, J. R., & Grassi‐Oliveira, R. (2020) · Experimental Brain Research · doi:10.1007/s00221-020-05859-y · Cited by 39 · see citing works
Schmidt, M., Lax, E., Zhou, R., Cheishvili, D., Ruder, A. M., Ludiro, A., Lapert, F., Macedo da Cruz, A., Sandrini, P., Calzoni, T., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-018-0348-7 · Cited by 37 · see citing works
Reshetnikov, V. V., Kovner, A. V., Lepeshko, A. A., Pavlov, K. S., Grinkevich, L. N., & Bondar, N. P. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12541 · Cited by 37 · see citing works
Risk Factors for Alzheimer’s Disease: Focus on Stress
Caruso, A., Nicoletti, F., Gaetano, A., & Scaccianoce, S. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00976 · Cited by 34 · see citing works
Reshetnikov, V. V., Ayriyants, K. A., Ryabushkina, Y. A., Sozonov, N. G., & Bondar, N. P. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113489 · Cited by 34 · see citing works
Barroca, N. C. B., Santa, G. D., Suchecki, D., Garcia‐Cairasco, N., & Umeoka, E. H. D. L. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104771 · Cited by 36 · see citing works
Xu, Y., Sheng, H., Wu, T., Bao, Q., Zheng, Y., Zhang, Y., Gong, Y., Lu, J., You, Z., Xia, Y., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201700948rr · Cited by 31 · see citing works
Xue, F., Xue, S., Liu, L., Sang, H., Ma, Q., Tan, Q., Wang, H., Zhou, C., & Peng, Z. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.03.018 · Cited by 30 · see citing works
Bonapersona, V., Damsteegt, R., Adams, M. L., van Weert, L. T. C. M., Meijer, O. C., Joëls, M., & Sarabdjitsingh, R. A. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00181 · Cited by 29 · see citing works
Self-citationSex-specific behavioral outcomes of early-life adversity and emerging microglia-dependent mechanisms
Garvin, M. M., & Bolton, J. L. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1013865 · Cited by 29 · see citing works
Early‐life stress diminishes the increase in neurogenesis after exercise in adult female mice
Abbink, M. R., Naninck, E. F. G., Lucassen, P. J., & Kőrösi, A. (2017) · Hippocampus · doi:10.1002/hipo.22745 · Cited by 29 · see citing works
Self-citationGlasper, E. R., Hyer, M. M., & Hunter, T. J. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00020 · Cited by 28 · see citing works
Zhang, X., Li, H., Sun, H., Jiang, Y., Wang, A., Kong, Y., Sun, X., Zhu, G., Li, Q., Du, Z., et al. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00709 · Cited by 27 · see citing works
Female pups receive more maltreatment from stressed dams
Keller, S. M., Nowak, A., & Roth, T. L. (2019) · Developmental Psychobiology · doi:10.1002/dev.21834 · Cited by 24 · see citing works
Lesuis, S. L., Catsburg, L. A. E., Lucassen, P. J., & Krugers, H. J. (2018) · Learning & Memory · doi:10.1101/lm.047811.118 · Cited by 24 · see citing works
Self-citationSolarz, A., Majcher‐Maślanka, I., Kryst, J., & Chocyk, A. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.11.005 · Cited by 24 · see citing works
Agarwal, P., Palin, N., Walker, S. L., & Glasper, E. R. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104610 · Cited by 23 · see citing works
Priorities in stress research: a view from the U.S. National Institute of Mental Health
Simmons, J. M., Winsky, L., Zehr, J. L., & Gordon, J. A. (2020) · Stress · doi:10.1080/10253890.2020.1781084 · Cited by 23 · see citing works
Karst, H., Droogers, W. J., van der Weerd, N., Damsteegt, R., van Kronenburg, N. C. H., Sarabdjitsingh, R. A., & Joëls, M. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109543 · Cited by 22 · see citing works
Self-citationLiu, X., Sun, Y., Zhang, C., Zhang, X., Zhang, Y., Wang, T., Ma, Y., Wang, H., Su, Y., Li, J., et al. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108468 · Cited by 21 · see citing works
Czarnabay, D., Dalmago, J., Martins, A. S., Queiroz, A., Sperling, L. E., Reis, K. P., Pranke, P. H. L., & Benetti, F. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107040 · Cited by 20 · see citing works
Kanatsou, S., ter Horst, J. P., Harris, A. P., Seckl, J. R., Krugers, H. J., & Joëls, M. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00374 · Cited by 20 · see citing works
Self-citationEffects of Early Life Adversities upon Memory Processes and Cognition in Rodent Models
Alves, J., Pereira, N. D. S. C., de Lima, R. M. S., Quillfeldt, J. A., & Dalmaz, C. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.023 · Cited by 23 · see citing works
Aleksić, D., Aksić, M., Radonjić, N. V., Jovanović, A., Marković, B., Petronijević, N., Radonjić, V., Mališ, M., & Filipović, B. (2016) · PubMed · Cited by 20 · see citing works
Why are maternally separated females inflexible? Brain activity pattern of COx and c-Fos
Banqueri, M., Méndez, M., & Arias, J. L. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.06.007 · Cited by 19 · see citing works
Benmhammed, H., Hayek, S. E., Nassiri, A., Bousalham, R., Mesfioui, A., Ouichou, A., & Hessni, A. E. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.01.005 · Cited by 21 · see citing works
Smith, E. A., Gursky, Z. H., & Klintsova, A. Y. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.993601 · Cited by 16 · see citing works
Upadhyaya, K., Sharma, P. K., Akhtar, A., & Sah, S. P. (2022) · Journal of Medicinal Food · doi:10.1089/jmf.2021.k.0141 · Cited by 15 · see citing works
FKBP51 in glutamatergic forebrain neurons promotes early life stress inoculation in female mice
van Doeselaar, L., Abromeit, A., Štark, T., Menegaz, D., Ballmann, M., Mitra, S., Yang, H., Rehawi, G., Huettl, R.-E., Bordes, J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57952-x · Cited by 14 · see citing works
Roque, A., Méndez, K. M. V., Ruiz, R., Pineda, E., & Lajud, N. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15193 · Cited by 15 · see citing works
Arvind, A., Sreelekshmi, S., & Dubey, N. (2025) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-025-01549-x · Cited by 16 · see citing works
Baram, T. Z., & Birnie, M. T. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100669 · Cited by 16 · see citing works
Transcriptomic signature of early life stress in male rat prefrontal cortex
Green, N. F. O., Maniam, J., Riese, J., Morris, M. J., & Voineagu, I. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100316 · Cited by 13 · see citing works
Adolescent cocaine induced persistent negative affect in female rats exposed to early-life stress
Bis‐Humbert, C., & García-Fuster, M. J. (2021) · Psychopharmacology · doi:10.1007/s00213-021-05955-z · Cited by 13 · see citing works
Impact of mothers’ experience and early‐life stress on aggression and cognition in adult male mice
Reshetnikov, V. V., Ryabushkina, Y. A., & Bondar, N. P. (2019) · Developmental Psychobiology · doi:10.1002/dev.21887 · Cited by 12 · see citing works
Lesuis, S. L., Lucassen, P. J., & Krugers, H. J. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.07.012 · Cited by 13 · see citing works
Self-citationQu, N., Zhang, S.-F., Xia, B., Xie, J., Wang, X., Liu, J., Xiong, J., Na, R., Wang, Y., Tian, Q., et al. (2019) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2019.10.002 · Cited by 12 · see citing works
Nassiri, A., Lamtai, M., Berkiks, I., Benmhammed, H., Coulibaly, S. M., Chakit, M., Ibouzine‐Dine, L., Mesfioui, A., & El-Hessni, A. (2024) · Advances in Animal and Veterinary Sciences · doi:10.17582/journal.aavs/2024/12.3.457.466 · Cited by 11 · see citing works
Brain Mineralocorticoid Receptors and Resilience to Stress.
Kanatsou, S., Joëls, M., & Krugers, H. (2019) · Vitamins and hormones · doi:10.1016/bs.vh.2018.11.001 · Cited by 7 · see citing works
Self-citationNutritional stress timing differentially programs cognitive abilities in young adult male mice
Berardino, B. G., Ballarini, F., Chertoff, M., Igaz, L. M., & Cánepa, E. T. (2020) · Nutritional Neuroscience · doi:10.1080/1028415x.2020.1751507 · Cited by 10 · see citing works
Differences in learning and memory between middle-aged female and male ratsPreprint
Colettis, N. C., Habif, M., Oberholzer, M. V., Filippin, F., & Jerusalinsky, D. A. (2022) · Learning & Memory · doi:10.1101/lm.053578.122 · Cited by 11 · see citing works
Sanguino‐Gómez, J., & Krugers, H. J. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100636 · Cited by 10 · see citing works
Neural correlates of learning and memory are altered by early-life stress
Sanguino‐Gómez, J., Huijgens, S., den Hartog, M., Schenk, I. J. M., Kluck, W., Versluis, T. D., & Krugers, H. J. (2024) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2024.107952 · Cited by 10 · see citing works
Lifetime Observation of Cognition and Physiological Parameters in Male Mice
Kahnau, P., Guenther, A., Boon, M. N., Terzenbach, J. D., Hanitzsch, E., Lewejohann, L., & Brust, V. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.709775 · Cited by 10 · see citing works
Madison, F. N., Palin, N., Whitaker, A. R., & Glasper, E. R. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.07.161 · Cited by 10 · see citing works
Introduction: Early adversity and brain development
Brummelte, S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.09.041 · Cited by 9 · see citing works
Challenges and opportunities in animal models of gambling-like behavior
Haar, C. V. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.10.013 · Cited by 8 · see citing works
The Mouse Gambling Task: Assessing Individual Decision-making Strategies in Mice
Pittaras, E., Rabat, A., & Granon, S. (2020) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3479 · Cited by 8 · see citing works
Cheng, F., Cui, S., Zhang, C., Zhang, L., Wang, L., Yuan, Q., Huang, C., Zhang, K., & Zhou, X. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00792 · Cited by 8 · see citing works
Effects of RU486 treatment after single prolonged stress depend on the post-stress interval
Ding, J., Chen, X., da Silva, M. S., Lingeman, J., Han, F., & Meijer, O. C. (2020) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2020.103541 · Cited by 8 · see citing works
Lee, B. H., Puri, T. A., & Galea, L. A. M. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819344-0.00010-7 · Cited by 8 · see citing works
Kim, S., Gacek, S. A., Mocchi, M. M., & Redei, E. E. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.779036 · Cited by 8 · see citing works
One Day Away from Mum has Lifelong Consequences on Brain and Behaviour
de Sá, N. F., Camarini, R., & Suchecki, D. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.06.013 · Cited by 7 · see citing works
Kaswan, Z. A. M., Bowers, C. A., Teplyakov, I., Sibtain, A., Munoz-Martin, J., Ahmed, S., Kaffman, L., Giuliano, L., Dietrich, M. O., & Kaffman, A. (2025) · eNeuro · doi:10.1523/eneuro.0249-25.2025 · Cited by 6 · see citing works
Miceli, M. D., Rossitto, M., Martinat, M., Marchaland, F., Kharbouche, S., GRALAND, M., Younes, F., Séré, A., Aubert, A., Khabbaz, L. R., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-80770-y · Cited by 4 · see citing works
Alves, J., dos Santos, A. P. B., Vieira, A. D. S., Martini, A. P. R., de Lima, R. M. S., Smaniotto, T. Â., de Moraes, R. O., Gomes, R. F., Acerbi, G. C. D. A., de Assis, E. Z. B., et al. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.06.020 · Cited by 4 · see citing works
Verdouw, P. M., van Esterik, J. C. J., Peeters, B. W. M. M., Millan, M. J., & Groenink, L. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.01.003 · Cited by 4 · see citing works
Nisar, S., Farooq, R. K., Nazir, S., Alamoudi, W., & Alhibshi, A. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112622 · Cited by 3 · see citing works
Surakul, P., Chutabhakdikul, N., Vanichviriyakit, R., Promthep, K., & Thangnipon, W. (2022) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2022.102085 · Cited by 3 · see citing works
Calado, C. M. S. D. S., Manhães‐de‐Castro, R., Gouveia, H. J. C. B., Nogueira, R. M. T. B. L., Souza, V. D. S., de Lira, A. V. S. M., Merencio, S. M. D. A., Lima, B. M. P., de Oliveira, M. V. P., & Toscano, A. E. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149924 · Cited by 2 · see citing works
Jardim, N. S., Müller, S. G., Pase, F. M., & Nogueira, C. W. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.11.023 · Cited by 2 · see citing works
Михайленко, В. А., Буткевич, И. П., & Vershinina, E. A. (2019) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-019-00734-y · Cited by 1 · see citing works
de Sá, N. F., Assad, N., Camarini, R., & Suchecki, D. (2026) · Neurobiology of Stress · doi:10.1016/j.ynstr.2026.100800 · Cited by 1 · see citing works
de Souza, A. J. M., Freire, A. I., de Souza, F. B. M., & Giestal‐de‐Araujo, E. (2020) · Research Society and Development · doi:10.33448/rsd-v9i11.9895 · Cited by 1 · see citing works
The brain mineralocorticoid receptor
Sarabdjitsingh, R. A., de Kloet, E. R., Joëls, M., & Vinkers, C. H. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00004-5
Self-citation
- Authors
- Loi, M., Mossink, J. C. L., Meerhoff, G. F., Den Blaauwen, J. L., Lucassen, P. J., & Joëls, M.
- Affiliations
- University Medical Center Utrecht (NL)
- University of Amsterdam (NL)
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 342
- Pages
- 101-119
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W1631193623
- Cited by
- 109
- References
- 121
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 8 · 2023: 5 · 2022: 10 · 2021: 10 · 2020: 15 · 2019: 23 · 2018: 12 · 2017: 9 · 2016: 6
- FWCI
- 4.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Utrecht University Repository (Utrecht University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Dutch Ministry of Education, Culture, and Science
- NWO (024.001.003)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Keywords
- early life stress, maternal deprivation, hippocampus, dentate gyrus, hippocampal neurogenesis, adult neurogenesis, mifepristone, glucocorticoid receptor, sex differences, anxiety, contextual memory, reward-based decision-making, child abuse, female rats
- MeSH terms
- Animals, Animals, Newborn, Anxiety, Cognition, Disease Models, Animal, Female, Gambling, Hippocampus, Hormone Antagonists, Maternal Deprivation, Memory, Neurons, Random Allocation, Receptors, Glucocorticoid, Sexual Maturation, Stress, Psychological, Mifepristone, Rats, Wistar, Treatment Failure, Neurogenesis
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