Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Comparison of stressors
Abstract
Repeated restraint stress induces an atrophy of apical dendrites of CA3c pyramidal neurons in the hippocampus, but the relationship between stress and adrenocortical activation has not been thoroughly investigated. In order to better understand the relationship between neural and non-neural indices of the severity of stress, we investigated the temporal relationship between CA3c dendritic atrophy and indices of adrenal steroid stress responsiveness. For this purpose, we used two different stress regimens: repeated restraint stress (6 h/day) and a chronic multiple stress paradigm (shaking, restraint and swimming, each day), differing in the degree of adrenal activation produced over 14 and 21 days. Atrophy of dendrites of CA3c neurons was found after 21 days of stress, but not after 14 days, and was of a similar magnitude for both stressors. However, non-neural measures differed between the two stress paradigms: (i) chronic restraint stress caused a significant habituation by day 21 in the corticosterone response to acute restraint, whereas chronic multiple stress exposure was not accompanied by habituation of the corticosterone response to restraint; (ii) chronic restraint stress caused neither adrenal hypertrophy nor thymus atrophy, but did reduce the rate of body weight gain throughout the 21 days, whereas chronic multiple stress caused a transient adrenal hypertrophy (on day 14), delayed suppression of thymus weight (on day 21) and transient reduction of body weight gain (on days 7 and 14, but not on day 21). Thus the non-neural indices of response to stress--although complex in their time course--suggest that the multiple stress regimen is a somewhat more potent chronic stressor for corticosterone and adrenal responses. Yet both stress regimens produced the same degree of apical dendritic atrophy in CA3c pyramidal neurons. These results are consistent with a model in which adrenocortical secretion plays a permissive role in enabling another agent, namely, excitatory amino acids, to produce the final effect.
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Regarding chronic stress, habituation occurs to a single stress, and sequential different stresses are required to maintain stress responses.
“Regarding chronic stress, habituation occurs to a single stress, and sequential different stresses are required to maintain stress responses.22,23”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [23]
Cites
Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons
Watanabe, Y., Gould, E., & McEwen, B. S. (1992) · Brain Research · doi:10.1016/0006-8993(92)91597-8 · Cited by 1,212 · see citing works
Self-citationWoolley, C. S., Gould, E., & McEwen, B. S. (1990) · Brain Research · doi:10.1016/0006-8993(90)90778-a · Cited by 1,020 · see citing works
Self-citationMagarin˜os, A. M., & McEwen, B. S. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00259-l · Cited by 863 · see citing works
Self-citationStarkman, M. N., Gebarski, S. S., Berent, S., & Schteingart, D. E. (1992) · Biological Psychiatry · doi:10.1016/0006-3223(92)90079-f · Cited by 840 · 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
Self-citationMelia, K. R., Ryabinin, A. E., Schroeder, R., Bloom, F. E., & Wilson, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-10-05929.1994 · Cited by 359 · see citing works
Phenytoin prevents stress‐ and corticosterone‐induced atrophy of CA3 pyramidal neurons
Watanabe, Y., Gould, E., Cameron, H. A., Daniels, D. C., & McEwen, B. S. (1992) · Hippocampus · doi:10.1002/hipo.450020410 · Cited by 350 · see citing works
Self-citationThe radiologic prediction of Alzheimer disease: the atrophic hippocampal formation.
de Leon, M. J., Golomb, J. B., GEORGE, A. E., Convit, A. J., Tarshish, C. Y., McRae, T., Santi, S. D., Smith, G. S., Ferris, S. H., & Noz, M. E. (1993) · PubMed Central · Cited by 322 · see citing works
Pitman, D. L., Ottenweller, J. E., & Natelson, B. H. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90097-2 · Cited by 295 · see citing works
Chan, R., Brown, E., Ericsson, A., Kovacs, K., & Sawchenko, P. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05126.1993 · Cited by 289 · see citing works
Golomb, J. B., Kluger, A., de Leon, M. J., Ferris, S. H., Convit, A. J., Mittelman, M. S., Cohen, J., Rusinek, H., Santi, S. D., & GEORGE, A. E. (1994) · Learning & Memory · doi:10.1101/lm.1.1.45 · Cited by 198 · see citing works
Hauger, R. L., Lorang, M. T., Irwin, M. R., & Aguilera, G. (1990) · Brain Research · doi:10.1016/0006-8993(90)91738-3 · Cited by 189 · see citing works
Effect of stressor intensity on habituation of the adrenocortical stress response
Natelson, B. H., Ottenweller, J. E., Cook, J. A., Pitman, D. L., McCarty, R. C., & Tapp, W. N. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90096-0 · Cited by 184 · see citing works
The ‘single’ section Golgi-impregnation procedure: methodological description
Gabbott, P. L. A., & Somogyi, J. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90084-0 · Cited by 127 · see citing works
Smith, M. A., Brady, L., Glowa, J., Gold, P., & Herkenham, M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90881-u · Cited by 122 · see citing works
Hippocampal volume losses in minimally impaired elderly.
Convit, A., de Leon, M. D., Tarshish, C., Santi, S. D. D., Kluger, A., Rusinek, H., & George, A. (1995) · The Lancet · doi:10.1016/s0140-6736(95)90265-1 · Cited by 121 · see citing works
Induction and habituation of c-fos and zif/268 by acute and repeated stressors
Watanabe, Y., Stone, E. A., & McEwen, B. S. (1994) · Neuroreport · doi:10.1097/00001756-199406270-00006 · Cited by 103 · see citing works
Self-citationThe glucocorticosterone response to novelty as a psychological stressor
Pfister, H. P. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90154-9 · Cited by 101 · see citing works
Akana, S. F., Jacobson, L., Cascio, C. S., Shinsako, J., & Dallman, M. F. (1988) · Endocrinology · doi:10.1210/endo-122-4-1337 · Cited by 78 · see citing works
Regulation of α and β components of noradrenergic cyclic AMP response in cortical slices
Stone, E. A., McEwen, B. S., Herrera, A. S., & Carr, K. D. (1987) · European Journal of Pharmacology · doi:10.1016/0014-2999(87)90551-6 · Cited by 71 · see citing works
Self-citationGannon, M. N., & McEwen, B. S. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb08849.x · Cited by 43 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
McEwen, B. S. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02950-4 · Cited by 1,827 · see citing works
Self-citationSynaptic plasticity and depression: new insights from stress and rapid-acting antidepressants
Duman, R. S., Aghajanian, G. K., Sanacora, G., & Krystal, J. H. (2016) · Nature Medicine · doi:10.1038/nm.4050 · Cited by 1,750 · see citing works
Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06810.2002 · Cited by 1,662 · see citing works
Hertzog, C., Kramer, A. F., Wilson, R. S., & Lindenberger, U. (2008) · Psychological Science in the Public Interest · doi:10.1111/j.1539-6053.2009.01034.x · Cited by 1,495 · see citing works
Shimizu, E., Hashimoto, K., Okamura, N., Koike, K., Komatsu, N., Kumakiri, C., Nakazato, M., Watanabe, H., Shinoda, N., Okada, S.-I., et al. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00181-1 · Cited by 1,151 · see citing works
Mood disorders and allostatic load
McEwen, B. S. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00177-x · Cited by 1,135 · see citing works
Self-citationThe stress system in the human brain in depression and neurodegeneration
Swaab, D. F., Bao, A.-M., & Lucassen, P. J. (2005) · Ageing Research Reviews · doi:10.1016/j.arr.2005.03.003 · Cited by 984 · see citing works
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864 · see citing works
Self-citationRepeated Stress Induces Dendritic Spine Loss in the Rat Medial Prefrontal Cortex
Radley, J. J., Rocher, A. B., Miller, M., Janssen, W. G. M., Liston, C., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi104 · Cited by 820 · see citing works
Self-citationDendritic Spine Pathology: Cause or Consequence of Neurological Disorders?
Fiala, J. C., Spacek, J., & Harris, K. M. (2002) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00158-3 · Cited by 811 · see citing works
Radley, J. J., Sisti, H. M., Hao, J., Rocher, A. B., McCall, T., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.01.006 · Cited by 769 · see citing works
Self-citationSousa, N., Lukoyanov, N. V., Madeira, M. D., Almeida, O. F. X., & Paula-Barbosa, M. M. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00050-6 · Cited by 758 · see citing works
Sex differences in stress-related psychiatric disorders: neurobiological perspectives
Bangasser, D. A., & Valentino, R. J. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.03.008 · Cited by 737 · see citing works
Glucocorticoids and the regulation of memory consolidation
Roozendaal, B. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00058-x · Cited by 665 · see citing works
Pathogenesis of depression: Insights from human and rodent studies
Ménard, C., Hodes, G. E., & Russo, S. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.053 · Cited by 593 · see citing works
Barlow, D. H., Ellard, K. K., Sauer-Zavala, S., Bullis, J. R., & Carl, J. R. (2014) · Perspectives on Psychological Science · doi:10.1177/1745691614544528 · Cited by 491 · see citing works
Mechanisms of late-onset cognitive decline after early-life stress
Brunson, K. L., Kramár, E., Lin, B., Chen, Y., Colgin, L. L., Yanagihara, T. K., Lynch, G., & Baram, T. Z. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2281-05.2005 · Cited by 479 · see citing works
Chronic Stress-induced Hippocampal Vulnerability: The Glucocorticoid Vulnerability Hypothesis
Conrad, C. D. (2008) · Reviews in the Neurosciences · doi:10.1515/revneuro.2008.19.6.395 · Cited by 425 · see citing works
Restraint stress in biobehavioral research: Recent developments
Buynitsky, T., & Mostofsky, D. I. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.004 · Cited by 426 · see citing works
Ivy, A. S., Rex, C. S., Chen, Y., Dubé, C., Maras, P. M., Grigoriadis, D. E., Gall, C. M., Lynch, G., & Baram, T. Z. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1784-10.2010 · Cited by 402 · see citing works
Neural control of chronic stress adaptation
Herman, J. P. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00061 · Cited by 384 · see citing works
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381 · see citing works
Effects of Chronic Stress on Structure and Cell Function in Rat Hippocampus and Hypothalamus
Joëls, M., Karst, H., Alfarez, D., Heine, V. M., Qin, Y., Riel, E. V., Verkuyl, M., Lucassen, P. J., & Krugers, H. J. (2004) · Stress · doi:10.1080/10253890500070005 · Cited by 330 · see citing works
Structural and synaptic plasticity in stress-related disorders
Christoffel, D. J., Golden, S. A., & Russo, S. J. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.044 · Cited by 334 · see citing works
Magariños, A. M., Deslandes, A., & McEwen, B. S. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00163-6 · Cited by 330 · see citing works
Self-citationZohar, J., Yahalom, H., Kozlovsky, N., Cwikel-Hamzany, S., Matar, M. A., Kaplan, Z., Yehuda, R., & Cohen, H. (2011) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2011.06.001 · Cited by 292 · see citing works
Regulation of hippocampal H3 histone methylation by acute and chronic stress
Hunter, R. G., McCarthy, K. J., Milne, T. A., Pfaff, D. W., & McEwen, B. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911143106 · Cited by 290 · see citing works
Self-citationStress, anxiety, and dendritic spines: What are the connections?
Leuner, B., & Shors, T. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.021 · Cited by 284 · see citing works
An excitatory synapse hypothesis of depression
Thompson, S. M., Kallarackal, A. J., Kvarta, M. D., Van Dyke, A. M., LeGates, T. A., & Cai, X. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.03.003 · Cited by 265 · see citing works
Spine synapse remodeling in the pathophysiology and treatment of depression
Duman, C. H., & Duman, R. S. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.01.022 · Cited by 257 · see citing works
Karatsoreos, I. N., Bhagat, S. M., Bowles, N. P., Weil, Z. M., Pfaff, D. W., & McEwen, B. S. (2010) · Endocrinology · doi:10.1210/en.2009-1436 · Cited by 260 · see citing works
Self-citationChen, Y., Rex, C. S., Rice, C. J., Dubé, C. M., Gall, C. M., Lynch, G., & Baram, T. Z. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003825107 · Cited by 256 · see citing works
Neighborhood matters: divergent patterns of stress-induced plasticity across the brain
Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4115 · Cited by 248 · see citing works
Stress, depression and Parkinson's disease
Hemmerle, A. M., Herman, J. P., & Seroogy, K. B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.09.035 · Cited by 225 · see citing works
Sex differences in spatial and non-spatial Y-maze performance after chronic stress
Conrad, C. D., Grote, K. A., Hobbs, R. J., & Ferayorni, A. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(02)00018-7 · Cited by 215 · see citing works
Inoculation stress hypothesis of environmental enrichment.
Crofton, E. J., Zhang, Y., & Green, T. A. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.017 · Cited by 206 · see citing works
Stewart, M. G., Davies, H. A., Sandi, C., Kraev, I. V., Rogachevsky, V. V., Peddie, C. J., Rodriguez, J. J., Cordero, M. I., Donohue, H. S., Gabbott, P. L. A., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.10.031 · Cited by 197 · see citing works
The neurobiology and neuroendocrinology of stress
McEwen, B. S. (2002) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(01)00009-0 · Cited by 184 · see citing works
Self-citationEpigenetic mechanisms of major depression: Targeting neuronal plasticity
Uchida, S., Yamagata, H., Seki, T., & Watanabe, Y. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12621 · Cited by 181 · see citing works
Induction of cyclooxygenase-2 accounts for restraint stress-induced oxidative status in rat brain
Madrigal, J. L. M., Moro, M. A., Lizasoain, I., Lorenzo, P., Fernández, A. P., Rodrigo, J., Boscá, L., & Leza, J. C. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300187 · Cited by 155 · see citing works
Soetanto, A., Wilson, R. S., Talbot, K., Un, A., Schneider, J. A., Sobiesk, M., Kelly, J., Leurgans, S., Bennett, D. A., & Arnold, S. E. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.48 · Cited by 148 · see citing works
Donohue, H. S., Gabbott, P. L. A., Davies, H. A., Rodríguez, J. J., Cordero, M. I., Sandi, C., Medvedev, N. I., Popov, V. I., Colyer, F. M., Peddie, C. J., et al. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.072 · Cited by 139 · see citing works
Adding fuel to the fire: the impact of stress on the ageing brain
Prenderville, J. A., Kennedy, P. J., Dinan, T. G., & Cryan, J. F. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2014.11.001 · Cited by 136 · see citing works
Hains, A. B., & Arnsten, A. F. T. (2008) · Learning & Memory · doi:10.1101/lm.921708 · Cited by 127 · see citing works
Lower cortisol levels in depressed patients with comorbid post-traumatic stress disorder
Oquendo, M. A., Echavarria, G., Galfalvy, H. C., Grunebaum, M. F., Burke, A., Barrera, A., Cooper, T. B., Malone, K. M., & John Mann, J. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300050 · Cited by 124 · see citing works
Maras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · 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).”
BackgroundEffect 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
Cunha, G. M. A., Canas, P. M., Oliveira, C. R., & Cunha, R. A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.024 · Cited by 108 · see citing works
Dagytė, G., Van der Zee, E. A., Postema, F., Luiten, P. G. M., Den Boer, J. A., Trentani, A., & Meerlo, P. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.05.053 · Cited by 105 · see citing works
Krugers (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00024 · Cited by 102 · see citing works
Dendritic remodeling of D1 neurons by RhoA/Rho-kinase mediates depression-like behavior
Fox, M. E., Chandra, R., Menken, M. S., Larkin, E. J., Nam, H., Engeln, M., Francis, T. C., & Lobo, M. K. (2020) · Molecular Psychiatry · doi:10.1038/s41380-018-0211-5 · Cited by 100 · see citing works
Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent
Chen, Y., Fenoglio, K. A., Dubé, C. M., Grigoriadis, D. E., & Baram, T. Z. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001863 · Cited by 98 · see citing works
Jett, J. D., Bulin, S. E., Hatherall, L. C., McCartney, C. M., & Morilak, D. A. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.01.017 · Cited by 92 · see citing works
Patel, D., Anilkumar, S., Chattarji, S., & Buwalda, B. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.03.034 · Cited by 93 · see citing works
Kvarta, M. D., Bradbrook, K. E., Dantrassy, H. M., Bailey, A. M., & Thompson, S. M. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00359.2015 · Cited by 86 · see citing works
Stress, Synaptic Plasticity, and Psychopathology
Garcia, R. (2002) · Reviews in the Neurosciences · doi:10.1515/revneuro.2002.13.3.195 · Cited by 81 · see citing works
Datta, D., & Arnsten, A. (2019) · Brain Sciences · doi:10.3390/brainsci9050113 · Cited by 78 · see citing works
Jett, J. D., Boley, A. M., Girotti, M., Shah, A., Lodge, D. J., & Morilak, D. A. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3957-3 · Cited by 75 · see citing works
Grillo, C. A., Piroli, G. G., Rosell, D. R., Hoskin, E. K., Mcewen, B. S., & Reagan, L. P. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00343-9 · Cited by 73 · see citing works
Self-citationRapid Acting Antidepressants in Chronic Stress Models: Molecular and Cellular Mechanisms
Hare, B. D., Ghosal, S., & Duman, R. S. (2017) · Chronic Stress · doi:10.1177/2470547017697317 · Cited by 67 · see citing works
Luo, C., Xu, H., & Li, X.-M. (2004) · Brain Research · doi:10.1016/j.brainres.2004.06.089 · Cited by 66 · see citing works
Karabeg, M. M., Grauthoff, S., Kollert, S. Y., Weidner, M., Heiming, R. S., Jansen, F., Popp, S., Kaiser, S., Lesch, K.-P., Sachser, N., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078238 · Cited by 56 · see citing works
McEwen, B. S. (2004) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2004.6.2/bmcewen · Cited by 54 · see citing works
Self-citationThe dose makes the poison: From glutamate-mediated neurogenesis to neuronal atrophy and depression
Rubio-Casillas, A., & Fernández-Guasti, A. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0066 · Cited by 49 · see citing works
Jett, J. D., & Morilak, D. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2012.216 · Cited by 41 · see citing works
Dagyte, G., Luiten, P. G., De Jager, T., Gabriel, C., Mocaër, E., Den Boer, J. A., & Van der Zee, E. A. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22697 · Cited by 32 · see citing works
Troppoli, T. A., Zanos, P., Georgiou, P., Gould, T. D., Rudolph, U., & Thompson, S. M. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.11.024 · Cited by 29 · see citing works
Lyttle, K., Ohmura, Y., Konno, K., Yoshida, T., Izumi, T., Watanabe, M., & Yoshioka, M. (2015) · Brain Research · doi:10.1016/j.brainres.2015.04.058 · Cited by 26 · see citing works
Deonaraine, K. K., Wang, Q., Cheng, H., Chan, K. L., Lin, H., Liu, K., Parise, L. F., Cathomas, F., Leclair, K. B., Flanigan, M. E., et al. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24724 · Cited by 21 · see citing works
- Authors
- Magarin˜os, A. M., & McEwen, B. S.
- Affiliations
- Rockefeller University (US)
- Corresponding author
- Magarin˜os, A.M.
- ORCID
- McEwen, B.S.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 1995-11
- Volume
- 69
- Issue
- 1
- Pages
- 83-88
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2057658065
- Cited by
- 571
- References
- 21
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 7 · 2023: 14 · 2022: 8 · 2021: 15 · 2020: 22 · 2019: 21 · 2018: 15 · 2017: 19 · 2016: 32 · 2015: 25 · 2014: 23 · 2013: 30 · 2012: 25
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1f05tw004499-01)
- National Institute of Mental Health (MH-41256)
- Fogarty International Center (FO5TWO4499)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- chronic stress, restraint stress, dendritic atrophy, apical dendrites, corticosterone, adrenocortical activation, adrenal hypertrophy, thymic atrophy, weight gain, excitatory amino acids
- MeSH terms
- Animals, Atrophy, Body Weight, Corticosterone, Dendrites, Habituation, Psychophysiologic, Hippocampus, Male, Neurons, Organ Size, Physical Stimulation, Restraint, Physical, Stress, Physiological, Swimming, Time Factors, Rats, Sprague-Dawley, Rats
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 ›
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