A longitudinal study of stress-induced hippocampal volume changes in mice that are susceptible or resilient to chronic social defeat
Abstract
Hippocampal shrinkage is a commonly found neuroanatomical change in stress‐related mood disorders such as depression and post‐traumatic stress disorders (PTSD). Since the onset and severity of these disorders have been found to be closely related to stressful life events, and as stress alone has been shown to reduce hippocampal volume in animal studies, vulnerability to mood disorders may be related to a susceptibility to stress‐induced hippocampal shrinkage. However, a smaller hippocampal volume before stress exposure has also been suggested to confer vulnerability of stressed individuals to PTSD or depression. In this study, we examined the contribution of either innate hippocampal volume differences or hippocampal susceptibility to stress‐induced shrinkage to the formation of stress‐related psychopathology using longitudinal MRI measurements of hippocampal volume in inbred C57 mice before and after chronic social defeat stress. We found that only half of the stressed C57 mice were susceptible to stress and developed psychopathological behaviors such as social avoidance. The other half was resilient to stress and exhibited no social avoidance. Before exposure to stress, we observed a positive correlation between hippocampal volume and social avoidance. After chronic social defeat stress, we found significant increases in left hippocampal volume in resilient and nonstressed control mice. Intriguingly, this increase in hippocampal volume was not found in susceptible mice, suggesting an arrestment of hippocampal growth in these mice. Our findings suggest that both a susceptibility to stress‐induced hippocampal volume changes and a larger hippocampus before stress exposure confer vulnerability to psychopathology after chronic stress. © 2014 Wiley Periodicals, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A recent longitudinal study suggested that stress-susceptible mice have larger hippocampal volume than resilient mice before stress onset.
“However, a recent longitudinal study suggested that stress-susceptible mice have larger hippocampal volume than resilient mice before stress onset (56).”
From Neuroanatomic differences associated with stress susceptibility and resilience (2016) · cites this paper as [56]
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258 · see citing works
Regional Brain Changes in Aging Healthy Adults: General Trends, Individual Differences and Modifiers
Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., Dahle, C., Gerstorf, D., & Acker, J. D. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi044 · Cited by 2,875 · see citing works
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Traumatic Events and Posttraumatic Stress Disorder in an Urban Population of Young Adults
Breslau, N. (1991) · Archives of General Psychiatry · doi:10.1001/archpsyc.1991.01810270028003 · Cited by 2,544 · see citing works
Causal Relationship Between Stressful Life Events and the Onset of Major Depression
Kendler, K. S., Karkowski, L. M., & Prescott, C. A. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.6.837 · Cited by 2,486 · cited 2× · see citing works
“…and trauma are closely associated with the onset and symptom severity of depression and post-traumatic stress disorder (PTSD, Breslau et al., 1991; Kendler et al., 1999; Lorenzetti et al., 2009; Muscatell et al., 2009), mood disorders that are frequently accompanied by hippocampal atrophy (McEwen…”
BackgroundKrishnan, V., Han, M.-H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., LaPlant, Q., Graham, A., Lutter, M., Lagace, D. C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.09.018 · Cited by 2,307 · cited 9× · see citing works
“Chronic social defeat was performed as previously described, with a test C57 mouse being placed into the space territorialized by a larger and aggressive CD1 retired breeder (Krishnan et al., 2007).”
BackgroundMethodInfluentialSelf-citationSTRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · 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
McEwen, B. S., & Sapolsky, R. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80028-x · Cited by 1,889 · see citing works
Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma
Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2002) · Nature Neuroscience · doi:10.1038/nn958 · Cited by 1,635 · see citing works
Hippocampal volume and depression: a meta-analysis of MRI studies
Videbech, P., & Ravnkilde, B. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.11.1957 · Cited by 1,590 · see citing works
Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis
Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.08.006 · Cited by 1,322 · see citing works
Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging
Sapolsky, R., Krey, L., & McEwen, B. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01222.1985 · Cited by 1,129 · see citing works
Hippocampal damage associated with prolonged glucocorticoid exposure in primates
Sapolsky, R., Uno, H., Rebert, C., & Finch, C. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-09-02897.1990 · Cited by 1,103 · see citing works
Gurvits, T. V., Shenton, M. E., Hokama, H., Ohta, H., Lasko, N. B., Gilbertson, M. W., Orr, S. P., Kikinis, R., Jolesz, F. A., McCarley, R. W., et al. (1996) · Biological Psychiatry · doi:10.1016/s0006-3223(96)00229-6 · Cited by 899 · see citing works
Magarin˜os, A. M., & McEwen, B. S. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00259-l · Cited by 863 · see citing works
Hippocampal damage associated with prolonged and fatal stress in primates
Uno, H., Tarara, R., Else, J., Suleman, M., & Sapolsky, R. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01705.1989 · Cited by 728 · see citing works
Lorenzetti, V., Allen, N. B., Fornito, A., & Yücel, M. (2009) · Journal of Affective Disorders · doi:10.1016/j.jad.2008.11.021 · Cited by 553 · see citing works
Medical Image Processing, Analysis and Visualization in clinical research
McAuliffe, M., Lalonde, F. M., McGarry, D. P., Gandler, W., Csaky, K. G., & Trus, B. L. (2002) · Proceedings - IEEE Symposium on Computer-Based Medical Systems · doi:10.1109/cbms.2001.941749 · Cited by 522 · see citing works
Smith, M. E. (2005) · Hippocampus · doi:10.1002/hipo.20102 · Cited by 395 · see citing works
Isgor, C., Kabbaj, M., Akil, H., & Watson, S. J. (2004) · Hippocampus · doi:10.1002/hipo.10207 · Cited by 341 · see citing works
Carrion, V. G., Weems, C. F., & Reiss, A. L. (2007) · PEDIATRICS · doi:10.1542/peds.2006-2028 · Cited by 327 · see citing works
Lifespan Mental Activity Predicts Diminished Rate of Hippocampal Atrophy
Valenzuela, M., Sachdev, P. S., Wen, W. X., Chen, X., & Brodaty, H. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002598 · Cited by 249 · see citing works
Stress, the hippocampus, and epilepsy
Joëls, M. (2008) · Epilepsia · doi:10.1111/j.1528-1167.2008.01902.x · Cited by 221 · see citing works
Decreased hippocampal volume in healthy girls at risk of depression
Chen, M. C., Hamilton, J. P., & Gotlib, I. H. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.202 · Cited by 220 · see citing works
Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00418.x · Cited by 198 · see citing works
Kilborn, S. H., Trudel, G., & Uhthoff, H. K. (2002) · PubMed · Cited by 198 · see citing works
Lee, T., Jarome, T., Li, S.-J., Kim, J. J., & Helmstetter, F. J. (2009) · NeuroReport · doi:10.1097/wnr.0b013e328332bb09 · Cited by 173 · see citing works
Lupien, S. J., Evans, A., Lord, C., Miles, J., Pruessner, M., Pike, B., & Pruessner, J. C. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.041 · Cited by 167 · see citing works
Lau, J. C., Lerch, J. P., Sled, J. G., Henkelman, R. M., Evans, A. C., & Bedell, B. J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.252 · Cited by 151 · see citing works
Pruessner, M., Pruessner, J. C., Hellhammer, D. H., Bruce Pike, G., & Lupien, S. J. (2007) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2006.12.007 · Cited by 150 · see citing works
Morphologic hippocampal asymmetry in male and female rats
Diamond, M. C., Murphy, G. M., Akiyama, K., & Johnson, R. E. (1982) · Experimental Neurology · doi:10.1016/0014-4886(82)90124-8 · Cited by 141 · see citing works
Early Life Stress and Inherited Variation in Monkey Hippocampal Volumes
Lyons, D. M., Yang, C., Sawyer-Glover, A. M., Moseley, M. E., & Schatzberg, A. F. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.12.1145 · Cited by 134 · see citing works
Stressful Life Events, Chronic Difficulties, and the Symptoms of Clinical Depression
Muscatell, K. A., Slavich, G. M., Monroe, S. M., & Gotlib, I. H. (2009) · Journal of Nervous & Mental Disease · doi:10.1097/nmd.0b013e318199f77b · Cited by 126 · see citing works
Maheswaran, S., Barjat, H., Rueckert, D., Bate, S. T., Howlett, D. R., Tilling, L. C., Smart, S., Pohlmann, A., Richardson, J. C., Hartkens, T., et al. (2009) · Brain Research · doi:10.1016/j.brainres.2009.02.045 · Cited by 103 · see citing works
Hippocampal but not amygdalar volume affects contextual fear conditioning in humans
Pohlack, S. T., Nees, F., Liebscher, C., Cacciaglia, R., Diener, S. J., Ridder, S., Woermann, F. G., & Flor, H. (2011) · Human Brain Mapping · doi:10.1002/hbm.21224 · Cited by 69 · see citing works
Zannas, A. S., McQuoid, D. R., Payne, M. E., Steffens, D. C., MacFall, J. R., Ashley-Koch, A., & Taylor, W. D. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.02.008 · Cited by 53 · see citing works
Hippocampal Asymmetry: Differences in Structures and Functions
Hou, G., Yang, X., & Yuan, T. (2013) · Neurochemical Research · doi:10.1007/s11064-012-0954-3 · Cited by 48 · see citing works
van der Beek, E. M., Wiegant, V. M., Schouten, W. G. P., Eerdenburg, F. J. C. M. V., Loijens, L. W. S., van der Plas, C., Benning, M. A., de Vries, H., de Kloet, E. R., & Lucassen, P. J. (2004) · Hippocampus · doi:10.1002/hipo.10213 · Cited by 44 · see citing works
Valdés, J. J., Mactutus, C. F., Cory, R. N., & Cameron, W. R. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90284-5 · Cited by 27 · see citing works
Sinkkonen, S. T., Vekovischeva, O. Y., Möykkynen, T. P., Ogris, W., Sieghart, W., Wisden, W., & Korpi, E. R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03684.x · Cited by 23 · see citing works
Liu, W., Shu, X., Chen, F.-Y., Zhu, C., Sun, X.-H., Liú, L., Ai, Y.-X., Li, Y., & Zhao, H. (2011) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.02.007 · Cited by 19 · see citing works
Zach, P., Mrzílková, J., Řezáčová, L., Stuchlı́k, A., & Valeš, K. (2010) · Physiological Research · doi:10.33549/physiolres.931904 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Nociception, pain, negative moods, and behavior selection
Baliki, M. N., & Apkarian, A. V. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.005 · Cited by 731 · see citing works
Animal models of major depression: drawbacks and challenges
Planchez, B., Surget, A., & Belzung, C. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02084-y · Cited by 480 · see citing works
Deslauriers, J., Tóth, M., Der‐Avakian, A., & Risbrough, V. B. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.11.019 · Cited by 253 · see citing works
Defeat stress in rodents: from behavior to molecules
Hammels, C., Pishva, E., De Vry, J., van den Hove, D. L. A., Prickaerts, J., van Winkel, R., Selten, J.-P., Lesch, K.-P., Daskalakis, N. P., Steinbusch, H. W. M., et al. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.10.006 · Cited by 230 · see citing works
Role of adult hippocampal neurogenesis in stress resilience
Levone, B. R., Cryan, J. F., & O'Leary, O. F. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.11.003 · Cited by 218 · see citing works
Neuroanatomic differences associated with stress susceptibility and resilience
Anacker, C., Scholz, J., O’Donnell, K. J., Allemang-Grand, R., Diorio, J., Bagot, R. C., Nestler, E. J., Hen, R., Lerch, J. P., & Meaney, M. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.009 · Cited by 167 · see citing works
A systematic review of the neural bases of psychotherapy for anxiety and related disorders
Brooks, S. J., & Stein, D. J. (2015) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2015.17.3/sbrooks · Cited by 134 · see citing works
Antidepressant effect of taurine in chronic unpredictable mild stress-induced depressive rats
Wu, G., Ren, S., Tang, R., Xu, C. S., Zhou, J., Lin, S., Feng, Y., Yang, Q., Hu, J., & Yang, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-05051-3 · Cited by 124 · see citing works
Maladaptive autonomic regulation in PTSD accelerates physiological aging
Williamson, J. B., Porges, E. C., Lamb, D. G., & Porges, S. W. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01571 · Cited by 116 · see citing works
“Chronic stress, such as is present with PTSD and depression, has a negative impact on hippocampal characteristics in both animal models (Uno et al., 1989; Magariños and McEwen, 1995; Luo et al., 2014; Tse et al., 2014) and in humans (Childress et al., 2013).”
BackgroundInfluentialThe interaction of acute and chronic stress impairs model-based behavioral control
Radenbach, C., Reiter, A. M. F., Engert, V., Sjoerds, Z., Villringer, A., Heinze, H., Deserno, L., & Schlagenhauf, F. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.12.017 · Cited by 117 · see citing works
Iñiguez, S. D., Aubry, A., Riggs, L. M., Alipio, J. B., Zanca, R. M., Flores-Ramirez, F. J., Hernandez, M. A., Nieto, S. J., Musheyev, D., & Serrano, P. A. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.07.001 · Cited by 105 · see citing works
Jangra, A., Sriram, C. S., Dwivedi, S., Gurjar, S. S., Hussain, M. I., Borah, P., & Lahkar, M. (2016) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-016-0344-5 · Cited by 96 · see citing works
Grandjean, J., Azzinnari, D., Seuwen, A., Sigrist, H., Seifritz, E., Pryce, C. R., & Rudin, M. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.08.013 · Cited by 92 · see citing works
Resilience and Vulnerability to Pain and Inflammation in the Hippocampus
Vasić, V., & Schmidt, M. H. H. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040739 · Cited by 84 · see citing works
Zhang, T. R., Larosa, A., Raddo, M.-E. D., Wong, V., Wong, A. S., & Wong, T. P. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1958-18.2019 · Cited by 84 · see citing works
Self-citationLeschik, J., Lutz, B., & Gentile, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147339 · Cited by 63 · see citing works
Encore: Behavioural animal models of stress, depression and mood disorders
Petković, A., & Chaudhury, D. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.931964 · Cited by 70 · see citing works
Huang, P., Li, C., Fu, T., Zhao, D., Yi, Z., Lü, Q., Guo, L., & Xu, X. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.004 · Cited by 66 · see citing works
Gururajan, A., van de Wouw, M., Boehme, M., Becker, T., O’Connor, R., Bastiaanssen, T. F. S., Moloney, G. M., Lyte, J. M., Silva, A. P. V., Merckx, B., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.05.004 · Cited by 63 · see citing works
Bastos, C. P., Pereira, L. M., Ferreira-Vieira, T. H., Drumond, L. E., Massensini, A. R., Moraes, M. F. D., & Pereira, G. S. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.03.020 · Cited by 49 · see citing works
Resilience Against Traumatic Stress: Current Developments and Future Directions
Snijders, C., Pries, L.-K., Sgammeglia, N., Jowf, G. I. A., Youssef, N. A., de Nijs, L., Gülöksüz, S., & Rutten, B. P. F. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00676 · Cited by 48 · see citing works
Molecular and neurocircuitry mechanisms of social avoidance
Gellner, A., Voelter, J., Schmidt, U., Beins, E. C., Stein, V., Philipsen, A., & Hurlemann, R. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03649-x · Cited by 51 · see citing works
Krzystyniak, A., Bączyńska, E., Magnowska, M., Antoniuk, S., Roszkowska, M., Zaręba-Kozioł, M., Das, N., Basu, S., Pikuła, M., & Włodarczyk, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20071726 · Cited by 46 · see citing works
Ayash, S., Schmitt, U., & Müller, M. B. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.10.001 · Cited by 45 · see citing works
Hippocampal Volume as an Amplifier of the Effect of Social Context on Adolescent Depression
Schriber, R. A., Anbari, Z., Robins, R. W., Conger, R. D., Hastings, P. D., & Guyer, A. E. (2017) · Clinical Psychological Science · doi:10.1177/2167702617699277 · Cited by 41 · see citing works
Early life stress-induced alterations in rat brain structures measured with high resolution MRI
Sarabdjitsingh, R. A., Loi, M., Joëls, M., Dijkhuizen, R. M., & van der Toorn, A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185061 · Cited by 41 · see citing works
Defeating the fear: New insights into the neurobiology of stress susceptibility
Krishnan, V. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.012 · Cited by 38 · see citing works
Khan, A. R., Hansen, B., Wiborg, O., Kroenke, C. D., & Jespersen, S. N. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.11.053 · Cited by 38 · see citing works
Zhu, Y., Wang, R., Fan, Z., Luo, D., Cai, G., Li, X., Han, J., Zhuo, L., Zhang, L., Zhang, H., et al. (2022) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-022-01218-3 · Cited by 35 · see citing works
Individual differences in inflammatory and oxidative mechanisms of stress-related mood disorders
Kalinichenko, L. S., Kornhuber, J., & Müller, C. P. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100783 · Cited by 34 · see citing works
Tse, Y. C., Lopez, J., Moquin, A., Wong, S.-M. A., Maysinger, D., & Wong, T. P. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0325-8 · Cited by 32 · see citing works
Self-citationPutative Inflammatory Sensitive Mechanisms Underlying Risk or Resilience to Social Stress
Finnell, J. E., & Wood, S. K. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00240 · Cited by 31 · see citing works
Oxidized Cell-Free DNA Role in the Antioxidant Defense Mechanisms under Stress
Filev, A. D., Шмарина, Г. В., Ershova, E. S., Вейко, Н. Н., Мартынов, А. В., Borzikova, M., Полеткина, А. А., Dolgikh, O. А., Вейко, В. П., Bekker, A. A., et al. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/1245749 · Cited by 30 · see citing works
Benefits of animal models to understand the pathophysiology of depressive disorders
Czéh, B., & Simon, M. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110049 · Cited by 30 · see citing works
Liu, X., Yuan, J., Guang, Y., Wang, X., & Feng, Z. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00613 · Cited by 25 · see citing works
Noda, Y., Asano, K., Shimizu, E., & Hirano, Y. (2018) · Disaster Medicine and Public Health Preparedness · doi:10.1017/dmp.2018.62 · Cited by 24 · see citing works
Walker, S. E., Wood, T., Cash, D., Mesquita, M. S., Williams, S., & Sandi, C. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14061 · Cited by 25 · see citing works
Modulation of Hippocampal Antioxidant Defense System in Chronically Stressed Rats by Lithium
Popović, N., Stojiljković, V., Pejić, S., Todorović, A., Pavlović, I., Gavrilović, L., & Pajović, S. B. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/8745376 · Cited by 22 · see citing works
Depressive behavior induced by social isolation of predisposed female rats
Zanier-Gomes, P. H., Silva, T. E. D. A., Zanetti, G. C., Benati, É. R., Pinheiro, N. M., Murta, B. M. T., & Crema, V. O. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.07.026 · Cited by 22 · see citing works
Overfeld, J., Entringer, S., Rasmussen, J. M., Heim, C. C., Styner, M. A., Gilmore, J. H., Wadhwa, P. D., & Buß, C. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100820 · Cited by 20 · see citing works
Hippocampal area CA2 activity supports social investigation following an acute social stress
Radzicki, D., McCann, K. E., Alexander, G. M., & Dudek, S. M. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02834-9 · Cited by 15 · see citing works
Inhibitory avoidance learning in CD1 mice: Effects of chronic social defeat stress
Monleón, S., Duque, A., & Vinader‐Caerols, C. (2015) · Behavioural Processes · doi:10.1016/j.beproc.2015.03.003 · Cited by 15 · see citing works
Riga, D., Schmitz, L. J. M., van Mourik, Y., Hoogendijk, W. J. G., Vries, T. J. D., Smit, A. B., & Spijker, S. (2018) · Addiction Biology · doi:10.1111/adb.12701 · Cited by 12 · see citing works
Temporal profiling of depression vulnerability in a preclinical model of sustained depression
Riga, D., Schmitz, L. J. M., Hoogendijk, W. J. G., Smit, A. B., & Spijker, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-06984-5 · Cited by 11 · see citing works
Levone, B. R., Moloney, G. M., Cryan, J. F., & O’Leary, O. F. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100331 · Cited by 10 · see citing works
Wright, B. J., Wilson, K.-E., Kingsley, M., Maruff, P. T., Li, J., Siegrist, J., & Horan, B. (2022) · Attention Perception & Psychophysics · doi:10.3758/s13414-022-02454-x · Cited by 10 · see citing works
Decline of stress resilience in aging rats: Focus on choroid plexus-cerebrospinal fluid-hippocampus
Liu, K., Li, H., Zeng, N.-X., Lu, W., Wu, X., Xu, H., Yan, C., & Wu, L. (2022) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2022.2151044 · Cited by 9 · see citing works
Canto‐de‐Souza, L., Baptista‐de‐Souza, D., Thiele, M., Garcia, V. L., Silva, K. C., de Souza, F. V., Crestani, C. C., & Nunes‐de‐Souza, R. L. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111313 · Cited by 8 · see citing works
Schultz, I. Z., Sepehry, A. A., & Greer, S. C. (2018) · Psychological Injury and Law · doi:10.1007/s12207-018-9322-1 · Cited by 8 · see citing works
Sex-Specific Retinal Anomalies Induced by Chronic Social Defeat Stress in Mice
Arsenault, E., Lavigne, A.-A., Mansouri, S., Gagné, A.-M., Francis, K., Bittar, T. P., Quessy, F., Abdallah, K., Barbeau, A., Hébert, M., et al. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.714810 · Cited by 7 · see citing works
Molecular laterality encodes stress susceptibility in the medial prefrontal cortex
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D., Lee, S., Kim, M., Jung, I., & Kim, D. (2021) · Molecular Brain · doi:10.1186/s13041-021-00802-w · Cited by 7 · see citing works
Factors Regulating Neurogenesis in the Adult Dentate Gyrus
Zhang, L., & Zhang, X.-H. (2018) · Hippocampus · doi:10.5772/intechopen.75631 · Cited by 4 · see citing works
Čulig, L., & Belzung, C. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-801977-1.00009-x · Cited by 5 · see citing works
Popović, N., Pajović, S. B., Stojiljković, V., Todorović, A., Pejić, S., Pavlović, I., & Gavrilović, L. (2017) · RAD Conference Proceedings. · doi:10.21175/radproc.2017.52 · Cited by 3 · see citing works
Changes of Hippocampal Noradrenergic Capacity in Stress Condition
Gavrilović, L., Popović, N., Stojiljković, V., Pejić, S., Todorović, A., Pavlović, I., & Pajović, S. B. (2020) · Folia Biologica · doi:10.14712/fb2020066020081 · Cited by 2 · see citing works
Iqbal, Z., Rosa, J. M., Yu, J., Cheng, T., Formolo, D. A., Hussain, A., Wong, T. P., Lee, T. M. C., So, K., & Yau, S. (2026) · Scientific Reports · doi:10.1038/s41598-026-48292-x · Cited by 1 · see citing works
Self-citationPopović, N., Pajović, S. B., Stojiljković, V., Todorović, A., Pejić, S., Pavlović, I., & Gavrilović, L. (2018) · Neurophysiology · doi:10.1007/s11062-019-09758-z
Zmavc, K., & Kramar, C. P. (2019) · University of Western Ontario Medical Journal · doi:10.5206/uwomj.v87is1.4878
Yau, S., Iqbal, Z., Rosa, J. M., Yu, J., Cheng, T., Formolo, D. A., Hussain, A., Wong, T. P., Lee, T. M. C., & So, K. (2025) · Research Square · doi:10.21203/rs.3.rs-6647892/v1
Self-citationChae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782903
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782906
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782894
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782891
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782888
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782897
Chae, S., Hong, J., Kang, K., Shin, A., Kim, D.-G., Lee, S., Kim, M.-Y., Jung, I., & Kim, D. (2021) · Figshare · doi:10.6084/m9.figshare.14782900
Network adaptability governs resilience and susceptibility to social defeat
Ayash, S., Koch, S., An, J., Schmitt, U., Mueller, S. G., Foddis, M., Candemir, E., Tüscher, O., Boehm‐Sturm, P., & Müller, M. B. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03899-4
- Authors
- Tse, Y. C., Montoya, I., Wong, A. S., Mathieu, A., Lissemore, J., Lagace, D. C., & Wong, T. P.
- Affiliations
- Douglas Mental Health University Institute (CA)
- University of Ottawa (CA)
- Corresponding author
- Wong, Tak Pan
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2014-05-07
- Volume
- 24
- Issue
- 9
- Pages
- 1120-1128
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- OpenAlex
- W2171193826
- Cited by
- 69
- References
- 44
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2022: 4 · 2021: 12 · 2020: 5 · 2019: 10 · 2018: 9 · 2017: 8 · 2016: 4 · 2015: 10 · 2014: 2
- FWCI
- 3.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (MOP-106649)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampal volume, chronic social defeat stress, stress vulnerability, stress resilience, hippocampal plasticity, social avoidance, depression, post-traumatic stress disorder, stress-related psychopathology, C57 mice, inbred mouse strains
- MeSH terms
- Animals, Avoidance Learning, Body Weight, Chronic Disease, Disease Models, Animal, Dominance-Subordination, Hippocampus, Functional Laterality, Longitudinal Studies, Magnetic Resonance Imaging, Male, Mice, Inbred C57BL, Organ Size, Social Behavior, Stress, Psychological, 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