Web of Science (Emerging Sources Citation Index)

Document Type: Review Article

Authors

1 Department of Neuroscience and Addiction Studies, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran

2 Semnan Neuroscience Society, Faculty of Medicine, Semnan University of Medical Sciences, Semnan, Iran

3 Pharmaceutical Sciences Research Center, Ardabil University of Medical Sciences, Ardabil, Iran

4 Department of Pharmacology, School of Pharmacy, Ardabil University of Medical Sciences, Ardabil, Iran

Abstract

Chronic exposure to stress has been demonstrated to increase the risk of developing neuropsychiatric disorders. Given the importance of effective therapeutic ways to overcome stress-related deficits,the present review focused on the therapeutic effects of environmental enrichment (EE) against chronic stress-induced cognitive-behavioral impairments. Chronic stress exposure has been shown to modify neuronal function and morphology in corticolimbic structures such as the prefrontal cortex (PFC), hippocampus, and amygdala, three brain regions greatly involved in mood regulation, fear processing, and cognition. It has been reported that chronic stress reduces brain-derived neurotrophic factor (BDNF) levels and its mRNA expression on the PFC, suggesting that downregulation of BDNF is a possible mechanism that mediates the effect of stress on anxiety or depression-like behaviors. There is an increasing demand for findings of effective intervention methods for alleviating the detrimental effects of chronic stress. EE is a beneficial intervention for improving anxiety and depression-like behaviors. A large body of research revealed that exposure to EE improves several conditions, including degenerative diseases, epilepsy, traumatic brain injury, anxiety, and depression. This article will provide an overview by discussing the influences of chronic stress on cognitive function and beneficial therapeutic effects of environmental enrichment (EE) against chronic stress.

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[1] A.L. Gold, L.M. Shin, S.P. Orr, M.A. Carson, S.L. Rauch, M.L. Macklin, N.B. Lasko, L.J. Metzger, D.D. Dougherty, N.M. Alpert. Psychol. Med., 2011, 41, 2563.

[2] C.D. Conrad. Neuro-Psychopharmacology Biol. Psychiatry., 2010, 34, 742–755.

[3] K. Wingenfeld, O.T. Wolf. Psy.neuro.endocrin., 2015, 51, 282–295.

[4] S.J. Lupien, B.S. McEwen, M.R. Gunnar, C. Heim. Nat. Rev. Neurosci., 2009, 10, 434–445.

[5] O. Horovitz, M.M. Tsoory, J. Hall, S. Jacobson-Pick, G. Richter-Levin. Neuroendo., 2012, 95, 56–64.

[6] R. Malik, S. Chattarji. J. Neurophysiol., 2012, 107, 1366–1378.

[7] A. Karl, M. Schaefer, L.S. Malta, D. Dörfel, N. Rohleder, A. Werner. Neurosci. Biobehav. Rev., 2006, 30, 1004–1031.

[8] H.S. Mohammadi, I. Goudarzi, T. Lashkarbolouki, K. Abrari, M.E. Salmani. Behav. Brain Res., 2014, 270, 196–205.

[9] C. Liston, B.S. McEwen, B.J. Casey, Proc. Natl. Acad. Sci., 2009, 106, 912–917.

[10] B.S. McEwen. Physiol. Rev., 2007, 87, 873–904.

[11] M. Koenigs, J. Grafman. Neurosci., 2009, 15, 540–548.

[12] A.L. Mahan, K.J. Ressler. Trends Neurosci., 2012, 35, 24–35.

[13] J.M. Bessa, D. Ferreira, I. Melo, F. Marques, J.J. Cerqueira, J.A. Palha, O.F.X. Almeida, N. Sousa. Mol. Psychiatry., 2009, 14, 764–773.

[14] S. Ghodrati-Jaldbakhan, A. Ahmadalipour, A. Rashidy-Pour, A.A. Vafaei, H. Miladi-Gorji, M. Alizadeh, Brain Res., 2017, 1663, 20–28.

[15] E. Dallé, M. V Mabandla. Mol. Brain., 2018, 11, 18.

[16] C.A. Murgatroyd, C.J. Peña, G. Podda, E.J. Nestler, B.C. Nephew. Neuropeptides., 2015, 52, 103–111.

[17] L. Zhang, Z.-X. Zhao. Neurosci. Bull., 2006, 22, 63–67.

[18] C. Rossi, A. Angelucci, L. Costantin, C. Braschi, M. Mazzantini, F. Babbini, M.E. Fabbri, L. Tessarollo, L. Maffei, N. Berardi. Eur. J. Neurosci., 2006, 24, 1850–1856.

[19] Q. Cheng, S.-H. Song, G.J. Augustine. Synaptic Neurosci., 2018, 10, 33.

[20] R. Molteni, S. Chourbaji, C. Brandwein, G. Racagni, P. Gass, M.A. Riva, J. Psychopharmacol., 2010, 24, 595–603.

[21] S. Hilfiker, V.A. Pieribone, A.J. Czernik, H.-T. Kao, G.J. Augustine, P. Greengard. B Biol. Sci., 1999, 354, 269–279.

[22] T. Jovanovic, K.J. Ressler. Am. J. Psychiatry., 2010, 167, 648–662.

[23] F.J. Mirza, S. Zahid. Neurosci. Bull., 2018, 34, 349–358.

[24] R. Silva, A.R. Mesquita, J. Bessa, J.C. Sousa, I. Sotiropoulos, P. Leão, O.F.X. Almeida, N. Sousa. Neurosci., 2008, 152, 656–669.

[25] N. Elizalde, P.M. Pastor, Á.L. Garcia‐García, F. Serres, E. Venzala, J. Huarte, M.J. Ramírez, J. Del Rio, T. Sharp, R.M. Tordera. J. Neurochem., 2010, 114, 1302–1314.

[26] S.K. Yeap, B.K. Beh, N.M. Ali, H. Mohd Yusof, W.Y. Ho, S.P. Koh, N.B. Alitheen, K. Long. Biomed Res. Int., 2014, 2014.

[27] R.R. Teixeira, A.V. de Souza, L.G. Peixoto, H.L. Machado, D.C. Caixeta, D.D. Vilela, N.B. Baptista, C.R. Franci, F.S. Espindola. Neurosci. Lett., 2017, 655, 179–185.

[28] S. Sorce, K.-H. Krause. Redox Signal., 2009, 11, 2481–2504.

[29] G. Lucca, C.M. Comim, S.S. Valvassori, G.Z. Réus, F. Vuolo, F. Petronilho, F. Dal-Pizzol, E.C. Gavioli, J. Quevedo. Neurochem. Int., 2009, 54, 358–362.

[30] A.M. Maluach, K.A. Misquitta, T.D. Prevot, C. Fee, E. Sibille, M. Banasr, A.C. Andreazza. Unpredictable Chronic Mild Stress, Chronic Stress, 2017, 1, 2470547017724744.

[31] S. Schiavone, S. Sorce, M. Dubois-Dauphin, V. Jaquet, M. Colaianna, M. Zotti, V. Cuomo, L. Trabace, K.-H. Krause. Biol. Psychiatry., 2009, 66, 384–392.

[32] F. Ng, M. Berk, O. Dean, A.I. Bush, Int. J. Neuropsychopharmacol., 2008, 11, 851–876.

[33] R.-J. Liu, G.K. Aghajanian. Proc. Natl. Acad. Sci., 2008, 105, 359–364.

[34] A. Dayi, F. Cetin, A.R. Sisman, I. Aksu, A. Tas, S. Gönenc, N. Uysal. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res., 2015, 21, 69.

[35] R.-R. Huang, W. Hu, Y.-Y. Yin, Y.-C. Wang, W.-P. Li, W.-Z. Li. Int. J. Mol. Med., 2015, 35, 553–559.

[36] R.S. Duman, G.K. Aghajanian. Science, 2012, 338, 68–72.

[37] S. Jin, Y. Zhao, Y. Jiang, Y. Wang, C. Li, D. Zhang, B. Lian, Z. Du, H. Sun, L. Neuroreport., 2018, 29, 643.

[38] B. Han, J.-H. Wang, Y. Geng, L. Shen, H.-L. Wang, Y.-Y. Wang, M.-W. Wang. Cell. Physiol. Biochem., 2017, 41, 1766–1776.

[39] Y. Wang, H. Kan, Y. Yin, W. Wu, W. Hu, M. Wang, W. Li, W. Li. Pharmacol. Biochem. Behav., 2014, 120, 73–81.

[40] K.A. Alkadhi, T.T. Tran. Brain Res., 2014, 1588, 150–158.

[41] A. Mika, G.J. Mazur, A.N. Hoffman, J.S. Talboom, H.A. Bimonte-Nelson, F. Sanabria, C.D. Conrad. Behav. Neurosci., 2012, 126, 605.

[42] R. Adamec, M. Hebert, J. Blundell, R.F. Mervis. Behav. Brain Res., 2012, 226, 133–146.

[43] M.E. Robinson, D.S. Teyhen, S.S. Wu, J.L. Dugan, A.C. Wright, J.D. Childs, G. Yang, S.Z. George. Mil. Med., 2009, 174, 572–577.

[44] K.M. Moench, C.L. Wellman. Neuroscience, 2017, 357, 145–159.

[45] M.R. Rosenzweig, D. Krech, E.L. Bennett, M.C. Diamond, Physiol. Psychol., 1962, 55, 429.

[46] B.M. Elliott, N.E. Grunberg. Behav. Brain Res., 2005, 165, 187–196.

[47] L.A. Toth, K. Kregel, L. Leon, T.I. Musch. Comp. Med., 2011, 61, 314–321.

[48] A. Fernández-Teruel, L. Giménez-Llort, R.M. Escorihuela, L. Gil, R. Aguilar, T. Steimer, A. Tobena. Pharmacol. Biochem. Behav., 2002, 73, 233–245.

[49] J. Nithianantharajah, H. Levis, M. Murphy. Neurobiol. Learn. Mem., 2004, 81, 200–210.

[50] H. Abikoff, L. Hechtman, R.G. Klein, R. Gallagher, K. Fleiss, J.O.Y. Etcovitch, L. Cousins, B. Greenfield, D. Martin, S. Pollack. Psychiatry., 2004, 43, 820–829.

[51] E.R. Kandel, J.H. Schwartz, T.M. Jessell, D. of B. and M.B.T. Jessell, S. Siegelbaum, A.J. Hudspeth. McGraw-hill New York, 2000.

[52] G. Kempermann. Nat. Rev. Neurosci., 2019, 20, 235–245.

[53] N. Moradi-Kor, A. Ghanbari, H. Rashidipour, B. Yousefi, A.R. Bandegi, A. Rashidy-Pour. Horm. Behav., 2019, 112, 20–31.

[54] M. Koehl, V. Lemaire, W. Mayo, D.N. Abrous, S. Maccari, P.V. Piazza, M. Le Moal, M. Vallée. Neurotox. Res., 2002, 4, 281–296.

[55] S. Morley Fletcher, M. Rea, S. Maccari, G. Laviola. Eur. J. Neurosci., 2003, 18, 3367–3374.

[56] M. Vallee, W. Mayo, F. Dellu, M. Le Moal, H. Simon, S. Maccari. J. Neurosci., 1997, 17, 2626–2636.

[57] J. Beauquis, P. Roig, A.F. De Nicola, F. Saravia. PLoS One., 2010, 5, e13993.

[58] A.M. Sirevaag, J.E. Black, W.T. Greenough. Exp. Neurol., 1991, 111, 74–79.

[59] D.R. Varman, K.E. Rajan. PLoS One., 2015, 10, e0127945.

[60] M. Li, M. Wang, S. Ding, C. Li, X. Luo. Acta Histochem. Cytochem., 2012, 11054.

[61] J. Nader, C. Claudia, R. El Rawas, L. Favot, M. Jaber, N. Thiriet, M. Solinas. Neuropsychopharmacol., 2012, 37, 1579–1587.