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Neurochemical Research

, Volume 44, Issue 6, pp 1306–1322 | Cite as

Functional Neurochemistry of the Ventral and Dorsal Hippocampus: Stress, Depression, Dementia and Remote Hippocampal Damage

  • Natalia V. GulyaevaEmail author
Original Paper

Abstract

The hippocampus is not a homogeneous brain area, and the complex organization of this structure underlies its relevance and functional pleiotropism. The new data related to the involvement of the ventral hippocampus in the cognitive function, behavior, stress response and its association with brain pathology, in particular, depression, are analyzed with a focus on neuroplasticity, specializations of the intrinsic neuronal network, corticosteroid signaling through mineralocorticoid and glucocorticoid receptors and neuroinflammation in the hippocampus. The data on the septo-temporal hippicampal gradient are analyzed with particular emphasis on the ventral hippocampus, a region where most important alteration underlying depressive disorders occur. According to the recent data, the existing simple paradigm “learning (dorsal hippocampus) versus emotions (ventral hippocampus)” should be substantially revised and specified. A new hypothesis is suggested on the principal involvement of stress response mechanisms (including interaction of released glucocorticoids with hippocampal receptors and subsequent inflammatory events) in the remote hippocampal damage underlying delayed dementia and depression induced by focal brain damage (e.g. post-stroke and post-traumatic). The translational validity of this hypothesis comprising new approaches in preventing post-stroke and post-trauma depression and dementia can be confirmed in experimental and clinical studies.

Keywords

Ventral hippocampus Dorsal hippocampus Stress Depression Stroke Head trauma 

Notes

Acknowledgements

This work was supported by Russian Science Foundation grant # 14‑25‑00136 (stress, depression) and Russian Academy of Sciences, Program Fundamental Bases of Physiological Adaptation Technologies (remote hippocampal damage).

References

  1. 1.
    McEwen BS, Bowles NP, Gray JD, Hill MN, Hunter RG, Karatsoreos IN, Nasca C (2015) Mechanisms of stress in the brain. Nat Neurosci 18:1353–1363.  https://doi.org/10.1038/nn.4086 Google Scholar
  2. 2.
    Gulyaeva NV (2017) Molecular mechanisms of neuroplasticity: an expanding universe. Biochemistry 82:237–242.  https://doi.org/10.1134/S0006297917030014 Google Scholar
  3. 3.
    McEwen BS, Nasca C, Gray JD (2016) Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41:3–23.  https://doi.org/10.1038/npp.2015.171 Google Scholar
  4. 4.
    Gulyaeva NV (2018) The neurochemistry of stress: the chemistry of the stress response and stress vulnerability. Neurochem J 12:117–120.  https://doi.org/10.1134/S1819712418020058 Google Scholar
  5. 5.
    Hibberd C, Yau JL, Seckl JR (2000) Glucocorticoids and the ageing hippocampus. J Anat 197(Pt 4):553–562Google Scholar
  6. 6.
    Oster H, Challet E, Ott V, Arvat E, de Kloet ER, Dijk DJ, Lightman S, Vgontzas A, Van Cauter E (2017) The functional and clinical significance of the 24-hour rhythm of circulating glucocorticoids. Endocr Rev 38:3–45.  https://doi.org/10.1210/er.2015-1080 Google Scholar
  7. 7.
    Juszczak GR, Stankiewicz AM (2018) Glucocorticoids, genes and brain function. Prog Neuropsychopharmacol Biol Psychiatry 82:136–168.  https://doi.org/10.1016/j.pnpbp.2017.11.020 Google Scholar
  8. 8.
    McEwen BS, Weiss J, Schwartz L (1968) Selective retention of corticosterone by limbic structures in rat brain. Nature 220:911–912Google Scholar
  9. 9.
    de Kloet ER, Karst H, Joëls M (2008) Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 29:268–272.  https://doi.org/10.1016/j.yfrne.2007.10.002 Google Scholar
  10. 10.
    Joëls M, Karst H, DeRijk R, de Kloet ER (2008) The coming out of the brain mineralocorticoid receptor. Trends Neurosci 31:1–7.  https://doi.org/10.1016/j.tins.2007.10.005 Google Scholar
  11. 11.
    DeRijk RH, de Kloet ER, Zitman FG, van Leeuwen N (2011) Mineralocorticoid receptor gene variants as determinants of HPA axis regulation and behavior. Endocr Dev 20:137–148.  https://doi.org/10.1159/000321235 Google Scholar
  12. 12.
    Groeneweg FL, Karst H, de Kloet ER, Joëls M (2011) Rapid non-genomic effects of corticosteroids and their role in the central stress response. J Endocrinol 209:153–167.  https://doi.org/10.1530/JOE-10-0472 Google Scholar
  13. 13.
    Groeneweg FL, Karst H, de Kloet ER, Joëls M (2012) Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol Cell Endocrinol 350:299–309.  https://doi.org/10.1016/j.mce.2011.06.020 Google Scholar
  14. 14.
    de Kloet ER (2013) Functional profile of the binary brain corticosteroid receptor system: mediating, multitasking, coordinating, integrating. Eur J Pharmacol 719:53–62.  https://doi.org/10.1016/j.ejphar.2013.04.053 Google Scholar
  15. 15.
    de Kloet ER, Otte C, Kumsta R, Kok L, Hillegers MH, Hasselmann H, Kliegel D, Joëls M (2016) Stress and depression: a crucial role of the mineralocorticoid receptor. J Neuroendocrinol.  https://doi.org/10.1111/jne.12379 Google Scholar
  16. 16.
    de Kloet ER, Joëls M (2017) Brain mineralocorticoid receptor function in control of salt balance and stress-adaptation. Physiol Behav 178:13–20.  https://doi.org/10.1016/j.physbeh.2016.12.045 Google Scholar
  17. 17.
    Joëls M, de Kloet ER (2017) 30 YEARS OF THE MINERALOCORTICOID RECEPTOR: the brain mineralocorticoid receptor: a saga in three episodes. J Endocrinol 234:T49–T66.  https://doi.org/10.1530/JOE-16-0660 Google Scholar
  18. 18.
    de Kloet ER, Meijer OC, de Nicola AF, de Rijk RH, Joëls M (2018) Importance of the brain corticosteroid receptor balance in metaplasticity, cognitive performance and neuro-inflammation. Front Neuroendocrinol 49:124–145.  https://doi.org/10.1016/j.yfrne.2018.02.003 Google Scholar
  19. 19.
    Joëls M (2018) Corticosteroids and the brain. J Endocrinol 238:R121–R130.  https://doi.org/10.1530/JOE-18-0226 Google Scholar
  20. 20.
    Kudryashova IV, Gulyaeva NV (2017) “Unpredictable Stress”: ambiguity of stress reactivity in studies of long-term plasticity. Neurosci Behav Physiol 47:948–959.  https://doi.org/10.1007/s11055-017-0496-x Google Scholar
  21. 21.
    Gądek-Michalska A, Tadeusz J, Rachwalska P, Bugajski J (2013) Cytokines, prostaglandins and nitric oxide in the regulation of stress-response systems. Pharmacol Rep 65:1655–1662Google Scholar
  22. 22.
    Stepanichev M, Dygalo NN, Grigoryan G, Shishkina GT, Gulyaeva N (2014) Rodent models of depression: neurotrophic and neuroinflammatory biomarkers. Biomed Res Int.  https://doi.org/10.1155/2014/932757 Google Scholar
  23. 23.
    Walker FR, Nilsson M, Jones K (2013) Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function. Curr Drug Targets 14:1262–1276Google Scholar
  24. 24.
    Piskunov A, Stepanichev M, Tishkina A, Novikova M, Levshina I, Gulyaeva N (2016) Chronic combined stress induces selective and long-lasting inflammatory response evoked by changes in corticosterone accumulation and signaling in rat hippocampus. Metab Brain Dis 31:445–454.  https://doi.org/10.1007/s11011-015-9785-7 Google Scholar
  25. 25.
    Onufriev MV, Freiman SV, Moiseeva YV, Stepanichev MY, Lazareva NA, Gulyaeva NV (2017) Accumulation of corticosterone and interleukin-1β in the hippocampus after focal ischemic damage of the neocortex: selective vulnerability of the ventral hippocampus. Neurochem J 11:236–241.  https://doi.org/10.1134/S1819712417030084 Google Scholar
  26. 26.
    Onufriev MV, Freiman SV, Peregud DI, Kudryashova IV, Tishkina AO, Stepanichev MY, Gulyaeva NV (2017) Neonatal proinflammatory stress induces accumulation of corticosterone and interleukin-6 in the hippocampus of juvenile rats: potential mechanism of synaptic plasticity impairments. Biochemistry 82:275–281.  https://doi.org/10.1134/S0006297917030051 Google Scholar
  27. 27.
    Brocca ME, Pietranera L, Meyer M, Lima A, Roig P, de Kloet ER, De Nicola AF (2017) Mineralocorticoid receptor associates with pro-inflammatory bias in the hippocampus of spontaneously hypertensive rats. J Neuroendocrinol.  https://doi.org/10.1111/jne.12489 Google Scholar
  28. 28.
    Schoenfeld TJ, Gould E (2012) Stress, stress hormones, and adult neurogenesis. Exp Neurol 233(1):12–21.  https://doi.org/10.1016/j.expneurol.2011.01.008 Google Scholar
  29. 29.
    Numakawa T, Odaka H, Adachi N (2017) Actions of brain-derived neurotrophic factor and glucocorticoid stress in neurogenesis. Int J Mol Sci.  https://doi.org/10.3390/ijms18112312 Google Scholar
  30. 30.
    Fitzsimons CP, Herbert J, Schouten M, Meijer OC, Lucassen PJ, Lightman S (2016) Circadian and ultradian glucocorticoid rhythmicity: Implications for the effects of glucocorticoids on neural stem cells and adult hippocampal neurogenesis. Front Neuroendocrinol 41:44–58.  https://doi.org/10.1016/j.yfrne.2016.05.001 Google Scholar
  31. 31.
    Lucassen PJ, Oomen CA, Naninck EF, Fitzsimons CP, van Dam AM, Czeh B, Korosi A (2015) Regulation of adult neurogenesis and plasticity by (early) stress, glucocorticoids, and inflammation. Cold Spring Harb Perspect Biol 7(9):a021303.  https://doi.org/10.1101/cshperspect.a021303 Google Scholar
  32. 32.
    Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19.  https://doi.org/10.1016/j.neuron.2009.11.031 Google Scholar
  33. 33.
    Tannenholz L, Jimenez JC, Kheirbek MA (2014) Local and regional heterogeneity underlying hippocampal modulation of cognition and mood. Front Behav Neurosci 8:147.  https://doi.org/10.3389/fnbeh.2014.00147 Google Scholar
  34. 34.
    O’Leary OF, Cryan JF (2014) A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharmacol Sci 35:675–687.  https://doi.org/10.1016/j.tips.2014.09.011 Google Scholar
  35. 35.
    Poppenk J, Evensmoen HR, Moscovitch M, Nadel L (2013) Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230–240.  https://doi.org/10.1016/j.tics.2013.03.005 Google Scholar
  36. 36.
    Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 5:655–669.  https://doi.org/10.1038/nrn3785 Google Scholar
  37. 37.
    Grigoryan G, Segal M (2016) lasting differential effects on plasticity induced by prenatal stress in dorsal and ventral hippocampus. Neural Plast. 2016:2540462.  https://doi.org/10.1155/2016/2540462 Google Scholar
  38. 38.
    Gulyaeva NV (2014) Effects of stress factors on the functioning of the adult hippocampus: molecular-cellular mechanisms and the dorsoventral gradient. Neurosci Behav Physiol 44:973–981.  https://doi.org/10.1007/s11055-014-0012-5 Google Scholar
  39. 39.
    Gulyaeva NV (2015) Ventral hippocampus, Stress and phychopathology: translational implications. Neurochem J 9:85–94.  https://doi.org/10.1134/S1819712415020075 Google Scholar
  40. 40.
    Brunec IK, Bellana B, Ozubko JD, Man V, Robin J, Liu ZX, Grady C, Rosenbaum RS, Winocur G, Barense MD, Moscovitch M (2018) Multiple scales of representation along the hippocampal anteroposterior axis in humans. Curr Biol 28:2129–2135.  https://doi.org/10.1016/j.cub.2018.05.016 Google Scholar
  41. 41.
    Nadel L, Hoscheidt S, Ryan LR (2013) Spatial cognition and the hippocampus: the anterior-posterior axis. J Cogn Neurosci 25:22–28.  https://doi.org/10.1162/jocn_a_00313 Google Scholar
  42. 42.
    McDonald RJ, Balog RJ, Lee JQ, Stuart EE, Carrels BB, Hong NS (2018) Rats with ventral hippocampal damage are impaired at various forms of learning including conditioned inhibition, spatial navigation, and discriminative fear conditioning to similar contexts. Behav Brain Res 351:138–151.  https://doi.org/10.1016/j.bbr.2018.06.003 Google Scholar
  43. 43.
    Jimenez JC, Su K, Goldberg AR, Luna VM, Biane JS, Ordek G, Zhou P, Ong SK, Wright MA, Zweifel L, Paninski L, Hen R, Kheirbek MA (2018) Anxiety cells in a hippocampal-hypothalamic circuit. Neuron 97:670–683.  https://doi.org/10.1016/j.neuron.2018.01.016 Google Scholar
  44. 44.
    Huckleberry KA, Shue F, Copeland T, Chitwood RA, Yin W, Drew MR (2018) Dorsal and ventral hippocampal adult-born neurons contribute to context fear memory. Neuropsychopharmacology.  https://doi.org/10.1038/s41386-018-0109-6 Google Scholar
  45. 45.
    Riaz S, Schumacher A, Sivagurunathan S, Van Der Meer M, Ito R (2017) Ventral, but not dorsal, hippocampus inactivation impairs reward memory expression and retrieval in contexts defined by proximal cues. Hippocampus 27:822–836.  https://doi.org/10.1002/hipo.22734 Google Scholar
  46. 46.
    Pierard C, Dorey R, Henkous N, Mons N, Béracochéa D (2017) Different implications of the dorsal and ventral hippocampus on contextual memory retrieval after stress. Hippocampus 27:999–1015.  https://doi.org/10.1002/hipo.22748 Google Scholar
  47. 47.
    Qi CC, Wang QJ, Ma XZ, Chen HC, Gao LP, Yin J, Jing YH (2018) Interaction of basolateral amygdala, ventral hippocampus and medial prefrontal cortex regulates the consolidation and extinction of social fear. Behav Brain Funct 14:7.  https://doi.org/10.1186/s12993-018-0139-6 Google Scholar
  48. 48.
    Chen YW, Akad A, Aderogba R, Chowdhury TG, Aoki C (2018) Dendrites of the dorsal and ventral hippocampal CA1 pyramidal neurons of singly housed female rats exhibit lamina-specific growths and retractions during adolescence that are responsive to pair housing. Synapse 72:e22034.  https://doi.org/10.1002/syn.22034 Google Scholar
  49. 49.
    Papatheodoropoulos C (2015) Higher intrinsic network excitability in ventral compared with the dorsal hippocampus is controlled less effectively by GABAB receptors. BMC Neurosci 16:75.  https://doi.org/10.1186/s12868-015-0213-z Google Scholar
  50. 50.
    Tidball P, Burn HV, Teh KL, Volianskis A, Collingridge GL, Fitzjohn SM (2017) Differential ability of the dorsal and ventral rat hippocampus to exhibit group I metabotropic glutamate receptor-dependent synaptic and intrinsic plasticity. Brain Neurosci Adv.  https://doi.org/10.1177/2398212816689792 Google Scholar
  51. 51.
    Kouvaros S, Papatheodoropoulos C (2017) Prominent differences in sharp waves, ripples and complex spike bursts between the dorsal and the ventral rat hippocampus. Neuroscience 352:131–143.  https://doi.org/10.1016/j.neuroscience.2017.03.050 Google Scholar
  52. 52.
    Babiec WE, Jami SA, Guglietta R, Chen PB, O’Dell TJ (2017) Differential regulation of NMDA receptor-mediated transmission by SK channels underlies dorsal-ventral differences in dynamics of Schaffer collateral synaptic function. J Neurosci 37:1950–1964.  https://doi.org/10.1523/JNEUROSCI.3196-16.2017 Google Scholar
  53. 53.
    Maggio N, Segal M (2010) Corticosteroid regulation of synaptic plasticity in the hippocampus. Sci World J 10:462–469.  https://doi.org/10.1100/tsw.2010.48 Google Scholar
  54. 54.
    Papaleonidopoulos V, Kouvaros S, Papatheodoropoulos C (2018) Effects of endogenous and exogenous D1/D5 dopamine receptor activation on LTP in ventral and dorsal CA1 hippocampal synapses. Synapse 72:e22033.  https://doi.org/10.1002/syn.22033 Google Scholar
  55. 55.
    Papaleonidopoulos V, Papatheodoropoulos C (2018) β-adrenergic receptors reduce the threshold for induction and stabilization of LTP and enhance its magnitude via multiple mechanisms in the ventral but not the dorsal hippocampus. Neurobiol Learn Mem 151:71–84.  https://doi.org/10.1016/j.nlm.2018.04.010 Google Scholar
  56. 56.
    Chawla MK, Sutherland VL, Olson K, McNaughton BL, Barnes CA (2018) Behavior-driven arc expression is reduced in all ventral hippocampal subfields compared to CA1, CA3, and dentate gyrus in rat dorsal hippocampus. Hippocampus 28:178–185.  https://doi.org/10.1002/hipo.22820 Google Scholar
  57. 57.
    Zhang TY, Keown CL, Wen X, Li J, Vousden DA, Anacker C, Bhattacharyya U, Ryan R, Diorio J, O’Toole N, Lerch JP, Mukamel EA, Meaney MJ (2018) Environmental enrichment increases transcriptional and epigenetic differentiation between mouse dorsal and ventral dentate gyrus. Nat Commun 9(1):298.  https://doi.org/10.1038/s41467-017-02748-x Google Scholar
  58. 58.
    Lee AR, Kim JH, Cho E, Kim M, Park M (2017) Dorsal and ventral hippocampus differentiate in functional pathways and differentially associate with neurological disease-related genes during postnatal development. Front Mol Neurosci 10:331.  https://doi.org/10.3389/fnmol.2017.00331 Google Scholar
  59. 59.
    Floriou-Servou A, von Ziegler L, Stalder L, Sturman O, Privitera M, Rassi A, Cremonesi A, Thöny B, Bohacek J (2018) Distinct proteomic, transcriptomic, and epigenetic stress responses in dorsal and ventral hippocampus. Biol Psychiatry.  https://doi.org/10.1016/j.biopsych.2018.02.003 Google Scholar
  60. 60.
    Fisher ML, LeMalefant RM, Zhou L, Huang G, Turner JR (2017) Distinct roles of CREB within the ventral and dorsal hippocampus in mediating nicotine withdrawal phenotypes. Neuropsychopharmacology 42:1599–1609.  https://doi.org/10.1038/npp.2016.257 Google Scholar
  61. 61.
    Nasca C, Bigio B, Zelli D, de Angelis P, Lau T, Okamoto M, Soya H, Ni J, Brichta L, Greengard P, Neve RL, Lee FS, McEwen BS (2017) Role of the astroglial glutamate exchanger xCT in ventral hippocampus in resilience to stress. Neuron 96:402–413.  https://doi.org/10.1016/j.neuron.2017.09.020 Google Scholar
  62. 62.
    Pacheco A, Aguayo FI, Aliaga E, Muñoz M, García-Rojo G, Olave FA, Parra-Fiedler NA, García-Pérez A, Tejos-Bravo M, Rojas PS, Parra CS, Fiedler JL (2017) Chronic stress triggers expression of immediate early genes and differentially affects the expression of AMPA and NMDA subunits in dorsal and ventral hippocampus of rats. Front Mol Neurosci 10:244.  https://doi.org/10.3389/fnmol.2017.00244 Google Scholar
  63. 63.
    Gulyaeva NV (2017) Interplay between brain BDNF and glutamatergic systems: a brief state of the evidence and association with the pathogenesis of depression. Biochemistry (Moscow) 82:301–307.  https://doi.org/10.1134/S0006297917030087 Google Scholar
  64. 64.
    Barfield ET, Gerber KJ, Zimmermann KS, Ressler KJ, Parsons RG, Gourley SL (2017) Regulation of actions and habits by ventral hippocampal trkB and adolescent corticosteroid exposure. PLoS Biol 15:e2003000.  https://doi.org/10.1371/journal.pbio.2003000 Google Scholar
  65. 65.
    Serra MP, Poddighe L, Boi M, Sanna F, Piludu MA, Corda MG, Giorgi O, Quartu M (2017) Expression of BDNF and trkB in the hippocampus of a rat genetic model of vulnerability (Roman low-avoidance) and resistance (Roman high-avoidance) to stress-induced depression. Brain Behav 7:e00861.  https://doi.org/10.1002/brb3.861 Google Scholar
  66. 66.
    Ergang P, Kuželová A, Soták M, Klusoňová P, Makal J, Pácha J (2014) Distinct effect of stress on 11beta-hydroxysteroid dehydrogenase type 1 and corticosteroid receptors in dorsal and ventral hippocampus. Physiol Res 63:255–261Google Scholar
  67. 67.
    Tanti A, Belzung C (2013) Neurogenesis along the septo-temporal axis of the hippocampus: are depression and the action of antidepressants region-specific? Neuroscience 252:234–252.  https://doi.org/10.1016/j.neuroscience.2013.08.017 Google Scholar
  68. 68.
    Zhang T, Hong J, Di T, Chen L (2016) MPTP impairs dopamine D1 receptor-mediated survival of newborn neurons in ventral hippocampus to cause depressive-like behaviors in adult mice. Front Mol Neurosci 9:101.  https://doi.org/10.3389/fnmol.2016.00101
  69. 69.
    Schoenfeld TJ, McCausland HC, Morris HD, Padmanaban V, Cameron HA (2017) Stress and loss of adult neurogenesis differentially reduce hippocampal volume. Biol Psychiatry 82:914–923.  https://doi.org/10.1016/j.biopsych.2017.05.013 Google Scholar
  70. 70.
    Reichel JM, Bedenk BT, Czisch M, Wotjak CT (2016) Age-related cognitive decline coincides with accelerated volume loss of the dorsal but not ventral hippocampus in mice. Hippocampus 27:28–35.  https://doi.org/10.1002/hipo.22668 Google Scholar
  71. 71.
    Maruszak A, Thuret S (2014) Why looking at the whole hippocampus is not enough-a critical role for anteroposterior axis, subfield and activation analyses to enhance predictive value of hippocampal changes for Alzheimer’s disease diagnosis. Front Cell Neurosci 8:95.  https://doi.org/10.3389/fncel.2014.00095 Google Scholar
  72. 72.
    Wright VL, Georgiou P, Bailey A, Heal DJ, Bailey CP, Wonnacott S (2018) Inhibition of alpha7 nicotinic receptors in the ventral hippocampus selectively attenuates reinstatement of morphine-conditioned place preference and associated changes in AMPA receptor binding. Addict Biol.  https://doi.org/10.1111/adb.12624 Google Scholar
  73. 73.
    Alvandi MS, Bourmpoula M, Homberg JR, Fathollahi Y (2017) Association of contextual cues with morphine reward increases neural and synaptic plasticity in the ventral hippocampus of rats. Addict Biol 22:1883–1894.  https://doi.org/10.1111/adb.12547 Google Scholar
  74. 74.
    Hudson R, Rushlow W, Laviolette SR (2018) Phytocannabinoids modulate emotional memory processing through interactions with the ventral hippocampus and mesolimbic dopamine system: implications for neuropsychiatric pathology. Psychopharmacology 235:447–458.  https://doi.org/10.1007/s00213-017-4766-7 Google Scholar
  75. 75.
    Pearson-Leary J, Eacret D, Chen R, Takano H, Nicholas B, Bhatnagar S (2017) Inflammation and vascular remodeling in the ventral hippocampus contributes to vulnerability to stress. Transl Psychiatry 7(6):e1160.  https://doi.org/10.1038/tp.2017.122 Google Scholar
  76. 76.
    Grigoryan GA, Gulyaeva NV. Modeling depression in animals: behavior as the basis for the methodology, assessment criteria, and classification. Neurosci Behav Physiol 47: 204–216.  https://doi.org/10.1007/s11055-016-0386-7
  77. 77.
    Tishkina A, Stepanichev M, Kudryashova I, Freiman S, Onufriev M, Lazareva N, Gulyaeva N (2016) Neonatal proinflammatory challenge in male Wistar rats: effects on behavior, synaptic plasticity, and adrenocortical stress response. Behav Brain Res 304:1–10.  https://doi.org/10.1016/j.bbr.2016.02.001 Google Scholar
  78. 78.
    Kvichansky AA, Volobueva MN, Manolova AO, Bolshakov AP, Gulyaeva NV (2017) Neonatal proinflammatory stress alters the expression of genes of corticosteroid receptors in the rat hippocampus: septo-temporal differences. Neurochem J 11:255–258.  https://doi.org/10.1134/S1819712417030059 Google Scholar
  79. 79.
    Kvichansky AA, Volobueva MN, Manolova AO, Bolshakov AP, Gulyaeva NV (2018) The influence of neonatal pro-inflammatory stress on the expression of genes associated with stress in the brains of juvenile rats: Septo-temporal specificity. Neurochem J 12:180–183.  https://doi.org/10.1134/S1819712418020083 Google Scholar
  80. 80.
    Onufriev MV, Uzakov SS, Freiman SV, Stepanichev M, Moiseeva YV, Lazareva NA, Markevich VA, Gulyaeva NV (2017) Dorsal and ventral hippocampus differ in their reactivity towards pro-inflammatory stress: corticosterone levels, cytokine expression, and synaptic plasticity. Zh Vyssh Nerv Deiat Im I P Pavlova 67:349–358.  https://doi.org/10.7868/S0044467717030078 Google Scholar
  81. 81.
    Ben-Ari Y, Lagowska Y, Le Gal La Salle G, Tremblay E, Ottersen OP, Naquet R (1978) Diazepam pretreatment reduces distant hippocampal damage induced by intra-amygdaloid injections of kainic acid. Eur J Pharmacol 52:419–420Google Scholar
  82. 82.
    Lerner-Natoli M, Rondouin G, Belaidi M, Baldy-Moulinier M, Kamenka JM (1991) N-[1-(2-thienyl)cyclohexyl]-piperidine (TCP) does not block kainic acid-induced status epilepticus but reduces secondary hippocampal damage. Neurosci Lett 122:174–178Google Scholar
  83. 83.
    Xie M, Yi C, Luo X, Xu S, Yu Z, Tang Y, Zhu W, Du Y, Jia L, Zhang Q, Dong Q, Zhu W, Zhang X, Bu B, Wang W (2011) Glial gap junctional communication involvement in hippocampal damage after middle cerebral artery occlusion. Ann Neurol 70:121–132.  https://doi.org/10.1002/ana.22386 Google Scholar
  84. 84.
    Schaapsmeerders P, van Uden IW, Tuladhar AM, Maaijwee NA, van Dijk EJ, Rutten-Jacobs LC, Arntz RM, Schoonderwaldt HC, Dorresteijn LD, de Leeuw FE, Kessels RP (2015) Ipsilateral hippocampal atrophy is associated with long-term memory dysfunction after ischemic stroke in young adults. Hum Brain Mapp 36:2432–2442.  https://doi.org/10.1002/hbm.22782 Google Scholar
  85. 85.
    Yang SH, Shetty RA, Liu R, Sumien N, Heinrich KR, Rutledge M, Thangthaeng N, Brun-Zinkernagel AM, Forster MJ (2006) Endovascular middle cerebral artery occlusion in rats as a model for studying vascular dementia. Age (Dordrecht) 28:297–307.  https://doi.org/10.1007/s11357-006-9026-4 Google Scholar
  86. 86.
    Uchida H, Fujita Y, Matsueda M, Umeda M, Matsuda S, Kato H, Kasahara J, Araki T (2010) Damage to neurons and oligodendrocytes in the hippocampal CA1 sector after transient focal ischemia in rats. Cell Mol Neurobiol 30:1125–1134.  https://doi.org/10.1007/s10571-010-9545-5 Google Scholar
  87. 87.
    Block F, Dihné M, Loos M (2005) Inflammation in areas of remote changes following focal brain lesion. Prog Neurobiol 75:342–365Google Scholar
  88. 88.
    Schmidt A, Diederich K, Strecker JK, Geng B, Hoppen M, Duning T, Schäbitz WR, Minnerup J (2015) Progressive cognitive deficits in a mouse model of recurrent photothrombotic stroke. Stroke 46:1127–1131.  https://doi.org/10.1161/STROKEAHA.115.008905 Google Scholar
  89. 89.
    Sharp FR, Lu A, Tang Y, Millhorn DE (2000) Multiple molecular penumbras after focal cerebral ischemia. J Cereb Blood Flow Metab 20:1011–1032Google Scholar
  90. 90.
    Xu CS, Liu AC, Chen J, Pan ZY, Wan Q, Li ZQ, Wang ZF (2015) Overactivation of NR2B-containing NMDA receptors through entorhinal-hippocampal connection initiates accumulation of hyperphosphorylated tau in rat hippocampus after transient middle cerebral artery occlusion. J Neurochem 134:566–577.  https://doi.org/10.1111/jnc.13134 Google Scholar
  91. 91.
    Ikonomidou C, Turski L (1996) Prevention of trauma-induced neurodegeneration in infant and adult rat brain: glutamate antagonists. Metab Brain Dis 11:125–141Google Scholar
  92. 92.
    Bernert H, Turski L (1996) Traumatic brain damage prevented by the non-N-methyl-D-aspartate antagonist 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo[f] quinoxaline. Proc Natl Acad Sci USA 93:5235–5240Google Scholar
  93. 93.
    Bittigau P, Pohl D, Sifringer M, Shimizu H, Ikeda M, Ishimaru M, Stadthaus D, Fuhr S, Dikranian K, Olney JW, Ikonomidou C (1998) Modeling pediatric head trauma: mechanisms of degeneration and potential strategies for neuroprotection. Restor Neurol Neurosci 13:11–23Google Scholar
  94. 94.
    Dietrich WD, Alonso O, Busto R, Globus MY, Ginsberg MD (1994) Post-traumatic brain hypothermia reduces histopathological damage following concussive brain injury in the rat. Acta Neuropathol 87:250–258Google Scholar
  95. 95.
    Komol’tsev IG, Volkova AA, Levshina IP, Novikova MR, Manolova AO, Stepanichev MY, Gulyaeva NV (2018) The number of IgG-positive neurons in the rat hippocampus increases after dosed traumatic brain injury. Neurochem J 12:256–261.  https://doi.org/10.1134/S1819712418030054 Google Scholar
  96. 96.
    Li DR, Zhang F, Wang Y, Tan XH, Qiao DF, Wang HJ, Michiue T, Maeda H (2012) Quantitative analysis of GFAP- and S100 protein-immunopositive astrocytes to investigate the severity of traumatic brain injury. Leg Med (Tokyo) 14:84–92.  https://doi.org/10.1016/j.legalmed.2011.12.007 Google Scholar
  97. 97.
    Braun H, Schäfer K, Höllt V (2002) BetaIII tubulin-expressing neurons reveal enhanced neurogenesis in hippocampal and cortical structures after a contusion trauma in rats. J Neurotrauma 19:975–983Google Scholar
  98. 98.
    Truettner J, Schmidt-Kastner R, Busto R, Alonso OF, Loor JY, Dietrich WD, Ginsberg MD (1999) Expression of brain-derived neurotrophic factor, nerve growth factor, and heat shock protein HSP70 following fluid percussion brain injury in rats. J Neurotrauma 16:471–486Google Scholar
  99. 99.
    Hussein OA, Abdel-Hafez AMM, Abd El Kareim A (2018) Rat hippocampal CA3 neuronal injury induced by limb ischemia/reperfusion: a possible restorative effect of alpha lipoic acid. Ultrastruct Pathol 42:133–154.  https://doi.org/10.1080/01913123.2018.1427165 Google Scholar
  100. 100.
    Ben Assayag E, Tene O, Korczyn AD, Shopin L, Auriel E, Molad J, Hallevi H, Kirschbaum C, Bornstein NM, Shenhar-Tsarfaty S, Kliper E, Stalder T (2017) High hair cortisol concentrations predict worse cognitive outcome after stroke: results from the TABASCO prospective cohort study. Psychoneuroendocrinology 82:133–139.  https://doi.org/10.1016/j.psyneuen.2017.05.013 Google Scholar
  101. 101.
    Tene O, Shenhar-Tsarfaty S, Korczyn AD, Kliper E, Hallevi H, Shopin L, Auriel E, Mike A, Bornstein NM, Assayag EB (2016) Depressive symptoms following stroke and transient ischemic attack: is it time for a more intensive treatment approach? Results from the TABASCO cohort study. J Clin Psychiatry 77:673–680.  https://doi.org/10.4088/JCP.14m09759 Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and NeurophysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Healthcare Department of MoscowMoscow Research and Clinical Center for NeuropsychiatryMoscowRussia

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