Environmental Enrichment Protects Against Sepsis-Associated Encephalopathy-Induced Learning and Memory Deficits by Enhancing the Synthesis and Release of Vasopressin in the Supraoptic Nucleus

References

• Rello J, Valenzuela-Sánchez F, Ruiz-Rodriguez M, Moyano S. Sepsis: a review of advances in management. Adv Ther 2017;34:2393–2411. doi:10.1007/s12325-017-0622-8
   PubMed Web of Science ®Google Scholar
• Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med. 2001;29:1303–1310. doi:10.1097/00003246-200107000-00002
   PubMed Web of Science ®Google Scholar
• McBride MA, Patil TK, Bohannon JK, Hernandez A, Sherwood ER, Patil NK. Immune checkpoints: novel therapeutic targets to attenuate sepsis-induced immunosuppression. Front Immunol. 2021;3(11):624272. doi:10.3389/fimmu.2020.624272
   Web of Science ®Google Scholar
• Gofton TE, Young GB. Sepsis-associated encephalopathy. Nat Rev Neurol 2012;8:557–566. doi:10.1038/nrneurol.2012.183
   PubMed Web of Science ®Google Scholar
• Imamura Y, Wang H, Matsumoto N, et al. Interleukin-1β causes long-term potentiation deficiency in a mouse model of septic encephalopathy. Neuroscience. 2011;187:63–69. doi:10.1016/j.neuroscience.2011.04.063
   PubMed Web of Science ®Google Scholar
• Iwashyna TJ, Ely EW, Smith DM, Langa KM. Long-term cognitive impairment and functional disability among survivors of severe sepsis. JAMA. 2010;304:1787–1794. doi:10.1001/jama.2010.1553
   PubMed Web of Science ®Google Scholar
• Semmler A, Widmann CN, Okulla T, et al. Persistent cognitive impairment, hippocampal atrophy and EEG changes in sepsis survivors. J Neurol Neurosurg Psychiatry. 2013;84:62–69. doi:10.1136/jnnp-2012-302883
   PubMed Web of Science ®Google Scholar
• Kaukonen KM, Bailey M, Suzuki S, Pilcher D, Bellomo R. Mortality related to severe sepsis and septic shock among critically ill patients in Australia and New Zealand, 2000–2012. JAMA. 2014;311:1308–1316. doi:10.1001/jama.2014.2637
   PubMed Web of Science ®Google Scholar
• Iwashyna TJ, Speelmon EC. Advancing a third revolution in critical care. Am J Respir Crit Care Med. 2016;194:782–783. doi:10.1164/rccm.201603-0619ED
   PubMed Web of Science ®Google Scholar
• Prescott HC. Variation in postsepsis readmission patterns: a cohort study of veterans affairs beneficiaries. Ann Am Thorac Soc. 2017;14:230–237. doi:10.1513/AnnalsATS.201605-398OC
   PubMed Web of Science ®Google Scholar
• Van, Praag H, Kempermann G, Gage FH. Neural consequences of environmental enrichment. Nat Rev Neurosci. 2000;1:191–198. doi:10.1038/35044558
   PubMed Web of Science ®Google Scholar
• Rojas-Carvajal M, Sequeira-Cordero A, Brenes JC. The environmental enrichment model revisited: a translatable paradigm to study the stress of our modern lifestyle. Eur J Neurosci. 2021. doi:10.1111/ejn.15160
   PubMed Web of Science ®Google Scholar
• Alwis DS, Yan EB, Johnstone V, et al. Environmental enrichment attenuates traumatic brain injury: induced neuronal hyperexcitability in supragranular layers of sensory cortex. J Neurotrauma. 2016;33:1084–1101. doi:10.1089/neu.2014.3774
   PubMed Web of Science ®Google Scholar
• Redell JB, Maynard ME, Underwood EL, Vita SM, Dash PK, Kobori N. Traumatic brain injury and hippocampal neurogenesis: functional implications. Exp Neurol. 2020;331:113372. doi:10.1016/j.expneurol.2020.113372
   PubMed Web of Science ®Google Scholar
• Tang BL. Axon regeneration induced by environmental enrichment- epigenetic mechanisms. Neural Regen Res. 2020;15:10–15. doi:10.4103/1673-5374.264440
   PubMed Web of Science ®Google Scholar
• Gaulke LJ, Horner PJ, Fink AJ, McNamara CL, Hicks RR. Environmental enrichment increases progenitor cell survival in the dentate gyrus following lateral fluid percussion injury. Brain Res Mol Brain Res. 2005;141:138–150. doi:10.1016/j.molbrainres.2005.08.011
   PubMedGoogle Scholar
• Horner PJ, Gage FH. Regenerating the damaged central nervous system. Nature. 2000;407:963–970. doi:10.1038/35039559
   PubMed Web of Science ®Google Scholar
• Gonçalves LV, Herlinger AL, Ferreira TAA, Coitinho JB, Pires RGW, Martins-Silva C. Environmental enrichment cognitive neuroprotection in an experimental model of cerebral ischemia: biochemical and molecular aspects. Behav Brain Res. 2018;348:171–183. doi:10.1016/j.bbr.2018.04.023
   PubMed Web of Science ®Google Scholar
• Zhang X, Yuan M, Yang S, et al. Enriched environment improves post-stroke cognitive impairment and inhibits neuroinflammation and oxidative stress by activating Nrf2-ARE pathway. Int J Neurosci. 2021;131:641–649. doi:10.1080/00207454.2020.1797722
   PubMed Web of Science ®Google Scholar
• Mestriner RG, Saur L, Bagatini PB, et al. Astrocyte morphology after ischemic and hemorrhagic experimental stroke has no influence on the different recovery patterns. Behav Brain Res. 2015;278:257–261. doi:10.1016/j.bbr.2014.10.005
   PubMed Web of Science ®Google Scholar
• Rodríguez-Ortega E, de la Fuente L, de Amo E, Cubero I. Environmental enrichment during adolescence acts as a protective and therapeutic tool for ethanol binge-drinking, anxiety-like, novelty seeking and compulsive-like behaviors in C57BL/6J mice during adulthood. Front Behav Neurosci. 2018;12:177. doi:10.3389/fnbeh.2018.00177
   PubMed Web of Science ®Google Scholar
• Rico-Barrio I, Peñasco S, Puente N, et al. Cognitive and neurobehavioral benefits of an enriched environment on young adult mice after chronic ethanol consumption during adolescence. Addict Biol. 2019;24:969–980. doi:10.1111/adb.12667
   PubMed Web of Science ®Google Scholar
• Diaz R, Miguel PM, Deniz BF, et al. Environmental enrichment attenuates the blood brain barrier dysfunction induced by the neonatal hypoxia-ischemia. Int J Dev Neurosci. 2016;53:35–45. doi:10.1016/j.ijdevneu.2016.06.006
   PubMed Web of Science ®Google Scholar
• Schuch CP, Diaz R, Deckmann I, Rojas JJ, Deniz BF, Pereira LO. Early environmental enrichment affects neurobehavioral development and prevents brain damage in rats submitted to neonatal hypoxia-ischemia. Neurosci Lett. 2016;617:101–107. doi:10.1016/j.neulet.2016.02.015
   PubMed Web of Science ®Google Scholar
• Galeano P, Blanco E, Logica Tornatore TM, et al. Life-long environmental enrichment counteracts spatial learning, reference and working memory deficits in middle-aged rats subjected to perinatal asphyxia. Front Behav Neurosci. 2015;8:406. doi:10.3389/fnbeh.2014.00406
   PubMed Web of Science ®Google Scholar
• Yuan H, Gao B, Duan L, et al. Acute hyperosmotic stimulus-induced Fos expression in neurons depends on activation of astrocytes in the supraoptic nucleus of rats. J Neurosci Res. 2010;88:1364–1373. doi:10.1002/jnr.22297
   PubMed Web of Science ®Google Scholar
• Brownstein MJ, Russell JT, Gainer H. Synthesis, transport, and release of posterior pituitary hormones. Science. 1980;207:373–378. doi:10.1126/science.6153132
   PubMed Web of Science ®Google Scholar
• Van Dessel P, Gawronski B, De Houwer J. Does explaining social behavior require multiple memory systems?. Trends Cogn Sci. 2019;23:368–369.
   PubMed Web of Science ®Google Scholar
• Alescio-Lautier B, Paban V, Soumireu-Mourat B. Neuromodulation of memory in the hippocampus by vasopressin. Eur J Pharmacol. 2000;405:63–72. doi:10.1016/S0014-2999(00)00542-2
   PubMed Web of Science ®Google Scholar
• Zhang L, Hernández VS. Synaptic innervation to rat hippocampus by vasopressin-immuno-positive fibres from the hypothalamic supraoptic and paraventricular nuclei. Neuroscience. 2013;228:139–162. doi:10.1016/j.neuroscience.2012.10.010
   PubMed Web of Science ®Google Scholar
• Mazeraud A, Pascal Q, Verdonk F, Heming N, Chrétien F, Sharshar T. Neuroanatomy and physiology of brain dysfunction in sepsis. Clin Chest Med. 2016;37:333–345. doi:10.1016/j.ccm.2016.01.013
   PubMed Web of Science ®Google Scholar
• Siami S, Bailly-Salin J, Polito A, et al. Osmoregulation of vasopressin secretion is altered in the postacute phase of septic shock. Crit Care Med. 2010;38:1962–1969. doi:10.1097/CCM.0b013e3181eb9acf
   PubMed Web of Science ®Google Scholar
• Sayiner FD, Öztürk DM, Ulupinar E, Velipasaoglu M, Corumlu EP. Stress caused by environmental effects on the birth process and some of the labor hormones at rats: ideal birth environment and hormones. J Matern Fetal Neonatal Med. 2021;34:2600–2608. doi:10.1080/14767058.2019.1670162
   PubMed Web of Science ®Google Scholar
• Sun X, Zhou R, Lei Y, Hu J, Li X. The ligand-gated ion channel P2X7 receptor mediates NLRP3/caspase-1-mediated pyroptosis in cerebral cortical neurons of juvenile rats with sepsis. Brain Res. 2020;1748:147109. doi:10.1016/j.brainres.2020.147109
   PubMed Web of Science ®Google Scholar
• Rocha M, Vieira A, Michels M, et al. Effects of S100B neutralization on the long-term cognitive impairment and neuroinflammatory response in an animal model of sepsis. Neurochem Int. 2021;142:104906. doi:10.1016/j.neuint.2020.104906
   PubMed Web of Science ®Google Scholar
• Briones TL, Klintsova AY, Greenough WT. Stability of synaptic plasticity in the adult rat visual cortex induced by complex environment exposure. Brain Res. 2004;1018:130–135. doi:10.1016/j.brainres.2004.06.001
   PubMed Web of Science ®Google Scholar
• Lippert-Gruener M, Maegele M, Garbe J, Angelov DN. Late effects of enriched environment (EE) plus multimodal early onset stimulation (MEOS) after traumatic brain injury in rats: ongoing improvement of neuromotor function despite sustained volume of the CNS lesion. Exp Neurol. 2007;203:82–94. doi:10.1016/j.expneurol.2006.07.025
   PubMed Web of Science ®Google Scholar
• Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11:47–60. doi:10.1016/0165-0270(84)90007-4
   PubMed Web of Science ®Google Scholar
• Tucker LB, Velosky AG, McCabe JT. Applications of the Morris water maze in translational traumatic brain injury research. Neurosci Biobehav Rev. 2018;88:187–200. doi:10.1016/j.neubiorev.2018.03.010
   PubMed Web of Science ®Google Scholar
• Ross HE, Freeman SM, Spiegel LL, Ren X, Terwilliger EF, Young LJ. Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. J Neurosci. 2009;29:1312–1318. doi:10.1523/JNEUROSCI.5039-08.2009
   PubMed Web of Science ®Google Scholar
• Serradeil-le Gal C, Wagnon J, Garcia C, et al. Biochemical and pharmacological properties of SR 49059, a new, potent, nonpeptide antagonist of rat and human vasopressin V1a receptors. J Clin Invest. 1993;92:224–231. doi:10.1172/JCI116554
   PubMed Web of Science ®Google Scholar
• Jiang S, Wang YQ, Xu CF, Li YN, Guo R, Li L. Involvement of connexin43 in the infrasonic noise-induced glutamate release by cultured astrocytes. Neurochem Res. 2014;39:833–842. doi:10.1007/s11064-014-1277-3
   PubMed Web of Science ®Google Scholar
• Porterfield VM, Gabella KM, Simmons MA, Johnson JD. Repeated stressor exposure regionally enhances beta-adrenergic receptor-mediated brain IL-1β production. Brain Behav Immun. 2012;26:1249–1255. doi:10.1016/j.bbi.2012.08.001
   PubMed Web of Science ®Google Scholar
• Alescio-Lautier B, Soumireu-Mourat B. Role of vasopressin in learning and memory in the hippocampus. Prog Brain Res. 1998;119:501–521.
   PubMed Web of Science ®Google Scholar
• Xiong Y, Liu R, Xu Y, et al. Effects of vagotomy, splanchnic nerve lesion, and fluorocitrate on the transmission of acute hyperosmotic stress signals to the supraoptic nucleus. J Neurosci Res. 2011;89:256–266. doi:10.1002/jnr.22548
   PubMed Web of Science ®Google Scholar
• Hernández VS, Hernández OR, Perez de la Mora M, et al. Hypothalamic vasopressinergic projections innervate central amygdala GABAergic neurons: implications for anxiety and stress coping. Front Neural Circuits. 2016;10:92. doi:10.3389/fncir.2016.00092
   PubMed Web of Science ®Google Scholar
• Barrett CE, Keebaugh AC, Ahern TH, Bass CE, Terwilliger EF, Young LJ. Variation in vasopressin receptor (Avpr1a) expression creates diversity in behaviors related to monogamy in prairie voles. Horm Behav. 2013;63:518–526. doi:10.1016/j.yhbeh.2013.01.005
   PubMed Web of Science ®Google Scholar
• Kartalou GI, Salgueiro-Pereira AR, Endres T, et al. Anti-inflammatory treatment with FTY720 starting after onset of symptoms reverses synaptic deficits in an AD mouse model. Int J Mol Sci. 2020;21:8957. doi:10.3390/ijms21238957
   PubMed Web of Science ®Google Scholar
• Li J, Cheng XY, Yang H, et al. Matrine ameliorates cognitive deficits via inhibition of microglia mediated neuroinflammation in an Alzheimer’s disease mouse model. Pharmazie. 2020;75:344–347. doi:10.1691/ph.2020.0395
   PubMed Web of Science ®Google Scholar
• Zhou Z, Hou J, Mo Y, et al. Geniposidic acid ameliorates spatial learning and memory deficits and alleviates neuroinflammation via inhibiting HMGB-1 and downregulating TLR4/2 signaling pathway in APP/PS1 mice. Eur J Pharmacol. 2020;869:172857. doi:10.1016/j.ejphar.2019.172857
   PubMed Web of Science ®Google Scholar
• Bourgognon JM, Cavanagh J. The role of cytokines in modulating learning and memory and brain plasticity. Brain Neurosci Adv. 2020;4:2398212820979802. doi:10.1177/2398212820979802
   Google Scholar
• Novkovic T, Mittmann T, Manahan-Vaughan D. BDNF contributes to the facilitation of hippocampal synaptic plasticity and learning enabled by environmental enrichment. Hippocampus. 2015;25:1–15.
   PubMed Web of Science ®Google Scholar
• Bekinschtein P, Oomen CA, Saksida LM, Bussey TJ. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable?. Semin Cell Dev Biol. 2011;22:536–542.
   PubMed Web of Science ®Google Scholar
• Comim CM, Cassol OJ Jr, Constantino LS, et al. Alterations in inflammatory mediators, oxidative stress parameters and energetic metabolism in the brain of sepsis survivor rats. Neurochem Res. 2011;36:304–311. doi:10.1007/s11064-010-0320-2
   PubMed Web of Science ®Google Scholar
• Adam N, Kandelman S, Mantz J, Chrétien F, Sharshar T. Sepsis-induced brain dysfunction. Expert Rev Anti Infect Ther. 2013;11:211–221. doi:10.1586/eri.12.159
   PubMed Web of Science ®Google Scholar
• Yuan M, Guo YS, Han Y, Gao ZK, Shen XY, Bi X. Effectiveness and mechanisms of enriched environment in post-stroke cognitive impairment. Behav Brain Res. 2021;410:113357.
   PubMed Web of Science ®Google Scholar
• Canning CG, Allen NE, Nackaerts E, Paul SS, Nieuwboer A, Gilat M. Virtual reality in research and rehabilitation of gait and balance in Parkinson disease. Nat Rev Neurol. 2020;16:409–425. doi:10.1038/s41582-020-0370-2
   PubMed Web of Science ®Google Scholar
• Terry AV Jr. Spatial navigation (Water Maze) tasks. In: Buccafusco JJ, editor. Methods of Behavior Analysis in Neuroscience. 2nd ed. Boca Raton (FL), USA: CRC Press/Taylor & Francis; 2009. Chapter 13.
   Google Scholar
• Boone M, Deen PM. Physiology and pathophysiology of the vasopressin-regulated renal water reabsorption. Pflugers Arch. 2008;456:1005–1024. doi:10.1007/s00424-008-0498-1
   PubMed Web of Science ®Google Scholar
• Caldwell HK, Lee HJ, Macbeth AH, Young WS 3rd. Vasopressin: behavioral roles of an “original” neuropeptide. Prog Neurobiol. 2008;84:1–24. doi:10.1016/j.pneurobio.2007.10.007
   PubMed Web of Science ®Google Scholar
• de Wied D, Diamant M, Fodor M. Central nervous system effects of the neurohypophyseal hormones and related peptides. Front Neuroendocrinol. 1993;14:251–302. doi:10.1006/frne.1993.1009
   PubMed Web of Science ®Google Scholar
• Neumann ID, Landgraf R. Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 2012;35:649–659. doi:10.1016/j.tins.2012.08.004
   PubMed Web of Science ®Google Scholar
• Cilz NI, Cymerblit-Sabba A, Young WS. Oxytocin and vasopressin in the rodent hippocampus. Genes Brain Behav. 2019;18:e12535. doi:10.1111/gbb.12535
   PubMed Web of Science ®Google Scholar
• Olson AK, Eadie BD, Ernst C, Christie BR. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus. 2006;16:250–260. doi:10.1002/hipo.20157
   PubMed Web of Science ®Google Scholar
• Segovia G, Yagüe AG, García-Verdugo JM, Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull. 2006;70:8–14. doi:10.1016/j.brainresbull.2005.11.005
   PubMed Web of Science ®Google Scholar
• Segovia G, Del, Arco A, Mora F. Environmental enrichment, prefrontal cortex, stress, and aging of the brain. J Neural Transm. 2009;116:1007–1016. doi:10.1007/s00702-009-0214-0
   PubMed Web of Science ®Google Scholar
• Hilario WF, Herlinger AL, Areal LB, et al. Cholinergic and dopaminergic alterations in nigrostriatal neurons are involved in environmental enrichment motor protection in a mouse model of parkinson’s disease. J Mol Neurosci. 2016;60:453–464. doi:10.1007/s12031-016-0831-7
   PubMed Web of Science ®Google Scholar
• Cao L, Jiao X, Zuzga DS, et al. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet. 2004;36:827–835. doi:10.1038/ng1395
   PubMed Web of Science ®Google Scholar
• Gong X, Chen Y, Chang J, Huang Y, Cai M, Zhang M. Environmental enrichment reduces adolescent anxiety- and depression-like behaviors of rats subjected to infant nerve injury. J Neuroinflammation. 2018;5:262. doi:10.1186/s12974-018-1301-7
   Web of Science ®Google Scholar
• Keymoradzadeh A, Hedayati Ch M, Abedinzade M, Gazor R, Rostampour M, Taleghani BK. Enriched environment effect on lipopolysaccharide-induced spatial learning, memory impairment and hippocampal inflammatory cytokine levels in male rats. Behav Brain Res. 2020;394:112814. doi:10.1016/j.bbr.2020.112814
   PubMed Web of Science ®Google Scholar
• Osso LA, Chan JR. Astrocytes underlie neuroinflammatory memory impairment. Cell. 2015;163:1574–1576. doi:10.1016/j.cell.2015.12.001
   PubMed Web of Science ®Google Scholar
• Ji MH, Qiu LL, Tang H, et al. Sepsis-induced selective parvalbumin interneuron phenotype loss and cognitive impairments may be mediated by NADPH oxidase 2 activation in mice. J Neuroinflammation. 2015;12:182. doi:10.1186/s12974-015-0401-x
   PubMed Web of Science ®Google Scholar
• Gardoni F, Boraso M, Zianni E, et al. Distribution of interleukin-1 receptor complex at the synaptic membrane driven by interleukin-1β and NMDA stimulation. J Neuroinflammation. 2011;8:14. doi:10.1186/1742-2094-8-14
   PubMed Web of Science ®Google Scholar
• Hoshino K, Uchinami Y, Uchida Y, Saito H, Morimoto Y. Interleukin-1β modulates synaptic transmission and synaptic plasticity during the acute phase of sepsis in the senescence-accelerated mouse hippocampus. Front Aging Neurosci. 2021;13:637703. doi:10.3389/fnagi.2021.637703
   PubMed Web of Science ®Google Scholar
• Balschun D, Wetzel W, Del Rey A, et al. Interleukin-6: a cytokine to forget. FASEB J. 2004;18:1788–1790. doi:10.1096/fj.04-1625fje
   PubMed Web of Science ®Google Scholar
• Tancredi V, D’Antuono M, Cafè C, et al. The inhibitory effects of interleukin-6 on synaptic plasticity in the rat hippocampus are associated with an inhibition of mitogen-activated protein kinase ERK. J Neurochem. 2000;75:634–643. doi:10.1046/j.1471-4159.2000.0750634.x
   PubMed Web of Science ®Google Scholar
• Nenov MN, Malkov AE, Konakov MV, Levin SG. Interleukin-10 and transforming growth factor-β1 facilitate long-term potentiation in CA1 region of hippocampus. Biochem Biophys Res Commun. 2019;518:486–491. doi:10.1016/j.bbrc.2019.08.072
   PubMed Web of Science ®Google Scholar
• Yang C, Zhang X, Gao J, Wang M, Yang Z. Arginine vasopressin ameliorates spatial learning impairments in chronic cerebral hypoperfusion via V1a receptor and autophagy signaling partially. Transl Psychiatry. 2017;7:e1174. doi:10.1038/tp.2017.121
   PubMed Web of Science ®Google Scholar
• Harris J, Lang T, Thomas JPW, Sukkar MB, Nabar NR, Kehrl JH. Autophagy and inflammasomes. Mol Immunol. 2017;86:10–15. doi:10.1016/j.molimm.2017.02.013
   PubMed Web of Science ®Google Scholar
• Santos-Junior NN, Catalão CH, Costa LH, et al. Alterations in hypothalamic synaptophysin and death markers may be associated with vasopressin impairment in sepsis survivor rats. J Neuroendocrinol. 2018;e12604. doi:10.1111/jne.12604
   PubMed Web of Science ®Google Scholar
• Panja D, Kenney JW, D’Andrea L, et al. Two-stage translational control of dentate gyrus LTP consolidation is mediated by sustained BDNF-TrkB signaling to MNK. Cell Rep. 2014;9:1430–1445. doi:10.1016/j.celrep.2014.10.016
   PubMed Web of Science ®Google Scholar
• Bambah-Mukku D, Travaglia A, Chen DY, Pollonini G, Alberini CM. A positive autoregulatory BDNF feedback loop via C/EBPβ mediates hippocampal memory consolidation. J Neurosci. 2014;34:12547–12559. doi:10.1523/JNEUROSCI.0324-14.2014
   PubMed Web of Science ®Google Scholar
• Johansson BB, Zhao L, Mattsson B. Environmental influence on gene expression and recovery from cerebral ischemia. Acta Neurochir Suppl. 1999;73:51–55.
   PubMedGoogle Scholar
• Esvald EE, Tuvikene J, Sirp A, Patil S, Bramham CR, Timmusk T. CREB family transcription factors are major mediators of BDNF transcriptional autoregulation in cortical neurons. J Neurosci. 2020;40:1405–1426. doi:10.1523/JNEUROSCI.0367-19.2019
   PubMed Web of Science ®Google Scholar
• Zhao L, Brinton RD. Vasopressin-induced cytoplasmic and nuclear calcium signaling in embryonic cortical astrocytes: dynamics of calcium and calcium-dependent kinase translocation. J Neurosci. 2003;23:4228–4239. doi:10.1523/JNEUROSCI.23-10-04228.2003
   PubMed Web of Science ®Google Scholar
• Balapattabi K, Little JT, Farmer GE, Cunningham JT. High salt loading increases brain derived neurotrophic factor in supraoptic vasopressin neurones. J Neuroendocrinol. 2018;30:e12639. doi:10.1111/jne.12639
   PubMed Web of Science ®Google Scholar
• Choe KY, Han SY, Gaub P, et al. High salt intake increases blood pressure via BDNF-mediated downregulation of KCC2 and impaired baroreflex inhibition of vasopressin neurons. Neuron. 2015;23:549–560. doi:10.1016/j.neuron.2014.12.048
   Web of Science ®Google Scholar
• Giustina AD, de Souza Goldim MP, Danielski LG, et al. Lipoic acid and fish oil combination potentiates neuroinflammation and oxidative stress regulation and prevents cognitive decline of rats after sepsis. Mol Neurobiol. 2020;57:4451–4466. doi:10.1007/s12035-020-02032-y
   PubMed Web of Science ®Google Scholar
• Tian J, Tai Y, Shi M, et al. Atorvastatin relieves cognitive disorder after sepsis through reverting inflammatory cytokines, oxidative stress, and neuronal apoptosis in hippocampus. Cell Mol Neurobiol. 2020;40:521–530. doi:10.1007/s10571-019-00750-z
   PubMed Web of Science ®Google Scholar
• Ji MH, Tang H, Luo D, et al. Environmental conditions differentially affect neurobehavioral outcomes in a mouse model of sepsis-associated encephalopathy. Oncotarget. 2017;8:82376–82389. doi:10.18632/oncotarget.19595
   PubMedGoogle Scholar
• Lu Q, Hu S. Sex differences of oxytocin and vasopressin in social behaviors. Handb Clin Neurol. 2021;180:65–88.
   PubMedGoogle Scholar
• Salehzadeh M, Hamden JE, Li MX, Bajaj H, Wu RS, Soma KK. Glucocorticoid production in lymphoid organs: acute effects of lipopolysaccharide in neonatal and adult mice. Endocrinology. 2021;bqab244. doi:10.1210/endocr/bqab244
   Web of Science ®Google Scholar