Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats
Open accessAbstract
Early life stressors in rodents, including maternal separation and social isolation, have been shown to disrupt brain development and profoundly affect a wide-range of behaviors in adult animals. In this study, we focus on the development of female Sprague-Dawley rats in the presence and absence of conspecifics during the critical period of social play. Similar studies in male rodents have shown that this form of social deprivation results in dysregulated dopaminergic and serotonergic functions in the brain with core features of neuropsychiatric disorders including anxiety disorder and schizophrenia. Here we examined the behavioral and biochemical effects of post-weaning social isolation in female rats. Our findings demonstrated that isolation rearing produced marked deficits in social interaction behaviors and increased anxiety in open-field and novelty-suppressed feeding tests. The expression of synaptic-associated proteins PSD95 and synapsin I as well as glutamate receptors subunits GluR1 and NR1 in the prefrontal cortex (PFC) were significantly reduced in isolation-reared female rats. Current findings provide evidence that in female rats, post-weaning environmental disruption can result in profound dysregulation of synapse-related proteins and behavior.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A study in females found that isolation from P19-70 also decreases sociability.
“This finding was mirrored by a study in females which found that isolation from P19–70 also decreases sociability (Hermes et al., 2011).”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Hermes et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants
Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., et al. (2003) · Science · doi:10.1126/science.1083328 · Cited by 4,321 · see citing works
Self-citationmTOR-Dependent Synapse Formation Underlies the Rapid Antidepressant Effects of NMDA Antagonists
Li, N., Lee, B., Liu, R.-J., Banasr, M., Dwyer, J. M., Iwata, M., Li, X.-Y., Aghajanian, G., & Duman, R. S. (2010) · Science · doi:10.1126/science.1190287 · Cited by 2,881 · see citing works
Self-citationImpairment of social and moral behavior related to early damage in human prefrontal cortex
Anderson, S. W., Bechara, A., Damasio, H., Tranel, D., & Damasio, A. R. (1999) · Nature Neuroscience · doi:10.1038/14833 · Cited by 1,539 · see citing works
Fone, K. C. F., & Porkess, M. V. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.003 · Cited by 864 · see citing works
A review of 25 years of the social interaction test
File, S. E., & Seth, P. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01273-1 · Cited by 744 · see citing works
Chaddock, L., Erickson, K. I., Prakash, R. S., Kim, J. S., Voss, M. W., VanPatter, M., Pontifex, M. B., Raine, L. B., Konkel, A., Hillman, C. H., et al. (2010) · Brain Research · doi:10.1016/j.brainres.2010.08.049 · Cited by 687 · see citing works
The neurobiology of social play behavior in rats
Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00020-6 · Cited by 559 · see citing works
A developmental change in NMDA receptor-associated proteins at hippocampal synapses
Sans, N., Petralia, R. S., Wang, Y.-X., Blahos, J., Hell, J. W., & Wenthold, R. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-03-01260.2000 · Cited by 537 · see citing works
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · see citing works
The oestrous cycle in the rat and its associated phenomena
Long, J. A., & Evans, H. M. (1922) · Medical Entomology and Zoology · Cited by 536 · see citing works
Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat
Weiss, I. C., Pryce, C. R., Jongen-Rêlo, A. L., Nanz-Bahr, N. I., & Feldon, J. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.10.015 · Cited by 512 · cited 1× · see citing works
“Other psychopathological disturbances associated with social isolation include hoarding [3] and anxiety [4].”
BackgroundOvarian steroids and the brain
McEwen, B. S., Alves, S. E., Bulloch, K., & Weiland, N. G. (1997) · Neurology · doi:10.1212/wnl.48.5_suppl_7.8s · Cited by 482 · see citing works
VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants
Warner-Schmidt, J. L., & Duman, R. S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610282104 · Cited by 438 · see citing works
Self-citationHeidbreder, C. A., Weiss, I. C., Domeney, A. M., Pryce, C., Homberg, J., Hedou, G., Feldon, J., Moran, M. C., & Nelson, P. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00336-5 · Cited by 404 · see citing works
A critical period for social isolation in the rat
Einon, D. F., & Morgan, M. J. (1977) · Developmental Psychobiology · doi:10.1002/dev.420100205 · Cited by 342 · see citing works
Tracking the estrogen receptor in neurons: Implications for estrogen-induced synapse formation
McEwen, B. S., Akama, K. T., Alves, S. E., Brake, W. G., Bulloch, K., Lee, S. D., Li, C., Yuen, G. S., & Milner, T. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.121146898 · Cited by 311 · see citing works
Developmental outcomes after early prefrontal cortex damage
Eslinger, P. J., Flaherty-Craig, C. V., & Benton, A. L. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00281-1 · Cited by 233 · see citing works
Bodnoff, S. R., Suranyi-Cadotte, B., Quirion, R., & Meaney, M. J. (1989) · Psychopharmacology · doi:10.1007/bf00442264 · Cited by 221 · see citing works
Isolation during the play period in infancy decreases adult social interactions in rats
Hol, T., Van den Berg, C. L., Van Ree, J. M., & Spruijt, B. M. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00116-8 · Cited by 212 · see citing works
Schneider, M., & Koch, M. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300634 · Cited by 160 · see citing works
The Phases of the Oestrous Cycle in the Adult White Rat
Mandl, A. M. (1951) · Journal of Experimental Biology · doi:10.1242/jeb.28.4.576 · Cited by 154 · see citing works
Brain Sex Differences and the Organisation of Juvenile Social Play Behaviour
Auger, A. P., & Olesen, K. M. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01871.x · Cited by 142 · see citing works
Day-Wilson, K. M., Jones, D. N. C., Southam, E., Cilia, J., & Totterdell, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.048 · Cited by 129 · see citing works
Meaney, M. J., & McEwen, B. S. (1986) · Brain Research · doi:10.1016/0006-8993(86)91492-7 · Cited by 122 · see citing works
Jelks, K. B., Wylie, R., Floyd, C. L., McAllister, A. K., & Wise, P. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0909-07.2007 · Cited by 111 · see citing works
Zhao, X., Sun, L., Jia, H., Meng, Q., Wu, S., Li, N., & He, S. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.06.016 · Cited by 105 · see citing works
Self-citationMelendez, R. I., Lee Gregory, M., Bardo, M. T., & Kalivas, P. W. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300507 · Cited by 104 · see citing works
Varty, G. B., Marsden, C. A., & Higgins, G. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01173-7 · Cited by 90 · see citing works
Levine, J. B., Youngs, R. M., MacDonald, M. L., Chu, M. S., Leeder, A., Francois Berthiaume, B., & Konradi, C. L. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.11.063 · Cited by 81 · see citing works
An environmental antiandrogen, vinclozolin, alters the organization of play behavior
Hotchkiss, A. K., Ostby, J. S., Vandenbergh, J. G., & Gray, L. E. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00093-3 · Cited by 77 · see citing works
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.2.275 · Cited by 73 · see citing works
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.275 · Cited by 73 · see citing works
Casto, J., Ward, O., & Bartke, A. (2003) · Physiology and Behavior · doi:10.1016/s0031-9384(03)00120-3 · Cited by 64 · see citing works
Peri-adolescence isolation rearing alters social behavior and nociception in rats
Meng, Q., Li, N., Xiao, H., Shao, F., & Wang, W. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.05.067 · Cited by 59 · see citing works
Self-citationA sensitive period for environmental regulation of eating behavior and leptin sensitivity
Mainardi, M., Scabia, G., Vottari, T., Santini, F., Pinchera, A., Maffei, L., Pizzorusso, T., & Maffei, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911832107 · Cited by 54 · see citing works
The effects of stress on play and home cage behaviors in adolescent male rats
Klein, Z. A., Padow, V. A., & Romeo, R. D. (2009) · Developmental Psychobiology · doi:10.1002/dev.20413 · Cited by 51 · see citing works
Li, N., Ping, J., Wu, R., Wang, C., Wu, X. H., & Li, L. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.1.107 · Cited by 44 · see citing works
Self-citationEating behavior: Social facilitation or social inhibition?
Shelley, H. P. (1965) · Psychonomic Science · doi:10.3758/bf03343264 · Cited by 40 · see citing works
Hall, F. S., Ghaed, S., Pert, A., & Xing, G. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00796-7 · Cited by 32 · see citing works
Bianchi, M., Fone, K. C. F., Shah, A. J., Atkins, A. R., Dawson, L. A., Heidbreder, C. A., Hagan, J. J., & Marsden, C. A. (2009) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2009.06.005 · Cited by 29 · see citing works
Tönjes, R., Döcke, F., & Dörner, G. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1210699 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sex differences in anxiety and emotional behavior
Donner, N. C., & Lowry, C. A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1271-7 · Cited by 379 · see citing works
Neurobiology and consequences of social isolation stress in animal model—A comprehensive review
Mumtaz, F., Khan, M. I., Zubair, M., & Dehpour, A. R. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.05.086 · Cited by 369 · see citing works
Animal models of social avoidance and social fear
Toth, I., & Neumann, I. D. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1636-4 · Cited by 275 · see citing works
A Role for Estrogen in Schizophrenia: Clinical and Preclinical Findings
Gogos, A., Sbisa, A. M., Sun, J., Gibbons, A. S., Udawela, M., & Dean, B. (2015) · International Journal of Endocrinology · doi:10.1155/2015/615356 · Cited by 232 · see citing works
Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
Understanding stress: Insights from rodent models
Atrooz, F., Alkadhi, K. A., & Salim, S. (2021) · Current Research in Neurobiology · doi:10.1016/j.crneur.2021.100013 · Cited by 201 · see citing works
Sarkar, A., & Kabbaj, M. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.025 · Cited by 133 · see citing works
Jiang, Z., Rompala, G. R., Zhang, S., Cowell, R. M., & Nakazawa, K. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.12.004 · Cited by 128 · see citing works
de Bartolomeis, A., Latte, G., Tomasetti, C., & Iasevoli, F. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8534-3 · Cited by 126 · see citing works
Wall, V. L., Fischer, E. K., & Bland, S. T. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.09.002 · Cited by 123 · see citing works
Deletion of Glutamate Delta-1 Receptor in Mouse Leads to Aberrant Emotional and Social Behaviors
Yadav, R., Gupta, S. C., Hillman, B. G., Bhatt, J. M., Stairs, D. J., & Dravid, S. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032969 · Cited by 123 · see citing works
Environmental programming of susceptibility and resilience to stress in adulthood in male mice
Peña, C. J., Nestler, E. J., & Bagot, R. C. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00040 · Cited by 97 · see citing works
Acute d-serine treatment produces antidepressant-like effects in rodents
Malkesman, O., Austin, D. R., Tragon, T. R., Wang, G., Rompala, G. R., Hamidi, A., Cui, Z., Young, W. S., Nakazawa, K., Zarate, C. A., et al. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001386 · Cited by 91 · see citing works
Schneider, P., Bindila, L., Schmahl, C., Bohus, M., Meyer-Lindenberg, A., Lutz, B., Spanagel, R., & Schneider, M. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00203 · Cited by 89 · see citing works
Yamamuro, K., Yoshino, H., Ogawa, Y., Makinodan, M., Toritsuka, M., Yamashita, M., Corfas, G., & Kishimoto, T. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhx010 · Cited by 86 · see citing works
Social isolation in rats: effects on animal welfare and molecular markers for neuroplasticity
Begni, V., Sanson, A., Pfeiffer, N., Brandwein, C., Inta, D., Talbot, S. R., Riva, M. A., Gass, P., & Mallien, A. S. (2020) · PLOS ONE · doi:10.1371/journal.pone.0240439 · Cited by 78 · see citing works
Play fighting and the development of the social brain: The rat’s tale
Pellis, S. M., Pellis, V. C., Ham, J. R., & Stark, R. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105037 · Cited by 76 · see citing works
Concordance and incongruence in preclinical anxiety models: Systematic review and meta-analyses
Mohammad, F., Ho, J., Woo, J. H., Lim, C. L., Poon, D., Lamba, B., & Claridge‐Chang, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.04.011 · Cited by 73 · see citing works
Duarte, J. M. N., & Xin, L. (2018) · Neurochemical Research · doi:10.1007/s11064-018-2521-z · Cited by 69 · see citing works
Aberrant H3.3 dynamics in NAc promote vulnerability to depressive-like behavior
Lepack, A. E., Bagot, R. C., Peña, C. J., Loh, Y.-H. E., Farrelly, L. A., Lu, Y., Powell, S. K., Lorsch, Z. S., Issler, O., Cates, H. M., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1608270113 · Cited by 63 · see citing works
Butler, T. R., Carter, E., & Weiner, J. L. (2014) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12476 · Cited by 63 · see citing works
The neuropeptide Pth2 dynamically senses others via mechanosensation
Anneser, L., Alcantara, I. C., Gemmer, A., Mirkes, K., Ryu, S., & Schuman, E. M. (2020) · Nature · doi:10.1038/s41586-020-2988-z · Cited by 60 · see citing works
Möller, M., Swanepoel, T., & Harvey, B. H. (2015) · ACS Chemical Neuroscience · doi:10.1021/cn5003368 · Cited by 59 · see citing works
Connors, E. J., Migliore, M. M., Pillsbury, S. L., Shaik, A. N., & Kentner, A. C. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.10.021 · Cited by 60 · see citing works
Leading compounds for the validation of animal models of psychopathology
Micale, V., Kučerová, J., & Šulcová, A. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1692-9 · Cited by 57 · see citing works
Jensen Peña, C., & Champagne, F. A. (2013) · Behavioral Neuroscience · doi:10.1037/a0031219 · Cited by 54 · see citing works
Gilabert‐Juan, J., Bellés, M., Sáez-Ibáñez, A. R., Carceller, H., Zamarbide-Forés, S., Moltó, M. D., & Nácher, J. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.07.008 · Cited by 53 · see citing works
Hong, Y.-P., Lee, H.-C., & Kim, H.-T. (2015) · Physical Activity and Nutrition · doi:10.5717/jenb.2015.19.1.11 · Cited by 52 · see citing works
Effects of social isolation on growth, stress response, and immunity of zebrafish
Forsatkar, M. N., Safari, O., & Boiti, C. (2017) · acta ethologica · doi:10.1007/s10211-017-0270-7 · Cited by 52 · see citing works
Post-weaning social isolation of female rats, anxiety-related behavior, and serotonergic systems
Lukkes, J. L., Engelman, G. H., Zelin, N. S., Hale, M. W., & Lowry, C. A. (2012) · Brain Research · doi:10.1016/j.brainres.2012.01.005 · Cited by 47 · see citing works
Neis, V. B., Bettio, L. E. B., Moretti, M., da Rosa, P. B., Ribeiro, C. M., Freitas, A. E., Gonçalves, F. M., Leal, R. B., & Rodrigues, A. L. S. (2016) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2016.10.004 · Cited by 44 · see citing works
Modulation of behavior by scaffolding proteins of the post-synaptic density
Gao, C., Tronson, N. C., & Radulović, J. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.04.014 · Cited by 41 · see citing works
Analysis of c-Fos induction in response to social interaction in male and female Fisher 344 rats
Perkins, A. E., Woodruff, E. R., Chun, L. E., Spencer, R. L., Varlinskaya, E. I., & Terrence Deak, B. (2017) · Brain Research · doi:10.1016/j.brainres.2017.07.022 · Cited by 37 · see citing works
Millard, S. J., Lum, J. S., Fernandez, F., Weston–Green, K., & Newell, K. A. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881118822141 · Cited by 36 · see citing works
Social isolation produces anxiety-like behaviors and changes PSD-95 levels in the forebrain
Zhang, Y., Zu, X., Luo, W., Yang, H., Luo, G., Zhang, M., & Tang, S. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.02.043 · Cited by 35 · see citing works
The Role of the N-Methyl-D-Aspartate Receptors in Social Behavior in Rodents
Zoicas, I., & Kornhuber, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225599 · Cited by 34 · see citing works
Tendilla‐Beltrán, H., Sanchez-Islas, N. D. C., Marina-Ramos, M., Leza, J. C., & Flores, G. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101967 · Cited by 34 · see citing works
Inta, D., Vogt, M. A., Elkin, H., Weber, T., Lima‐Ojeda, J. M., Schneider, M., Luoni, A., Riva, M. A., Gertz, K. R., Hellmann‐Regen, J., et al. (2013) · Hippocampus · doi:10.1002/hipo.22236 · Cited by 33 · see citing works
Sylvester, M. A., Goodell, D. J., Adams, J., & Bland, S. T. (2015) · Brain Research · doi:10.1016/j.brainres.2015.11.006 · Cited by 33 · see citing works
Age-related impact of social isolation in mice: Young vs middle-aged
Magalhães, D. M., Mampay, M., Sebastião, A. M., Sheridan, G. K., & Valente, C. A. (2024) · Neurochemistry International · doi:10.1016/j.neuint.2024.105678 · Cited by 32 · see citing works
Goh, J.-Y., O’Sullivan, S. E., Shortall, S. E., Zordan, N., Piccinini, A. M., Potter, H. G., Fone, K. C. F., & King, M. V. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.05.076 · Cited by 33 · see citing works
Ferrara, N. C., Trask, S., & Rosenkranz, J. A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.021 · Cited by 32 · see citing works
Grotewold, S. K., Wall, V. L., Goodell, D. J., Hayter, C., & Bland, S. T. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3470-0 · Cited by 31 · see citing works
Reconsidering depression as a risk factor for substance use disorder: Insights from rodent models
Rappeneau, V., & Bérod, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.001 · Cited by 32 · see citing works
Marquardt, A. E., VanRyzin, J. W., Fuquen, R. W., & McCarthy, M. M. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1076765 · Cited by 31 · see citing works
Riga, D., Schmitz, L. J. M., van der Harst, J. E., van Mourik, Y., Hoogendijk, W. J. G., Smit, A. B., Vries, T. J. D., & Spijker, S. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.311 · Cited by 29 · see citing works
Park, H., Kim, S., Kang, W. S., Chung, J., & Kim, J. (2013) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12202 · Cited by 29 · see citing works
Liu, Z., Yu, Y., Lü, C., Jiang, N., Wang, X., Xiao, S.-Y., & Liu, X. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00021 · Cited by 28 · see citing works
Ago, Y., Condro, M. C., Tan, Y., Ghiani, C. A., Colwell, C. S., Cushman, J. D., Fanselow, M. S., Hashimoto, H., & Waschek, J. A. (2015) · Psychopharmacology · doi:10.1007/s00213-014-3848-z · Cited by 27 · see citing works
Double Helix: Reciprocity between juvenile play and brain development
Cooke, B. M., & Shukla, D. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.001 · Cited by 27 · see citing works
Kinley, B. L., Kyne, R. F., Lawton‐Stone, T. S., Walker, D. M., & Paul, M. J. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15520 · Cited by 27 · see citing works
Long INterspersed element‐1 mobility as a sensor of environmental stresses
Re, B. D., & Giorgi, G. (2020) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22366 · Cited by 23 · see citing works
Fontenot, J., Loetz, E. C., Ishiki, M., & Bland, S. T. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.038 · Cited by 19 · see citing works
Singh, A. K., Xie, Y., Davis, A. R., & Wang, Z.-J. (2022) · Psychopharmacology · doi:10.1007/s00213-021-06024-1 · Cited by 20 · see citing works
Swerdlow, N. R., Light, G. A., Trim, R. S., Breier, M. R., Hines, S. R., & Powell, S. B. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.09.005 · Cited by 19 · see citing works
Goodell, D. J., Sylvester, M. A., Baynard, J., Wall, V. L., & Bland, S. T. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.025 · Cited by 17 · see citing works
Ojelade, O. C., Iyasere, O. S., Durosaro, S. O., Abdulraheem, I., & Akinde, A. O. (2022) · animal · doi:10.1016/j.animal.2022.100521 · Cited by 17 · see citing works
Corcoba, A., Rolf Gruetter, A., Kim, Q., & Duarte, J. M. N. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14116 · Cited by 17 · see citing works
Okudan, N., & Belviranlı, M. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.07.045 · Cited by 17 · see citing works
Shirenova, S. D., Khlebnikova, N. N., & Krupina, N. A. (2023) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-023-01395-8 · Cited by 16 · see citing works
Evaluating negative-symptom-like behavioural changes in developmental models of schizophrenia
Moser, P. C. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.11.004 · Cited by 16 · see citing works
The sequel to COVID-19: the antithesis to life
Bhandari, S., Shaktawat, A. S., Patel, B., Dube, A., Kakkar, S., Tak, A., Gupta, J., & Rankawat, G. (2020) · Journal of Ideas in Health · doi:10.47108/jidhealth.vol3.issspecial1.69 · Cited by 14 · see citing works
Dimatelis, J. J., Stein, D. J., & Russell, V. A. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0071-z · Cited by 14 · see citing works
Stress Varies Along the Social Density Continuum
Love, J., & Zelikowsky, M. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.582985 · Cited by 14 · see citing works
Wu, Z., Yang, Z., Zhang, M., Bao, X., Han, F., & Li, L. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000352 · Cited by 13 · see citing works
Zhang, X., Jiang, H., Xu, L., Yang, S., Wang, G.-Z., Jiang, H.-D., Wu, T., Du, H., Yu, Z.-P., Zhao, Q.-Q., et al. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108231 · Cited by 13 · see citing works
Prefrontal Disinhibition in Social Fear: A Vital Action of Somatostatin Interneurons
Wang, J., Tian, Y., Zeng, L., & Xu, H. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.611732 · Cited by 12 · see citing works
Pitcairn, S. R., Ortelli, O. A., & Weiner, J. L. (2024) · Alcohol, clinical & experimental research · doi:10.1111/acer.15397 · Cited by 13 · see citing works
Effects of ethanol on social avoidance induced by chronic social defeat stress in mice
Favoretto, C. A., Macedo, G. C., & Quadros, I. M. (2017) · Stress · doi:10.1080/10253890.2017.1280667 · Cited by 11 · see citing works
Pubertal LPS treatment selectively alters PSD-95 expression in male CD-1 mice
Kolmogorova, D., & Ismail, N. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.07.025 · Cited by 11 · see citing works
Perkins, A. E., Varlinskaya, E. I., & Terrence Deak, B. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.05.005 · Cited by 10 · see citing works
Andaloussi, Z. I. L., Lauer, W., Zulu, S. S., Taghzouti, K., & Abboussi, O. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173290 · Cited by 10 · see citing works
Postweaning isolation affects responses to incentive contrast in adulthood
Cuenya, L., Mustaca, A., & Kamenetzky, G. (2015) · Developmental Psychobiology · doi:10.1002/dev.21273 · Cited by 9 · see citing works
Epigenetic-Mediated N -Methyl-D-Aspartate Receptor Changes in the Brain of Isolated Reared Rats
Loureiro, C. M., Fachim, H., Zuelli, F. M. D. G. C., Shuhama, R., Joca, S. R. L., Menezes, P. R., Dalton, C., Del‐Ben, C. M., Louzada‐Júnior, P., & Reynolds, G. P. (2020) · Epigenomics · doi:10.2217/epi-2020-0151 · Cited by 8 · see citing works
Somalwar, A. R., Choudhary, A. G., Balasubramanian, N., Sakharkar, A. J., Subhedar, N. K., & Kokare, D. M. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146595 · Cited by 8 · see citing works
Post-weaning social isolation alters sociability in a sex-specific manner
Myers, T., Birmingham, E. A., Rhoads, B. T., McGrath, A. G., Miles, N. A., Schuldt, C. B., & Briand, L. A. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1444596 · Cited by 7 · see citing works
El-Deen, H. M. G., Essawy, A. E., Mohammed, N. A., Abdelfattah, M. S., Fathalla, A. S., El‐Khadragy, M. F., & Moniem, A. E. A. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1680380 · Cited by 7 · see citing works
Yamamoto, M., Hirakata, H., & Toda, K. (2026) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2026.1777975 · Cited by 10 · see citing works
Malin, D. H., Tsai, P.-H., Campbell, J. R., Moreno, G. L., Chapman, H. L., Suzaki, A., Keivan, M. S., Gibbons, K. M., Morales, E. R., Burstein, E. S., et al. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175437 · Cited by 7 · see citing works
Gondora, N., Pople, C. B., Tandon, G., Robinson, M. J., Solomon, E., Beazely, M. A., & Mielke, J. G. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.136016 · Cited by 7 · see citing works
Tamura, H., Miyazaki, A., Kawamura, T., Gotoh, H., Yamamoto, N., & Narita, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-62534-w · Cited by 5 · see citing works
Chronic early-life social isolation enhances spatial memory in male and female rats
Davari, S., D’Costa, N., Ramezan, R., & Mielke, J. G. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114433 · Cited by 5 · see citing works
Modulation of long interspersed nuclear element-1 in the mouse hippocampus during maturation
Ueno, M., Okamura, T., Mishina, M., & Ishizaka, Y. (2016) · Mobile Genetic Elements · doi:10.1080/2159256x.2016.1211980 · Cited by 5 · see citing works
Wang, Y., Yue, S., Yang, F., Chen, L., Singh, A., Marciniak, M., Wei, W., & Wang, Z.-J. (2025) · Nature Communications · doi:10.1038/s41467-025-64585-7 · Cited by 4 · see citing works
Goh, J.-Y., Rueda, P., Taylor, J., Rathbone, A., Scott, D., LANGMEAD, C. J., Fone, K. C. F., Stewart, G. D., & King, M. V. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100679 · Cited by 4 · see citing works
Mao, L., Mathur, N., & Wang, J. Q. (2022) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2022.05.007 · Cited by 3 · see citing works
Comparing Various Types of Chronic Psychological Stress on Cognitive Functions and Behaviors in Rats
Adavi, H., Kowsar, R., Radahmadi, M., & Alaei, H. (2024) · Basic and Clinical Neuroscience Journal · doi:10.32598/bcn.2023.2346.4 · Cited by 3 · see citing works
Hurst, C., Zobel, G., Young, W., Olson, T., Parkar, N., Bracegirdle, J., Hannaford, R., Anderson, R. C., & Dalziel, J. E. (2025) · Brain and Behavior · doi:10.1002/brb3.70621 · Cited by 2 · see citing works
The (un-)Social Brain in Isolation
Fishman, A., Grinin, P., & RILJAK, V. (2025) · Physiological Research · doi:10.33549/physiolres.935565 · Cited by 2 · see citing works
Penagos-Corzo, J. C., Pérez-Acosta, A. M., & Hernández, I. M. (2015) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 2 · see citing works
Roles of Medial Prefrontal Cortex Activity in Human and Animal Social Learning
Nieves, N., & von Schroder, C. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1298 · Cited by 2 · see citing works
Regulation of sociability by the cortico-habenula pathway in an animal model of depression
Park, H.-Y., & Chung, C. (2025) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2025.102799 · Cited by 1 · see citing works
Standardized Protocol for Novel Social Defeat-Induced Specific Social Fear in Mice
Ye, H., Li, H., Sun, Y., Qiu, M. S., & Xu, H. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01550-w · Cited by 1 · see citing works
Selecting an appropriate stress model of depression in rodents
Lu, X.-X., Tang, H., & Li, X. (2025) · World Journal of Psychiatry · doi:10.5498/wjp.v15.i12.113433 · Cited by 2 · see citing works
Factors Modulating the Effects of Juvenile Social Isolation on Adult Social Behavior in Rodents
Leventhal, M. B., Kawatake-Kuno, A., Lidoski, A., & Morishita, H. (2026) · Developmental Psychobiology · doi:10.1002/dev.70129 · Cited by 1 · see citing works
Hong, Y.-P., & Kim, H.-T. (2012) · Journal of Life Science · doi:10.5352/jls.2012.22.9.1180 · Cited by 1 · see citing works
Effect of Socialization on Impulsivity in the Domestic Dog
Alexandra, M. (2015) · The Atrium (University of Guelph) · Cited by 1 · see citing works
D’Costa, N. (2019) · UWSpace (University of Waterloo)
Roles of Medial Prefrontal Cortex Activity in Human and Animal Social Learning
Nieves, N., & von Schroder, C. (2017) · Springer eBooks · doi:10.1007/978-3-319-47829-6_1298-1
Odenwald, N. (2019) · TSpace (University of Toronto)
- Authors
- Hermes, G., Li, N., Duman, C., & Duman, R.
- Affiliations
- Yale University (US)
- Corresponding author
- Hermes, Gretchen
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 2011-08
- Volume
- 104
- Issue
- 2
- Pages
- 354-359
- ISSN
- 0031-9384 (ISSN-L)
- PMC
- PMC3387788
- OpenAlex
- W2065919724
- Cited by
- 111
- References
- 43
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 6 · 2023: 4 · 2022: 5 · 2021: 8 · 2020: 10 · 2019: 8 · 2018: 2 · 2017: 11 · 2016: 7 · 2015: 10 · 2014: 3 · 2013: 14 · 2012: 5
- FWCI
- 3.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (5T32 MH-19961, T32MH019961, R25MH071584)
- National Institute on Drug Abuse (K24DA017899)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- post-weaning social isolation, early life stress, female rats, prefrontal cortex, PSD-95, synapsin I, GluR1, NR1, glutamate receptors, anxiety, social interaction deficits, social play, synaptic dysfunction, sex differences
- MeSH terms
- Disks Large Homolog 4 Protein, Age Factors, Animals, Animals, Newborn, Behavioral Symptoms, Body Weight, Estriol, Estrus, Exploratory Behavior, Female, Food Deprivation, Membrane Proteins, Pregnancy, Social Isolation, Receptors, N-Methyl-D-Aspartate, Synapsins, Rats, Sprague-Dawley, Prefrontal Cortex, Receptors, AMPA, Gene Expression Regulation, Developmental, Intracellular Signaling Peptides and Proteins, 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