[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Springer Nature Link
Log in

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

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gulyaeva NV (2017) Molecular mechanisms of neuroplasticity: an expanding universe. Biochemistry 82:237–242. https://doi.org/10.1134/S0006297917030014

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  5. Hibberd C, Yau JL, Seckl JR (2000) Glucocorticoids and the ageing hippocampus. J Anat 197(Pt 4):553–562

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  8. McEwen BS, Weiss J, Schwartz L (1968) Selective retention of corticosterone by limbic structures in rat brain. Nature 220:911–912

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  19. Joëls M (2018) Corticosteroids and the brain. J Endocrinol 238:R121–R130. https://doi.org/10.1530/JOE-18-0226

    Article  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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 65:1655–1662

    Article  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  23. Walker FR, Nilsson M, Jones K (2013) Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function. Curr Drug Targets 14:1262–1276

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  39. Gulyaeva NV (2015) Ventral hippocampus, Stress and phychopathology: translational implications. Neurochem J 9:85–94. https://doi.org/10.1134/S1819712415020075

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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 63:255–261

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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. 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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. 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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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 52:419–420

    Article  CAS  Google Scholar 

  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 122:174–178

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  87. Block F, Dihné M, Loos M (2005) Inflammation in areas of remote changes following focal brain lesion. Prog Neurobiol 75:342–365

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  89. Sharp FR, Lu A, Tang Y, Millhorn DE (2000) Multiple molecular penumbras after focal cerebral ischemia. J Cereb Blood Flow Metab 20:1011–1032

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  91. Ikonomidou C, Turski L (1996) Prevention of trauma-induced neurodegeneration in infant and adult rat brain: glutamate antagonists. Metab Brain Dis 11:125–141

    Article  CAS  Google Scholar 

  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 93:5235–5240

    Article  CAS  Google Scholar 

  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 13:11–23

    CAS  PubMed  Google Scholar 

  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 87:250–258

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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 19:975–983

    Article  Google Scholar 

  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 16:471–486

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Butlerova street 5a, Moscow, Russia, 117485

    Natalia V. Gulyaeva

  2. Healthcare Department of Moscow, Moscow Research and Clinical Center for Neuropsychiatry, Donskaya 43, Moscow, Russia, 115419

    Natalia V. Gulyaeva

Authors
  1. Natalia V. Gulyaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalia V. Gulyaeva.

Additional information

Special Issue: In honor of Prof. Anthony J. Turner.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gulyaeva, N.V. Functional Neurochemistry of the Ventral and Dorsal Hippocampus: Stress, Depression, Dementia and Remote Hippocampal Damage. Neurochem Res 44, 1306–1322 (2019). https://doi.org/10.1007/s11064-018-2662-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-018-2662-0

Keywords

Search

Navigation