The enduring effects of an adolescent social stressor on synaptic density, part II: Poststress reversal of synaptic loss in the cortex by adinazolam and MK‐801
Abstract
Experience programs synaptic development to match the needs of the environment. This process depends on the nature and timing of the experience. Exposure to stress during adolescence selectively reduces synaptic density in the prefrontal cortex (a later maturing region), while sparing hippocampal synapses (an earlier maturing region). To determine whether the anatomical effects of an adolescent social stressor in rats endures into adulthood and are reversible, male subjects were isolation or group housed between days 30 and 35 and then treated with vehicle, adinazolam, MK-801, or tianeptine between days 40 and 55. At day 60, immunohistochemistry revealed a 13.5% +/- 5.3% reduction in synaptophysin in the infralimbic cortex and cingulate gyrus in isolation-housed subjects. MK-801 and adinazolam restored cortical synaptic density to within 2% of group-housed values, suggesting that the synaptic loss induced by stress during adolescence is modulated through reduced glutamatergic activity directly by NMDA antagonism or indirectly by enhancing GABAergic activity. Tianeptine did not modulate adolescent stress effects in the prefrontal cortex. None of these drugs increased cortical synaptophysin in group-housed controls. Increased synaptophysin was observed in the group-housed condition in the hippocampus, striatum, and nucleus accumbens following drug exposure. Although stress did not decrease synaptic density in these regions, drug exposure failed to increase synaptic density when…
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Lack of social play experience during postweaning development causes long-lasting changes in PFC circuitry and function.
“Lack of social play experience during postweaning development has been reported to cause long-lasting changes in PFC circuitry and function (Leussis et al., 2008;Bell et al., 2010;Baarendse et al., 2013;Vanderschuren and Trezza, 2014).”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Leussis et al., 2008
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Ledent, C. A., Valverde, O., Cossu, G., Petitet, F., Aubert, J.-F., Beslot, F., Böhme, G. A., Impérato, A., Pedrazzini, T., Roques, B. P., et al. (1999) · Science · doi:10.1126/science.283.5400.401 · Cited by 3,612 · see citing works
Heim, C., & Nemeroff, C. B. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01157-x · Cited by 2,791 · see citing works
Trajectories of brain development: point of vulnerability or window of opportunity?
Andersen, S. L. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00005-8 · Cited by 1,503 · see citing works
Self-citationThe neurobiological consequences of early stress and childhood maltreatment
Teicher, M. H., Andersen, S. L., Polcari, A., Anderson, C. M., Navalta, C. P., & Kim, D. M. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00007-1 · Cited by 1,465 · see citing works
Self-citationBremner, J. D., Randall, P., Vermetten, E., Staib, L., Bronen, R. A., Mazure, C., Capelli, S., McCarthy, G., Innis, R. B., & Charney, D. S. (1997) · Biological Psychiatry · doi:10.1016/s0006-3223(96)00162-x · Cited by 1,283 · see citing works
Hippocampal volume in women victimized by childhood sexual abuse
STEIN, M. B., KOVEROLA, C., HANNA, C., TORCHIA, M. G., & McCLARTY, B. (1997) · Psychological Medicine · doi:10.1017/s0033291797005242 · Cited by 924 · see citing works
Nemeroff, C. B., Heim, C. M., Thase, M. E., Klein, D. N., Rush, A. J., Schatzberg, A. F., Ninan, P. T., McCullough, J. P., Weiss, P. M., Dunner, D. L., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2336126100 · Cited by 829 · see citing works
Early-Life Blockade of the 5-HT Transporter Alters Emotional Behavior in Adult Mice
Ansorge, M. S., Zhou, M., Lira, A., Hen, R., & Gingrich, J. A. (2004) · Science · doi:10.1126/science.1101678 · Cited by 817 · see citing works
Andersen, S. L., Tomada, A., Vincow, E. S., Valente, E., Polcari, A., & Teicher, M. H. (2008) · The Journal of Neuropsychiatry and Clinical Neurosciences · doi:10.1176/jnp.2008.20.3.292 · Cited by 788 · see citing works
Self-citationBremner, J. D., Vythilingam, M., Vermetten, E. H. G. J. M., Southwick, S. M., McGlashan, T. H., Nazeer, A., Khan, S., Vaccarino, V., Soufer, R., Garg, P. K., et al. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.5.924 · Cited by 721 · see citing works
Effects of adverse experiences for brain structure and function
McEwen, B. S. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00964-1 · Cited by 639 · see citing works
Development of the dopaminergic innervation in the prefrontal cortex of the rat
Kalsbeek, A., Voorn, P., Buijs, R. M., Pool, C. W., & Uylings, H. B. M. (1988) · Journal of Comparative Neurology · doi:10.1002/cne.902690105 · Cited by 545 · see citing works
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · 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
“In this sense, it differs from the more strenuous stressor of social isolation that spans across weeks of adolescent development and affects the prefrontal cortex (Hall, 1998; Weiss et al., 2004).”
Hall, F. S. (1998) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v12.i1-2.50 · Cited by 512 · see citing works
YEHUDA, R., HALLIGAN, S. L., & GROSSMAN, R. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003170 · Cited by 490 · see citing works
Dynamic mapping of normal human hippocampal development
Gogtay, N., Nugent, T. F., Herman, D. H., Ordonez, A., Greenstein, D., Hayashi, K. M., Clasen, L., Toga, A. W., Giedd, J. N., Rapoport, J. L., et al. (2006) · Hippocampus · doi:10.1002/hipo.20193 · Cited by 426 · see citing works
Stress Effects on Morphology and Function of the Hippocampusa
McEwen, B. S., & Magariños, A. M. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48286.x · Cited by 393 · see citing works
Lewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388 · see citing works
Tianeptine attenuates stress-induced morphological changes in the hippocampus
Watanabe, Y., Gould, E., Daniels, D. C., Cameron, H. A., & McEwen, B. S. (1992) · European Journal of Pharmacology · doi:10.1016/0014-2999(92)90830-w · Cited by 338 · see citing works
Bellis, M. D. D., Hall, J., Boring, A. M., Frustaci, K., & Moritz, G. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01105-2 · 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
Delayed Effects of Early Stress on Hippocampal Development
Andersen, S. L., & Teicher, M. H. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300528 · Cited by 313 · see citing works
Self-citationBenes, F. M. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.10.1014 · Cited by 268 · see citing works
Bredy, T. W., Humpartzoomian, R., Cain, D. P., & Meaney, M. J. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00918-1 · Cited by 248 · see citing works
Meaney, M. J., & Aitken, D. H. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90183-x · Cited by 234 · see citing works
Leussis, M. P., & Andersen, S. L. (2008) · Synapse · doi:10.1002/syn.20462 · Cited by 220 · see citing works
Self-citationReznikov, L. R., Grillo, C. A., Piroli, G. G., Pasumarthi, R. K., Reagan, L. P., & Fadel, J. R. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05560.x · Cited by 201 · see citing works
Segmented Hippocampal Volume in Children and Adolescents with Posttraumatic Stress Disorder
Tupler, L. A., & Bellis, M. D. D. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.08.007 · Cited by 183 · see citing works
Age-related differences in glucocorticoid receptor mRNA levels in the human brain
Perlman, W. R., Webster, M. J., Herman, M. M., Kleinman, J. E., & Weickert, C. S. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.01.010 · Cited by 152 · see citing works
McEwen, B. S. (2000) · Neurochemical Research · doi:10.1023/a:1007687911139 · Cited by 142 · see citing works
Andersen, S. L., & Navalta, C. P. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.06.002 · Cited by 139 · see citing works
Self-citationNMDA receptor activation limits the number of synaptic connections during hippocampal development
Lüthi, A., Schwyzer, L., Mateos, J. M., Gähwiler, B. H., & McKinney, R. A. (2001) · Nature Neuroscience · doi:10.1038/nn744 · Cited by 138 · see citing works
Brake, W. G., Flores, G., Francis, D. D., Meaney, M. J., Srivastava, L. K., & Gratton, A. P. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00002-6 · Cited by 138 · see citing works
Wilde, M. I., & Benfield, P. (1995) · Drugs · doi:10.2165/00003495-199549030-00007 · Cited by 128 · see citing works
Reduction of Synaptophysin Immunoreactivity in the Prefrontal Cortex of Subjects With Schizophrenia
Glantz, L. A. (1997) · Archives of General Psychiatry · doi:10.1001/archpsyc.1997.01830190088009 · Cited by 122 · see citing works
Structural plasticity and tianeptine: cellular and molecular targets
McEwen, B. S., Magarinos, A. M., & Reagan, L. P. (2002) · European Psychiatry · doi:10.1016/s0924-9338(02)00650-8 · Cited by 108 · see citing works
Shors, T. J., Falduto, J., & Leuner, B. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.03065.x · Cited by 105 · see citing works
Owens, M. J., Bissette, G., & Nemeroff, C. B. (1989) · Synapse · doi:10.1002/syn.890040304 · Cited by 86 · see citing works
Kehoe, P. G., Triano, L., Hoffman, J., Shoemaker, W. J., & Arons, C. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.6.1435 · Cited by 75 · see citing works
Tianeptine increases brain-derived neurotrophic factor expression in the rat amygdala
Reagan, L. P., Hendry, R. M., Reznikov, L. R., Piroli, G. G., Wood, G. E., McEwen, B. S., & Grillo, C. A. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.02.023 · Cited by 69 · see citing works
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Stress, sensitive periods and maturational events in adolescent depression
Andersen, S. L., & Teicher, M. H. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.01.004 · Cited by 1,005 · see citing works
Self-citationAdolescence as a neurobiological critical period for the development of higher-order cognition
Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 562 · see citing works
Stress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 491 · see citing works
Andersen, S. L., & Teicher, M. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.009 · Cited by 326 · see citing works
Self-citationMcCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276 · see citing works
Howes, O., & Shatalina, E. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.06.017 · Cited by 233 · see citing works
Romeo, R. D. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.021 · Cited by 226 · see citing works
Baarendse, P. J. J., Counotte, D. S., O'Donnell, P., & Vanderschuren, L. J. M. J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.47 · Cited by 206 · see citing works
Vanderschuren, L. J. M. J., & Trezza, V. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-662-45758-0_268 · Cited by 200 · see citing works
Prefrontal cortical inputs to the basal amygdala undergo pruning during late adolescence in the rat
Cressman, V. L., Balaban, J., Steinfeld, S., Shemyakin, A., Graham, P., Parisot, N., & Moore, H. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22359 · Cited by 161 · see citing works
Social behavior and social stress in adolescence: A focus on animal models
Buwalda, B., Geerdink, M., Vidal, J., & Koolhaas, J. M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.004 · Cited by 149 · see citing works
Lopez, M. F., Doremus-Fitzwater, T. L., & Becker, H. C. (2011) · Alcohol · doi:10.1016/j.alcohol.2010.08.017 · Cited by 146 · see citing works
Neuroimaging in schizophrenia: an overview of findings and their implications for synaptic changes
Howes, O. D., Cummings, C., Chapman, G. E., & Shatalina, E. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01426-x · Cited by 149 · see citing works
Sheth, C. S., McGlade, E., & Yurgelun-Todd, D. A. (2017) · Chronic Stress · doi:10.1177/2470547017715645 · Cited by 136 · see citing works
Haller, S. P., Kadosh, K. C., Scerif, G., & Lau, J. Y. F. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.02.002 · Cited by 133 · see citing works
Watt, M. J., Weber, M. A., Davies, S. R., & Forster, G. L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.06.015 · Cited by 94 · see citing works
Stress, sensitive periods, and substance abuse
Andersen, S. L. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100140 · Cited by 92 · see citing works
Self-citationLopez, M. F., & Laber, K. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.012 · Cited by 87 · see citing works
Life stress in adolescence predicts early adult reward-related brain function and alcohol dependence
Casement, M. D., Shaw, D. S., Sitnick, S. L., Musselman, S. C., & Forbes, E. E. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu061 · Cited by 82 · see citing works
Reducing substance use during adolescence: a translational framework for prevention
Stanis, J. J., & Andersen, S. L. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3393-1 · Cited by 69 · see citing works
Self-citationNeuroinflammation, Early-Life Adversity, and Brain Development
Andersen, S. L. (2022) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000325 · Cited by 70 · see citing works
Self-citationLee, T. T. Y., & Hill, M. N. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.017 · Cited by 67 · see citing works
Madra, M., & Zeltser, L. M. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.35 · Cited by 64 · see citing works
Drzewiecki, C. M., & Juraska, J. M. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173044 · Cited by 67 · see citing works
Borsini, A., Giacobbe, J., Mandal, G., & Boldrini, M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02229-2 · Cited by 59 · see citing works
Hinwood, M., Tynan, R. J., Day, T. A., & Walker, F. R. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq080 · Cited by 58 · see citing works
Kumari, A., Singh, P., Baghel, M. S., & Thakur, M. K. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.02.032 · Cited by 57 · see citing works
Watt, M. J., Roberts, C. L., Scholl, J. L., Meyer, D. L., Miiller, L. C., Barr, J. L., Novick, A. M., Renner, K. J., & Forster, G. L. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3353-9 · Cited by 56 · see citing works
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.0524-22.2022 · Cited by 54 · see citing works
Daily stress increases risky decision‐making in adolescents: A preliminary study
Galván, A., & McGlennen, K. M. (2011) · Developmental Psychobiology · doi:10.1002/dev.20602 · Cited by 56 · see citing works
Barfield, E. T., & Gourley, S. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.10.015 · Cited by 53 · see citing works
Zhang, F., Yuan, S., Shao, F., & Wang, W. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00149 · Cited by 51 · see citing works
Adolescent social defeat decreases spatial working memory performance in adulthood
Novick, A. M., Miiller, L. C., Forster, G. L., & Watt, M. J. (2013) · Behavioral and Brain Functions · doi:10.1186/1744-9081-9-39 · Cited by 47 · see citing works
Adolescent social defeat alters markers of adult dopaminergic function
Novick, A. M., Forster, G. L., Tejani‐Butt, S. M., & Watt, M. J. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.06.009 · Cited by 47 · see citing works
Lukkes, J. L., Meda, S., Thompson, B. S., Freund, N., & Andersen, S. L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.04.053 · Cited by 46 · see citing works
Self-citationRodríguez‐Arias, M., Montagud‐Romero, S., Carrión, A. M. G., Perez, C. F., Pérez‐Villalba, A., Marco, E. M., López‐Gallardo, M., Viveros, M., & Miñarro, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206421 · Cited by 41 · see citing works
Smith, B. L., Morano, R. L., Ulrich‐Lai, Y. M., Myers, B., Solomon, M. B., & Herman, J. P. (2017) · Stress · doi:10.1080/10253890.2017.1402883 · Cited by 38 · see citing works
Persistent behavioral and neurobiological consequences of social isolation during adolescence
Li, D. C., Hinton, E. A., & Gourley, S. L. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.017 · Cited by 36 · see citing works
Perica, M. I., & Luna, B. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105378 · Cited by 34 · see citing works
Novick, A. M., Mears, M., Forster, G. L., Lei, Y., Tejani‐Butt, S. M., & Watt, M. J. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.02.013 · Cited by 33 · see citing works
Hall, F. S., & Perona, M. T. G. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.05.014 · Cited by 33 · see citing works
Wright, L., Muir, K. E., & Perrot, T. S. (2011) · Developmental Psychobiology · doi:10.1002/dev.20575 · Cited by 31 · see citing works
Romeo, R. D., & Karatsoreos, I. N. (2011) · Wiley eBooks · doi:10.1002/9781118083222.ch13 · Cited by 28 · see citing works
Cuesta, S., Funes, A., & Pacchioni, A. M. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00466-x · Cited by 26 · see citing works
Lee, T. T.-Y., Hill, M. N., Hillard, C. J., & Gorzalka, B. B. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.07.021 · Cited by 26 · see citing works
Early-Life Experiences: Enduring Behavioral, Neurological, and Endocrinological Consequences
Romeo, R., Tang, A. C., & Sullivan, R. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00062-0 · Cited by 30 · see citing works
Champroux, A., Tang, Y., Dickson, D. A., Meng, A., Harrington, A. N., Liaw, L., Marzi, M. J., Nicassio, F., Schlaeger, T. M., & Feig, L. A. (2024) · Epigenetics · doi:10.1080/15592294.2024.2346694 · Cited by 22 · see citing works
Crestani, C. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.027 · Cited by 22 · see citing works
Hodges, T. E., Louth, E. L., Bailey, C. D. C., & McCormick, C. M. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1789-8 · Cited by 22 · see citing works
Raineki, C., Morgan, E., Ellis, L. A., & Weinberg, J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.05.019 · Cited by 19 · see citing works
Begni, V., Zampar, S., Longo, L., & Riva, M. A. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.04.018 · Cited by 17 · see citing works
Chohan, T. W., Nguyen, A. P., Todd, S. M., Bennett, M. R., Callaghan, P. D., & Arnold, J. C. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00298 · Cited by 16 · see citing works
Aoki, C. J., Chen, Y., Chowdhury, T. G., & Piper, W. T. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.24035 · Cited by 16 · see citing works
Barfield, E. T., & Gourley, S. L. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00237 · Cited by 16 · see citing works
Uliana, D. L., Gomes, F. V., & Grace, A. A. (2020) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2020.04.004 · Cited by 16 · see citing works
Structure of distress call: implication for specificity and activation of dopaminergic system
Mariappan, S., Bogdanowicz, W., Raghuram, H., Marimuthu, G., & Rajan, K. E. (2015) · Journal of Comparative Physiology A · doi:10.1007/s00359-015-1053-0 · Cited by 16 · see citing works
Play and welfare in domestic cats: Current knowledge and future directions
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Karanges, E. A., & McGregor, I. S. (2011) · Future Neurology · doi:10.2217/fnl.11.51 · Cited by 15 · see citing works
Herrero-Roldán, S., & Martín-Rodríguez, A. (2025) · Biomedicines · doi:10.3390/biomedicines13071565 · Cited by 14 · see citing works
Huzián, O., Baka, J., Csakvari, E., Dobos, N., Leranth, C., Siklós, L., Duman, R. S., Farkas, T., & Hajszán, T. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.01.029 · Cited by 14 · see citing works
Barfield, E. T., Sequeira, M. K., Parsons, R. G., & Gourley, S. L. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.00045 · Cited by 12 · see citing works
In Vivo Positron Emission Tomography Imaging of Adenosine A2A Receptors
Sun, M.-J., Liu, F., Zhao, Y., & Wu, X. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.599857 · Cited by 12 · see citing works
Aleksic, M., Brkic, Z., Petrovic, Z., Francija, E., Lukić, I., & Adžić, M. (2022) · Journal of Neuroscience Research · doi:10.1002/jnr.25032 · Cited by 11 · see citing works
Animal Models of Developmental Psychopathology
Howell, B., Neigh, G. N., & Sánchez, M. M. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy205 · Cited by 10 · see citing works
How Postnatal Insults May Program Development: Studies in Animal Models
Dalmaz, C., Noschang, C. G., Krolow, R., Raineki, C., & Lucion, A. B. (2014) · Advances in neurobiology · doi:10.1007/978-1-4939-1372-5_7 · Cited by 9 · see citing works
Drzewiecki, C. M., Willing, J., Cortes, L. R., & Juraska, J. M. (2021) · Developmental Psychobiology · doi:10.1002/dev.22111 · Cited by 9 · see citing works
Masoudi, M., Goodarzi, M., Rahmani, M. A., Rajabi, M., Mahdizadeh, M., Gharaei, M., & Beheshti, F. (2024) · Nutritional Neuroscience · doi:10.1080/1028415x.2024.2389499 · Cited by 8 · see citing works
Sex-dependent long-term effects of prepubescent stress on the posterior parietal cortex
Fariborzi, M., Park, S. B., Ozgur, A., & Lür, G. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100295 · Cited by 8 · see citing works
Disasters and Their Effects on Child Development
Hussaini, M. H. A., Kausar, N., & Indriani, F. (2022) · International Journal of Learning Reformation in Elementary Education · doi:10.56741/ijlree.v1i02.165 · Cited by 6 · see citing works
Champroux, A., Sadat‐Shirazi, M., Chen, X., Hacker, J., Yang, Y., & Feig, L. A. (2025) · Epigenetics · doi:10.1080/15592294.2025.2457176 · Cited by 6 · see citing works
Childhood Trauma in Depressive Disorders
Aas, M., & Étain, B. (2020) · Springer eBooks · doi:10.1007/978-3-030-49414-8_9 · Cited by 6 · see citing works
Impact of early social isolation on social circuits and behavior: relevance to schizophrenia
Kawatake-Kuno, A., Leventhal, M. B., & Morishita, H. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02156-6 · Cited by 7 · see citing works
The Neurochemistry of Social Play Behaviour in Rats
Trezza, V., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2018) · Cambridge University Press eBooks · doi:10.1017/9781108131384.003 · Cited by 5 · see citing works
Early-Life Experiences: Enduring Behavioral, Neurological, and Endocrinological Consequences
Romeo, R. D., Tang, A. C., & Sullivan, R. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00099-7 · Cited by 5 · see citing works
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.01.070540 · Cited by 4 · see citing works
Anxiety Impact on the Children Brain: Consequences for Children Emotional Capacities
Hussaini, M. H. A., Abbas, M. K., Fatima, R., & Noureen, A. (2022) · Journal of Mental Health Issues and Behavior · doi:10.55529/jmhib.31.8.15 · Cited by 2 · see citing works
Adolescent neurocognitive development
Ravindranath, O., Parr, A. C., Perica, M. I., Elliott, S., & Luna, B. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-818872-9.00105-9 · Cited by 4 · see citing works
Funes, A., Ramirez, A. I., Konjuh, C. N., Rosso, S. B., Cuesta, S., & Pacchioni, A. M. (2025) · Journal of Molecular Neuroscience · doi:10.1007/s12031-025-02341-8 · Cited by 1 · see citing works
Zhang, Y., Chen, S., Zhang, S., Li, Y., Wang, Y., Cao, M., Jin, Y., Wang, Z., Ding, S., & Xiao, M. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01534-w · Cited by 1 · see citing works
Effect of Anxiety on the Children Brain Structure: Consequences for Children Emotional Healthiness
MuzamilHussainAlHussaini, M. (2022) · Qubahan Academic Journal · doi:10.48161/qaj.v2n3a132 · Cited by 2 · see citing works
Borsini, A., Giacobbe, J., Mandal, G., & Boldrini, M. (2022) · Preprints.org · doi:10.20944/preprints202206.0343.v1 · Cited by 1 · see citing works
Waters, P. (2011) · Brock University Digital Repository (Brock University)
Bingham, B. C. (2010) · ScholarlyCommons (University of Pennsylvania)
Adaptive and Maladaptive Regulations in Response to Environmental Stress in Adolescent Rodents
Macrı̀, S., & Laviola, G. (2012) · Springer eBooks · doi:10.1007/978-1-4614-5605-6_12
Uban, K. A. (2013) · cIRcle (University of British Columbia) · doi:10.14288/1.0073514
Wright, L. (2011) · Library and Archives Canada (Government of Canada)
Hodges, T. E. (2018) · Brock University Digital Repository (Brock University)
White, G. (2020) · TSpace (University of Toronto)
Jadhav, K. S., Hoffman, A. F., Burgisser, M., Rossetti, C., Aeschlimann, L., Lupica, C. R., & Boutrel, B. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.21.469381
Positron emission tomography imaging of neuroinflammation
(2023) · Advances in magnetic resonance technology and applications · doi:10.1016/b978-0-323-91771-1.00007-1
Adolescent Brain Development Under Stress and Trauma: Evidence-Based Treatments
Pappas, I., Yu, T. L. T., Liu, O., & Srinivasan, N. (2025) · Berkeley Pharma Tech Journal of Medicine · doi:10.52243/bptjm.v5i1.73
- Authors
- Leussis, M. P., Lawson, K., Stone, K., & Andersen, S. L.
- Affiliations
- Harvard University (US)
- Corresponding author
- Andersen, Susan L.
- Venue
- Synapse
- Publisher
- Wiley
- Published
- 2007-12-14
- Volume
- 62
- Issue
- 3
- Pages
- 185-192
- ISSN
- 0887-4476 (ISSN-L)
- 1098-2396
- OpenAlex
- W2124453851
- Cited by
- 95
- References
- 42
- Citations by year
- 2025: 6 · 2024: 2 · 2023: 4 · 2022: 11 · 2021: 5 · 2020: 9 · 2019: 1 · 2018: 7 · 2017: 7 · 2016: 8 · 2015: 4 · 2014: 5 · 2013: 5 · 2012: 5
- FWCI
- 1.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Synapse (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- isolation stress, synaptic density, prefrontal cortex, synaptophysin, adinazolam, MK-801, tianeptine, NMDA receptor antagonism, GABAergic activity, glutamatergic activity, hippocampus, striatum, nucleus accumbens, synapse maturation
- MeSH terms
- Age Factors, Animals, Animals, Newborn, Behavior, Animal, Benzodiazepines, Brain, Disease Models, Animal, Male, Random Allocation, Social Isolation, Stress, Physiological, Synapses, Dizocilpine Maleate, Synaptophysin, Rats, Sprague-Dawley, Gene Expression Regulation, Developmental, Excitatory Amino Acid Antagonists, Rats
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