Unpredictable chronic stress in juvenile or adult rats has opposite effects, respectively, promoting and impairing resilience
Open accessAbstract
We evaluated the effects of early maternal deprivation (MD; age 7-14 days) alone or in combination with unpredictable chronic stress (UCS; MDUN; 28-84 days) on anxiety and learning in 90 days old adult rats. We hypothesized that exposure to both stressors (MDUN) would be more detrimental than exposure to one or neither. Unexpectedly, adult rats from the MDUN group did not differ from control animals, whereas adult MD animals exhibited impaired avoidance learning. We next investigated the effect of juvenile-onset (30-90 days) versus adult-onset (60-90 days) stress on avoidance learning in adulthood (90 days). We found that adult-onset chronic stress impaired avoidance learning and memory whereas juvenile-onset stress did not. Thus, the results again indicate that juvenile exposure to UCS induces resilience rather than impairment.
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?
Maternal deprivation early combined with chronic unpredictable stress during juvenile periods promoted greater stress resilience than maternal deprivation alone or combined with adult chronic unpredictable stress.
“A recent study showed that maternal deprivation during early periods combined with chronic unpredictable stress (CUS; exposure to varying physical stresses) during juvenile periods promoted a greater degree of stress resilience than maternal deprivation alone or when combined with adult CUS46.”
From Neurobiology of resilience (2012) · cites this paper as [46]
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
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · see citing works
Repeated stress causes reversible impairments of spatial memory performance.
Luine, V., Villegas, M., Martinez, C., & McEwen, B. (1994) · Brain Research · doi:10.1016/0006-8993(94)91778-7 · Cited by 813 · see citing works
McAllister, T. W., Saykin, A. J., Flashman, L. A., Sparling, M. B., Johnson, S. C., Guerin, S. J., Mamourian, A. C., Weaver, J. B., & Yanofsky, N. (1999) · Neurology · doi:10.1212/wnl.53.6.1300 · Cited by 476 · see citing works
Roceri, M., Hendriks, W. J. A. J., Racagni, G., Ellenbroek, B. A., & Riva, M. A. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001036 · Cited by 465 · see citing works
Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice
Mineur, Y. S., Belzung, C., & Crusio, W. E. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.029 · Cited by 459 · see citing works
Liu, Caldji, Sharma, Plotsky, & Meaney (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00422.x · Cited by 451 · see citing works
Bondi, C. O., Rodriguez, G., Gould, G. G., Frazer, A., & Morilak, D. A. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301410 · Cited by 398 · see citing works
The Maudsley Reactive and Nonreactive strains of rats: A survey
Broadhurst, P. L. (1975) · Behavior Genetics · doi:10.1007/bf01073201 · Cited by 354 · 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
Mash, E. J., & Wolfe, D. A. (2004) · Cited by 326 · see citing works
Incubated in terror: Neurodevelopmental factors in the "cycle of violence."
Perry, B. D. (1997) · Cited by 303 · see citing works
Neurotransmitters as morphogens
Lauder, J. M. (1988) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60516-6 · Cited by 257 · see citing works
Avital, A., & Richter‐Levin, G. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145704004808 · Cited by 219 · see citing works
Self-citationAge‐dependent effects of chronic stress on brain plasticity and depressive behavior
Tóth, E., Gersner, R., Wilf‐Yarkoni, A., Raizel, H., Dar, D. E., Richter‐Levin, G., Levit, O., & Zangen, A. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05642.x · Cited by 193 · see citing works
Self-citationOitzl, M. S., Workel, J. O., Fluttert, M., van Loenen-Frösch, F., & de Kloet, E. R. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00231.x · Cited by 184 · see citing works
Ferdman, N., MURMU, R., Bock, J., Braun, K., & Leshem, M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.03.011 · Cited by 173 · see citing works
Self-citationTsoory, M., Cohen, H., & Richter‐Levin, G. (2006) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2006.06.007 · Cited by 165 · see citing works
Self-citationComplete 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
Tsoory, M., & Richter‐Levin, G. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705006255 · Cited by 132 · see citing works
Self-citationEffect of Chronic Stress on Synaptic Currents in Rat Hippocampal Dentate Gyrus Neurons
Karst, H., & Joëls, M. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00691.2002 · Cited by 111 · see citing works
The Long-Term Effects of Maternal Deprivation Depend on the Genetic Background
Ellenbroek, B. A. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00088-9 · Cited by 105 · see citing works
Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus
Shors, T. J., Foy, M. R., Levine, S., & Thompson, R. F. (1990) · Brain Research Bulletin · doi:10.1016/0361-9230(90)90005-k · Cited by 100 · see citing works
Jacobson‐Pick, S., & Richter‐Levin, G. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.036 · Cited by 98 · see citing works
Self-citationMaternal Deprivation Stress Exacerbates Cognitive Deficits in Immature Rats with Recurrent Seizures
Huang, L., Holmes, G. L., Lai, M., Hung, P., Wang, C., Wang, T., Yang, C., Liou, C., & Yang, S. N. (2002) · Epilepsia · doi:10.1046/j.1528-1157.2002.14602.x · Cited by 94 · see citing works
Avital, A., Ram, E., Maayan, R., Weizman, A., & Richter‐Levin, G. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.09.015 · Cited by 85 · see citing works
Self-citationBenetti, F., Mello, P. B., Bonini, J. S., Monteiro, S. C., Cammarota, M., & Izquierdo, I. (2008) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2008.09.200 · Cited by 81 · see citing works
Papas, M. A., Black, M. M., & Krishnakumar, A. (2000) · Child Abuse & Neglect · doi:10.1016/s0145-2134(00)00126-5 · Cited by 81 · see citing works
Vázquez, D. M., Bailey, C., Dent, G. W., Okimoto, D. K., Steffek, A. E., López, J. F., & Levine, S. D. (2006) · Brain Research · doi:10.1016/j.brainres.2006.08.104 · Cited by 77 · 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
Avital, A. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00286-x · Cited by 67 · see citing works
Tóth, E., Avital, A., Leshem, M., Richter‐Levin, G., & Braun, K. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.012 · Cited by 60 · see citing works
Self-citationVaid, R. R., Yee, B. K., Shalev, U., Rawlins, J. N. P., Weiner, I., Feldon, J., & Totterdell, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05599.1997 · Cited by 52 · see citing works
Effect of maternal separation on feeding behavior of rats in later life
Iwasaki, S., Inoue, K., Kiriike, N., & Hikiji, K. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00305-x · Cited by 50 · see citing works
Teunis, M., Heijnen, C. J., Sluyter, F., Bakker, J. M., van Dam, A., Hof, M., Cools, A. R., & Kavelaars, A. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00351-x · Cited by 47 · see citing works
Antidepressants in chronic unpredictable mild stress (CUMS)-induced deficit of fighting behavior.
Ossowska, G., Danilczuk, Z., Klenk-Majewska, B., Czajkowski, L., & Zebrowska-Łupina, I. (2004) · PubMed · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Russo, S. J., Murrough, J. W., Han, M.-H., Charney, D. S., & Nestler, E. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3234 · Cited by 1,206 · see citing works
Suri, D., Veenit, V., Sarkar, A., Thiagarajan, D., Kumar, A., Nestler, E. J., Galande, S., & Vaidya, V. A. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.10.023 · Cited by 208 · see citing works
Peripheral and central mechanisms of stress resilience
Pfau, M. L., & Russo, S. J. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.09.004 · Cited by 170 · see citing works
Predictable chronic mild stress in adolescence increases resilience in adulthood
Suo, L., Zhao, L., Si, J., Liu, J., Zhu, W., Chai, B., Zhang, Y., Feng, J., Ding, Z., Luo, Y., et al. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.67 · Cited by 122 · see citing works
Zaidan, H., Leshem, M., & Gaisler-Salomon, I. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.04.014 · Cited by 94 · see citing works
Self-citation
- Authors
- Ricon, T., Toth, E., Leshem, M., Braun, K., & Richter-Levin, G.
- Affiliations
- University of Haifa (IL)
- Nagoya University (JP)
- Otto-von-Guericke-Universität Magdeburg (DE)
- Corresponding author
- Ricon, T.
- Venue
- Stress
- Publisher
- Informa UK Limited
- Published
- 2011-06-19
- Volume
- 15
- Issue
- 1
- Pages
- 11-20
- ISSN
- 1025-3890 (ISSN-L)
- 1607-8888
- OpenAlex
- W1753989155
- Cited by
- 55
- References
- 36
- Citations by year
- 2025: 3 · 2024: 2 · 2023: 1 · 2022: 6 · 2021: 1 · 2020: 1 · 2018: 4 · 2017: 5 · 2016: 7 · 2015: 4 · 2014: 9 · 2013: 6 · 2012: 5
- FWCI
- 2.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Stress (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Clinical Psychology › Resilience and Mental Health
- Keywords
- unpredictable chronic stress, maternal deprivation, early life stress, resilience, anxiety, avoidance learning, memory impairment
- MeSH terms
- Aging, Animals, Anxiety, Avoidance Learning, Exploratory Behavior, Food Deprivation, Male, Maternal Deprivation, Memory, Stress, Psychological, Swimming, Maze Learning, Rats, Resilience, Psychological
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
