Abstract
Early life stress (ELS) is one of the most critical factors that could modify brain plasticity, memory and learning abilities, behavioral reactions, and emotional response in adulthood leading to development of different mental disorders. Prenatal and early postnatal periods appear to be the most sensitive periods of brain development in mammals, thereby action of various factors at these stages of brain development might result in neurodegeneration, memory impairment, and mood disorders at later periods of life. Deciphering the processes underlying aberrant neurogenesis, synaptogenesis, and cerebral angiogenesis as well as deeper understanding the effects of ELS on brain development will provide novel approaches to prevent or to cure psychiatric and neurological deficits caused by stressful conditions at the earliest stages of ontogenesis. Neuropeptide oxytocin serves as an amnesic, anti-stress, pro-angiogenic, and neurogenesis-controlling molecule contributing to dramatic changes in brain plasticity in ELS. In the current review, we summarize recent data on molecular mechanisms of ELS-driven changes in brain plasticity with the particular focus on oxytocin-mediated effects on neurogenesis and angiogenesis, memory establishment, and forgetting.
Funding source: Russian Foundation for Basic Research (RFBR)
Award Identifier / Grant number: project number 20-015-00472\20
Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: The study was funded by the Russian Foundation for Basic Research (RFBR), project number 20-015-00472\20.
Conflict of interest statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Abbink, M.R., van Deijk, A.-L.F., Heine, V.M., Verheijen, M.H., and Korosi, A. (2019). The involvement of astrocytes in early-life adversity induced programming of the brain. Glia 67: 1637–1653, https://doi.org/10.1002/glia.23625.Search in Google Scholar PubMed PubMed Central
Adlaf, E.W., Vaden, R.J., Niver, A.J., Manuel, A.F., Onyilo, V.C., Araujo, M.T., Dieni, C.V., Vo, H.T., King, G.D., Wadiche, J.I., et al.. (2017). Adult-born neurons modify excitatory synaptic transmission to existing neurons. eLife 6: e19886, https://doi.org/10.7554/elife.19886.Search in Google Scholar PubMed PubMed Central
Alberini, C.M. and Travaglia, A. (2017). Infantile amnesia: a critical period of learning to learn and remember. J. Neurosci. 37: 5783–5795, https://doi.org/10.1523/jneurosci.0324-17.2017.Search in Google Scholar PubMed PubMed Central
Aust, S., Stasch, J., Jentschke, S., Alkan Härtwig, E., Koelsch, S., Heuser, I., and Bajbouj, M. (2014). Differential effects of early life stress on hippocampus and amygdala volume as a function of emotional abilities. Hippocampus 24: 1094–1101, https://doi.org/10.1002/hipo.22293.Search in Google Scholar PubMed
Baek, S.S., Jun, T.W., Kim, K.J., Shin, M.S., Kang, S.Y., and Kim, C.J. (2012). Effects of postnatal treadmill exercise on apoptotic neuronal cell death and cell proliferation of maternal-separated rat pups. Brain Dev. 34: 45–56, https://doi.org/10.1016/j.braindev.2011.01.011.Search in Google Scholar PubMed
Banqueri, M., Méndez, M., Gómez-Lázaro, E., and Arias, J.L. (2019). Early life stress by repeated maternal separation induces long-term neuroinflammatory response in glial cells of male rats. Stress 22: 563–570, https://doi.org/10.1080/10253890.2019.1604666.Search in Google Scholar PubMed
Baracz, S.J., Everett, N.A., and Cornish, J.L. (2020). The impact of early life stress on the central oxytocin system and susceptibility for drug addiction: applicability of oxytocin as a pharmacotherapy. Neurosci. Biobehav. Rev. 110: 114–132, https://doi.org/10.1016/j.neubiorev.2018.08.014.Search in Google Scholar PubMed
Barry, D.N. and Commins, S. (2017). Temporal dynamics of immediate early gene expression during cellular consolidation of spatial memory. Behav. Brain Res. 327: 44–53, https://doi.org/10.1016/j.bbr.2017.03.019.Search in Google Scholar PubMed
Bekinschtein, P., Weisstaub, N.V., Gallo, F., Renner, M., and Anderson, M.C. (2018). A retrieval-specific mechanism of adaptive forgetting in the mammalian brain. Nat. Commun. 9: 4660–4660, https://doi.org/10.1038/s41467-018-07128-7.Search in Google Scholar PubMed PubMed Central
Bessières, B., Travaglia, A., Mowery, T.M., Zhang, X., and Alberini, C.M. (2020). Early life experiences selectively mature learning and memory abilities. Nat. Commun. 11: 628–628, https://doi.org/10.1038/s41467-020-14461-3.Search in Google Scholar PubMed PubMed Central
Blankenship, S.L., Botdorf, M., Riggins, T., and Dougherty, L.R. (2019). Lasting effects of stress physiology on the brain: cortisol reactivity during preschool predicts hippocampal functional connectivity at school age. Dev. Cognit. Neurosci. 40: 100736–100736, https://doi.org/10.1016/j.dcn.2019.100736.Search in Google Scholar
Bloodgood, B.L., Sharma, N., Browne, H.A., Trepman, A.Z., and Greenberg, M.E. (2013). The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition. Nature 503: 121–125, https://doi.org/10.1038/nature12743.Search in Google Scholar
Brunson, K.L., Chen, Y., Avishai-Eliner, S., and Baram, T.Z. (2003). Stress and the developing hippocampus: a double-edged sword? Mol. Neurobiol. 27: 121–136, https://doi.org/10.1385/mn:27:2:121.10.1385/MN:27:2:121Search in Google Scholar
Cain, C.K., Maynard, G.D., and Kehne, J.H. (2012). Targeting memory processes with drugs to prevent or cure PTSD. Expet Opin. Invest. Drugs 21: 1323–1350, https://doi.org/10.1517/13543784.2012.704020.Search in Google Scholar
Cattaneo, M.G., Lucci, G., and Vicentini, L.M. (2009). Oxytocin stimulates in vitro angiogenesis via a Pyk-2/Src-dependent mechanism. Exp. Cell Res. 315: 3210–3219, https://doi.org/10.1016/j.yexcr.2009.06.022.Search in Google Scholar
Çelik, K., Bilim, P., Garip, G., Durmaz, B., Giray, Y., Şura, P., Sozmen, E., and Meral, B. (2019). Effects of prenatal stress prior to early life seizures on progenitor/stem cells, angiogenesis and object recognition.Search in Google Scholar
Chocyk, A., Dudys, D., Przyborowska, A., Maćkowiak, M., and Wędzony, K. (2010). Impact of maternal separation on neural cell adhesion molecules expression in dopaminergic brain regions of juvenile, adolescent and adult rats. Pharmacol. Rep. 62: 1218–1224, https://doi.org/10.1016/s1734-1140(10)70385-6.Search in Google Scholar
Coelho-Santos, V. and Shih, A.Y. (2020). Postnatal development of cerebrovascular structure and the neurogliovascular unit. Wiley interdisciplinary reviews. Dev. Biol. 9: e363–e363, https://doi.org/10.1002/wdev.363.Search in Google Scholar
Cremer, H., Chazal, G., Lledo, P.-M., Rougon, G., Montaron, M., Mayo, W., Moal, M., and Abrous, D. (2000). PSA-NCAM: an important regulator of hippocampal plasticity. Int. J. Dev. Neurosci. 18: 213–220, https://doi.org/10.1016/s0736-5748(99)00090-8.Search in Google Scholar
Cui, Y., Cao, K., Lin, H., Cui, S., Shen, C., Wen, W., Mo, H., Dong, Z., Bai, S., and Yang, L., et al.. (2020). Early-life stress induces depression-like behavior and synaptic-plasticity changes in a maternal separation rat model: gender difference and metabolomics study. Front. Pharmacol. 11: 102, https://doi.org/10.3389/fphar.2020.00102.Search in Google Scholar
de Campo, D.M., Cameron, J.L., Miano, J.M., Lewis, D.A., Mirnics, K., and Fudge, J.L. (2017). Maternal deprivation alters expression of neural maturation gene tbr1 in the amygdala paralaminar nucleus in infant female macaques. Dev. Psychobiol. 59: 235–249, https://doi.org/10.1002/dev.21493.Search in Google Scholar PubMed PubMed Central
Dudek, K.A., Dion-Albert, L., Lebel, M., LeClair, K., Labrecque, S., Tuck, E., Ferrer Perez, C., Golden, S.A., Tamminga, C., Turecki, G., et al.. (2020). Molecular adaptations of the blood-brain barrier promote stress resilience vs. depression. Proc. Natl. Acad. Sci. U.S.A. 117: 3326–3336, https://doi.org/10.1073/pnas.1914655117.Search in Google Scholar PubMed PubMed Central
Ershov, N.I., Bondar, N.P., Lepeshko, A.A., Reshetnikov, V.V., Ryabushkina, J.A., and Merkulova, T.I. (2018). Consequences of early life stress on genomic landscape of H3K4me3 in prefrontal cortex of adult mice. BMC Genom. 19: 93, https://doi.org/10.1186/s12864-018-4479-2.Search in Google Scholar PubMed PubMed Central
Estes, M.K., Freels, T.G., Prater, W.T., and Lester, D.B. (2019). Systemic oxytocin administration alters mesolimbic dopamine release in mice. Neuroscience 408: 226–238, https://doi.org/10.1016/j.neuroscience.2019.04.006.Search in Google Scholar PubMed
Feliciano, D.M. and Bordey, A. (2013). Newborn cortical neurons: only for neonates? Trends Neurosci. 36: 51–61, https://doi.org/10.1016/j.tins.2012.09.004.Search in Google Scholar PubMed PubMed Central
Ferguson, B.R. and Gao, W.J. (2018). PV Interneurons: critical regulators of E/I balance for prefrontal cortex-dependent behavior and psychiatric disorders. Front. Neural Circ. 12: 37, https://doi.org/10.3389/fncir.2018.00037.Search in Google Scholar PubMed PubMed Central
Filova, B., Reichova, A., Zatkova, M., Srancikova, A., Bukatova, S., Bacova, Z., and Bakos, J. (2020). Expression of synaptic proteins in the hippocampus is modulated by neonatal oxytocin treatment. Neurosci. Lett. 725: 134912, https://doi.org/10.1016/j.neulet.2020.134912.Search in Google Scholar PubMed
Fontana, B.D., Gibbon, A.J., Cleal, M., Sudwarts, A., Pritchett, D., Miletto Petrazzini, M.E., Brennan, C.H., and Parker, M.O. (2020). Moderate early life stress improves adult zebrafish (Danio rerio) working memory but does not affect social and anxiety-like responses. Dev. Psychobiol. 1–11, https://doi.org/10.1002/dev.21986.Search in Google Scholar PubMed
Fonzo, G.A., Ramsawh, H.J., Flagan, T.M., Simmons, A.N., Sullivan, S.G., Allard, C.B., Paulus, M.P., and Stein, M.B. (2016). Early life stress and the anxious brain: evidence for a neural mechanism linking childhood emotional maltreatment to anxiety in adulthood. Psychol. Med. 46: 1037–1054, https://doi.org/10.1017/s0033291715002603.Search in Google Scholar PubMed PubMed Central
Fujisawa, T.X., Nishitani, S., Takiguchi, S., Shimada, K., Smith, A.K., and Tomoda, A. (2019). Oxytocin receptor DNA methylation and alterations of brain volumes in maltreated children. Neuropsychopharmacology 44: 2045–2053, https://doi.org/10.1038/s41386-019-0414-8.Search in Google Scholar PubMed PubMed Central
García-Muse, T. and Aguilera, A. (2016). Transcription–replication conflicts: how they occur and how they are resolved. Nat. Rev. Mol. Cell Biol. 17: 553–563, https://doi.org/10.1038/nrm.2016.88.Search in Google Scholar PubMed
González-Pardo, H., Arias, J.L., Vallejo, G., and Conejo, N.M. (2019). Environmental enrichment effects after early stress on behavior and functional brain networks in adult rats. PloS One 14: e0226377, https://doi.org/10.1371/journal.pone.0226377.Search in Google Scholar
Gouin, J.P., Zhou, Q.Q., Booij, L., Boivin, M., Côté, S.M., Hébert, M., Ouellet-Morin, I., Szyf, M., Tremblay, R.E., Turecki, G., et al.. (2017). Associations among oxytocin receptor gene (OXTR) DNA methylation in adulthood, exposure to early life adversity, and childhood trajectories of anxiousness. Sci. Rep. 7: 7446, https://doi.org/10.1038/s41598-017-07950-x.Search in Google Scholar
Gunn, B.G., Cunningham, L., Cooper, M.A., Corteen, N.L., Seifi, M., Swinny, J.D., Lambert, J.J., and Belelli, D. (2013). Dysfunctional astrocytic and synaptic regulation of hypothalamic glutamatergic transmission in a mouse model of early-life adversity: relevance to neurosteroids and programming of the stress response. J. Neurosci. 33: 19534–19554, https://doi.org/10.1523/jneurosci.1337-13.2013.Search in Google Scholar
Heim, C., Meinlschmidt, G., and Nemeroff, C. (2003). The neurobiology of early-life stress and its relationship to PTSD. Psychiatr. Ann. 33: 18–26, https://doi.org/10.3928/0048-5713-20030101-05.Search in Google Scholar
Heinrichs, M., Meinlschmidt, G., Wippich, W., Ehlert, U., and Hellhammer, D. (2004). Selective amnesic effects of oxytocin on human memory. Physiol. Behav. 83: 31–38, https://doi.org/10.1016/s0031-9384(04)00346-4.Search in Google Scholar
Higashida, H., Yokoyama, S., Kikuchi, M., and Munesue, T. (2012). CD38 and its role in oxytocin secretion and social behavior. Horm. Behav. 61: 351–358, https://doi.org/10.1016/j.yhbeh.2011.12.011.Search in Google Scholar PubMed
Hoeijmakers, L., Ruigrok, S.R., Amelianchik, A., Ivan, D., van Dam, A.M., Lucassen, P.J., and Korosi, A. (2017). Early-life stress lastingly alters the neuroinflammatory response to amyloid pathology in an Alzheimer’s disease mouse model. Brain Behav. Immun. 63: 160–175, https://doi.org/10.1016/j.bbi.2016.12.023.Search in Google Scholar PubMed
Holahan, M.R., Tzakis, N., and Oliveira, F.A. (2019). Developmental aspects of glucose and calcium availability on the persistence of memory function over the lifespan. Front. Aging Neurosci. 11: 253–253, https://doi.org/10.3389/fnagi.2019.00253.Search in Google Scholar PubMed PubMed Central
Josselyn, S.A. and Frankland, P.W. (2012). Infantile amnesia: a neurogenic hypothesis. Learn. Mem. 19: 423–433, https://doi.org/10.1101/lm.021311.110.Search in Google Scholar PubMed
Katche, C., Tomaiuolo, M., Dorman, G., Medina, J.H., and Viola, H. (2016). Novelty during a late postacquisition time window attenuates the persistence of fear memory. Sci. Rep. 6: 35220, https://doi.org/10.1038/srep35220.Search in Google Scholar PubMed PubMed Central
Kompier, N.F., Keysers, C., Gazzola, V., Lucassen, P.J., and Krugers, H.J. (2019). Early life adversity and adult social behavior: focus on arginine vasopressin and oxytocin as potential mediators. Front. Behav. Neurosci. 13: 143–143, https://doi.org/10.3389/fnbeh.2019.00143.Search in Google Scholar PubMed PubMed Central
König, R., Benedetti, B., Rotheneichner, P., O’ Sullivan, A., Kreutzer, C., Belles, M., Nacher, J., Weiger, T.M., Aigner, L., and Couillard-Després, S. (2016). Distribution and fate of DCX/PSA-NCAM expressing cells in the adult mammalian cortex: a local reservoir for adult cortical neuroplasticity? Front. Biol. 11: 193–213, https://doi.org/10.1007/s11515-016-1403-5.Search in Google Scholar
Koutmani, Y. and Karalis, K.P. (2015). Neural stem cells respond to stress hormones: distinguishing beneficial from detrimental stress. Front. Physiol. 6: 77–77, https://doi.org/10.3389/fphys.2015.00077.Search in Google Scholar PubMed PubMed Central
Kozberg, M.G. and Hillman, E.M.C. (2016). Neurovascular coupling develops alongside neural circuits in the postnatal brain. Neurogenesis 3: e1244439–e1244439, https://doi.org/10.1080/23262133.2016.1244439.Search in Google Scholar PubMed PubMed Central
Krol, K.M., Moulder, R.G., Lillard, T.S., Grossmann, T., and Connelly, J.J. (2019). Epigenetic dynamics in infancy and the impact of maternal engagement. Sci. Adv. 5: eaay0680, https://doi.org/10.1126/sciadv.aay0680.Search in Google Scholar PubMed PubMed Central
Kuvacheva, N.V., Morgun, A.V., Malinovskaya, N.A., Gorina, Y.V., Khilazheva, E.D., Pozhilenkova, E.A., Panina, Y.A., Boytsova, E.B., Ruzaeva, V.A., Trufanova, L.V., et al.. (2016). Tight junction proteins of cerebral endothelial cells in early postnatal development. Cell Tissue Biol. 10: 372–377, https://doi.org/10.1134/s1990519x16050084.Search in Google Scholar
Lacoste, B. and Gu, C. (2015). Control of cerebrovascular patterning by neural activity during postnatal development. Mech. Dev. 138: 43–49, https://doi.org/10.1016/j.mod.2015.06.003.Search in Google Scholar PubMed PubMed Central
Lee, M.M., Reif, A., and Schmitt, A.G. (2013). Major depression: a role for hippocampal neurogenesis? Curr. Top Behav. Neurosci. 14: 153–179, https://doi.org/10.1007/7854_2012_226.Search in Google Scholar PubMed
Leonzino, M., Busnelli, M., Antonucci, F., Verderio, C., Mazzanti, M., and Chini, B. (2016). The timing of the excitatory-to-inhibitory GABA switch is regulated by the oxytocin receptor via KCC2. Cell Rep. 15: 96–103, https://doi.org/10.1016/j.celrep.2016.03.013.Search in Google Scholar PubMed PubMed Central
Lesuis, S.L., Lucassen, P.J., and Krugers, H.J. (2019). Early life stress impairs fear memory and synaptic plasticity; a potential role for GluN2B. Neuropharmacology 149: 195–203, https://doi.org/10.1016/j.neuropharm.2019.01.010.Search in Google Scholar PubMed
Leuner, B., Caponiti, J.M., and Gould, E. (2012). Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22: 861–868, https://doi.org/10.1002/hipo.20947.Search in Google Scholar PubMed PubMed Central
Lin, Y.-T., Chen, C.-C., Huang, C.-C., Nishimori, K., and Hsu, K.-S. (2017). Oxytocin stimulates hippocampal neurogenesis via oxytocin receptor expressed in CA3 pyramidal neurons. Nat. Commun. 8: 537, https://doi.org/10.1038/s41467-017-00675-5.Search in Google Scholar PubMed PubMed Central
Lopatina, O., Inzhutova, A., Pichugina, Y.A., Okamoto, H., Salmina, A.B., and Higashida, H. (2011). Reproductive experience affects parental retrieval behaviour associated with increased plasma oxytocin levels in wild-type and CD38-knockout mice. J. Neuroendocrinol. 23: 1125–1133, https://doi.org/10.1111/j.1365-2826.2011.02136.x.Search in Google Scholar PubMed
Lopatina, O., Inzhutova, A., Salmina, A.B., and Higashida, H. (2012). The roles of oxytocin and CD38 in social or parental behaviors. Front. Neurosci. 6: 182, https://doi.org/10.3389/fnins.2012.00182.Search in Google Scholar PubMed PubMed Central
Lopatina, O.L., Malinovskaya, N.A., Komleva, Y.K., Gorina, Y.V., Shuvaev, A.N., Olovyannikova, R.Y., Belozor, O.S., Belova, O.A., Higashida, H., and Salmina, A.B. (2019). Excitation/inhibition imbalance and impaired neurogenesis in neurodevelopmental and neurodegenerative disorders. Rev. Neurosci. 30: 807–820, https://doi.org/10.1515/revneuro-2019-0014.Search in Google Scholar PubMed
Lopresto, D., Schipper, P., and Homberg, J.R. (2016). Neural circuits and mechanisms involved in fear generalization: implications for the pathophysiology and treatment of posttraumatic stress disorder. Neurosci. Biobehav. Rev. 60: 31–42, https://doi.org/10.1016/j.neubiorev.2015.10.009.Search in Google Scholar PubMed
Lovallo, W.R., Acheson, A., Cohoon, A.J., Sorocco, K.H., Vincent, A.S., Hodgkinson, C.A., and Goldman, D. (2019). Working memory reflects vulnerability to early life adversity as a risk factor for substance use disorder in the FKBP5 cortisol cochaperone polymorphism, rs9296158. PloS One 14: e0218212, https://doi.org/10.1371/journal.pone.0218212.Search in Google Scholar PubMed PubMed Central
Luzzati, F., Bonfanti, L., Fasolo, A., and Peretto, P. (2009). DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cerebr. Cortex 19: 1028–1041, https://doi.org/10.1093/cercor/bhn145.Search in Google Scholar PubMed
Malinovskaya, N.A., Komleva, Y.K., Salmin, V.V., Morgun, A.V., Shuvaev, A.N., Panina, Y.A., Boitsova, E.B., and Salmina, A.B. (2016). Endothelial progenitor cells physiology and metabolic plasticity in brain angiogenesis and blood-brain barrier modeling. Front. Physiol. 7: 599–599, https://doi.org/10.3389/fphys.2016.00599.Search in Google Scholar PubMed PubMed Central
Malinovskaya, N.A., Morgun, A.V., Lopatina, O.L., Panina, Y.A., Volkova, V.V., Gasymly, E.L., Taranushenko, T.E., and Salmina, A.B. (2018). Early life stress: consequences for the development of the brain. Neurosci. Behav. Physiol. 48: 233–250, https://doi.org/10.1007/s11055-018-0557-9.Search in Google Scholar
Mao, Y., Xiao, H., Ding, C., and Qiu, J. (2020). The role of attention in the relationship between early life stress and depression. Sci. Rep. 10: 6154, https://doi.org/10.1038/s41598-020-63351-7.Search in Google Scholar
Markram, K., Lopez Fernandez, M.A., Abrous, D.N., and Sandi, C. (2007). Amygdala upregulation of NCAM polysialylation induced by auditory fear conditioning is not required for memory formation, but plays a role in fear extinction. Neurobiol. Learn. Mem. 87: 573–582, https://doi.org/10.1016/j.nlm.2006.11.007.Search in Google Scholar
Martínez, M.C., Alen, N., Ballarini, F., Moncada, D., and Viola, H. (2012). Memory traces compete under regimes of limited Arc protein synthesis: implications for memory interference. Neurobiol. Learn. Mem. 98: 165–173, https://doi.org/10.1016/j.nlm.2012.05.007.Search in Google Scholar
Martínez, M.C., Villar, M.E., Ballarini, F., and Viola, H. (2014). Retroactive interference of object-in-context long-term memory: role of dorsal hippocampus and medial prefrontal cortex. Hippocampus 24: 1482–1492, https://doi.org/10.1002/hipo.22328.Search in Google Scholar
Maud, C., Ryan, J., McIntosh, J.E., and Olsson, C.A. (2018). The role of oxytocin receptor gene (OXTR) DNA methylation (DNAm) in human social and emotional functioning: a systematic narrative review. BMC Psychiatr. 18: 154, https://doi.org/10.1186/s12888-018-1740-9.Search in Google Scholar
Medina, J.H. (2018). Neural, cellular and molecular mechanisms of active forgetting. Front. Syst. Neurosci. 12: 3–3, https://doi.org/10.3389/fnsys.2018.00003.Search in Google Scholar
Nacher, J., Alonso-Llosa, G., Rosell, D., and McEwen, B. (2002). PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res. 927: 111–121, https://doi.org/10.1016/s0006-8993(01)03241-3.Search in Google Scholar
Nacher, J., Lanuza, E., and McEwen, B. (2002). Distribution of PSA-NCAM expression in the amygdala of the adult rat. Neuroscience 113: 479–484, https://doi.org/10.1016/s0306-4522(02)00219-1.Search in Google Scholar
Nacher, J., Pham, K., Gil-Fernandez, V., and McEwen, B.S. (2004). Chronic restraint stress and chronic corticosterone treatment modulate differentially the expression of molecules related to structural plasticity in the adult rat piriform cortex. Neuroscience 126: 503–509, https://doi.org/10.1016/j.neuroscience.2004.03.038.Search in Google Scholar PubMed
Naninck, E.F., Hoeijmakers, L., Kakava-Georgiadou, N., Meesters, A., Lazic, S.E., Lucassen, P.J., and Korosi, A. (2015). Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice. Hippocampus 25: 309–328, https://doi.org/10.1002/hipo.22374.Search in Google Scholar PubMed
Nelson, C.A.3rd and Gabard-Durnam, L.J. (2020). Early adversity and critical periods: neurodevelopmental consequences of violating the expectable environment. Trends Neurosci. 43: 133–143, https://doi.org/10.1016/j.tins.2020.01.002.Search in Google Scholar PubMed PubMed Central
Neumann, I.D., Wigger, A., Torner, L., Holsboer, F., and Landgraf, R. (2000). Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J. Neuroendocrinol. 12: 235–243, https://doi.org/10.1046/j.1365-2826.2000.00442.x.Search in Google Scholar PubMed
Olff, M., Frijling, J.L., Kubzansky, L.D., Bradley, B., Ellenbogen, M.A., Cardoso, C., Bartz, J.A., Yee, J.R., and van Zuiden, M. (2013). The role of oxytocin in social bonding, stress regulation and mental health: an update on the moderating effects of context and interindividual differences. Psychoneuroendocrinology 38: 1883–1894, https://doi.org/10.1016/j.psyneuen.2013.06.019.Search in Google Scholar PubMed
Opendak, M., Offit, L., Monari, P., Schoenfeld, T.J., Sonti, A.N., Cameron, H.A., and Gould, E. (2016). Lasting adaptations in social behavior produced by social disruption and inhibition of adult neurogenesis. J. Neurosci. 36: 7027–7038, https://doi.org/10.1523/jneurosci.4435-15.2016.Search in Google Scholar
Ouali-Hassenaoui, S., Bendjelloul, M., Dekar, A., and Theodosis, D. (2011). Distribution of osmoregulatory peptides and neuronal-glial configuration in the hypothalamic magnocellular nuclei of desert rodents. Comptes Rendus Biol. 334: 855–862, https://doi.org/10.1016/j.crvi.2011.09.001.Search in Google Scholar PubMed
Park, S.-S., Kim, T.-W., Park, H.-S., Seo, T.-B., and Kim, Y.-P. (2020). Effects of treadmill exercise on activity, short-term memory, vascular dysfunction in maternal separation rats. J. Exerc. Rehabil. 16: 118–123, https://doi.org/10.12965/jer.2040234.117.Search in Google Scholar PubMed PubMed Central
Pearson-Leary, J., Eacret, D., Chen, R., Takano, H., Nicholas, B., and Bhatnagar, S. (2017). Inflammation and vascular remodeling in the ventral hippocampus contributes to vulnerability to stress. Transl. Psychiatry 7: e1160–e1160, https://doi.org/10.1038/tp.2017.122.Search in Google Scholar PubMed PubMed Central
Pervanidou, P., Makris, G., Chrousos, G., and Agorastos, A. (2020). Early life stress and pediatric posttraumatic stress disorder. Brain Sci. 10: 169, https://doi.org/10.3390/brainsci10030169.Search in Google Scholar PubMed PubMed Central
Pesarico, A.P., Bueno-Fernandez, C., Guirado, R., Gómez-Climent, M.Á., Curto, Y., Carceller, H., and Nacher, J. (2019). Chronic stress modulates interneuronal plasticity: effects on PSA-NCAM and perineuronal nets in cortical and extracortical regions. Front. Cell. Neurosci. 13: 197–197, https://doi.org/10.3389/fncel.2019.00197.Search in Google Scholar PubMed PubMed Central
Pozhilenkova, E.A., Lopatina, O.L., Komleva, Y.K., Salmin, V.V., and Salmina, A.B. (2017). Blood-brain barrier-supported neurogenesis in healthy and diseased brain. Rev. Neurosci. 28: 397, https://doi.org/10.1515/revneuro-2016-0071.Search in Google Scholar PubMed
Quartu, M., Serra, M.P., Boi, M., Ibba, V., Melis, T., and Del Fiacco, M. (2008). Polysialylated-neural cell adhesion molecule (PSA-NCAM) in the human trigeminal ganglion and brainstem at prenatal and adult ages. BMC Neurosci. 9: 108, https://doi.org/10.1186/1471-2202-9-108.Search in Google Scholar PubMed PubMed Central
Raber, J., Arzy, S., Bertolus, J.B., Depue, B., Haas, H.E., Hofmann, S.G., Kangas, M., Kensinger, E., Lowry, C.A., Marusak, H.A., et al.. (2019). Current understanding of fear learning and memory in humans and animal models and the value of a linguistic approach for analyzing fear learning and memory in humans. Neurosci. Biobehav. Rev. 105: 136–177, https://doi.org/10.1016/j.neubiorev.2019.03.015.Search in Google Scholar PubMed
Rai, D., Golding, J., Magnusson, C., Steer, C., Lewis, G., and Dalman, C. (2012). Prenatal and early life exposure to stressful life events and risk of autism spectrum disorders: population-based studies in Sweden and England. PloS One 7: e38893, https://doi.org/10.1371/journal.pone.0038893.Search in Google Scholar PubMed PubMed Central
Raineki, C., Opendak, M., Sarro, E., Showler, A., Bui, K., McEwen, B.S., Wilson, D.A., and Sullivan, R.M. (2019). During infant maltreatment, stress targets hippocampus, but stress with mother present targets amygdala and social behavior. Proc. Nat. Acad. Sci. 116: 22821–22832, https://doi.org/10.1073/pnas.1907170116.Search in Google Scholar PubMed PubMed Central
Rajamani, K.T., Wagner, S., Grinevich, V., and Harony-Nicolas, H. (2018). Oxytocin as a modulator of synaptic plasticity: implications for neurodevelopmental disorders. Front. Synaptic Neurosci. 10: 17–17, https://doi.org/10.3389/fnsyn.2018.00017.Search in Google Scholar PubMed PubMed Central
Reincke, S.A.J. and Hanganu-Opatz, I.L. (2017). Early-life stress impairs recognition memory and perturbs the functional maturation of prefrontal-hippocampal-perirhinal networks. Sci. Rep. 7: 42042, https://doi.org/10.1038/srep42042.Search in Google Scholar PubMed PubMed Central
Reshetnikov, V.V., Kovner, A.V., Lepeshko, A.A., Pavlov, K.S., Grinkevich, L.N., and Bondar, N.P. (2020). Stress early in life leads to cognitive impairments, reduced numbers of CA3 neurons and altered maternal behavior in adult female mice. Gene Brain Behav. 19: e12541, https://doi.org/10.1111/gbb.12541.Search in Google Scholar PubMed
Ruzaeva, V.A., Morgun, A.V., Khilazheva, E.D., Kuvacheva, N.V., Pozhilenkova, E.A., Boitsova, E.B., Martynova, G.P., Taranushenko, T.E., and Salmina, A.B. (2016). Development of blood-brain barrier under the modulation of HIF activity in astroglialand neuronal cells in vitro. Biomed. Khim. 62: 664–669, https://doi.org/10.18097/pbmc20166206664.Search in Google Scholar PubMed
Ryabushkina, Y.A., Reshetnikov, V.V., and Bondar, N.P. (2020). Maternal separation early in life alters the expression of genes Npas4 and Nr1d1 in adult female mice: correlation with social behavior. Behav. Neurol. 7830469, https://doi.org/10.1155/2020/7830469.Search in Google Scholar PubMed PubMed Central
Salmina, A.B., Kuvacheva, N.V., Morgun, A.V., Komleva, Y.K., Pozhilenkova, E.A., Lopatina, O.L., Gorina, Y.V., Taranushenko, T.E., and Petrova, L.L. (2015). Glycolysis-mediated control of blood-brain barrier development and function. Int. J. Biochem. Cell Biol. 64: 174–184, https://doi.org/10.1016/j.biocel.2015.04.005.Search in Google Scholar PubMed
Salmina, A.B., Lopatina, O., Kuvacheva, N.V., and Higashida, H. (2013). Integrative neurochemistry and neurobiology of social recognition and behavior analyzed with respect to CD38-dependent brain oxytocin secretion. Curr. Top. Med. Chem. 13: 2965–2977, https://doi.org/10.2174/15680266113136660211.Search in Google Scholar PubMed
Sanai, N., Nguyen, T., Ihrie, R.A., Mirzadeh, Z., Tsai, H.H., Wong, M., Gupta, N., Berger, M.S., Huang, E., Garcia-Verdugo, J.M., et al.. (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478: 382–386, https://doi.org/10.1038/nature10487.Search in Google Scholar PubMed PubMed Central
Schaeffer, E.L., Kuhn, F., Schmitt, A., Gattaz, W.F., Gruber, O., Schneider-Axmann, T., and Falkai, P. (2013). Increased cell proliferation in the rat anterior cingulate cortex following neonatal hypoxia: relevance to schizophrenia. J. Neural. Transm. 120: 187–195, https://doi.org/10.1007/s00702-012-0859-y.Search in Google Scholar PubMed PubMed Central
Schoenfeld, T.J., Rhee, D., Martin, L., Smith, J.A., Sonti, A.N., Padmanaban, V., and Cameron, H.A. (2019). New neurons restore structural and behavioral abnormalities in a rat model of PTSD. Hippocampus 29: 848–861, https://doi.org/10.1002/hipo.23087.Search in Google Scholar PubMed PubMed Central
Segovia, G., Del Arco, A., De Blas, M., Garrido, P., and Mora, F. (2010). Environmental enrichment increases the in vivo extracellular concentration of dopamine in the nucleus accumbens: a microdialysis study. J. Neural. Transm. 117: 1123–1130, https://doi.org/10.1007/s00702-010-0447-y.Search in Google Scholar PubMed
Sorrells, S.F., Paredes, M.F., Velmeshev, D., Herranz-Pérez, V., Sandoval, K., Mayer, S., Chang, E.F., Insausti, R., Kriegstein, A.R., Rubenstein, J.L., et al.. (2019). Immature excitatory neurons develop during adolescence in the human amygdala. Nat. Commun. 10: 2748, https://doi.org/10.1038/s41467-019-10765-1, 2748.Search in Google Scholar PubMed PubMed Central
Suberbielle, E., Sanchez, P.E., Kravitz, A.V., Wang, X., Ho, K., Eilertson, K., Devidze, N., Kreitzer, A.C., and Mucke, L. (2013). Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-β. Nat. Neurosci. 16: 613–621, https://doi.org/10.1038/nn.3356.Search in Google Scholar PubMed PubMed Central
Syed, S.A., and Nemeroff, C.B. (2017). Early life stress, mood, and anxiety disorders. Chron. Stress 1: 2470547017694461, https://doi.org/10.1177/2470547017694461.Search in Google Scholar PubMed PubMed Central
Talarowska, M. (2020). Epigenetic mechanisms in the neurodevelopmental theory of depression. Depress Res. Treat. 2020: 6357873–6357873, https://doi.org/10.1155/2020/6357873.Search in Google Scholar PubMed PubMed Central
Teissier, A., Le Magueresse, C., Olusakin, J., Andrade da Costa, B.L.S., De Stasi, A.M., Bacci, A., Imamura Kawasawa, Y., Vaidya, V.A., and Gaspar, P. (2020). Early-life stress impairs postnatal oligodendrogenesis and adult emotional behaviour through activity-dependent mechanisms. Mol. Psychiatr. 25: 1159–1174, https://doi.org/10.1038/s41380-019-0493-2.Search in Google Scholar PubMed PubMed Central
Teles, M.C., Cardoso, S.D., and Oliveira, R.F. (2016). Social plasticity relies on different neuroplasticity mechanisms across the brain social decision-making network in zebrafish. Front. Behav. Neurosci. 10: 16, https://doi.org/10.3389/fnbeh.2016.00016.Search in Google Scholar PubMed PubMed Central
Tsoory, M., Guterman, A., and Richter-Levin, G. (2008). Exposure to stressors during juvenility disrupts development-related alterations in the PSA-NCAM to NCAM expression ratio: potential relevance for mood and anxiety disorders. Neuropsychopharmacology 33: 378–393, https://doi.org/10.1038/sj.npp.1301397.Search in Google Scholar PubMed
Valk, S.L., Bernhardt, B.C., Trautwein, F.-M., Böckler, A., Kanske, P., Guizard, N., Collins, D.L., and Singer, T. (2017). Structural plasticity of the social brain: differential change after socio-affective and cognitive mental training. Sci. Adv. 3: e1700489, https://doi.org/10.1126/sciadv.1700489.Search in Google Scholar PubMed PubMed Central
van der Borght, K. and Brundin, P. (2007). Reduced expression of PSA-NCAM in the hippocampus and piriform cortex of the R6/1 and R6/2 mouse models of Huntington’s disease. Exp. Neurol. 204: 473–478, https://doi.org/10.1016/j.expneurol.2006.10.014.Search in Google Scholar PubMed
Vutskits, L., Gascon, E., and Kiss, J. (2003). Removal of PSA from NCAM affects the survival of magnocellular vasopressin- and oxytocin-producing neurons in organotypic cultures of the paraventricular nucleus. Eur. J. Neurosci. 17: 2119–2126, https://doi.org/10.1046/j.1460-9568.2003.02660.x.Search in Google Scholar PubMed
Weisz, V.I. and Argibay, P.F. (2012). Neurogenesis interferes with the retrieval of remote memories: forgetting in neurocomputational terms. Cognition 125: 13–25, https://doi.org/10.1016/j.cognition.2012.07.002.Search in Google Scholar PubMed
West, A.E. and Greenberg, M.E. (2011). Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harbor Perspect. Biol. 3: a005744, https://doi.org/10.1101/cshperspect.a005744.Search in Google Scholar PubMed PubMed Central
Whiteus, C., Freitas, C., and Grutzendler, J. (2014). Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period. Nature 505: 407–411, https://doi.org/10.1038/nature12821.Search in Google Scholar PubMed PubMed Central
Wirth, M.M. (2015). Hormones, stress, and cognition: the effects of glucocorticoids and oxytocin on memory. Adapt. Human Behav. Physiol. 1: 177–201, https://doi.org/10.1007/s40750-014-0010-4.Search in Google Scholar PubMed PubMed Central
Xiao, Y., Wang, J., Siegel, P.B., Cline, M.A., and Gilbert, E.R. (2020). Early-life stress induced epigenetic changes of corticotropin-releasing factor gene in anorexic low body weight-selected chicks. Life 10: 51, https://doi.org/10.3390/life10050051.Search in Google Scholar PubMed PubMed Central
Yang, S., Li, J., Han, L., and Zhu, G. (2017). Early maternal separation promotes apoptosis in dentate gyrus and alters neurological behaviors in adolescent rats. Int. J. Clin. Exp. Pathol. 10: 10812–10820.Search in Google Scholar
Youssef, M., Atsak, P., Cardenas, J., Kosmidis, S., Leonardo, E.D., and Dranovsky, A. (2019). Early life stress delays hippocampal development and diminishes the adult stem cell pool in mice. Sci. Rep. 9: 4120, https://doi.org/10.1038/s41598-019-40868-0.Search in Google Scholar PubMed PubMed Central
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Articles in the same Issue
- Frontmatter
- Early life stress and brain plasticity: from molecular alterations to aberrant memory and behavior
- A review on preventive role of ketogenic diet (KD) in CNS disorders from the gut microbiota perspective
- Genetic parkinsonisms and cancer: a systematic review and meta-analysis
- Prevalence of sports-related spinal injury stratified by competition level and return to play guidelines
- The basal ganglia corticostriatal loops and conditional learning
- VEGF levels in patients with glioma: a systematic review and meta-analysis
- The therapeutic potential of mitochondrial transplantation for the treatment of neurodegenerative disorders
- CNS implications of COVID-19: a comprehensive review
- COVID-19 in age-related neurodegenerative diseases: is there a role for vitamin D3 as a possible therapeutic strategy?
Articles in the same Issue
- Frontmatter
- Early life stress and brain plasticity: from molecular alterations to aberrant memory and behavior
- A review on preventive role of ketogenic diet (KD) in CNS disorders from the gut microbiota perspective
- Genetic parkinsonisms and cancer: a systematic review and meta-analysis
- Prevalence of sports-related spinal injury stratified by competition level and return to play guidelines
- The basal ganglia corticostriatal loops and conditional learning
- VEGF levels in patients with glioma: a systematic review and meta-analysis
- The therapeutic potential of mitochondrial transplantation for the treatment of neurodegenerative disorders
- CNS implications of COVID-19: a comprehensive review
- COVID-19 in age-related neurodegenerative diseases: is there a role for vitamin D3 as a possible therapeutic strategy?