Long-term changes in open field behaviour following a single social defeat in rats can be reversed by sleep deprivation
Abstract
The long-term consequences of a single social defeat on open field behaviour in rats were studied, with special emphasis on the time course of stress-induced changes. Animals were subjected to social defeat by placing them into the territory of an aggressive male conspecific for 1 h. After the defeat session experimental animals were returned to their home cage and their own room, receiving no further cues from the resident. Other animals serving as controls were placed in a clean and empty cage for 1 h. Five-minute open field tests were performed on days 1, 2, 7, 14, and 28 after defeat, with independent groups of rats. Locomotion of the animals was recorded and analyzed with an automated video system. Social defeat resulted in a strong subsequent reduction in open field activity, which lasted till at least 7 days after the conflict. Differences in total travelled distance were no longer significant 2 weeks after the conflict. The latency for moving to the outer ring of the open field arena after the start of the test was still significantly longer 4 weeks after defeat. The stress-induced reduction in open field locomotion could be reversed by 12-h sleep deprivation during the resting phase, an intervention known to have antidepressant effects in humans. Possible relevance of the present findings with respect to human affective disorders is discussed.
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 12-hour sleep deprivation applied by a slowly rotating drum reverses the decreased open-field behavior induced by a single social defeat.
“Interestingly, a 12-hour sleep deprivation that is applied by using a slowly rotating drum which minimizes physical stress, but does produce locomotor activity, reversed the decreased open-field behavior induced by a single social defeat.40”
From Protective and damaging effects of stress mediators: central role of the brain (2006) · cites this paper as [40]
Cites
Transduction of psychosocial stress into the neurobiology of recurrent affective disorder
(1992) · American Journal of Psychiatry · doi:10.1176/ajp.149.8.999 · Cited by 1,848 · see citing works
The validity of animal models of depression
Willner, P. (1984) · Psychopharmacology · doi:10.1007/bf00427414 · Cited by 1,415 · see citing works
Katz, R. J., Roth, K. A., & Carroll, B. J. (1981) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(81)90005-1 · Cited by 889 · see citing works
Wu, J. C., & Bunney, W. E. (1990) · American Journal of Psychiatry · doi:10.1176/ajp.147.1.14 · Cited by 614 · see citing works
Heritable variation for aggression as a reflection of individual coping strategies
Benus, R. F., Bohus, B., Koolhaas, J. M., & van Oortmerssen, G. A. (1991) · Cellular and Molecular Life Sciences · doi:10.1007/bf01923336 · Cited by 478 · see citing works
Self-citationDepression: The predisposing influence of stress
Anisman, H., & Zacharko, R. M. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00010633 · Cited by 433 · see citing works
The Flinders sensitive line rats: a genetic animal model of depression
Overstreet, D. H. (1993) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80230-1 · Cited by 369 · see citing works
Sleep-deprivation: Effects on sleep and EEG in the rat
Borb�ly, A. A., & Neuhaus, H. U. (1979) · Journal of Comparative Physiology A · doi:10.1007/bf00663111 · Cited by 284 · see citing works
Enhancement of some 5-HT-dependent behavioural responses following repeated immobilization in rats
Kennett, G. A., Dickinson, S. L., & Curzon, G. (1985) · Brain Research · doi:10.1016/0006-8993(85)90684-5 · Cited by 254 · see citing works
Stress: From synapse to syndrome.
Stanford, S. C., & Salmon, P. J. (1993) · Academic Press eBooks · Cited by 244 · see citing works
(1981) · Springer eBooks · doi:10.1007/978-94-009-8609-1 · Cited by 243 · see citing works
Chapter 6 Neuroendocrine states and behavioral and physiological stress responses
Bohus, B., Benus, R. F., Fokkema, D. S., Koolhaas, J. M., Nyakas, C. J., van Oortmerssen, G. A., Prins, A. J. A., de Ruiter, A. J. H., Scheurink, A. J. W., & Steffens, A. B. (1987) · Progress in brain research · doi:10.1016/s0079-6123(08)60196-x · Cited by 211 · see citing works
Self-citationAnimal Models in Psychopharmacology
Olivier, B., Mos, J., & Slangen, J. L. (1991) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-6419-0 · Cited by 209 · see citing works
Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats
van Dijken, H. H., der Heyden, J. A. M. V., Mos, J., & Tilders, F. J. H. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90117-k · Cited by 202 · see citing works
Raab, A., Dantzer, R., Michaud, B., Mormède, P., Taghzouti, K., Simon, H., & Moal, M. L. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90007-7 · Cited by 198 · see citing works
Multiple neurochemical and behavioral consequences of stressors: Implications for depression
Anisman, H., & Zacharko, R. M. (1990) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(90)90039-5 · Cited by 196 · see citing works
Changes in daily rhythms of body temperature and activity after a single social defeat in rats
Meerlo, P. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02182-5 · Cited by 187 · see citing works
Self-citationAnimal Models in Psychopharmacology
Deakin, J. F. W. (1991) · Behavioural Pharmacology · doi:10.1097/00008877-199112000-00012 · Cited by 187 · see citing works
Behavioural models in psychopharmacology : theoretical, industrial, and clinical perspectives
Willner, P. (1990) · Cambridge University Press eBooks · Cited by 174 · see citing works
Tornatzky, W., & Miczek, K. A. (1994) · Psychopharmacology · doi:10.1007/bf02245339 · Cited by 168 · see citing works
The sleep therapies of depression
Gillin, J. C. (1983) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(83)90123-9 · Cited by 167 · see citing works
Kuhs, H., & Tölle, R. (1991) · Biological Psychiatry · doi:10.1016/0006-3223(91)90255-k · Cited by 124 · see citing works
Depression as a Consequence of Inadequate Neurochemical Adaptation in Response to Stressors
Anisman, H., & Zacharko, R. M. (1992) · The British Journal of Psychiatry · doi:10.1192/s0007125000296669 · Cited by 124 · see citing works
Neurobiology of stress ulcers.
Glavin, G. B., Murison, R. C. C., Overmier, J. B., Paré, W. P., Bakke, H.-K., Henke, P. G., & Hernández, D. E. (1990) · PubMed · Cited by 120 · see citing works
(1990) · Springer eBooks · doi:10.1007/978-94-009-1990-7 · Cited by 115 · see citing works
A chronic stress state in rats: Effects of repeated stress on basal corticosterone and behavior
Ottenweller, J. E., Servatius, R. J., Tapp, W. N., Drastal, S. D., Bergen, M. T., & Natelson, B. H. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90104-a · Cited by 111 · see citing works
(1990) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(90)90484-4 · Cited by 97 · see citing works
Tacrine in Alzheimer's Disease
Eagger, S. A., Morant, N. J., Levy, R., & Sahakian, B. J. (1992) · The British Journal of Psychiatry · doi:10.1192/bjp.160.1.36 · Cited by 95 · see citing works
Koolhaas, J., Hermann, P., Kemperman, C. J. F., Bohus, B., Vandenhoofdakker, R., & Beersma, D. G. M. (1990) · University of Groningen research database (University of Groningen / Centre for Information Technology) · Cited by 91 · see citing works
Self-citationCarli, M., Prontera, C., & SAMANIN, R. (1989) · Neuropharmacology · doi:10.1016/0028-3908(89)90081-6 · Cited by 83 · see citing works
The effect of sleep deprivation and recovery sleep on plasma corticosterone in the rat
Tobler, I., Murison, R. C. C., Ursin, R., Ursin, H., & Borbély, A. A. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90333-6 · Cited by 79 · see citing works
Long-term effects of inescapable stress on daily running activity and antagonism by desipramine
Desan, P. H., Silbert, L. H., & Maier, S. F. (1988) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(88)90420-0 · Cited by 74 · see citing works
On the contribution of sleep wake physiology to the explanation and the treatment of depression
van den Hoofdakker, R. H., & Beersma, D. G. M. (1988) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1988.tb08555.x · Cited by 65 · see citing works
Płaźnik, A., Tamborska, E., Hauptmann, M., Bidziński, A., & Kostowski, W. (1988) · Brain Research · doi:10.1016/0006-8993(88)90972-9 · Cited by 64 · see citing works
Chronobiological Theories of Nonseasonal Affective Disorders and Their Implications for Treatment
van den Hoofdakker, R. H. (1994) · Journal of Biological Rhythms · doi:10.1177/074873049400900206 · Cited by 61 · see citing works
Short and Long Term Physiological and Neurochemical Adaptations to Social Conflict
Miczek, K. A., Thompson, M. L., & Tornatzky, W. (1990) · Springer eBooks · doi:10.1007/978-94-009-1990-7_2 · Cited by 38 · see citing works
Rosellini, R. A., & Widman, D. R. (1989) · Journal of comparative psychology · doi:10.1037/0735-7036.103.4.339 · Cited by 28 · see citing works
George, M. S. (1990) · Neurology · doi:10.1212/wnl.40.6.1015-b · Cited by 26 · see citing works
Circadian effects of escapable and inescapable shock on the food intake and wheelrunning of rats
Bauman, R. A., & Kant, G. J. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90219-r · Cited by 25 · see citing works
Alterations of exploratory patterns induced by uncontrollable shock
Bruto, V., & Anisman, H. (1983) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(83)91368-7 · Cited by 23 · see citing works
Proactive Actions of Psychological Stress on Gastric Ulceration in Rats—Real Psychobiologya
Murison, R. C. C., & Overmier, J. B. (1990) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1990.tb16167.x · Cited by 23 · see citing works
Gonadal Hormones and Sex Differences in Aggression in Rats
van de Poll, N. E., Swanson, H. H., & van Oyen, H. G. (1981) · Springer eBooks · doi:10.1007/978-94-009-8609-1_18 · Cited by 23 · see citing works
Basis of Development of Animal Models in Psychiatry: An Overview
McKinney, W. T. (1989) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-6762-8_1 · Cited by 22 · see citing works
Hernández, D. E., & Glavin, G. B. (1990) · Medical Entomology and Zoology · Cited by 13 · see citing works
Long-Lasting Behavioural Changes after a Single Footshock Stress Session. A Model of Depression?
van Dijken, H. H., der Heyden, J. A. M. V., Mos, J., & Tilders, F. J. H. (1991) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-6419-0_22 · Cited by 9 · see citing works
Flagged first, then by citations
4 of the 50 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
Protective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/bmcewen · Cited by 1,220 · see citing works
“Interestingly, a 12-hour sleep deprivation that is applied by using a slowly rotating drum which minimizes physical stress, but does produce locomotor activity, reversed the decreased open-field behavior induced by a single social defeat.(40)”
BackgroundEthoVision: A versatile video tracking system for automation of behavioral experiments
Noldus, L. P. J. J., Spink, A., & Tegelenbosch, R. A. J. (2001) · Behavior Research Methods, Instruments, & Computers · doi:10.3758/bf03195394 · Cited by 713 · see citing works
Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load
McEwen, B. S. (2006) · Metabolism · doi:10.1016/j.metabol.2006.07.008 · Cited by 624 · see citing works
“Interestingly, a 12-hour sleep deprivation that is applied by using a slowly rotating drum, which minimizes physical stress but does produce locomotor activity, reversed the decreased open field behavior induced by a single social defeat [39].”
BackgroundAnimal models of social stress: Effects on behavior and brain neurochemical systems
Blanchard, R. J., McKittrick, C. R., & Blanchard, D. C. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00449-8 · Cited by 595 · see citing works
Anhedonia and motivational deficits in rats: Impact of chronic social stress
Rygula, R., Abumaria, N., Flügge, G., Fuchs, E., Rüther, E., & Havemann-Reinecke, U. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.009 · Cited by 554 · see citing works
Millan, M. J. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.11.006 · Cited by 549 · see citing works
Social stress, therapeutics and drug abuse: Preclinical models of escalated and depressed intake
MICZEK, K., YAP, J., & COVINGTONIII, H. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.07.006 · Cited by 338 · see citing works
The temporal dynamics of the stress response
Koolhaas, J. M., Meerlo, P., de Boer, S. F., STRUBBE, J. H., & Bohus, B. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00057-7 · Cited by 331 · see citing works
Self-citationLong-term effects of social stress on brain and behavior: a focus on hippocampal functioning
Buwalda, B., Kole, M. H. P., Veenema, A. H., Huininga, M., de Boer, S. F., Korte, S. M., & Koolhaas, J. M. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.05.005 · Cited by 304 · see citing works
“Sleep deprivation [27,59], antidepressant drugs like clomipramine [27,54,60], imipramine [52,53] and fluoxetine [31] as well as social interaction [47–49] prevented many of the consequences of social stress.”
BackgroundSelf-citationBehavioral animal models of depression
Yan, H., Cao, X., Das, M. K., Zhu, X., & Gao, T. (2010) · Neuroscience Bulletin · doi:10.1007/s12264-010-0323-7 · Cited by 298 · see citing works
“[57] Meerlo P, Overkamp GJ, Benning MA, Koolhaas JM, Van den Hoofdakker RH.”
Social Defeat as an Animal Model for Depression
Hollis, F., & Kabbaj, M. (2014) · ILAR Journal · doi:10.1093/ilar/ilu002 · Cited by 270 · see citing works
Ruis, M. A. W., Brake, J. H. A. T., Buwalda, B., de Boer, S. F., Meerlo, P., Korte, S. M., Blokhuis, H. J., & Koolhaas, J. M. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00050-x · Cited by 275 · see citing works
“The retardation of growth may be at least partly due to the fact that food intake may be reduced (Meerlo et al., 1996c, 1997; Willner, 1993).”
BackgroundMethodInfluentialSelf-citationEpigenetic influence of social experiences across the lifespan
Champagne, F. A. (2010) · Developmental Psychobiology · doi:10.1002/dev.20436 · Cited by 273 · see citing works
Sleep restriction alters the hypothalamic-pituitary-adrenal response to stress
Meerlo, P., Koehl, M., Van Der Borght, K., & Turek, F. W. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00790.x · Cited by 250 · see citing works
Self-citationSex differences in the elevated plus-maze test and large open field test in adult Wistar rats.
Knight, P., Chellian, R., Wilson, R., Behnood-Rod, A., Panunzio, S., & Bruijnzeel, A. W. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173168 · Cited by 252 · see citing works
Octopamine and Experience-Dependent Modulation of Aggression in Crickets
Stevenson, P. A., Dyakonova, V. E., Rillich, J., & Schildberger, K. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4258-04.2005 · Cited by 241 · see citing works
“In rodents, social defeat leads to physiological and behavioral changes seen in depressive humans (Meerlo et al., 1996a), which can be reversed by the influence of physical activity or sleep deprivation on aminergic neurotransmission (Meerlo et al., 1996b; Prevot et al., 1996; Mallick et al., 2000;…”
BackgroundThe Influence of Postnatal Handling on Adult Neuroendocrine and Behavioural Stress Reactivity
Meerlo, P., Horvath, Nagy, �., Bohus, & Koolhaas (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00409.x · Cited by 217 · see citing works
Self-citationChanges in Behaviour and Body Weight Following a Single or Double Social Defeat in Rats
Meerlo, P., Overkamp, G. J. F., Daan, S., van den Hoofdakker, R. H., & Koolhaas, J. M. (1996) · Stress · doi:10.3109/10253899609001093 · Cited by 215 · see citing works
Self-citationVadnie, C. A., & McClung, C. A. (2017) · Neural Plasticity · doi:10.1155/2017/1504507 · Cited by 199 · see citing works
“Sleep deprivation also produces antidepressant-like effects in some animal models [316, 317].”
Individual response profiles of male Wistar rats in animal models for anxiety and depression
Ho, Y., Eichendorff, J., & Schwarting, R. K. W. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00089-x · Cited by 189 · see citing works
“These behaviors, however, seem to reflect largely DAergic and cholinergic brain mechanisms in relation to psychomotor activation, novelty responding, motivation, addiction and stress [7,35,42].”
BackgroundEpigenetic Influence of Stress and the Social Environment
Gudsnuk, K. M., & Champagne, F. A. (2012) · ILAR Journal · doi:10.1093/ilar.53.3-4.279 · Cited by 185 · see citing works
Individual Differences and Social Influences on the Neurobehavioral Pharmacology of Abused Drugs
Bardo, M. T., Neisewander, J. L., & Kelly, T. H. (2013) · Pharmacological Reviews · doi:10.1124/pr.111.005124 · Cited by 167 · see citing works
“The decrease in alcohol consumption is consistent with the general suppressant effects that stressors have on ongoing behavior in rats (e.g., Meerlo et al., 1996).”
ResultSocial stress, autonomic neural activation, and cardiac activity in rats
Sgoifo, A., Koolhaas, J. M., de Boer, S. F., Musso, E., Stilli, D., Buwalda, B., & Meerlo, P. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00025-1 · Cited by 160 · see citing works
Self-citationProtective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62128-7 · Cited by 158 · see citing works
Social stress induces high intensity sleep in rats
Meerlo, P., Pragt, B. J., & Daan, S. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00180-8 · Cited by 154 · see citing works
“during the activity phase of the rats, six of the animals were subjected to social defeat by placing them in the cage of an aggressive male conspecific for 1 h [11,12].”
MethodSelf-citationFureix, C., & Meagher, R. K. (2015) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2015.08.036 · Cited by 149 · see citing works
Neuronal Correlates of Depression
Chaudhury, D., Liu, H., & Han, M.-H. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2044-6 · Cited by 139 · see citing works
“SD has been shown to reverse CSD stress-induced anxiety [285] and induce phase shifts in circadian”
BackgroundBerton, O., Durand, M., Aguerre, S., Mormède, P., & Chaouloff, F. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00742-8 · Cited by 139 · see citing works
Buwalda, de Boer, S. F., Schmidt, Felszeghy, Nyakas, Sgoifo, A., der Vegt, V., Tilders, Bohus, & Koolhaas (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00350.x · Cited by 135 · see citing works
Meerlo, P., Sgoifo, A., de Boer, S. F., & Koolhaas, J. M. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.6.1283 · Cited by 127 · see citing works
Self-citationClark, M. S., Sexton, T. J., McClain, M. E., Root, D., Kohen, R., & Neumaier, J. F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04550.2002 · Cited by 119 · see citing works
“The OFT has been used to model “emotionality” or behavioral anxiety in rodents, whose open-field behavior is altered by both stressors and antidepressants (Stockert et al., 1988; Kelly and Leonard, 1994; Pare, 1994; Meerlo et al., 1996; Izumi et al., 1997; Ramos et al., 1997; Durand et al., 1999).”
BackgroundMethodPTSD and stress sensitisation: A tale of brain and body Part 2: Animal models
Stam, R. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.001 · Cited by 114 · see citing works
Automated measurement of spatial preference in the open field test with transmitted lighting
Kulikov, V. A., Tikhonova, M. A., & Kulikov, V. A. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.01.024 · Cited by 113 · see citing works
Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice
Bartolomucci, A., Carola, V., Pascucci, T., Puglisi‐Allegra, S., Cabib, S., Lesch, K., Parmigiani, S., Palanza, P., & Gross, C. T. (2010) · Disease Models & Mechanisms · doi:10.1242/dmm.004614 · Cited by 112 · see citing works
“in 5-HTT+/– mice exposed to psychosocial stress It has been argued that depression of locomotor activity is an animal equivalent of the locomotor disturbances and depressed mood that are observed in depressed human individuals (Bartolomucci et al., 2009a; Fuchs et al., 1996; Meerlo et al., 1996).”
BackgroundHollis, F., Wang, H., Dietz, D., Gunjan, A., & Kabbaj, M. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1869-9 · Cited by 109 · see citing works
“Some of these changes in behavior can be long lasting and persist when the stressor is no longer present (Koolhaas et al. 1997; Meerlo et al. 1996a, b; Ruis et al. 1999).”
BackgroundThe Effects of Social Defeat and Other Stressors on the Expression of Circadian Rhythms
Meerlo, P., Sgoifo, A., & Turek, F. W. (2002) · Stress · doi:10.1080/102538902900012323 · Cited by 111 · see citing works
“Changes in rythmicity were found after a single aggressive confrontation (Meerlo et al., 1996b; Meerlo et al., 1997a; Meerlo et al., 1999) and after repeated conflicts (Tornatzky and Miczek, 1993; Meerlo et al., 1997b).”
BackgroundSelf-citationHollis, F., Duclot, F., Gunjan, A., & Kabbaj, M. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.09.005 · Cited by 107 · see citing works
“, 1996); reduced aggression and sexual behavior (Meerlo et al., 1996); increased submissive behavior and anxiety (Ruis et al.”
Liu, L., Orozco, I. J., Planel, E., Wen, Y., Bretteville, A., Krishnamurthy, P., Wang, L., Herman, M., Figueroa, H. Y., Yu, W. H., et al. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.03.005 · Cited by 108 · see citing works
Citalopram counteracts depressive-like symptoms evoked by chronic social stress in rats
Rygula, R., Abumaria, N., Flügge, G., Hiemke, C., Fuchs, E., Rüther, E., & Havemann-Reinecke, U. (2006) · Behavioural Pharmacology · doi:10.1097/01.fbp.0000186631.53851.71 · Cited by 104 · see citing works
“Also, in rodents, a single social defeat by an aggressive male produces a variety of behavioural and physiological alterations (Koolhaas et al., 1990; Meerlo et al., 1996; Buwalda et al., 1999; Von Frijtag et al., 2000).”
BackgroundMeerlo, P., Overkamp, G. J. F., & Koolhaas, J. M. (1997) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(96)00047-9 · Cited by 102 · see citing works
Self-citationSocial isolation after a single defeat reduces striatal dopamine transporter binding in rats
Isovich, E., Engelmann, M., Landgraf, R., & Fuchs, E. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01492.x · Cited by 96 · see citing works
Novati, A., Hulshof, H. J., Koolhaas, J. M., Lucassen, P. J., & Meerlo, P. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.027 · Cited by 94 · see citing works
“An open field test was performed to assess effects of SR on general explorative activity and anxiety (Meerlo et al., 1996).”
Self-citationBuwalda, B., de Boer, S. F., van Kalkeren, A. A., & Koolhaas, J. M. (1997) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(97)00032-2 · Cited by 89 · see citing works
Self-citationNeisewander, J. L., Peartree, N. A., & Pentkowski, N. S. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2853-3 · Cited by 87 · see citing works
“The decrease in alcohol consumption is consistent with the general suppressant effects that stressors have on ongoing behavior (e.g., Meerlo et al. 1996).”
ResultMeerlo, P., van den Hoofdakker, R. H., Koolhaas, J. M., & Daan, S. (1997) · Journal of Biological Rhythms · doi:10.1177/074873049701200109 · Cited by 86 · see citing works
Self-citationBelda, X., Fuentes, S., Nadal, R. A., & Armario, A. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.07.003 · Cited by 85 · see citing works
“However, long-lasting reduction of activity in different types of openfield tests has been described after electric foot-shock or social defeat (e.g. Meerlo et al., 1996; Stam et al., 2002; Van Dijken et al., 1992a, 1992b, 1992c, 1993).”
The socially stressed heart. Insights from studies in rodents
Sgoifo, A., Carnevali, L., & Grippo, A. J. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.12.005 · Cited by 83 · see citing works
Social environment determines the long-term effects of social defeat
de Jong, J. G., van der Vegt, B. J., Buwalda, B., & Koolhaas, J. M. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.10.013 · Cited by 79 · see citing works
“Following a single defeat, long-term changes in behavior and physiology develop, including changes in body growth, circadian rhythmicity, neuroendocrine functioning and behavioral responses to novel stressors [5,8–15].”
BackgroundSelf-citationGuimarães, A. T. B., Freitas, Í. N., Mubarak, N. M., Rahman, M. M., Rodrigues, F. P., Rodrigues, A. S. D. L., Barceló, ., Islam, A. R. M. T., & Malafaia, G. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.130004 · Cited by 77 · see citing works
Proteomic analysis of rat hippocampus after repeated psychosocial stress
Carboni, L., Piubelli, C., Pozzato, C., Astner, H., Arban, R., Righetti, P. G., Hamdan, M. H., & Domenici, E. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.045 · Cited by 72 · see citing works
Interplay Between Social Experiences and the Genome: Epigenetic Consequences for Behavior
Champagne, F. A. (2012) · Advances in genetics · doi:10.1016/b978-0-12-387687-4.00002-7 · Cited by 72 · see citing works
“As is the case for early life adversity, this manipulation of the adult social environment results in reduced locomotion, social avoidance, and increased HPA activity (Blanchard et al., 1993; Keeney and Hogg, 1999; Meerlo et al., 1996; Raab et al., 1986).”
BackgroundRadwan, B., Liu, H., & Chaudhury, D. (2018) · Brain Research · doi:10.1016/j.brainres.2018.11.031 · Cited by 72 · see citing works
Gao, W., Wang, W., Liu, G., Zhang, J., Yang, J. M., & Deng, Z. (2018) · Metabolic Brain Disease · doi:10.1007/s11011-018-0342-z · Cited by 64 · see citing works
Engler, H., & Stefanski, V. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00117-8 · Cited by 60 · see citing works
Wang, D., Gao, K., Li, X., Shen, X., Zhang, X., Ma, C., Qin, C., & Zhang, L. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.03.013 · Cited by 58 · see citing works
Walker, F. R., Masters, L. M., Dielenberg, R. A., & Day, T. A. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.04.041 · Cited by 58 · see citing works
Marini, F., Pozzato, C., Andreetta, V., Jansson, B., Arban, R., Domenici, E., & Carboni, L. (2005) · Brain Research · doi:10.1016/j.brainres.2005.10.002 · Cited by 57 · see citing works
The responses of growing pigs to a chronic-intermittent stress treatment
Rutherford, K., Haskell, M. J., Glasbey, C. A., & Lawrence, A. B. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.08.006 · Cited by 58 · see citing works
Tilders, F. J. H., & Schmidt, E. D. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09550.x · Cited by 58 · see citing works
Repeated social defeat stress induces chronic hyperthermia in rats
Hayashida, S., Oka, T., Mera, T., & Tsuji, S. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.04.027 · Cited by 57 · see citing works
“In addition to immobility time in the forced swim test, there exist other methods for assessing depressive-like states, such as exploratory activity in an open field [32] or preference for a sucrose solution [27].”
BackgroundMethodFunk, D. R., Vohra, S., & L�, A. D. (2004) · Psychopharmacology · doi:10.1007/s00213-004-1859-x · Cited by 57 · see citing works
The Neurobiology of Depression: Perspectives from Animal and Human Sleep Studies
Shaffery, J. P., Hoffmann, R. F., & Armitage, R. (2003) · The Neuroscientist · doi:10.1177/1073858402239594 · Cited by 54 · see citing works
Subacute manganese exposure in rats is a neurochemical model of early manganese toxicity
O’Neal, S. L., Lee, J., Zheng, W., & Cannon, J. R. (2014) · NeuroToxicology · doi:10.1016/j.neuro.2014.08.001 · Cited by 53 · see citing works
“The duration used in this study, 5 min, is commonly used by other researchers (Meerlo et al., 1996; Pechlivanova et al., 2010; Careau et al., 2012); however it”
García-Pardo, M. P., Blanco-Gandía, M. C., Valiente-Lluch, M., Rodríguez‐Arias, M., Miñarro, J., & Aguilar, M. A. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.06.006 · Cited by 53 · see citing works
Acute Social Defeat Stress Increases Sleep in Mice
Fujii, S., Kaushik, M. K., Zhou, X., Korkutata, M., & Lazarus, M. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00322 · Cited by 50 · see citing works
Gandhi, W., Becker, S., & Schweinhardt, P. (2013) · European Journal of Pain · doi:10.1002/j.1532-2149.2012.00281.x · Cited by 51 · see citing works
“Animals exposed to single (Meerlo et al., 1996) or repeated defeat (Rygula et al.”
BackgroundRegion-specific alteration in brain glutamate: Possible relationship to risk-taking behavior
Cortese, B. M., Mitchell, T. R., Galloway, M. P., Prevost, K. E., Fang, J., Moore, G. J., & Uhde, T. W. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.12.005 · Cited by 50 · see citing works
Total sleep deprivation decreases immobility in the forced-swim test
Lopez-Rodriguez, F., Kim, J., & Poland, R. E. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300406 · Cited by 49 · see citing works
“In one study, rats were sleep deprived by placing them in a slowly rotating cylinder, an intervention that reversed the effects of social defeat on open field behavior (Meerlo et al, 1996).”
BackgroundWinner–loser effects overrule aggressiveness during the early stages of contests between pigs
Oldham, L., Camerlink, I., Arnott, G., Doeschl-Wilson, A. B., Farish, M., & Turner, S. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-69664-x · Cited by 46 · see citing works
Kamphuis, J., Lancel, M., Koolhaas, J. M., & Meerlo, P. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.12.022 · Cited by 41 · see citing works
“Moreover, the experience of defeat in a social conflict is a rather dramatic event associated with behavioral and physiological changes that can last for several days up to weeks after the conflict (Meerlo et al., 1996a,b; Miczek et al., 1990).”
BackgroundSelf-citationMontagud‐Romero, S., Montesinos, J., Pascual, M., Aguilar, M. A., Roger-Sánchez, C., Guerri, C., Miñarro, J., & Rodríguez‐Arias, M. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.04.016 · Cited by 42 · see citing works
“…such as decreased aggression and sexual behaviors (Meerlo et al., 1996; García-Pardo et al., 2015), locomotor activity (Koolhaas et al., 1997;Meerlo et al., 1996), anhedonia (Rygula et al., 2005), heightened defensive/submissive behaviors, anxiety and impaired learning (Ruis et al., 1999;…”
BackgroundIezhitsa, I. N., Спасов, А. А., Kharitonova, M. V., & Кравченко, М. С. (2011) · Nutritional Neuroscience · doi:10.1179/174313211x12966635733277 · Cited by 40 · see citing works
Clinard, C. T., Bader, L. R., Sullivan, M. A., & Cooper, M. A. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.016 · Cited by 42 · see citing works
“Social stress has been shown to reduce locomotion in an open-field (Bader et al., 2014; Meerlo et al., 1996; Raab et al., 1986), and anxiolytic drugs such as diazepam have been shown to reverse the stress-induced reduction in locomotion (Carli et al., 1989).”
BackgroundRazzoli, M., Roncari, E., Guidi, A., Carboni, L., Arban, R., Gerrard, P., & Bacchi, F. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.03.007 · Cited by 39 · see citing works
Swim stress triggers the release of vasopressin within the suprachiasmatic nucleus of male rats
Engelmann, M., Ebner, K., Landgraf, R., & Wotjak, C. T. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00243-1 · Cited by 39 · see citing works
A single social defeat transiently suppresses the anti-viral immune response in mice
de Groot, J., van Milligen, F. J., Moonen-Leusen, B., Thomas, G., & Koolhaas, J. M. (1999) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(99)00005-3 · Cited by 39 · see citing works
Self-citationRazzoli, M., Carboni, L., & Arban, R. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.04.018 · Cited by 38 · see citing works
Social stress-induced hypothyroidism is attenuated by antidepressant treatment in rats
Olivares, E. L., Almeida, C. D. S., Pestana, F. M., Sonoda‐Côrtes, R., Araujo, I. G., Rodrigues, N. C., Mecawi, A. S., Côrtes, W. D. S., Marassi, M. P., Reis, L. C., et al. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.035 · Cited by 36 · see citing works
“Although some works have demonstrated behavioral effects of acute social defeat exposure (Meerlo et al., 1996; Berton et al., 1999), only recently the effects of repeated social defeat exposure have been more explored.”
Neurobiology of the metabolic syndrome: An allostatic perspective
van Dijk, G., & Buwalda, B. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.079 · Cited by 37 · see citing works
“They showed long-term deterioration of mood (Meerlo et al., 1996), and displayed a reduced performance in a so-called novel object recognition paradigm (van Dijk and Buwalda, unpublished observation).”
BackgroundKinn, A. M., Grønli, J., Fiske, E., Kuipers, S. D., Ursin, R., Murison, R. C. C., & Portas, C. M. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.07.031 · Cited by 36 · see citing works
“This was surprising because socially defeated rats have earlier shown decreased activity after a single exposure to the open field [25], an effect seen one, two and seven days after a single social defeat (different animals were used each day to prevent habituation).”
BackgroundMethodErschbamer, M., Pham, T. M., Zwart, M., Baumans, V., & Olson, L. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.04.003 · Cited by 34 · see citing works
Effects of Social Stress on Hormones, Brain, and Behavior
Blanchard, D. C., McKittrick, C. R., Blanchard, R. J., & Hardy, M. P. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50015-9 · Cited by 33 · see citing works
Wang, D., Li, X., Gao, K., Lü, D., Zhang, X., Ma, C., Ye, F., & Zhang, L. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.03.003 · Cited by 32 · see citing works
“The amount of time spent in the peripheral zone is a manifestation of thigmotaxis (Meerlo et al., 1996).”
BackgroundRød, A. M. K., Milde, A. M., Grønli, J., Jellestad, F. K., Sundberg, H., & Murison, R. C. C. (2012) · Stress · doi:10.3109/10253890.2012.663836 · Cited by 32 · see citing works
Vidal, J., Buwalda, B., & Koolhaas, J. M. (2011) · Behavioural Processes · doi:10.1016/j.beproc.2011.03.004 · Cited by 28 · see citing works
Self-citationPrepubertal Social Subjugation and Anabolic Androgenic Steroid‐Induced Aggression in Male Rats
Cunningham, R. L., & McGinnis, M. Y. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01756.x · Cited by 26 · see citing works
Holubová, K., Nekovářová, T., Pistovčáková, J., Šulcová, A., Stuchlík, A. (., & Valeš, K. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00130 · Cited by 26 · see citing works
“Among the most often noted behavioral responses is the decrease in activity and exploration in the open field (Meerlo et al., 1996; Rygula et al., 2005; Razzoli et al., 2009).”
BackgroundHarvey, M. L., Swallows, C. L., & Cooper, M. A. (2012) · Behavioral Neuroscience · doi:10.1037/a0029047 · Cited by 25 · see citing works
Parrish, J. B., & Teske, J. A. (2016) · Obesity · doi:10.1002/oby.21703 · Cited by 24 · see citing works
“12 h) (22,23), or gentle handling (4–6 h) (24,25).”
ResultShimozuru, M., Kikusui, T., Takeuchi, Y., & Mori, Y. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.05.018 · Cited by 24 · see citing works
Aggressive and Sexual Social Stimuli Do not Phase Shift the Orcadian Temperature Rhythm in Rats
Meerlo, P., & Daan, S. (1998) · Chronobiology International · doi:10.3109/07420529808998686 · Cited by 23 · see citing works
Self-citationPsychosocial stress alters ethanol's effect on open field behaviors
Blakley, G. G., & Pohorecky, L. A. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.04.005 · Cited by 22 · see citing works
Risk assessment and avoidance in juvenile golden hamsters exposed to repeated stress
Bastida, C. C., Puga, F., & Delville, Y. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.09.009 · Cited by 19 · see citing works
SUMNER, B. E. H., D’Eath, R. B., Farnworth, M. J., Robson, S. K., Russell, J. A., Lawrence, A. B., & Jarvis, S. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.05.004 · Cited by 17 · see citing works
Khoswanto, C. (2019) · European Journal of Dentistry · doi:10.1055/s-0039-1694312 · Cited by 17 · see citing works
5-HT1A receptor activation reduces fear-related behavior following social defeat in Syrian hamsters
Bader, L. R., Carboni, J. D., Burleson, C. A., & Cooper, M. A. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2014.03.024 · Cited by 17 · see citing works
“…behavior in the elevated plus maze (Heinrichs et al., 1992; Berton et al., 1998), altered circadian rhythmicity (Tornatzky and Miczek, 1993; Meerlo et al., 1996a), reduced body weight (Bartolomucci et al., 2004; Iio et al., 2012), and reduced locomotor activity (Rygula et al., 2005; amily…”
Stress and Aggressive Behaviors
Blanchard, D. C., & Blanchard, R. J. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195168761.003.0012 · Cited by 17 · see citing works
Effects of social defeat on sleep and behaviour: Importance of the confrontational behaviour
Rød, A. M. K., Murison, R. C. C., Mrdalj, J., Milde, A. M., Jellestad, F. K., Øvernes, L. A., & Grønli, J. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.01.010 · Cited by 16 · see citing works
Social Stress Effects on Hormones, Brain, and Behavior
McKittrick, C. R., Blanchard, D. C., Hardy, M. P., & Blanchard, R. J. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00009-7 · Cited by 14 · see citing works
- Authors
- Meerlo, P., Overkamp, G. J. F., Benning, M. A., Koolhaas, J. M., & Van Den Hoofdakker, R. H.
- Affiliations
- University of Groningen (NL)
- Corresponding author
- Meerlo, P.
- ORCID
- Meerlo, P.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1996-07
- Volume
- 60
- Issue
- 1
- Pages
- 115-119
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2032960831
- Cited by
- 151
- References
- 50
- Citations by year
- 2025: 2 · 2023: 1 · 2022: 7 · 2021: 2 · 2020: 3 · 2019: 3 · 2018: 6 · 2017: 2 · 2016: 7 · 2015: 7 · 2014: 12 · 2013: 6 · 2012: 9
- FWCI
- 3.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- social defeat, sleep deprivation, open field behavior, locomotor activity, stress, antidepressant effects, mood disorders, rats, territorial aggression
- MeSH terms
- Affect, Aggression, Agonistic Behavior, Animals, Arousal, Dominance-Subordination, Exploratory Behavior, Male, Motor Activity, Rats, Inbred Strains, Reaction Time, Sleep Deprivation, 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 ›
Are you an author, or do you see a problem with this page? Request a review
