NMDA glutamate receptor inhibition in the dorsal hippocampus reduced the maintenance of electric foot shock stress -induced anxiety and depression like behaviors in mice

authors:

avatar Elham Samkhaniani , avatar Davud Nodehei , avatar Fatemeh Salem , avatar Mohammad Hossein Zarghami , avatar Maryam Khosravi , avatar Boshra Hatef , avatar Hedayat Sahraei , avatar Hassan Ghoshooni , *

Koomesh: Vol.21, issue 4; 716-725
published online: December 01, 2019
article type: Research Article
received: October 01, 2018
accepted: May 01, 2019

how to cite: Samkhaniani E, Nodehei D, Salem F, Zarghami M H, Khosravi M, et al. NMDA glutamate receptor inhibition in the dorsal hippocampus reduced the maintenance of electric foot shock stress -induced anxiety and depression like behaviors in mice. koomesh. 2019;21(4):e153137. 

Abstract

Introduction: In the present study, the effect of inhibition of glutamate NMDA receptors located in the dorsal hippocampus on the maintenance of anxiety and depression like behaviors induced by electric foot shock stress was investigated. Materials and Methods: NMARI male mice were divided into two categories. The first category received electro foot shock for 30 minutes after injection of memantine (1, 5 and 10 mg/kg) or saline (1ml/kg) intraperitoneally. The second category was bilaterally cannulated in the dorsal hippocampus and one week later, the animals first received different doses of memantine (1, 5 and 10 μg /mouse) intra-hippocampally and five min before stress. Remarkably, this procedure was repeated for 4 consecutive days. Six days after stress termination, maintenance of anxiety in animals was examined using the elevated plus maze. Two days after the anxiety test, forced swimming test was conducted for depression like behavior maintenance evaluation. Results: Stress reduced the open arm time in the elevated plus maze. Intraperitoneal administration of memantine prevented the stress effect. Also, intra-dorsal hippocampus administration of memantine preventd the maintenance of anxiety induced by stress. Stress also increased the immobility time in the forced swimming test. Both intraperitoneal and intra-dorsal hippocampus administration of memantine inhibited the maintenance of depression induced by stress. Conclusion: Electric foot shock can lead to persistence anxiety and depression like behavior in mice. Inhibition of NMDA glutamate receptors in the dorsal hippocampus reduced the stress response.

References

  • 1.

    Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H. Chronic restraint stress causes anxiety-and depression-like behaviors, down regulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuro-Psychoph 2012; 39: 112-119.

  • 2.

    Nasca C, Zelli D, Bigio B, Piccinin S, Scaccianoce S, Nistic R, McEwen BS. Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Nat Acad Sci 2015; 112: 14960-14965.

  • 3.

    Li M, Li X, Zhang X, Ren J, Jiang H, Wang Y, et al. Effects of prenatal chronic mild stress exposure on hippocampal cell proliferation, expression of GSK-3, and NR2B in adult offspring during fear extinction in rats. Int J Dev Neur 2014; 35: 16-24.

  • 4.

    Boyle LM. A neuroplasticity hypothesis of chronic stress in the basolateral amygdala. Yale J Biol Med 2013; 86: 117-125.

  • 5.

    Christian KM, Miracle AD, Wellman CL, Nakazawa K. Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 2011; 174: 26-36.

  • 6.

    Shekhar A, Truitt W, Rainnie D, Sajdyk T. Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety. Stress 2005; 8: 209-219.

  • 7.

    Calabrese F, Guidotti G, Molteni R, Racagni G, Mancini M, Riva MA. Stress-induced changes of hippocampal NMDA receptors: modulation by duloxetine treatment. PloS One 2012; 7: e37916.

  • 8.

    Mathew SJ, Coplan JD, Smith EL, Schoepp DD, Rosenblum LA, Gorman JM. Glutamatehypothalamic-pituitary-adrenal axis interactions: implications for mood and anxiety disorders. CNS Spectrums 2001; 6: 555-564.

  • 9.

    Roberto M, Gilpin NW, Siggins GR. The central amygdala and alcohol: role of -aminobutyric acid, glutamate, and neuropeptides. Cold Spring Harb Perspect Med 2012; 2: a012195.

  • 10.

    Meng FT, Zhao J, Fang H, Liu YJ. The influence of chronic stress on anxiety-like behavior and cognitive function in different human GFAP-ApoE transgenic adult male mice. Stress 2015; 18: 419-426.

  • 11.

    Zhu S, Wang J, Zhang Y, Li V, Kong J, He J, Li XM. Unpredictable chronic mild stress induces anxiety and depression-like behaviors and inactivates AMP-activated protein kinase in mice. Brain Res 2014; 1576: 81-90.

  • 12.

    Zhu S, Shi R, Wang J, Wang JF, Li XM. Unpredictable chronic mild stress not chronic restraint stress induces depressive behaviours in mice. Neuroreport 2014; 25: 1151-1155.

  • 13.

    Kavushansky A, Richter-Levin G. Effects of stress and corticosterone on activity and plasticity in the amygdala. J Neurosci Res 2006; 84: 1580-1587.

  • 14.

    Maroun M, Ioannides PJ, Bergman KL, Kavushansky A, Holmes A, Wellman CL. Fear extinction deficits following acute stress associate with increased spine density and dendritic retraction in basolateral amygdala neurons. Eur J Neurosci 2013; 38: 2611-2620.

  • 15.

    Masneuf S, Lowery-Gionta E, Colacicco G, Pleil KE, Li C, Crowley N, et al. Glutamatergic mechanisms associated with stress-induced amygdala excitability and anxiety-related behavior. Neuropharmacology 2014; 85: 190-197.

  • 16.

    Chen H, Pellegrini J, Aggarwal S, Lei SZ, Warach S, Jensen FE, et al. Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity. J Neuroscience 1992; 12: 4427-4436.

  • 17.

    Johnson JW, Kotermanski SE. Mechanism of action of memantine. Curr Opin Pharmacol 2006; 6: 61-67.

  • 18.

    Schwartz TL, Siddiqui UA, Raza S. Memantine as an augmentation therapy for anxiety disorders. Case Rep Psychiatry 2012; 2012: 749796.

  • 19.

    Maeng S, Zarate CA. The role of glutamate in mood disorders: results from the ketamine in major depression study and the presumed cellular mechanism underlying its antidepressant effects. Curr Psychiatr Rep 2007; 9: 467-474.

  • 20.

    Rus GZ, Abelaira HM, Stringari RB, Fries GR, Kapczinski F, Quevedo J. Memantine treatment reverses anhedonia, normalizes corticosterone levels and increases BDNF levels in the prefrontal cortex induced by chronic mild stress in rats. Metab Brain Dis 22012; 7: 175-182.

  • 21.

    Sadeghi BA, Sahraei HE, Zardooz H, Alibeik HE, Sarahian N. Effects of intra-amygdala memantine infusion on metabolic symptoms induced by chronic stress in male NMRI mice. Koomesh 2015; 16: 376-383. (Persian).

  • 22.

    Osanloo N, Sarahian N, Zardooz H, Sahraei H, Sahraei M, Sadeghi B. Effects of memantine, an NMDA antagonist, on metabolic syndromes in female NMRI mice. Basic Clin Neurosci 2015; 6: 239-252.

  • 23.

    Rus GZ, Stringari RB, Kirsch TR, Fries GR, Kapczinski F, Roesler R, et al. Neurochemical and behavioural effects of acute and chronic memantine administration in rats: Further support for NMDA as a new pharmacological target for the treatment of depression? Brain Res Bull 2012; 81: 585-589.

  • 24.

    Zarrindast MR, Nasehi M, Piri M, Heidari N. Effects of cholinergic system of dorsal hippocampus of rats on MK-801 induced anxiolytic-like behavior. Neurosci Lett 2011; 505: 65-70.

  • 25.

    Musazzi L, Racagni G, Popoli M. Stress, glucocorticoids and glutamate release: effects of antidepressant drugs. Neurochem Int 2011; 59: 138-149.

  • 26.

    Paxinos G, Franklin kBJ. The mouse brain in stereotaxic coordinates. California: Elsevier Science 2001.

  • 27.

    Komada M, Takao K, Miyakawa T. Elevated plus maze for mice. JoVE 2008; 22.

  • 28.

    Can A, Dao DT, Arad M, Terrillion CE, Piantadosi SC, Gould TD. The mouse forced swim test. Journal of visualized experiments: JoVE 2012; 59.

  • 29.

    Gulyaeva NV. Functional neurochemistry of the ventral and dorsal hippocampus: Stress, depression, dementia and remote hippocampal damage. Neurochem Res 2018; 44: 1-17.

  • 30.

    Barbas H, Blatt GJ. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 1995; 5: 511-533.

  • 31.

    Verwer RW, Meijer RJ, Van Uum HF, Witter MP. Collateral projections from the rat hippocampal formation to the lateral and medial prefrontal cortex. Hippocampus 1997; 7: 397-402.

  • 32.

    Carrasco GA, Van de Kar LD. Neuroendocrine pharmacology of stress. Eur J Pharmacol 2003; 463: 235-272.

  • 33.

    Miller DB, O'Callaghan JP. Neuroendocrine aspects of the response to stress. Metab-Clin Experiment 2002; 51: 5-10.

  • 34.

    Maghami S, Sadeghimahalli F, Zardooz H. Effects of maternal separation stress on glucose homeostasis in pubertal male rats. Koomesh 2017; 19: 887-893. (Persian).

  • 35.

    Bijani S, Najafi Abedi A, Ranjbaran M, Sadeghi Gharajeh Daghi S, Ghoshooni H, Zardooz H, et al. Effects of noise pollution stress during pregnancy on anatomical and functional brain cortex development of the off springs of NMRI mice. Koomesh 2013; 14: 192-199. (Persian).

  • 36.

    Duvarci S, Pare D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 2007; 27: 4482-4491.

  • 37.

    Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 1997; 17: 2492-2498.

  • 38.

    McEwen BS. Stress and hippocampal plasticity. Ann Rev Neurosci 1999; 22: 105-122.

  • 39.

    Popoli M, Yan Z, McEwen BS, Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 2012; 13: 22-37.

  • 40.

    Lau CG, Zukin RS. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 2007; 8: 413-426.

  • 41.

    Nasca C, Bigio B, Zelli D, Nicoletti F, McEwen BS. Mind the gap: Glucocorticoids modulate hippocampal glutamate tone underlying individual differences in stress susceptibility. Mol Psychiatry 2015; 20: 755-763.

  • 42.

    Lehner M, Wisowska-Stanek A, Gryz M, Sobolewska A, Turzyska D, Chmielewska N, et al. The co-expression of GluN2B subunits of the NMDA receptors and glucocorticoid receptors after chronic restraint stress in low and high anxiety rats. Behav Brain Res 2017; 319: 124-134.

  • 43.

    Li N, Liu RJ, Dwyer JM, Banasr M, Lee B, Son H, et al. Glutamate N-methyl-Daspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol Psychiatry 2011; 69: 754-761.

  • 44.

    Liu L, Zhang L, Wang T, Chen L. Dopamine D1 receptor in the medial prefrontal cortex mediates anxiety-like behaviors induced by blocking glutamatergic activity of the ventral hippocampus in rats. Brain Res 2019; 1704: 59-67.##.

  • 45.

    Grecksch G, Bartzsch K, Widera A, Becker A, Hllt V, Koch T. Development of tolerance and sensitization to different opioid agonists in rats. Psychopharmacology 2006; 186: 177-184.

  • 46.

    Vezina P. Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci Biobehav Rev 2004; 27: 827-839.

  • 47.

    Diazgranados N, Ibrahim L, Brutsche NE, Newberg A, Kronstein P, Khalife S, et al. A randomized add-on trial of an N-methyl-D-aspartate antagonist in treatment resistant bipolar depression. Arch Gen Psychiatry 2010; 67: 793-802.##.