Skip to main content

Advertisement

Log in

Neonatal Proinflammatory Stress and the Maturation of Intercellular Communication in the Hippocampus

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Neuroinflammatory processes, particularly those induced by infectious agents, are associated with activation of the microglia and subsequent increases in the secretion of proinflammatory cytokines. Proinflammatory stimuli acting in early postnatal ontogeny are stress factors and, along with neuroinflammation, trigger the mechanisms of the stress response. If the proinflammatory signal is sufficiently powerful, the response to it can lead to modification of the body’s stress resistance and an increase in the risk of developing psychopathology accompanied by cognitive impairments at later stages of ontogeny, including in adults. This review considers several mechanisms linked in particular with the functions of the transmitter systems and the neurotrophin, cytokine, and glucocorticoid systems, which determine maturation of intercellular communications in the hippocampus on the background of neuroinflammation and the sequelae of impairments to this process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abareshi, A., Hosseini, M., Beheshti, F., et al., “The effects of captopril on lipopolysaccharide induced learning and memory impairments and the brain cytokine levels and oxidative damage in rats,” Life Sci., 167, 46–56 (2016).

    CAS  PubMed  Google Scholar 

  • Abraham, W. C. and Williams, J. M., “LTP maintenance and its protein synthesis-dependence,” Neurobiol. Learn. Mem., 89, 260–268 (2008).

    CAS  PubMed  Google Scholar 

  • Anaeigoudari, A., Soukhtanloo, M., Reisi, P., et al., “Inducible nitric oxide inhibitor aminoguanidine, ameliorates deleterious effects of lipopolysaccharide on memory and long term potentiation in rat,” Life Sci., 158, 22–30 (2016).

    CAS  PubMed  Google Scholar 

  • Balaban, P. M. and Gulyaeva, N. V., “Universality of the molecular mechanisms of neuroplasticity and neuropathology: an integrative approach,” Ros. Fiziol. Zh., 92, 145–151 (2006).

    CAS  Google Scholar 

  • Balschun, D., Wetzel, W., Del Rey, A., et al., “Interleukin-6: a cytokine to forget,” FASEB J., 18, 1788–1790 (2004).

    CAS  PubMed  Google Scholar 

  • Bath, K. G., Manzano-Nieves, G., and Goodwill, H., “Early life stress accelerates behavioral and neural maturation of the hippocampus in male mice,” Horm. Behav., 82, 64–71 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beattie, E. C., Stellwagen, D., Morishita, W., et al., “Control of synaptic strength by glial TNFalpha,” Science, 295, 2282–2285 (2002).

    CAS  PubMed  Google Scholar 

  • Ben Achour, S. and Pascual, O., “Glia: the many ways to modulate synaptic plasticity,” Neurochem. Int., 57, 440–445 (2010).

    CAS  PubMed  Google Scholar 

  • Ben Menachem-Zidon, O., Avital, A., Ben-Menahem, Y., et al., “Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling,” Brain Behav. Immun., 25, 1008–1016 (2011).

    CAS  PubMed  Google Scholar 

  • Besedovsky, H. O. and del Rey, A., “Central and peripheral cytokines mediate immune-brain connectivity,” Neurochem. Res., 36, 1–6 (2011).

    CAS  PubMed  Google Scholar 

  • Besedovsky, H., del Rey, A., Sorkin, E., and Dinarello, C. A., “Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones,” Science, 233, 652–654 (1986).

    CAS  PubMed  Google Scholar 

  • Bilbo, S. D., Barrientos, R. M., Eads, A. S., et al., “Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood,” Brain Behav. Immun., 22, 451–455 (2008).

    CAS  PubMed  Google Scholar 

  • Bilbo, S. D., Biedenkapp, J. C., Der-Avakian, A., et al., “Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition,” J. Neurosci., 25, 8000–8009 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bilimoria, P. M. and Stevens, B., “Microglia function during brain development: new insights from animal models,” Brain Res., 1617, 7–17 (2015).

    CAS  PubMed  Google Scholar 

  • Bitzer-Quintero, O. K. and Gonzalez-Burgos, I., “Immune system in the brain: a modulatory role on dendritic spine morphophysiology?” Neural Plast., 2012, 348642 (2012).

  • Blume, J., Douglas, S. D., and Evans, D. L., “Immune suppression and immune activation in depression,” Brain Behav. Immun., 25, 221– 229 (2011).

    CAS  PubMed  Google Scholar 

  • Blundon, J. A. and Zakharenko, S. S., “Dissecting the components of longterm potentiation,” Neuroscientist, 14, 598–608 (2008).

    PubMed  PubMed Central  Google Scholar 

  • Brennan, F. X., Beck, K. D., and Servatius, R. J., “Low doses of interleukin-1beta improve the leverpress avoidance performance of Sprague– Dawley rats,” Neurobiol. Learn. Mem., 80, 168–171 (2003).

    CAS  PubMed  Google Scholar 

  • Bronzino, J. D., Kehoe, P., Austin-LaFrance, R. J., et al., “Neonatal isolation alters LTP in freely moving juvenile rats: sex differences,” Brain Res. Bull., 41, 175–183 (1996).

    CAS  PubMed  Google Scholar 

  • Brunson, K. L., Kramár, E., Lin, B., et al., “Mechanisms of late-onset cognitive decline after early-life stress,” J. Neurosci., 25, 9328–9338 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butler, M. P., O’Connor, J. J., and Moynagh, P. N., “Dissection of tumor-necrosis factor-alpha inhibition of long-term potentiation (LTP) reveals a p38 mitogen-activated protein kinase-dependent mechanism which maps to early-but not late-phase LTP,” Neuroscience, 124, 319–326 (2004).

    CAS  PubMed  Google Scholar 

  • Cambonie, G., Hirbec, H., Michaud, M., et al., “Prenatal infection obliterates glutamate-related protection against free hydroxyl radicals in neonatal rat brain,” J. Neurosci. Res., 75, 125–132 (2004).

    CAS  PubMed  Google Scholar 

  • Capuron, L. and Miller, A. H., “Immune system to brain signaling: neuropsychopharmacological implications,” Pharmacol. Therap., 130, 226–238 (2011).

    CAS  Google Scholar 

  • Champagne, D. L., Bagot, R. C., van Hasselt, F., et al., “Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress,” J. Neurosci., 28, 6037–6045 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, Y. H., Kuo, T. T., Chu, M. T., et al., “Postnatal systemic inflammation exacerbates impairment of hippocampal synaptic plasticity in an animal seizure model,” Neuroimmunomodulation, 20, 223–232 (2013).

    CAS  PubMed  Google Scholar 

  • Chen, Z., Jalabi, W., Hu, W., et al., “Microglial displacement of inhibitory synapses provides neuroprotection in the adult brain,” Nat. Commun., 5, 4486 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Custódio, C. S., Mello, B. S. F., Filho, A. J. M. C., et al., “Neonatal immune challenge with lipopolysaccharide triggers long-lasting sex- and age-related behavioral and immune/neurotrophic alterations in mice: relevance to autism spectrum disorders,” Mol. Neurobiol., 55, 3775–3788 (2018).

    PubMed  Google Scholar 

  • de Kloet, E. R., Joëls, M., and Holsboer, F., “Stress and the brain: from adaptation to disease,” Nat. Rev. Neurosci., 6, 463–475 (2005).

    PubMed  Google Scholar 

  • Del Rey, A., Roggero, E., Randolf, A., “IL-1 resets glucose homeostasis at central levels,” Proc. Natl. Acad. Sci. USA, 103, 16039–16044 (2006).

    PubMed  Google Scholar 

  • Derks, N. A., Krugers, H. J., Hoogenraad, C. C., et al., “Effects of early life stress on synaptic plasticity in the developing hippocampus of male and female rats,” PLoS One, 11, e0164551 (2016).

    PubMed  PubMed Central  Google Scholar 

  • Diamond, D. M., Bennett, M. C., Fleshner, M., and Rose, G. M., “Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation,” Hippocampus, 2, 421–430 (1992).

    CAS  PubMed  Google Scholar 

  • Dinel, A., Joffre, C., Trifilieff, P., et al., “Inflammation early in life is a vulnerability factor for emotional behavior at adolescence and for lipopolysaccharide-induced spatial memory and neurogenesis alteration at adulthood,” J. Neuroinflammation, 11, 55 (2014).

  • Dissing-Olesen, L., LeDue, J. M., Rungta, R. L., et al., “Activation of neuronal NMDA receptors triggers transient ATP-mediated microglial process outgrowth,” J. Neurosci., 34, 10511–10527 (2014).

    PubMed  PubMed Central  Google Scholar 

  • Donzis, E. J. and Tronson, N. C., “Modulation of learning and memory by cytokines: signaling mechanisms and long term consequences,” Neurobiol. Learn. Mem., 115, 68–77 (2014).

    CAS  PubMed  Google Scholar 

  • Dumas, T. C., “Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors,” Hippocampus, 15, 562–578 (2005).

    CAS  PubMed  Google Scholar 

  • Escobar, M., Crouzin, N., Cavalier, M., et al., “Early, time-dependent disturbances of hippocampal synaptic transmission and plasticity after in utero immune challenge,” Biol. Psychiatry, 70, 992–999 (2011).

    PubMed  Google Scholar 

  • Eyo, U. B. sand Wu, L. J., “Bidirectional microglia-neuron communication in the healthy brain,” Neural Plast., 2013, 456857 (2013).

  • Eyre, H. and Baune, B. T., “Neuroplastic changes in depression: a role for the immune system,” Psychoneuroendocrinology, 37, 1397–1416 (2012).

    CAS  PubMed  Google Scholar 

  • Fan, L. W., Tien, L. T, Mitchell, H. J., et al., “Alpha-phenyl-n-tert-butylnitrone ameliorates hippocampal injury and improves learning and memory in juvenile rats following neonatal exposure to lipopolysaccharide,” Eur. J. Neurosci., 27, 1475–1484 (2008).

    PubMed  Google Scholar 

  • Finsterwald, C. and Alberini, C. M., “Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: from adaptive responses to psychopathologies,” Neurobiol. Learn. Mem., 112, 17–29 (2014).

    CAS  PubMed  Google Scholar 

  • Foley, K. A., Ossenkopp, K.-P., Kavaliers, M., and MacFabe, D. F., “Pre and neonatal exposure to lipopolysaccharide or the enteric metabolite, propionic acid, alters development and behavior in adolescent rats in a sexually dimorphic manner,” PLoS One, 9, e87072 (2014).

    PubMed  PubMed Central  Google Scholar 

  • Fontainhas, A. M., Wang, M., Liang, K. J., et al., “Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission,” PLoS One, 6, e15973 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gal-Ben-Ari, S., Kenney, J. W., Ounalla-Saad, H., et al., “Consolidation and translation regulation,” Learn. Mem., 19, 410–422 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galic, M. A., Riazi, K., Heida, J. G., et al., “Postnatal infl ammation increases seizure susceptibility in adult rats,” J. Neurosci., 28, 6904–6913 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Girard-Joyal, O., Faragher, A., Bradley, K., et al., “Age and sex differences in c-Fos expression and serum corticosterone concentration following LPS treatment,” Neuroscience, 305, 293–301 (2015).

    CAS  PubMed  Google Scholar 

  • Giridharan, V. V., Réus, G. Z., Selvaraj, S., et al., “Maternal deprivation increases microglial activation and neuroinfl ammatory markers in the prefrontal cortex and hippocampus of infant rats,” J. Psychiatr. Res., 115, 13–20 (2019).

    PubMed  Google Scholar 

  • Golan, H., Levav, T., Mendelsohn, A., and Huleihel, M., “Involvement of tumor necrosis factor alpha in hippocampal development and function,” Cereb. Cortex, 14, 97–105 (2004).

    CAS  PubMed  Google Scholar 

  • Goshen, I., Kreisel, T., Ounallah-Saad, H., et al., “A dual role for interleukin-1 in hippocampal-dependent memory processes,” Psychoneuroendocrinology, 32, 1106–1115 (2007).

    CAS  PubMed  Google Scholar 

  • Grigor’yan, G. A., Dygalo, N. N., Gekht, A. B., et al., “Molecular-cellular mechanisms od depression. The role of glucocorticoids, cytokines, neurotransmitters, and trophic factors in the genesis of depressive disorders,” Usp. Fiziol. Nauk., 45, 3–19 (2014).

    Google Scholar 

  • Guan, Z. and Fang, J., “Peripheral immune activation by lipopolysaccharide decreases neurotrophins in the cortex and hippocampus in rats,” Brain Behav. Immun., 20, 64–71 (2006).

    CAS  PubMed  Google Scholar 

  • Gullo, F., Amadeo, A., Donvito, G., et al., “Atypical “seizure-like” activity in cortical reverberating networks in vitro can be caused by LPSinduced inflammation: a multi-electrode array study from a hundred neurons,” Front. Cell. Neurosci., 8, 361 (2014).

  • Gulyaeva, N. V., “Interplay between brain BDNF and glutamatergic systems: a brief state of the evidence and association with the pathogenesis of depression,” Biochemistry (Mosc.), 82, 301–307 (2017b).

    CAS  Google Scholar 

  • Gulyaeva, N. V., “Molecular mechanisms of neuroplasticity: an expanding universe,” Biochemistry (Mosc.), 82, 237–242 (2017a).

    CAS  Google Scholar 

  • Han, Q., Lin, Q., Huang, P., et al., “Microglia-derived IL-1β contributes to axon development disorders and synaptic deficit through p38- MAPK signal pathway in septic neonatal rats,” J. Neuroinflammation, 14, 52 (2017).

    PubMed  PubMed Central  Google Scholar 

  • Harré, E. M., Galic, M. A., Mouihate, A., et al., “Neonatal inflammation produces selective behavioural defi cits and alters N-methyl-Daspartate receptor subunit mRNA in the adult rat brain,” Eur. J. Neurosci., 27, 644–653 (2008).

    PubMed  PubMed Central  Google Scholar 

  • Harrison, N. A., Brydon, L., Walker, C., et al., “Inflammation causes mood changes through alterations in subgenual cingulate activity and mesolimbic connectivity,” Biol. Psychiatry, 66, 407–414 (2009).

    PubMed  PubMed Central  Google Scholar 

  • Hayashi, Y., Ishibashi, H., Hashimoto, K., and Nakanishi, H., “Potentiation of the NMDA receptor-mediated responses through the activation of the glycine site by microglia secreting soluble factors,” Glia, 53, 660–668 (2006).

    PubMed  Google Scholar 

  • Hennigan, A., Trotter, C., and Kelly, A. M., “Lipopolysaccharide impairs long-term potentiation and recognition memory and increases p75NTR expression in the rat dentate gyrus,” Brain Res., 1130, 158–166 (2007).

    CAS  PubMed  Google Scholar 

  • Hoeijmakers, L., Lucassen, P. J., and Korosi, A., “The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function,” Front. Mol. Neurosci., 7, 103 (2015).

  • Howland, J. G. and Wang, Y. T., “Synaptic plasticity in learning and memory: stress effects in the hippocampus,” Prog. Brain Res., 169, 145– 158 (2008).

    CAS  PubMed  Google Scholar 

  • Huang, C. C., Yang, C. H., and Hsu, K. S., “Do stress and long-term potentiation share the same molecular mechanisms?” Mol. Neurobiol., 32, 223–235 (2005).

    CAS  PubMed  Google Scholar 

  • Islam, O., Gong, X., Rose-John, S., and Heese, K., “Interleukin-6 and neural stem cells: more than gliogenesis,” Mol. Biol. Cell., 20, 188–199 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Järlestedt, K., Naylor, A. S., Dean, J., et al., “Decreased survival of newborn neurons in the dorsal hippocampus after neonatal LPS exposure in mice,” Neuroscience, 253, 21–28 (2013).

    PubMed  PubMed Central  Google Scholar 

  • Ji, K., Akgul, G., Wollmuth, L. P., and Tsirka, S. E., “Microglia actively regulate the number of functional synapses,” PLoS One, 8, e56293 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joels, M. and Krugers, H. J., “LTP after stress: up or down?” Neural Plast., 2007, 93202 (2007).

  • Joels, M., Krugers, H. J., Lucassen, P. J., and Karst, H., “Corticosteroid effects on cellular physiology of limbic cells,” Brain Res., 293, 91– 100 (2009).

    Google Scholar 

  • Joels, M., Krugers, H., and Karst, H., “Stress-induced changes in hippocampal function,” Prog. Brain Res., 167, 3–15 (2008).

    CAS  PubMed  Google Scholar 

  • Joëls, M., Sarabdjitsingh, R. A., and Karst, H., “Unraveling the time domains of corticosteroid hormone infl uences on brain activity: rapid, slow, and chronic modes,” Pharmacol. Rev., 64, 901–938 (2012).

    PubMed  Google Scholar 

  • Joels, M., Velzing, E., Nair, W., et al., “Acute stress increases calcium current amplitude in rat hippocampus: temporal changes in physiology and gene expression,” Eur. J. Neurosci., 18, 1315–1324 (2003).

    CAS  PubMed  Google Scholar 

  • Kamal, A., Ramakers, G. M., Altinbilek, B., and Kas, M. J., “Social isolation stress reduces hippocampal long-term potentiation: effect of animal strain and involvement of glucocorticoid receptors,” Neuroscience, 256, 262–270 (2014).

    CAS  PubMed  Google Scholar 

  • Kellom, M., Basselin, M., Keleshian, V. L., et al., “Dose-dependent changes in neuroinflammatory and arachidonic acid cascade markers with synaptic marker loss in rat lipopolysaccharide infusion model of neuroinflammation,” BMC Neurosci., 13, 50 (2012).

  • Kettenmann, H., Kirchhoff, F., and Verkhratsky, A., “Microglia: new roles for the synaptic stripper,” Neuron, 77, 10–18 (2013).

    CAS  PubMed  Google Scholar 

  • Khairova, R. A., Machado-Vieira, R., Du, J., and Manji, H. K., “A potential role for pro-inflammatory cytokines in regulating synaptic plasticity in major depressive disorder,” Int. J. Neuropsychopharmacol., 12, 561–578 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, J. J., Song, E. Y., and Kosten, T. A., “Stress effects in the hippocampus: synaptic plasticity and memory,” Stress, 9, 1–11 (2006).

    CAS  PubMed  Google Scholar 

  • Kohman, R. A. and Rhodes, J. S., “Neurogenesis, inflammation and behavior,” Brain Behav. Immun., 27, 22–32 (2013).

    CAS  PubMed  Google Scholar 

  • Kohman, R. A., Tarr, A. J., Sparkman, N. L., et al., “Neonatal endotoxin exposure impairs avoidance learning and attenuates endotoxin-induce d sickness behavior and central IL-1 gene transcription in adulthood,” Behav. Brain Res., 194, 25–31 (2008).

    CAS  PubMed  Google Scholar 

  • Krebs, V. L., Okay, T. S., Okay, Y., and Vaz, F. A., “Tumor necrosis factor-alpha, interleukin-1beta and interleukin-6 in the cerebrospinal fluid of newborn with meningitis,” Arq. Neuropsiquiatr., 63, 7–13 (2005).

    PubMed  Google Scholar 

  • Krishnadas, R. and Cavanagh, J., “Depression: an inflammatory illness?” J. Neurol. Neurosurg. Psychiatry, 83, 495–502 (2012).

    PubMed  Google Scholar 

  • Kubera, M., Obuchowicz, E., Goehler, L., et al., “In animal models, psychosocial stress-induced (neuro)infl ammation, apoptosis and reduced neurogenesis are associated to the onset of depression,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 35, 744–759 (2010).

    PubMed  Google Scholar 

  • Kudryashova, I. V. and Gulyaeva, N. V., “Unpredictable stress: the ambiguity of stress-reactivity in studies of long-term plasticity,” Zh. Vyssh. Nerv. Deyat., 66, 414–428 (2016).

    CAS  Google Scholar 

  • Kudryashova, I. V., “Analysis of the conditions for onset of the process of consolidation in a model of long-term synaptic potentiation,” Neirokhimiya, 30, 207–215 (2013).

    Google Scholar 

  • Kudryashova, I. V., “Plasticity of inhibitory synapses as a factor in longterm modification,” Neirokhimiya, 32, 181–191 (2015).

    Google Scholar 

  • Kudryashova, I. V., “Relationship between long-term potentiation and the initial properties of CA3–CA1 synapses: importance for studies of the effects of external factors on synaptic plasticity in the hippocampus,” Zh. Vyssh. Nerv. Deyat.., 67, 831–846 (2017).

    Google Scholar 

  • Kudryashova, I. V., Tishkina, A. O., and Gulyaeva, N. V., “Neonatal proinflammatory stress and defi ciency of the induction of long-term potentiation in the hippocampus in rats: gender differences,” Zh. Vyssh. Nerv. Deyat., 68, 524–536 (2018).

    Google Scholar 

  • Labrousse, V. F., Costes, L., Aubert, A., et al., “Impaired interleukin-1beta and c-Fos expression in the hippocampus is associated with a spatial memory deficit in P2X(7) receptor-deficient mice,” PLoS One, 4, e6006 (2009).

    PubMed  PubMed Central  Google Scholar 

  • Lai, A. Y., Swayze, R. D., El-Husseini, A., and Song, C., “Interleukin-1 beta modulates AMPA receptor expression and phosphorylation in hippocampal neurons,” J. Neuroimmunol., 175, 97–106 (2006).

    CAS  PubMed  Google Scholar 

  • Lan, K. M., Tien, L. T., Pang, Y., et al., “IL-1 receptor antagonist attenuates neonatal lipopolysaccharide-induced long-lasting learning impairment and hippocampal injury in adult rats,” Toxicol. Lett., 234, 30–39 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lante, F., Meunier, J., Guiramand, J., et al., “Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation,” Hippocampus, 18, 602–609 (2008).

    CAS  PubMed  Google Scholar 

  • Lante, F., Meunier, J., Guiramand, J., et al., “Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain,” Free Radic. Biol. Med., 42, 1231–1245 (2007).

    CAS  PubMed  Google Scholar 

  • Levin, S. G. and Godukhin, O. V., “Modulating effect of cytokines on mechanisms of synaptic plasticity in the brain,” Biochemistry (Mosc.), 82, 264–274 (2017).

    CAS  Google Scholar 

  • Li, Y., Du, X. F., Liu, C. S., et al., “Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo,” Dev. Cell, 23, 1189–12 (2012).

    CAS  PubMed  Google Scholar 

  • Liao, D. and Malinow, R., “Deficiency in induction but not expression of LTP in hippocampal slices from young rats,” Learn. Mem., 3, 138–149 (1996).

    CAS  PubMed  Google Scholar 

  • Lim, S. H., Park, E., You, B., et al., “Neuronal synapse formation induced by microglia and interleukin 10,” PLoS One, 8, e81218 (2013).

    PubMed  PubMed Central  Google Scholar 

  • Lin, Y. C. and Koleske, A. J., “Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders,” Annu. Rev. Neurosci., 33, 349–378 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liraz-Zaltsman, S., Yaka, R., Shabashov, D., et al., “Neuroinflammationinduced memory deficits are amenable to treatment with D-cycloserin,” J. Mol. Neurosci., 60, 46–62 (2016).

    CAS  PubMed  Google Scholar 

  • Liston, C., and Gan, W. B., “Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo,” Proc. Natl. Acad. Sci. USA, 108, 16074–16079 (2011).

    CAS  PubMed  Google Scholar 

  • MacRae, M., Macrina, T., Khoury, A., et al., “Tracing the trajectory of behavioral impairments and oxidative stress in an animal model of neonatal inflammation,” Neuroscience, 298, 455–466 (2015).

    CAS  PubMed  Google Scholar 

  • Maes, M., Mihaylova, I., Kubera, M., and Ringel, K., “Activation of cell-mediated immunity in depression: association with inflammation, melancholia, clinical staging and the fatigue and somatic symptom cluster of depression,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 36, 169–175 (2012).

    PubMed  Google Scholar 

  • Maggio, N. and Segal, M., “Cellular basis of a rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices,” Hippocampus, 22, 267–275 (2012).

    CAS  PubMed  Google Scholar 

  • Maggio, N., Shavit-Stein, E., Dori, A., et al., “Prolonged systemic inflammation persistently modifies synaptic plasticity in the hippocampus: modulation by the stress hormones,” Front. Mol. Neurosci., 6, 46 (2013).

  • Malinovskaya, N. A., Morgun, A. V., Lopatina, O. L., et al., “Stress in the early period of life: consequences for brain development,” Zh. Vyssh. Nerv. Deyat., 66, 643–668 (2016).

    Google Scholar 

  • Martin, S., Henley, J. M., Holman, D., et al., “Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity,” PLoS One, 4, e4714 (2009).

    PubMed  PubMed Central  Google Scholar 

  • Matcovitch-Natan, O., Winter, D. R., Giladi, A., et al., “Microglia development follows a stepwise program to regulate brain homeostasis,” Science, 353, aad8670 (2016).

    Google Scholar 

  • Mathews, I. Z., Wilton, A., Styles, A., and McCormick, C. M., “Increased depressive behaviour in females and heightened corticosterone release in males to swim stress after adolescent social stress in rats,” Behav. Brain Res., 190, 33–40 (2008).

    CAS  PubMed  Google Scholar 

  • McEachern, J. C. and Shaw, C. A., “The plasticity pathology continuum: defining a role for the LTP phenomenon,” J. Neurosci. Res., 58, 42–61 (1999).

    CAS  PubMed  Google Scholar 

  • McEwen, B. S., “Physiology and neurobiology of stress and adaptation: central role of the brain,” Physiol. Rev., 87, 873–904 (2007).

    PubMed  Google Scholar 

  • McFadden, L. M., Paris, J. J., Mitzelfelt, M. S., et al., “Sex-dependent effects of chronic unpredictable stress in the water maze,” Physiol. Behav., 102, 266–275 (2011).

    CAS  PubMed  Google Scholar 

  • Medzhitov, R. and Janeway, C., “Advances in immunology: innate immunity,” New Engl. J. Med., 343, 338–344 (2000).

    CAS  PubMed  Google Scholar 

  • Michaluk, P., Wawrzyniak, M., Alot, P., et al., “Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology,” J. Cell Sci., 124, 3369–3380 (2011).

    CAS  PubMed  Google Scholar 

  • Mosser, C. A., Baptista, S., Arnoux, I., and Audinat, E., “Microglia in CNS development: Shaping the brain for the future,” Prog. Neurobiol., 149–150, 1–20 (2017).

  • Mottahedin, A., Ardalan, M., Chumak, T., et al., “Effect of neuroinflammation on synaptic organization and function in the developing brain: implications for neurodevelopmental and neurodegenerative disorders,” Front. Cell. Neurosci, 11, 190 (2017).

  • Mouihate, A., “Long-lasting impact of early life immune stress on neuroimmune functions,” Med. Princ. Pract., 22, 3–7 (2013).

    PubMed  PubMed Central  Google Scholar 

  • Neniskyte, U. and Gross, C. T., “Errant gardeners: glial-cell-dependent synaptic pruning and neurodevelopmental disorders,” Nat. Rev. Neurosci., 18, 658–670 (2017).

    CAS  PubMed  Google Scholar 

  • Nikzad, S., Vafaei, A. A., Rashidy-Pour, A., and Haghighi, S., “Systemic and intrahippocampal administrations of the glucocorticoid receptor antagonist RU38486 impairs fear memory reconsolidation in rats,” Stress, 14, 459–464 (2011).

    CAS  PubMed  Google Scholar 

  • Nouel, D., Burt, M., Zhang, Y., et al., “Prenatal exposure to bacterial endotoxin reduces the number of GAD67- and reelin-immunoreactive neurons in the hippocampus of rat offspring,” Eur. Neuropsychopharmacol., 22, 300–307 (2012).

    CAS  PubMed  Google Scholar 

  • Okulski, P., Jay, T. M., Jaworski, J., et al., “TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex,” Biol. Psychiatry, 62, 359–362 (2007).

    CAS  PubMed  Google Scholar 

  • Onufriev, M. V., Freiman, S. V., Peregud, D. I., et al., “Neonatal proinflammatory stress induces accumulation of corticosterone and interleukin-6 in the hippocampus of juvenile rats: potential mechanism of synaptic plasticity impairments,” Biochemistry (Mosc.), 82, 275–281 (2017).

    CAS  Google Scholar 

  • Osborne, B. F., Caulfield, J. I., Solomotis, S. A., and Schwarz, J. M., “Neonatal infection produces significant changes in immune function with no associated learning deficits in juvenile rats,” Dev. Neurobiol., 77, 1221–1236 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pace, T. W., Hu, F., and Miller, A. H., “Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression,” Brain Behav. Immun., 21, 9–19 (2007).

    CAS  PubMed  Google Scholar 

  • Pang, Y., Dai, X., Roller, A., et al., “Early postnatal lipopolysaccharide exposure leads to enhanced neurogenesis and impaired communicative functions in rats,” PLoS ONE, 11, e0164403 (2016).

    PubMed  PubMed Central  Google Scholar 

  • Park, H. J., Lee, S., Jung, J. W., et al., “Glucocorticoid- and long-term stress-induced aberrant synaptic plasticity are mediated by activation of the glucocorticoid receptor,” Arch. Pharm. Res., 38, 1204– 1212 (2015).

    CAS  PubMed  Google Scholar 

  • Park, K. M. and Bowers, W. J., “Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction,” Cell Signal, 22, 977–983 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parkhurst, C. N., Yang, G., Ninan, I., et al., “Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor,” Cell, 155, 1596–1609 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pascual, O., Achour, S. B., Rostaing, P., et al., “Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission,” Proc. Natl. Acad. Sci. USA, 109, E197–E205 (2012).

    CAS  PubMed  Google Scholar 

  • Peregud, D. I., Freiman, S. V., Tishkina, A. O., et al., “Effects of early proinflammatory stress on the expression of different BDNF transcripts in areas of the brain in male rats of prepubertal age,” Vavilov. Zh. Genet. Selekts., 20, 191–197 (2016).

    Google Scholar 

  • Polman, J. A., de Kloet, E. R., and Datson, N. A., “Two populations of glucocorticoid receptor-binding sites in the male rat hippocampal genome,” Endocrinology, 154, 1832–1844 (2013).

    PubMed  Google Scholar 

  • Pribiag, H. and Stellwagen, D., “Neuroimmune regulation of homeostatic synaptic plasticity,” Neuropharmacology, 78, 13–22 (2014).

    CAS  PubMed  Google Scholar 

  • Pribiag, H. and Stellwagen, D., “TNF-alpha downregulates inhibitory neurotransmission through protein phosphatase 1-dependent trafficking of GABA(A) receptors,” J. Neurosci., 33, 15,879–15,893 (2013).

    Google Scholar 

  • Radahmadi, M., Hosseini, N., and Nasimi, A., “Effect of chronic stress on short and long-term plasticity in dentate gyrus; study of recovery and adaptation,” Neuroscience, 280, 121–129 (2014).

    CAS  PubMed  Google Scholar 

  • Réus, G. Z., Fernandes, G. C., de Moura, A. B., et al., “Early life experience contributes to the developmental programming of depressive-like behaviour, neuroinflammation and oxidative stress,” J. Psychiatr. Res., 95, 196–207 (2017).

    PubMed  Google Scholar 

  • Rex, C. S., Chen, L. Y., Sharma, A., et al., “Different Rho GTPasedependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation,” J. Cell Biol., 186, 85–97 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riazi, K., Galic, M. A., Kentner, A. C., et al., “Microglia-dependent alteration of glutamatergic synaptic transmission and plasticity in the hippocampus during peripheral infl ammation,” J. Neurosci., 35, 4942–4952 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rideau Batista Novais, A., Crouzin, N., Cavalier, M., et al., “Tiagabine improves hippocampal long-term depression in rat pups subjected to prenatal inflammation,” PLoS One, 9, e106302 (2014).

    PubMed  PubMed Central  Google Scholar 

  • Rodenas-Ruano, A., Chávez, A. E., Cossio, M. J., et al., “REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors,” Nat. Neurosci., 15, 1382–1390 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers, J. T., Morganti, J. M., Bachstetter, A. D., et al., “CX3CR1 defi ciency leads to impairment of hippocampal cognitive function and synaptic plasticity,” J. Neurosci., 31, 16241–16250 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rösch, H., Schweigreiter, R., Bonhoeffer, T., et al., “The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus,” Proc. Natl. Acad. Sci. USA, 102, 7362–7367 (2005).

    PubMed  Google Scholar 

  • Routtenberg, A. and Rekart, J. L., “Post-translational protein modification as the substrate for long-lasting memory,” Trends Neurosci., 28, 12–19 (2005).

    CAS  PubMed  Google Scholar 

  • Sachs, B. D., Ni, J. R., and Caron, M. G., “Sex differences in response to chronic mild stress and congenital serotonin defi ciency, Psychoneuroendocrinology, 40, 123–129 (2014).

    CAS  PubMed  Google Scholar 

  • Santello, M. and Volterra, A., “TNFalpha in synaptic function: switching gears,” Trends Neurosci., 35, 638–647 (2012).

    CAS  PubMed  Google Scholar 

  • Schafer, D. P., Lehrman, E. K., and Stevens, B., “The “quad-partite” synapse: microglia-synapse interactions in the developing and mature CNS,” Glia, 61, 24–36 (2013).

    PubMed  Google Scholar 

  • Schafer, D. P., Lehrman, E. K., Kautzman, A. G., et al., “Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner,” Neuron, 74, 691–705 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid, A. W., Lynch, M. A., and Herron, C. E., “The effects of IL-1 receptor antagonist on beta amyloid mediated depression of LTP in the rat CA1 in vivo,” Hippocampus, 19, 670–676 (2009).

    CAS  PubMed  Google Scholar 

  • Schneider, H., Pitossi, F., Balschun, D., et al., “A neuromodulatory role of interleukin-1beta in the hippocampus,” Proc. Natl. Acad. Sci. USA, 95, 7778–7783 (1998).

    CAS  PubMed  Google Scholar 

  • Schwartz, M., Shaked, I., Fisher, J., et al., “Protective autoimmunity against the enemy within: fighting glutamate toxicity,” Trends Neurosci., 26, 297-302 (2003).

    CAS  PubMed  Google Scholar 

  • Schwarz, J. M. and Bilbo, S. D., “Sex, glia, and development: Interactions in health and disease,” Horm. Behav., 62, 243–253 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shanks, N., Larocque, S., and Meaney, M. J., “Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: early illness and later responsivity to stress,” J. Neurosci., 15, 376–384 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharvit, A., Segal, M., Kehat, O., et al., “Differential modulation of synaptic plasticity and local circuit activity in the dentate gyrus and CA1 regions of the rat hippocampus by corticosterone,” Stress, 18, 319–327 (2015).

    CAS  PubMed  Google Scholar 

  • Shaw, K. N., Commins, S., and O’Mara, S. M., “Lipopolysaccharide causes deficits in spatial learning in the watermaze but not in BDNF expression in the rat dentate gyrus,” Behav. Brain Res., 124, 47–54 (2001).

    CAS  PubMed  Google Scholar 

  • Sidor, M. M., Amath, A., MacQueen, G., and Foster, J. A., “A developmental characterization of mesolimbocortical serotonergic gene expression changes following early immune challenge, Neuroscience, 171, 734–746 (2010).

    CAS  PubMed  Google Scholar 

  • Skrebitskii, V. G. and Shtark, M. B., “Fundamental bases of nervous system plasticity,” Vestn. Ross. Akad. Med. Nauk, 9, 39–44 (2012).

    Google Scholar 

  • Sominsky, L., Fuller, E. A., Bondarenko, E., et al., “Functional programming of the autonomic nervous system by early life immune exposure: implications for anxiety,” PLoS One, 8, e57700 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sominsky, L., Walker, A. K., Ong, L. K., et al., “Increased microglial activation in the rat brain following neonatal exposure to a bacterial mimetic,” Behav. Brain Res., 226, 351–356 (2012).

    CAS  PubMed  Google Scholar 

  • Spencer, S. J., Martin, S., Mouihate, A., and Pittman, Q. J., “Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge,” Neuropsychopharmacology, 31, 1910–1918 (2006).

    CAS  PubMed  Google Scholar 

  • Spulber, S., Mateos, L., Oprica, M., et al., “Impaired long term memory consolidation in transgenic mice overexpressing the human soluble form of IL-1ra in the brain,” J. Neuroimmunol., 208, 46–53 (2009).

    CAS  PubMed  Google Scholar 

  • Stellwagen, D. and Malenka, R. C., “Synaptic scaling mediated by glial TNF-alpha,” Nature, 440, 1054–1059 (2006).

    CAS  PubMed  Google Scholar 

  • Stepanichev, M. Yu., “Cytokines as neuromodulators in the central nervous system,” Neirokhimiya, 22, 5–11 (2005).

    Google Scholar 

  • Stepanichev, M., Dygalo, N. N., Grigoryan, G., et al., “Rodent models of depression: neurotrophic and neuroinfl ammatory biomarkers,” Biomed. Res. Int., 2014, 932757 (2014).

  • Stephan, A. H., Barres, B. A., and Stevens, B., “The complement system: an unexpected role in synaptic pruning during development and disease,” Annu. Rev. Neurosci., 35, 369–389 (2012).

    CAS  PubMed  Google Scholar 

  • Streit, W. J., Mrak, R. E., Griffin, W., and Sue, T., “Microglia and neuroinflammation: a pathological perspective,” J. Neuroinflammation, 1, 14 (2004).

    PubMed  PubMed Central  Google Scholar 

  • Tay, T. L., Savage, J. C., Hui, C. W., et al., “Microglia across the lifespan: from origin to function in brain development, plasticity and cognition,” J. Physiol., 595, 1929–1945 (2017).

    CAS  PubMed  Google Scholar 

  • Tishkina, A. O., Stepanichev, M. Yu., Aniol, V. A., and Gulyaeva, N. V., “Functions of the microglia in the healthy brain: focus on neuroplasticity,” Usp. Fiziol. Nauk., 45, 3–18 (2014).

    CAS  PubMed  Google Scholar 

  • Tishkina, A., Stepanichev, M., Kudryashova, I., et al., “Neonatal proinflammatory challenge in male Wistar rats: Effects on behavior, synaptic plasticity, and adrenocortical stress response,” Behav. Brain Res., 304, 1–10 (2016).

    PubMed  Google Scholar 

  • Tremblay, M. E. and Majewska, A. K., “A role for microglia in synaptic plasticity?” Commun. Integr. Biol., 4, 220–222 (2011).

    PubMed  PubMed Central  Google Scholar 

  • Trofimov, A., Strekalova, T., Mortimer, N., et al., “Postnatal LPS challenge impacts escape learning and expression of plasticity factors Mmp9 and Timp1 in rats: effects of repeated training,” Neurotox. Res., 32, 175–186 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vafadari, B., Salamian, A., and Kaczmarek, L., “MMP-9 in translation: from molecule to brain physiology, pathology, and therapy,” J. Neurochem., S2: 91–114 (2016).

    Google Scholar 

  • van Vliet, E. O., de Kieviet, J. F., Oosterlaan, J., and van Elburg, R. M., “Perinatal infections and neurodevelopmental outcome in very preterm and very low-birth-weight infants: a meta-analysis,” JAMA Pediatr., 167, 662–668 (2013).

    PubMed  Google Scholar 

  • Vereker, E., Campbell, V., Roche, E., et al., “Lipopolysaccharide inhibits long term potentiation in the rat dentate gyrus by activating caspase-1,” J. Biol. Chem., 275, 26252–26258 (2000), http://www.jbc.org/content/275/34/26252.

    CAS  PubMed  Google Scholar 

  • Vezzani, A., Balosso, S., and Ravizza, T., “The role of cytokines in the pathophysiology of epilepsy,” Brain Behav. Immun., 22, 797–803 (2008).

    CAS  PubMed  Google Scholar 

  • Viviani, B., Bartesaghi, S., Gardoni, F., et al., “Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases,” J. Neurosci., 23, 8692–8700 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Viviani, B., Gardoni, F., and Marinovich, M., “Cytokines and neuronal ion channels in health and disease,” Int. Rev. Neurobiol., 82, 247–263 (2007).

    CAS  PubMed  Google Scholar 

  • Walker, A. K., Nakamura, T., Byrne, R. J., et al., “Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis,” Psychoneuroendocrinology, 34, 1515–1525 (2009).

    CAS  PubMed  Google Scholar 

  • Walker, C. D., Bath, K. G., Joels, M., et al., “Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential,” Stress, 20, 421–448 (2017).

    PubMed  PubMed Central  Google Scholar 

  • Walker, F. R., March, J. D., and Hodgson, M., “Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat,” Behav. Brain Res., 154, 63–69 (2004).

    CAS  PubMed  Google Scholar 

  • Wang, K. C., Fan, L. W., Kaizaki, A., et al., “Neonatal lipopolysaccharide exposure induces long-lasting learning impairment, less anxiety-like response and hippocampal injury in adult rats,” Neuroscience, 234, 146–157 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Bozdagi, O., Nikitczuk, J. S., et al., “Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately,” Proc. Natl. Acad. Sci. USA, 105, 19,520–19,525 (2008).

  • Wei, H., Zou, H., Sheikh, A. M., et al., “IL-6 is increased in the cerebellum of autistic brain and alters neural cell adhesion, migration and synaptic formation,” J. Neuroinfl ammation, 8, 52 (2011).

    CAS  Google Scholar 

  • Wenzel, A., Fritschy, J. M., Mohler, H., and Benke, D., “NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins,” J. Neurochem., 68, 469–478 (1997).

    CAS  PubMed  Google Scholar 

  • Williamson, L. L. and Bilbo, S. D., “Chemokines and the hippocampus: a new perspective on hippocampal plasticity and vulnerability,” Brain Behav. Immun., 30, 186–194 (2013).

    CAS  PubMed  Google Scholar 

  • Williamson, L. L. and Bilbo, S. D., “Neonatal infection modulates behavioral flexibility and hippocampal activation on a Morris Water Maze task,” Physiol. Behav., 129, 152–159 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson, L. L., Chao, A., and Bilbo, S. D., “Environmental enrichment alters glial antigen expression and neuroimmune function in the adult rat hippocampus,” Brain Behav. Immun., 26, 500–510 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson, L. L., Sholar, P. W., Mistry, R. S., et al., “Microglia and memory: modulation by early-life infection,” J. Neurosci., 31, 15511–15521 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, C. Y., Hsieh, H. L., Sun, C. C., and Yang, C. M., “IL-1β induces MMP-9 expression via a Ca2+-dependent CaMKII/JNK/c-Jun cascade in rat brain astrocytes,” Glia, 57, 1775–17 (2009).

    PubMed  Google Scholar 

  • Wu, Y., Dissing-Olesen, L., MacVicar, B. A., and Stevens, B., “Microglia: dynamic mediators of synapse development and plasticity,” Trends Immunol., 36, 605–6 (2015).

    PubMed  PubMed Central  Google Scholar 

  • Yamada, K., McEwen, B. S., and Pavlides, C., “Site and time dependent effects of acute stress on hippocampal long-term potentiation in freely behaving rats,” Exp. Brain Res., 152, 52–59 (2003).

    CAS  PubMed  Google Scholar 

  • Yang P.-C., Yang C.-H., Huang C.-C., and Hsu K.-S., “Phosphatidylinositol 3-kinase activation is required for stress protocol-induced modification of hippocampal synaptic plasticity,” J. Biol. Chem., 283, 2631–2643 (2008).

    CAS  PubMed  Google Scholar 

  • Yirmiya, R. and Goshen, I., “Immune modulation of learning, memory, neural plasticity and neurogenesis,” Brain Behav. Immun., 25, 181–213 (2011).

    CAS  PubMed  Google Scholar 

  • Yuen, E. Y., Liu, W., Karatsoreos, I. N., et al., “Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory,” Mol. Psychiatry, 16, 156–170 (2011).

    CAS  PubMed  Google Scholar 

  • Zoladz, P. R., Warnecke, A. J., Woelke, S. A., et al., “Pre-learning stress that is temporally removed from acquisition exerts sex-specific effects on long-term memory,” Neurobiol. Learn. Mem., 100, 77–87 (2013).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. V. Kudryashova.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 69, No. 6, pp. 680–699, November–December, 2019.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kudryashova, I.V., Stepanichev, M.Y. & Gulyaeva, N.V. Neonatal Proinflammatory Stress and the Maturation of Intercellular Communication in the Hippocampus. Neurosci Behav Physi 50, 730–742 (2020). https://doi.org/10.1007/s11055-020-00971-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-020-00971-6

Keywords

Navigation