Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows
Abstract
The present study provides evidence for the hypothesis that the extent and the direction of experience-induced synaptic changes in cortical areas correlates with time windows of neuronal as well as endocrine development. Repeated brief exposure to maternal separation prior to the stress hyporesponsive period (SHRP) of the hypothalamic-pituitary-adrenal (HPA) axis induced significantly reduced dendritic spine density (-16%) in layer II/III pyramidal neurons of the anterior cingulate cortex (ACd) of 21-day-old rats, whereas separation after termination of the SHRP resulted in increased spine densities (+16%) in this neuron type. In addition, rats of both groups displayed elevated basal plasma levels of corticosterone at this age. Separation during the SHRP (postnatal days 5-7) did not influence spine density in the ACd, and basal corticosterone levels remained unchanged. In contrast, pyramidal neurons in the somatosensory cortex (SSC) displayed significantly enhanced spine densities (up to 52% increase) independent from the time of separation. These results indicate that alterations in the synaptic balance in limbic and sensory cortical regions in response to early emotional experience are region-specific and related to the maturational stage of endocrine and neuronal systems.
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Maternal separation or other disruptions to the early environment change neuronal morphology of the frontal cortex in rodents.
“Studies assessing the effects of stress during the first weeks of life in rodents indicate that maternal separation or other disruptions to the early environment change neuronal morphology of the frontal cortex (Brenhouse et al., 2013; Bock et al., 2005; Chocyk et al., 2013; Monroy et al., 2010; Muhammad and Kolb, 2011; Yang et al., 2015).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Bock et al., 2005
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Synaptic Activity and the Construction of Cortical Circuits
Katz, L. C., & Shatz, C. J. (1996) · Science · doi:10.1126/science.274.5290.1133 · Cited by 3,048 · 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
Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex
Trachtenberg, J. T., Chen, B. E., Knott, G. W., Feng, G., Sanes, J. R., Welker, E., & Svoboda, K. (2002) · Nature · doi:10.1038/nature01273 · Cited by 1,927 · 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
Experience and brain development
Greenough, W. T., Black, J. E., & Wallace, C. S. (1987) · Child Development · doi:10.2307/1130197 · Cited by 1,398 · see citing works
Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons
Watanabe, Y., Gould, E., & McEwen, B. S. (1992) · Brain Research · doi:10.1016/0006-8993(92)91597-8 · Cited by 1,212 · see citing works
Harris, K., & Kater, S. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.002013 · Cited by 1,032 · see citing works
Woolley, C. S., Gould, E., & McEwen, B. S. (1990) · Brain Research · doi:10.1016/0006-8993(90)90778-a · Cited by 1,020 · see citing works
Psychobiology of plasticity: Effects of training and experience on brain and behavior
Rosenzweig, M. R., & Bennett, E. L. (1996) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00216-2 · Cited by 972 · see citing works
Heidbreder, C. A., & Groenewegen, H. J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2003.09.003 · Cited by 882 · see citing works
Meaney, M. J., Diorio, J., Francis, D., Widdowson, J., LaPlante, P., Caldji, C., Sharma, S., Seckl, J. R., & Plotsky, P. M. (2010) · Developmental Neuroscience · doi:10.1159/000111395 · Cited by 878 · see citing works
Magariños, A. M., McEwen, B. S., Flügge, G., & Fuchs, E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03534.1996 · Cited by 864 · see citing works
Radley, J. J., Sisti, H. M., Hao, J., Rocher, A. B., McCall, T., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.01.006 · Cited by 769 · see citing works
Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys
Bourgeois, J.-P., Goldman-Rakic, P. S., & Rakic, P. (1994) · Cerebral Cortex · doi:10.1093/cercor/4.1.78 · Cited by 687 · see citing works
Wellman, C. L. (2001) · Journal of Neurobiology · doi:10.1002/neu.1079 · Cited by 594 · see citing works
Stress, hypercortisolism and corticosteroid receptors in depression: implicatons for therapy
Holsboer, F. (2001) · Journal of Affective Disorders · doi:10.1016/s0165-0327(00)00352-9 · Cited by 575 · see citing works
Agid, O., Shapira, B., Zislin, J., Ritsner, M., Hanin, B., Murad, H., Troudart, T., Bloch, M., Heresco‐Levy, U., & Lerer, B. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000473 · Cited by 568 · see citing works
Preclinical models: status of basic research in depression
Nestler, E. J., Gould, E., & Manji, H. K. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01405-1 · Cited by 559 · see citing works
Early determinants of behaviour: evidence from primate studies
Suomi, S. J. (1997) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a011598 · Cited by 483 · see citing works
Pryce, C. R., & Feldon, J. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00009-5 · Cited by 460 · see citing works
Turner, A. M., & Greenough, W. T. (1985) · Brain Research · doi:10.1016/0006-8993(85)90525-6 · Cited by 459 · see citing works
Levine, S. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00496-6 · Cited by 428 · see citing works
Sánchez, M. M., Young, L. J., Plotsky, P. M., & Insel, T. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-12-04657.2000 · Cited by 420 · see citing works
Glaser, E. M., & der Loos, H. V. (1981) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(81)90045-5 · Cited by 374 · see citing works
Christof Koch, A., & Zador, A. M. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-02-00413.1993 · Cited by 374 · see citing works
Differential rearing effects on rat visual cortex synapses.
Sirevaag, A. M., & Greenough, W. T. (1987) · Brain Research · doi:10.1016/0006-8993(87)91477-6 · Cited by 370 · see citing works
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.10.007 · Cited by 368 · see citing works
Sullivan, R. M., & Gratton, A. P. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00038-5 · Cited by 321 · see citing works
The effects of an early stressful life event on sensorimotor gating in adult rats
Ellenbroek, B. A., van den Kroonenberg, P. T. J. M., & Cools, A. R. (1998) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00149-7 · Cited by 265 · see citing works
Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain
Patel, P. D., Lopez, J. F., Lyons, D. M., Burke, S., Wallace, M., & Schatzberg, A. F. (2000) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(00)00035-2 · Cited by 252 · see citing works
Meaney, M. J., Aitken, D. H., Bhatnagar, S., & Sapolsky, R. M. (1991) · Neurobiology of Aging · doi:10.1016/0197-4580(91)90036-j · Cited by 250 · see citing works
Multifactorial regulation of the hypothalamic-pituitary-adrenal axis during development
Rosenfeld, P., Suchecki, D., & Levine, S. D. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80196-4 · Cited by 230 · see citing works
A technique for estimating total spine numbers on golgi‐impregnated dendrites
Feldman, M. L., & Peters, A. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901880403 · Cited by 194 · see citing works
Delayed Maturation and Sensitive Periods in the Auditory Cortex
Kral, A., Hartmann, R., Tillein, J., Heid, S., & Klinke, R. (2001) · Audiology and Neurotology · doi:10.1159/000046845 · Cited by 192 · see citing works
Huot, R. L., Gonzalez, M. E., Ladd, C. O., Thrivikraman, K. V., & Plotsky, P. M. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00028-3 · Cited by 191 · see citing works
Joseph, R. (1999) · Child Psychiatry & Human Development · doi:10.1023/a:1022660923605 · Cited by 161 · see citing works
The cortical component of experience-dependent synaptic plasticity in the rat barrel cortex
Fox, K. D. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07665.1994 · Cited by 143 · see citing works
[3H]Dexamethasone binding in rat frontal cortex
Meaney, M. J., & Aitken, D. H. (1985) · Brain Research · doi:10.1016/0006-8993(85)91340-x · Cited by 133 · see citing works
Wallhäusser, E., & Scheich, H. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90080-0 · Cited by 125 · see citing works
Levine, S. D. (2002) · Neurotoxicity Research · doi:10.1080/10298420290030569 · Cited by 118 · see citing works
Bock, J., & Braun, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.2485 · Cited by 113 · see citing works
Lehmann, J., Russig, H. D., Feldon, J., & Pryce, C. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00788-8 · Cited by 111 · see citing works
Poeggel, G., Helmeke, C., Abraham, A., Schwabe, T., Friedrich, P., & Braun, K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2434663100 · Cited by 107 · see citing works
Helmeke, C. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.8.717 · Cited by 106 · see citing works
Ovtscharoff, W. A., & Braun, K. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00059-8 · Cited by 104 · see citing works
Goldin, M. M., Segal, M., & Avignone, E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00186.2001 · Cited by 100 · see citing works
Daily injections alter spine density in rat medial prefrontal cortex
Seib, L. M., & Wellman, C. L. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01287-9 · Cited by 100 · see citing works
Molecular basis for induction of ocular dominance plasticity
Bear, M. F., & Rittenhouse, C. D. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199910)41:1 · Cited by 99 · see citing works
Horner, C. H., & Arbuthnott, E. R. (1991) · Europe PMC (PubMed Central) · Cited by 90 · see citing works
Avishai‐Eliner, S., Hatalski, C. G., Tabachnik, E., Eghbal-Ahmadi, M., & Baram, T. Z. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00031-0 · Cited by 63 · see citing works
Helmeke, C., Poeggel, G., & Braun, K. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00201-9 · Cited by 60 · see citing works
Bock, J., & Braun, K. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00713.x · Cited by 50 · see citing works
Bock, J., & Braun, K. (1998) · Neural Plasticity · doi:10.1155/np.1998.17 · Cited by 43 · see citing works
Dendritic spines: elementary structural units of neuronal plasticity
Segal, M. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)38070-1 · Cited by 32 · see citing works
Synaptic remodelling and elimination as integral processes of synaptogenesis.
Wolff, J. R., & Missler, M. (1993) · PubMed · Cited by 28 · see citing works
The dynamics of spine density changes
Lieshoff, C., & Bischof, H. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00271-1 · Cited by 16 · see citing works
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2
Flagged first, then by citations
Cited by
Sorted by citations
The effects of childhood maltreatment on brain structure, function and connectivity
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.111 · Cited by 1,856 · see citing works
Lasting epigenetic influence of early-life adversity on the BDNF gene
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.028 · Cited by 1,273 · 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
Anatomy of the Prefrontal Cortex
Fuster, J. M. (2008) · The Prefrontal Cortex · doi:10.1016/b978-0-12-373644-4.00002-5 · Cited by 364 · see citing works
Murmu, M. S., Salomon, S., Biala, Y., Weinstock, M., Braun, K., & Bock, J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05024.x · Cited by 278 · see citing works
Self-citationAnatomy of the Prefrontal Cortex
Fuster, J. M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-407815-4.00002-7 · Cited by 272 · see citing works
Spine synapse remodeling in the pathophysiology and treatment of depression
Duman, C. H., & Duman, R. S. (2015) · Neuroscience Letters · doi:10.1016/j.neulet.2015.01.022 · Cited by 257 · see citing works
Epigenetic marking of the BDNF gene by early-life adverse experiences
Roth, T. L., & Sweatt, J. D. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.05.005 · Cited by 196 · see citing works
Virtual Reality for Neurorehabilitation and Cognitive Enhancement
Георгиев, Д., Georgieva, I., Gong, Z., Nanjappan, V., & Georgiev, G. V. (2021) · Brain Sciences · doi:10.3390/brainsci11020221 · Cited by 213 · see citing works
Monroy, E., Hernández‐Torres, E., & Flores, G. (2010) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2010.05.005 · Cited by 182 · see citing works
den Bergh, B. R. H. V. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.04057.x · Cited by 179 · see citing works
Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression
Licznerski, P., & Duman, R. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.057 · Cited by 157 · see citing works
Paternal Influences on Offspring Development: Behavioural and Epigenetic Pathways
Braun, K., & Champagne, F. A. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12174 · Cited by 157 · see citing works
Self-citationChocyk, A., Bobula, B., Dudys, D., Przyborowska, A., Majcher-Maślanka, I., Hess, G., & Wędzony, K. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12208 · Cited by 153 · see citing works
Rapid infant prefrontal cortex development and sensitivity to early environmental experience
Hodel, A. S. (2018) · Developmental Review · doi:10.1016/j.dr.2018.02.003 · Cited by 160 · see citing works
Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex
Muhammad, A., Carroll, C., & Kolb, B. E. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.041 · Cited by 146 · see citing works
Perinatal programming of emotional brain circuits: an integrative view from systems to molecules
Bock, J., Rether, K., Gröger, N., Xie, L., & Braun, K. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00011 · Cited by 143 · see citing works
Koss, K. J., Mliner, S. B., Donzella, B., & Gunnar, M. R. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.12.018 · Cited by 133 · see citing works
Dendritic Branch Typing and Spine Expression Patterns in Cortical Nonpyramidal Cells
Kawaguchi, Y., Karube, F., & Kubota, Y. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj015 · Cited by 125 · see citing works
Lesuis, S. L., Hoeijmakers, L., Kőrösi, A., de Rooij, S. R., Swaab, D. F., Kessels, H. W. H. G., Lucassen, P. J., & Krugers, H. J. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0422-7 · Cited by 120 · see citing works
Stress-induced alterations in large-scale functional networks of the rodent brain
Henckens, M. J. A. G., van der Marel, K., van der Toorn, A., Pillai, A. G., Fernández, G., Dijkhuizen, R. M., & Joëls, M. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.037 · Cited by 110 · see citing works
Koe, A. S., Ashokan, A., & Mitra, R. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.217 · Cited by 109 · see citing works
Muhammad, A., & Kolb, B. E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.015 · Cited by 105 · see citing works
Potential programming of dopaminergic circuits by early life stress
Rodrigues, A.-J., Leão, P., Carvalho, M., Almeida, O. F. X., & Sousa, N. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2085-3 · Cited by 97 · see citing works
Sullivan, R. M., Wilson, D. A., Feldon, J., Yee, B. K., Meyer, U., Richter‐Levin, G., Avital, A., Tsoory, M., Gruß, M., Bock, J., et al. (2006) · Developmental Psychobiology · doi:10.1002/dev.20170 · Cited by 98 · see citing works
Yang, X.-D., Liao, X.-M., Uribe-Mariño, A., Liu, R., Xie, X.-M., Jia, J., Su, Y.-A., Li, J.-T., Schmidt, M. V., Wang, X.-D., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.304 · Cited by 93 · see citing works
Xie, L., Korkmaz, K., Braun, K., & Bock, J. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12210 · Cited by 92 · see citing works
Farrell, M. R., Holland, F. H., Shansky, R. M., & Brenhouse, H. C. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.009 · Cited by 90 · see citing works
Goodfellow, N. M., Benekareddy, M., Vaidya, V. A., & Lambe, E. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1960-09.2009 · Cited by 90 · see citing works
Early secure attachment as a protective factor against later cognitive decline and dementia
Walsh, E., Blake, Y., Donati, A., Stoop, R., & von Gunten, A. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00161 · Cited by 84 · see citing works
Richards, S., Mychasiuk, R., Kolb, B. E., & Gibb, R. L. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.02.043 · Cited by 84 · see citing works
Social Origins of Developmental Risk for Mental and Physical Illness
Cameron, J. L., Eagleson, K. L., Fox, N. A., Hensch, T. K., & Levitt, P. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1822-17.2017 · Cited by 81 · see citing works
Helmeke, C., Ovtscharoff, W. A., Poeggel, G., & Braun, K. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.12.023 · Cited by 77 · see citing works
The neurobiological effects of childhood maltreatment on brain structure, function, and attachment
Tomoda, A., Nishitani, S., Takiguchi, S., Fujisawa, T. X., Sugiyama, T., & Teicher, M. H. (2024) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-024-01779-y · Cited by 96 · see citing works
The prefrontal–limbic network in depression: A core pathology of synapse regression
Bennett, M. R. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.01.001 · Cited by 74 · see citing works
Lack of paternal care affects synaptic development in the anterior cingulate cortex
Ovtscharoff, W. A., Helmeke, C., & Braun, K. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.106 · Cited by 70 · see citing works
Chorna, O. D., Solomon, J., Slaughter, J. C., Stark, A. R., & Maitre, N. L. (2014) · Archives of Disease in Childhood Fetal & Neonatal · doi:10.1136/archdischild-2014-306486 · Cited by 69 · see citing works
Evolution, development, and plasticity of the human brain: from molecules to bones
Hrvoj-Mihić, B., Bienvenu, T., Stefanacci, L., Muotri, A. R., & Semendeferi, K. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00707 · Cited by 67 · see citing works
Kambali, M., Anshu, K., Kutty, B. M., Muddashetty, R. S., & Laxmi, T. R. (2019) · Experimental Brain Research · doi:10.1007/s00221-019-05567-2 · Cited by 65 · see citing works
Structural Plasticity within the Barrel Cortex during Initial Phases of Whisker-Dependent Learning
Kuhlman, S. J., O’Connor, D. H., Fox, K. D., & Svoboda, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4919-12.2014 · Cited by 61 · see citing works
Gruss, M., Braun, K., Frey, J. U., & Korz, V. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2007.12.033 · Cited by 64 · see citing works
Braun, K. (2011) · Clinics in Perinatology · doi:10.1016/j.clp.2011.08.013 · Cited by 63 · see citing works
Gröger, N., Matas, E., Gos, T., Lesse, A., Poeggel, G., Braun, K., & Bock, J. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1570-1 · Cited by 61 · see citing works
Pascual, R., & Zamora-León, S. (2007) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2007-1663 · Cited by 74 · see citing works
Environmental and genetic influences on early attachment
Gervai, J. (2009) · Child and Adolescent Psychiatry and Mental Health · doi:10.1186/1753-2000-3-25 · Cited by 59 · see citing works
Nietzer, S., Bonn, M., Jansen, F., Heiming, R. S., Lewejohann, L., Sachser, N., Asan, E., Lesch, K., & Schmitt, A. G. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.01.011 · Cited by 59 · see citing works
Early maternal separation impacts cognitive flexibility at the age of first independence in mice
Thomas, A. W., Caporale, N., Wu, C., & Wilbrecht, L. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.09.005 · Cited by 57 · see citing works
Adrenarche in comparative perspective
Campbell, B. (2010) · American Journal of Human Biology · doi:10.1002/ajhb.21111 · Cited by 56 · see citing works
Rincel, M., Lépinay, A. L., Janthakhin, Y., Soudain, G., Yvon, S., Silva, S. D., Joffre, C., Aubert, A., Séré, A., Layé, S., et al. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1526-8 · Cited by 56 · see citing works
Chocyk, A., Majcher-Maślanka, I., Dudys, D., Przyborowska, A., & Wędzony, K. (2013) · Pharmacological Reports · doi:10.1016/s1734-1140(13)71506-8 · Cited by 55 · see citing works
Gos, T., Bock, J., Poeggel, G., & Braun, K. (2007) · Synapse · doi:10.1002/syn.20477 · Cited by 55 · see citing works
Early-life stress increases the motility of microglia in adulthood
Takatsuru, Y., Nabekura, J., Ishikawa, T., Kohsaka, S., & Koibuchi, N. (2015) · The Journal of Physiological Sciences · doi:10.1007/s12576-015-0361-z · Cited by 55 · see citing works
Braun, K., & Bock, J. (2011) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2011.04056.x · Cited by 54 · see citing works
Bock, J., Poeschel, J., Schindler, J., Börner, F., Shachar-Dadon, A., Ferdman, N., Gaisler‐Salomon, I., Leshem, M., Braun, K., & Poeggel, G. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0940-4 · Cited by 53 · see citing works
Gunnar, M. R., Wenner, J. A., Thomas, K. M., Glatt, C. E., McKenna, M. C., & Clark, A. G. (2012) · Development and Psychopathology · doi:10.1017/s095457941200065x · Cited by 53 · see citing works
Glucocorticoids and neuro- and behavioural development
Mesquita, A. R., Wegerich, Y., Patchev, A. V., de Oliveira, M. C., Leão, P., Sousa, N., & Almeida, O. F. X. (2008) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2008.11.002 · Cited by 51 · see citing works
The epileptic hypothesis: Developmentally related arguments based on animal models
Galanopoulou, A. S., & Moshé, S. L. (2009) · Epilepsia · doi:10.1111/j.1528-1167.2009.02217.x · Cited by 50 · see citing works
Early Life Stress and Pediatric Posttraumatic Stress Disorder
Pervanidou, P., Makris, G., Chrousos, G. P., & Agorastos, A. (2020) · Brain Sciences · doi:10.3390/brainsci10030169 · Cited by 50 · see citing works
Sexual Differentiation of the Brain and ADHD: What Is a Sex Difference in Prevalence Telling Us?
Waddell, J., & McCarthy, M. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_114 · Cited by 45 · see citing works
Rodríguez, D. A. L., & Dueñas, Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068010 · Cited by 56 · see citing works
van Hasselt, F. N., de Visser, L., Tieskens, J. M., Cornelisse, S., Baars, A. M., Lavrijsen, M., Krugers, H. J., van den Bos, R., & Joëls, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037820 · Cited by 49 · see citing works
Maternal separation in rodents: a journey from gut to brain and nutritional perspectives
Rincel, M., & Darnaudéry, M. (2019) · Proceedings of The Nutrition Society · doi:10.1017/s0029665119000958 · Cited by 50 · see citing works
The burden of early life stress on the nociceptive system development and pain responses
Melchior, M., Kuhn, P., & Poisbeau, P. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15153 · Cited by 49 · see citing works
Callaghan, B., Graham, B. M., Li, S., & Richardson, R. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00090 · Cited by 45 · see citing works
Mychasiuk, R., Hehar, H., Ma, I. W. Y., Kolb, B. E., & Esser, M. J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.034 · Cited by 47 · see citing works
Miller, M. M., Morrison, J. H., & McEwen, B. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.029 · Cited by 46 · see citing works
Seidel, K., Helmeke, C., Poeggel, G., & Braun, K. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20651 · Cited by 44 · see citing works
Yang, Y., Cheng, Z., Tang, H., Jiao, H., Sun, X., Cui, Q., Luo, F., Pan, H., Ma, C., & Li, B. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw121 · Cited by 124 · see citing works
Gos, T., Becker, K., Bock, J., Malecki, U., Bogerts, B., Poeggel, G., & Braun, K. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.078 · Cited by 42 · see citing works
Stress inoculation in mice induces global resilience
Ayash, S., Schmitt, U., Lyons, D. M., & Müller, M. B. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-00889-0 · Cited by 41 · see citing works
A study on fear memory retrieval and REM sleep in maternal separation and isolation stressed rats
Sampath, D., Sabitha, K. R., Hegde, P., Jayakrishnan, H. R., Kutty, B. M., Chattarji, S., Rangarajan, G., & Laxmi, T. R. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.034 · Cited by 40 · see citing works
The impact of perinatal stress on the functional maturation of prefronto-cortical synaptic circuits
Bock, J., & Braun, K. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53884-0.00023-3 · Cited by 39 · see citing works
Maternal separation decreases the stability of mushroom spines in adult mice somatosensory cortex
Takatsuru, Y., Yoshitomo, M., Nemoto, T., Eto, K., & Nabekura, J. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.092 · Cited by 39 · see citing works
Brain development, experience, and behavior
Kolb, B. E., Mychasiuk, R., & Gibb, R. L. (2013) · Pediatric Blood & Cancer · doi:10.1002/pbc.24908 · Cited by 40 · see citing works
Fachim, H., Zuelli, F. M. D. G. C., Loureiro, C. M., Iamjan, S.-A., Shuhama, R., Joca, S. R. L., Menezes, P. R., Heald, A. H., Louzada‐Júnior, P., Dalton, C., et al. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110188 · Cited by 38 · see citing works
Alteba, S., Zer‐Aviv, T. M., Tenenhaus, A., David, G. B., Adelman, J. W., Hillard, C. J., Doron, R., & Akirav, I. (2020) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2020.08.005 · Cited by 37 · see citing works
Gender- and anxiety level-dependent effects of perinatal stress exposure on medial prefrontal cortex
Söztutar, E., Çolak, E., & Ulupınar, E. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.06.005 · Cited by 38 · see citing works
Kunzler, J., Braun, K., & Bock, J. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0688-2 · Cited by 38 · see citing works
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Lux, V. (2018) · Current Genomics · doi:10.2174/1389202919666180307151358 · Cited by 35 · see citing works
Xiong, G.-J., Yang, Y., Wang, L.-P., Xu, L., & Mao, R.-R. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.015 · Cited by 43 · see citing works
Bustamante, C., Henríquez, R., Medina, F., Reinoso, C., Vargas-Foitzick, R., & Pascual, R. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.02.007 · Cited by 35 · see citing works
Bock, J., Nielsen, R. M., Ferdman, N., Leshem, M., & Braun, K. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20622 · Cited by 35 · see citing works
Cao, B., Wang, J., Zhang, X., Yang, X., Poon, D. C.-H., Jelfs, B., Chan, R. H. M., Wu, J. C., & Li, Y. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.09.015 · Cited by 33 · see citing works
Orłowski, D., & Bjarkam, C. R. (2012) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2012.05.009 · Cited by 34 · see citing works
Mareckova, K., Miles, A., Andryskova, L., Brazdil, M., & Nikolova, Y. S. (2020) · Human Brain Mapping · doi:10.1002/hbm.25163 · Cited by 32 · see citing works
Zhang, B. (2017) · PubMed Central · doi:10.13918/j.issn.2095-8137.2017.002 · Cited by 31 · see citing works
Merz, E. C., Myers, B., Hansen, M., Simon, K. R., Strack, J., & Noble, K. G. (2023) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2023.10.004 · Cited by 30 · see citing works
Early‐life‐stress affects the homeostasis of glutamatergic synapses
Toya, S., Takatsuru, Y., Kokubo, M., Amano, I., Shimokawa, N., & Koibuchi, N. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12728 · Cited by 30 · see citing works
Brief maternal separation affects brain α1-adrenoceptors and apoptotic signaling in adult mice
Coccurello, R., Bielawski, A., Zelek-Molik, A., Vetulani, J., Kowalska, M., D'Amato, F. R., & Nalepa, I. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.10.004 · Cited by 30 · see citing works
Hescham, S., Grace, L. K., Kellaway, L. A., Bugarith, K., & Russell, V. A. (2009) · Metabolic Brain Disease · doi:10.1007/s11011-009-9165-2 · Cited by 30 · see citing works
Ahmadi, B. B. M., Afarinesh, M. R., Jafaripour, L., & Sheibani, V. (2022) · Brain and Behavior · doi:10.1002/brb3.2993 · Cited by 29 · see citing works
Gruss, M., Westphal, S., Luley, C. H., & Braun, K. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.08.017 · Cited by 28 · see citing works
Brain Plasticity and Experience
Kolb, B. E. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804036-2.00013-3 · Cited by 28 · see citing works
Wang, H., Meyer, K., & Korz, V. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.06.004 · Cited by 28 · see citing works
Ontogeny of the HPA axis of the CD1 mouse following 24 h maternal deprivation at pnd 3
Enthoven, L., Schmidt, M. V., Cheung, Y. H., van der Mark, M. H., de Kloet, E. R., & Oitzl, M. S. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.10.006 · Cited by 27 · see citing works
de Melo, S. R., Antoniazzi, C. T. D. D., Hossain, S., & Kolb, B. E. (2018) · Developmental Neuroscience · doi:10.1159/000486619 · Cited by 28 · see citing works
Köhler, J. C., Gröger, N., Lesse, A., Guara Ciurana, S., Rether, K., Fegert, J., Bock, J., & Braun, K. (2019) · Molecular Neurobiology · doi:10.1007/s12035-018-1199-1 · Cited by 28 · see citing works
Stress and prefrontal cortical plasticity in the developing brain
Kolb, B. E., Harker, A., Mychasiuk, R., de Melo, S. R., & Gibb, R. L. (2017) · Cognitive Development · doi:10.1016/j.cogdev.2017.01.001 · Cited by 27 · see citing works
Long term effects of early life stress on HPA circuit in rodent models
Babicola, L., Ventura, R., D’Addario, S. L., Ielpo, D., Andolina, D., & Segni, M. D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111125 · Cited by 27 · see citing works
- Authors
- Bock, J., Gruss, M., Becker, S., & Braun, K.
- Affiliations
- Otto-von-Guericke-Universität Magdeburg (DE)
- Corresponding author
- Bock, Jörg
- ORCID
- Braun, Katharina
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2004-09-15
- Volume
- 15
- Issue
- 6
- Pages
- 802-808
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2142364482
- Cited by
- 175
- References
- 57
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 6 · 2023: 2 · 2022: 5 · 2021: 4 · 2020: 10 · 2019: 5 · 2018: 12 · 2017: 14 · 2016: 9 · 2015: 10 · 2014: 21 · 2013: 14 · 2012: 11
- FWCI
- 1.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Leibniz-Gemeinschaft
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- dendritic spine density, experience-dependent synaptic plasticity, maternal separation, stress hyporesponsive period, hypothalamic-pituitary-adrenal axis, corticosterone, anterior cingulate cortex, somatosensory cortex, pyramidal neurons, cortical development, emotional experience
- MeSH terms
- Animals, Body Weight, Corticosterone, Gyrus Cinguli, Hypothalamo-Hypophyseal System, Limbic System, Male, Organ Size, Pituitary-Adrenal System, Social Isolation, Somatosensory Cortex, Stress, Psychological, Rats, Wistar, Prefrontal Cortex, Pyramidal Cells, Dendritic Spines, Rats
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