Effects of individual stressors used in a battery of “chronic unpredictable stress” on long - term plasticity in the hippocampus of juvenile rats

• Autorzy: Gorbunova A.A. , Kudryashova I.V. , Manolova A.O. , Novikova M.R. , Stepanichev M.Y. , Gulyaeva N.V.
• Języki publikacji: EN

Abstrakty

EN

We have studied alterations in the properties of long‑term potentiation (LTP) in hippocampal slices of juvenile rats induced by the exposure of animals to different individual stressors usually used in batteries of chronic unpredictable stress (CUS), a widely used model of depression. Social isolation for 16 h did substantially affect neither the magnitude and nor the development of LTP. The effects of stroboscopic illumination and water deprivation appeared most severe, though opposite: the first stressor had activating effect, whereas the second one inhibited the development of LTP. In addition to the effects of these factors on the LTP magnitude, they also affected the patterns of LTP development. In this study weak tetanization with different probability of maintenance was used, and most of stressors, in spite of the similar LTP magnitude, influenced significantly on the process of consolidation. In hippocampal slices from rats maintained on wet bedding for 16 h, the time course but not magnitude of LTP significantly differed from that observed in the control or socially isolated rats. The weakest effect on LTP was observed in hippocampal slices of the rats exposed to food deprivation. In these animals, only some differences were observed in the development of LTP as compared to socially isolated rats. These data allow ranging stressors used in CUS paradigms according to the severity of their potential effects on neuronal function and animal behavior.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2017
• Tom: 77
• Numer: 3
• Opis fizyczny: p.244-253,fig.,ref.

Twórcy

autor

Gorbunova A.A.

• Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia
• Department of Biological and Medical Physics, Moscow Physical and Technical Institute (State University), Dolgoprudnyi, Moscow Region, Russia

autor

Kudryashova I.V.

• Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

autor

Manolova A.O.

• Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia
• Department of Biological and Medical Physics, Moscow Physical and Technical Institute (State University), Dolgoprudnyi, Moscow Region, Russia

autor

Novikova M.R.

• Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

autor

Stepanichev M.Y.

• Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

autor

Gulyaeva N.V.

• Department of Functional Biochemistry of the Nervous System, Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

Bibliografia

• Ahmed T, Frey JU, Korz V (2006) Long‑term effects of brief acute stress on cellular signaling and hippocampal LTP. J Neurosci 26: 3951–3958.
• Akirav I, Richter‑Levin G (1999) Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci 19: 10530–10535.
• Alfarez DN, Wiegert O, Joëls M, Krugers HJ (2002) Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience 115: 1119–1126.
• Alfarez DN, Joëls M, Krugers HJ (2003) Chronic unpredictable stress impairs long‑term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 17: 1928–1934.
• Armario A, Nadal R (2013) Individual differences and the characterization of animal models of psychopathology: a strong challenge and a good opportunity. Front Pharmacol 4: 137.
• Artola A, von Frijtag JC, Fermont PC, Gispen WH, Schrama LH, Kamal A, Spruijt BM (2006) Long‑lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci 23: 261–272.
• Avital A, Segal M, Richter‑Levin G, (2006) Contrasting roles of corticosteroid receptors in hippocampal plasticity. J Neurosci 26: 9130–9134.
• Badowska‑Szalewska E, Krawczyk R, Ludkiewicz B, Moryś J (2015) The effect of mild stress stimulation on the nerve growth factor (NGF) and tyrosine kinase receptor A (TrkA) immunoreactivity in the paraventricular nucleus (PVN) of the hypothalamus and hippocampus in aged vs. adult rats. Neuroscience 290: 346–356.
• Berezova IV, Shishkina GT, Kalinina TS, Dygalo NN (2011). Behavior in the forced‑swimming test and expression of BDNF and Bcl‑xl genes in the rat brain (in Russian). Zh Vyssh Nerv Deiat im I.P. Pavlova 61: 332–339.
• Berman RM, Cappiello A, Anand A, Oren DA, Heninger GR, Charney DS, Krystal JH (2000) Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 47: 351–354.
• Burgdorf J, Kroes RA, Zhang XL, Gross AL, Schmidt M, Weiss C, Disterhoft JF, Burch RM, Stanton PK, Moskal JR (2015) Rapastinel (GLYX‑13) has therapeutic potential for the treatment of post‑traumatic stress disorder: Characterization of a NMDA receptor‑mediated metaplasticity process in the medial prefrontal cortex of rats. Behav Brain Res 294: 177–185.
• Castren E (2013) Neuronal network plasticity and recovery from depression. JAMA Psychiatry 70: 983–989.
• Cazakoff BN, Howland JG (2010) Acute stress disrupts paired pulse facilitation and long‑term potentiation in rat dorsal hippocampus through activation of glucocorticoid receptors. Hippocampus 20: 1327–1331.
• Christoffel DJ, Golden SA, Russo SJ (2011) Structural and synaptic plasticity in stress‑related disorders. Rev Neurosci 22: 535–549.
• Conner JM, Franks KM, Titterness AK, Russell K, Merrill DA, Christie BR, Sejnowski TJ, Tuszynski MH (2009) NGF is essential for hippocampal plasticity and learning. J Neurosci 29: 10883–10889.
• de Kloet ER, Joëls  M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463–475.
• Diamond DM, Bennett MC, Fleshner  M, Rose GM (1992) Inverted‑U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2: 421–430.
• Grigoryan G, Ardi Z, Albrecht A, Richter‑Levin G, Segal  M (2015) Juvenile stress alters LTP in ventral hippocampal slices: involvement of noradrenergic mechanisms. Behav Brain Res 278: 559–562.
• Grigoryan GA, Dygalo NN, Gekht AB, Stepanichev MIu, Guliaeva NV (2014) Molecular and cellular mechanisms of depression. Role of glucocorticoids, cytokines, neurotransmitters, and trophic factors in genesis of depressive disorders( in Russian). Usp Fiziol Nauk 45: 3–19.
• Groc L, Choquet D, Chaouloff F (2008) The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 11: 868–870.
• Gulyaeva NV, Kudryashov  IE, Kudryashova IV (2003) Caspase activity is essential for long‑term potentiation. J Neurosci Res 73: 853–864.
• Han J, Wang LU, Bian H, Zhou X, Ruan C (2015) Effects of paroxetine on spatial memory function and protein kinase C expression in a rat model of depression. Exp The. Med 10: 1489–1492.
• Hindmarch C, Fry  M, Yao ST, Smith PM, Murphy D, Ferguson AV (2008) Microarray analysis of the transcriptome of the subfornical organ in the rat: regulation by fluid and food deprivation. Am J Physiol Regul Integr Comp Physiol 295: R1914–R1920.
• Hiraide S, Saito Y, Matsumoto M, Yanagawa Y, Ishikawa S, Kubo Y, Inoue S, Yoshioka M, Togashi H (2012) Possible modulation of the amygdala on metaplasticity deficits in the hippocampal CA1 field in early postnatally stressed rats. J Pharmacol Sci 119: 64–72.
• Hirata R, Matsumoto M, Judo C, Yamaguchi T, Izumi T, Yoshioka M, Togashi H (2009) Possible relationship between the stress‑induced synaptic response and metaplasticity in the hippocampal CA1 field of freely moving rats. Synapse 63: 549–556.
• Holderbach R, Clark K, Moreau JL, Bischofberger J, Normann C (2007) Enhanced long‑term synaptic depression in an animal model of depression. Biol Psychiatry 62: 92–100.
• Hollis F, Isgor C, Kabbaj M (2013) The consequences of adolescent chronic unpredictable stress exposure on brain and behavior. Neuroscience 249: 232–241.
• Howland JG, Wang YT (2008) Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 169: 145–158.
• Huang CC, Yang CH, Hsu KS (2005) Do stress and long‑term potentiation share the same molecular mechanisms? Mol Neurobiol 32: 223–235.
• Inoue  W, Baimoukhametova DV, Fuzesi T, Wamsteeker Cusulin JI, Koblinger K, Whelan PJ, Pittman QJ, Bains JS (2013) Noradrenaline is a stress‑associated metaplastic signal at GABA synapses. Nat Neurosci 16: 605–612.
• Jin Y, Kanno T, Nishizaki T (2015) Acute restraint stress impairs induction of long‑term potentiation by activating GSK‑3β. Neurochem Res 40: 36–40.
• Joëls M, Karst H, DeRijk R, de Kloet ER (2008) The coming out of the brain mineralocorticoid receptor. Trend Neurosci 31: 1–7.
• Joëls  M (2006) Corticosteroid effects in the brain: U‑shape it. Trend Pharmacol Sci 27: 244–250.
• Joëls  M, Karst H, Alfarez D, Heine VM, Qin Y, van Riel E, Verkuyl  M, Lucassen PJ, Krugers HJ (2004) Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7: 221–231.
• Joëls M, Krugers HJ (2007) LTP after Stress: Up or Down? Neural Plast 2007: 93202 Joëls M,
• Krugers HJ, Lucassen PJ, Karst H (2009) Corticosteroid effects on cellular physiology of limbic cells. Brain Res 293: 91–100.
• Kallarackal AJ, Kvarta MD, Cammarata E, Jaberi  L, Cai X, Bailey AM, Thompson SM (2013) Chronic stress induces a  selective decrease in AMPA receptor‑mediated synaptic excitation at hippocampal temporoammonic‑CA1 synapses. J Neurosci 33: 15669–15674.
• Kamal A, Ramakers GM, Altinbilek B, Kas MJ (2014) Social isolation stress reduces hippocampal long‑term potentiation: effect of animal strain and involvement of glucocorticoid receptors. Neuroscience 256: 262–270.
• Katz RJ, Roth KA, Carroll BJ (1981) Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci Biobehav Rev 5: 247–251.
• Kavushansky A, Vouimba RM, Cohen H, Richter‑Levin G (2006) Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus 16: 35–42.
• Kim JJ, Song EY, Kosten TA (2006) Stress effects in the hippocampus: synaptic plasticity and memory. Stress 9: 1–11.
• Krugers HJ, Alfarez DN, Karst H, Parashkouhi K, van Gemert N, Joëls  M (2005) Corticosterone shifts different forms of synaptic potentiation in opposite directions. Hippocampus 15: 697–703.
• Leal G, Afonso PM, Salazar IL, Duarte CB (2015) Regulation of hippocampal synaptic plasticity by BDNF. Brain Res 1621: 82–101.
• Li  W, Liu  L, Liu YY, Luo J, Lin JY, Li X, Wang B, Min S (2012) Effects of electroconvulsive stimulation on long‑term potentiation and synaptophysin in the hippocampus of rats with depressive behavior. J ECT 28: 111–117.
• Luo DD, An SC, Zhang X (2008) Involvement of hippocampal serotonin and neuropeptide Y in depression induced by chronic unpredicted mild stress. Brain Res Bull 77: 8–12.
• Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behavior and cognition. Nat Rev Neurosci 10: 434–445.
• Lynch MA (1998) Age‑related impairment in long‑term potentiation in hippocampus: a role for the cytokine, interleukin‑1 beta? Prog Neurobiol 56: 571–589.
• Maccari S, Krugers HJ, Morley‑Fletcher S, Szyf  M, Brunton PJ (2014) The consequences of early‑life adversity: neurobiological, behavioural and epigenetic adaptations. J Neuroendocrinol 26: 707–723.
• Maggio N, Segal M (2007) Striking variations in corticosteroid modulation of long‑term potentiation along the septotemporal axis of the hippocampus. J Neurosci 27: 5757–5765.
• Maggio N, Segal  M (2012) Cellular basis of a  rapid effect of mineralocorticosteroid receptors activation on LTP in ventral hippocampal slices. Hippocampus 22: 267–275.
• Marsden WN (2013) Synaptic plasticity in depression: molecular, cellularand functional correlates. Prog Neuropsychopharmacol Biol Psychiatry 43: 168–184.
• Martin S, Henley JM, Holman D, Zhou  M, Wiegert O, van Spronsen  M, Joëls M, Hoogenraad CC, Krugers HJ (2009) Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One 4: e4714.
• McReynolds JR, Donowho K, Abdi A, McGaugh JL, Roozendaal B, McIntyre CK (2010) Memory‑enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiol Learn Mem 93: 312–321.
• Musazzi L, Racagni G, Popoli M (2011) Stress, glucocorticoids and glutamate release: Effects of antidepressant drugs. Neurochem Int 59: 138–149.
• Olijslagers JE, de Kloet ER, Elgersma Y, van Woerden GM, Joëls M, Karst H (2008) Rapid changes in hippocampal CA1 pyramidal cell function via pre‑ as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 27: 2542–2550.
• Papp  M, Gruca P, Boyer PA, Mocaor E (2003) Effect of agomelatine in the chronic mild stress model of depression in the rat. Neuropsychopharmacology 28: 694–703.
• Park HJ, Lee S, Jung JW, Kim BC, Ryu JH, Kim DH (2015) Glucocorticoid‑ and long‑term stress‑induced aberrant synaptic plasticity are mediated by activation of the glucocorticoid receptor. Arch Pharm Res 38: 1204–1212.
• Peterlik D, Flor PJ, Uschold‑Schmidt N (2016) The emerging role of metabotropic glutamate receptors in the pathophysiology of chronic stress‑related disorders Curr Neuropharmacol 14: 514–539.
• Popoli M, Yan Z, McEwen BS, Sanacora G (2011) The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13: 22–37.
• Qiao H, An SC, Ren W, Ma XM (2014) Progressive alterations of hippocampal CA3‑CA1 synapses in an animal model of depression. Behav Brain Res 275: 191–200.
• Qiao H, Li MX, Xu C, Chen HB, An SC, Ma XM (2016) Dendritic spines in depression: what we learned from animal models. Neural Plast 2016: 805637.
• Radahmadi  M, Hosseini N, Nasimi A (2014) Effect of chronic stress on short and long‑term plasticity in dentate gyrus; study of recovery and adaptation. Neuroscience 280: 121–129.
• Remus JL, Stewart LT, Camp RM, Novak CM, Johnson JD (2015) Interaction of metabolic stress with chronic mild stress in altering brain cytokines and sucrose preference. Behav Neurosci 129: 321–330.
• Saito J, Ozaki Y, Ohnishi H, Nakamura T, Ueta Y (2003) Osmotic stimuli increase brain‑derived neurotrophic factor mRNA level in the rat subfornical organ. Neurosci Lett 347: 65–68.
• Schmidt MV, Abraham WC, Maroun  M, Stork O, Richter‑Levin G (2013) Stress‑induced metaplasticity: from synapses to behavior. Neuroscience 250: 112–120.
• Segal  M, Richter‑Levin G, Maggio N (2010) Stress‑induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20: 1332–1338.
• Seidenbecher T, Balschun D, Reymann KG (1995) Drinking after water deprivation prolongs “unsaturated” LTP in the dentate gyrus of rats. Physiol Behav 57: 1001–4.
• Sharvit A, Segal  M, Kehat O, Stork O, Richter‑Levin G (2015) 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.
• Shishkina GT, Kalinina TS, Berezova IV, Bulygina VV, Dygalo NN (2010) Resistance to the development of stress‑induced behavioral despair in the forced swim test associated with elevated hippocampal Bcl‑xl expression. Behav Brain Res 213: 218–224.
• Spyrka J, Danielewicz J, Hess G (2011) Brief neck restraint stress enhances long‑term potentiation and suppresses long‑term depression in the dentate gyrus of the mouse. Brain Res Bull 85: 363–367.
• Spyrka J, Hess G (2010) Repeated restraint‑induced modulation of long‑term poten‑tiation in the dentate gyrus of the mouse. Brain Res 1320: 28–33.
• Stepanichev M, Dygalo NN, Grigoryan G, Shishkina GT, Gulyaeva N (2014) Rodent models of depression: neurotrophic and neuroinflammatory biomarkers. Biomed Res Int 2014: 932757.
• Stepanichev MY, Tishkina AO, Novikova MR, Levshina IP, Freiman SV, Onufriev MV, Levchenko OA, Lazareva NA, Gulyaeva NV (2016). Anhedonia but not passive floating is an indicator of depressive‑like behavior in two chronic stress paradigm. Acta Neurobiol Exp 76: 324–333.
• Suri D, Vaidya VA (2015) The adaptive and maladaptive continuum of stress responses – a hippocampal perspective. Rev Neurosci 26: 415–442.
• 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.
• Wang D, An SC, Zhang X (2008) Prevention of chronic stress‑induced depression‑like behavior by inducible nitric oxide inhibitor. Neurosci Lett 433: 59–64.
• Wang J, Jing  L, Toledo‑Salas J‑C, Xu  L (2015) Rapid‑onset antidepressant efficacy of glutamatergic system modulators: The neural plasticity hypothesis of depression. Neurosci Bull 31: 75–86.
• WHO Depression 2016. http://www.who.int/mediacentre/factsheets/fs369/en/. Willner P (1997) Validity, reliability and utility of the chronic mild stress model of depression: a  10‑year review and evaluation. Psychopharmacology 134: 319–329.
• Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural‑neurobiological concordance in the effects of CMS. Neuropsychobiology 52: 90–110.
• Willner P, Towell A, Sampson D, Sophokleous S, Muscat R (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93: 358–364.
• Wong DL, Tai TC, Wong‑Faull DC, Claycomb R, Meloni EG, Myers KM, Carlezon WA Jr, Kvetnansky R (2012) Epinephrine: a short‑ and long‑term regulator of stress and development of illness: a potential new role for epinephrine in stress. Cell Mol Neurobiol 32: 737–748.
• Wright JW, Reichert JR, Davis CJ, Harding JW (2002) Neural plasticity and the brain renin‑angiotensin system. Neurosci Biobehav Rev 26: 529–52.
• Wright JW, Yamamoto BJ, Harding JW (2008) Angiotensin receptor subtype mediated physiologies and behaviors: new discoveries and clinical targets. Prog Neurobiol 84: 157–81.
• Yu  M, Zhang Y, Chen X, Zhang T (2016) Antidepressant‑like effects and possible mechanisms of amantadine on cognitive and synaptic deficits in a rat model of chronic stress. Stress 19: 104–113.
• Zarate CA Jr, Brutsche NE, Ibrahim  L, Franco‑Chaves J, Diazgranados N, Cravchik A, Selter J, Marquardt CA, Liberty  V, Luckenbaugh DA (2012) Replication of ketamine’s antidepressant efficacy in bipolar depression: a randomized controlled add‑on trial. Biol Psychiatry 71: 939–946.