Anxiolytic effects of muscarinic acetylcholine receptors agonist oxotremorine in chronically stressed rats and related changes in BDNF and FGF2 levels in the hippocampus and prefrontal cortex

Psychopharmacology

Volumn 234, Issue 4, 2017, Pages 559-573

  Di Liberto, Valentina ^a   Frinchi, Monica ^a   Verdi, Vincenzo ^a   Vitale, Angela ^a   Plescia, Fulvio ^a   Cannizzaro, Carla ^a   Massenti, Maria F ^a   Belluardo, Natale ^a   Mudò, Giuseppa ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Anxiety; Behavioral test; Cerebral cortex; Chronic restraint stress; Elevated plus maze test; Forced swimming test; mAChR; Neurotrophins; Novelty suppressed feeding test

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE 1; OXOTREMORINE; ANXIOLYTIC AGENT; MUSCARINIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BODY WEIGHT; CELL SURVIVAL; CONTROLLED STUDY; DEPRESSION; DORSAL HIPPOCAMPUS; ELEVATED PLUS MAZE TEST; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FORCED SWIM TEST; HYDROCORTISONE BLOOD LEVEL; LIGHT DARK BOX TEST; MEDIAL PREFRONTAL CORTEX; MENTAL STRESS; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NOVELTY SUPPRESSED FEEDING TEST; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPATIAL LEARNING; SPATIAL MEMORY; TRANQUILIZING ACTIVITY; TREATMENT DURATION; VENTRAL HIPPOCAMPUS; WESTERN BLOTTING; ANIMAL; ANXIETY; DRUG EFFECTS; DRUG THERAPY; HIPPOCAMPUS; MALE; METABOLISM; NERVE CELL; PREFRONTAL CORTEX; WISTAR RAT;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BRAIN-DERIVED NEUROTROPHIC FACTOR; FIBROBLAST GROWTH FACTOR 2; HIPPOCAMPUS; MALE; MUSCARINIC AGONISTS; NEURONS; OXOTREMORINE; PREFRONTAL CORTEX; RATS; RATS, WISTAR; STRESS, PSYCHOLOGICAL;

EID: 85003875998     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-016-4498-0     Document Type: Article

References (101)

1. Bachis A, Mallei A, Cruz MI, Wellstein A, Mocchetti I (2008) Chronic antidepressant treatments increase basic fibroblast growth factor and fibroblast growth factor-binding protein in neurons. Neuropharmacology 55:1114–1120. doi:10.1016/j.neuropharm.2008.07.014
2. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus—memory and anxiety. Neurosci Biobehav Rev 28:273–283. doi:10.1016/j.neubiorev.2004.03.004
3. Barathi VA, Weon SR, Beuerman RW (2009) Expression of muscarinic receptors in human and mouse sclera and their role in the regulation of scleral fibroblasts proliferation. Mol Vis 15:1277–1293
4. Belluardo N, Blum M, Mudo G, Andbjer B, Fuxe K (1998) Acute intermittent nicotine treatment produces regional increases of basic fibroblast growth factor messenger RNA and protein in the tel- and diencephalon of the rat. Neuroscience 83:723–740
5. Bennett MR, Lagopoulos J (2014) Stress and trauma: BDNF control of dendritic-spine formation and regression. Prog Neurobiol 112:80–99. doi:10.1016/j.pneurobio.2013.10.005
6. Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler EJ (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311:864–868. doi:10.1126/science.1120972
7. Borroto-Escuela DO, Romero-Fernandez W, Mudo G, Perez-Alea M, Ciruela F, Tarakanov AO, Narvaez M, Di LV, Agnati LF, Belluardo N, Fuxe K (2012) Fibroblast growth factor receptor 1-5-hydroxytryptamine 1A heteroreceptor complexes and their enhancement of hippocampal plasticity. Biol Psychiatry 71:84–91. doi:10.1016/j.biopsych.2011.09.012
8. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS (2000) Hippocampal volume reduction in major depression. Am J Psychiatry 157:115–118. doi:10.1176/ajp.157.1.115
9. Brown SM, Henning S, Wellman CL (2005) Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 15:1714–1722. doi:10.1093/cercor/bhi048
10. Caruana DA, Warburton EC, Bashir ZI (2011) Induction of activity-dependent LTD requires muscarinic receptor activation in medial prefrontal cortex. J Neurosci 31:18464–18478. doi:10.1523/JNEUROSCI.4719-11.2011
11. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301:386–389. doi:10.1126/science.1083968
12. Chau DT, Rada P, Kosloff RA, Taylor JL, Hoebel BG (2001) Nucleus accumbens muscarinic receptors in the control of behavioral depression: antidepressant-like effects of local M1 antagonist in the Porsolt swim test. Neuroscience 104:791–798
13. Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H (2012) Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 39:112–119. doi:10.1016/j.pnpbp.2012.05.018
14. Christensen T, Bisgaard CF, Nielsen HB, Wiborg O (2010) Transcriptome differentiation along the dorso-ventral axis in laser-captured microdissected rat hippocampal granular cell layer. Neuroscience 170:731–741. doi:10.1016/j.neuroscience.2010.07.016
15. Colman I, Ataullahjan A (2010) Life course perspectives on the epidemiology of depression 3. Can J Psychiatry 55:622–632
16. Cook SC, Wellman CL (2004) Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60:236–248. doi:10.1002/neu.20025
17. Degroot A, Treit D (2004) Anxiety is functionally segregated within the septo-hippocampal system. Brain Res 1001:60–71. doi:10.1016/j.brainres.2003.10.065
18. Dennis SH, Pasqui F, Colvin EM, Sanger H, Mogg AJ, Felder CC, Broad LM, Fitzjohn SM, Isaac JT, Mellor JR (2016) Activation of muscarinic M1 acetylcholine receptors induces long-term potentiation in the hippocampus. Cereb Cortex 26:414–426. doi:10.1093/cercor/bhv227
19. Di Liberto V, Mudo G, Belluardo N (2011) mGluR2/3 agonist LY379268, by enhancing the production of GDNF, induces a time-related phosphorylation of RET receptor and intracellular signaling Erk1/2 in mouse striatum. Neuropharmacology 61:638–645. doi:10.1016/j.neuropharm.2011.05.006
20. Di Liberto V, Mudo G, Fuxe K, Belluardo N (2014) Interactions between cholinergic and fibroblast growth factor receptors in brain trophism and plasticity. Curr Protein Pept Sci 15:691–702
21. Drever BD, Riedel G, Platt B (2011) The cholinergic system and hippocampal plasticity. Behav Brain Res. 221:505–514. doi:10.1016/j.bbr.2010.11.037
22. Drevets WC, Price JL, Simpson JR Jr, Todd RD, Reich T, Vannier M, Raichle ME (1997) Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386:824–827. doi:10.1038/386824a0
23. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127. doi:10.1016/j.biopsych.2006.02.013
24. Dwivedi Y, Rizavi HS, Conley RR, Roberts RC, Tamminga CA, Pandey GN (2003) Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch Gen Psychiatry 60:804–815. doi:10.1001/archpsyc.60.8.804
25. Eadie BD, Zhang WN, Boehme F, Gil-Mohapel J, Kainer L, Simpson JM, Christie BR (2009) Fmr1 knockout mice show reduced anxiety and alterations in neurogenesis that are specific to the ventral dentate gyrus. Neurobiol Dis 36:361–373. doi:10.1016/j.nbd.2009.08.001
26. Elsayed M, Banasr M, Duric V, Fournier NM, Licznerski P, Duman RS (2012) Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol Psychiatry 72:258–265. doi:10.1016/j.biopsych.2012.03.003
27. Engin E, Treit D (2007) The role of hippocampus in anxiety: intracerebral infusion studies. Behav Pharmacol 18:365–374. doi:10.1097/FBP.0b013e3282de7929
28. Eren-Kocak E, Turner CA, Watson SJ, Akil H (2011) Short-hairpin RNA silencing of endogenous fibroblast growth factor 2 in rat hippocampus increases anxiety behavior. Biol Psychiatry 69:534–540. doi:10.1016/j.biopsych.2010.11.020
29. Eskelund A, Budac DP, Sanchez C, Elfving B, Wegener G (2016) Female flinders sensitive line rats show estrous cycle-independent depression-like behavior and altered tryptophan metabolism. Neuroscience 329:337–348. doi:10.1016/j.neuroscience.2016.05.024
30. Evans SJ, Choudary PV, Neal CR, Li JZ, Vawter MP, Tomita H, Lopez JF, Thompson RC, Meng F, Stead JD, Walsh DM, Myers RM, Bunney WE, Watson SJ, Jones EG, Akil H (2004) Dysregulation of the fibroblast growth factor system in major depression. Proc Natl Acad Sci USA 101:15506–15511. doi:10.1073/pnas.0406788101
31. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19. doi:10.1016/j.neuron.2009.11.031
32. First M, Gil-Ad I, Taler M, Tarasenko I, Novak N, Weizman A (2011) The effects of fluoxetine treatment in a chronic mild stress rat model on depression-related behavior, brain neurotrophins and ERK expression. J Mol Neurosci 45:246–255. doi:10.1007/s12031-011-9515-5
33. Frinchi M, Di LV, Olivieri M, Fuxe K, Belluardo N, Mudo G (2010) FGF-2/FGFR1 neurotrophic system expression level and its basal activation do not account for the age-dependent decline of precursor cell proliferation in the subventricular zone of rat brain. Brain Res 1358:39–45. doi:10.1016/j.brainres.2010.08.083
34. Gaughran F, Payne J, Sedgwick PM, Cotter D, Berry M (2006) Hippocampal FGF-2 and FGFR1 mRNA expression in major depression, schizophrenia and bipolar disorder. Brain Res Bull 70:221–227. doi:10.1016/j.brainresbull.2006.04.008
35. Gibbons AS, Scarr E, McLean C, Sundram S, Dean B (2009) Decreased muscarinic receptor binding in the frontal cortex of bipolar disorder and major depressive disorder subjects. J Affect Disord 116:184–191. doi:10.1016/j.jad.2008.11.015
36. Gong S, Miao YL, Jiao GZ, Sun MJ, Li H, Lin J, Luo MJ, Tan JH (2015) Dynamics and correlation of serum cortisol and corticosterone under different physiological or stressful conditions in mice. PLoS One 10:e0117503. doi:10.1371/journal.pone.0117503
37. Govindarajan A, Rao BS, Nair D, Trinh M, Mawjee N, Tonegawa S, Chattarji S (2006) Transgenic brain-derived neurotrophic factor expression causes both anxiogenic and antidepressant effects. Proc Natl Acad Sci USA 103:13208–13213. doi:10.1073/pnas.0605180103
38. Hill MN, Hellemans KG, Verma P, Gorzalka BB, Weinberg J (2012) Neurobiology of chronic mild stress: parallels to major depression. Neurosci Biobehav Rev 36:2085–2117. doi:10.1016/j.neubiorev.2012.07.001
39. Hoffman AN, Armstrong CE, Hanna JJ, Conrad CD (2010) Chronic stress, cyclic 17beta-estradiol, and daily handling influences on fear conditioning in the female rat. Neurobiol Learn Mem 94:422–433. doi:10.1016/j.nlm.2010.08.010
40. Hohmann CF, Potter ED, Levey AI (1995) Development of muscarinic receptor subtypes in the forebrain of the mouse. J Comp Neurol 358:88–101. doi:10.1002/cne.903580106
41. Holmes A, Wellman CL (2009) Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev. 33:773–783. doi:10.1016/j.neubiorev.2008.11.005
42. Janowsky DS, el-Yousef MK, Davis JM, Sekerke HJ (1972) A cholinergic-adrenergic hypothesis of mania and depression. Lancet 2:632–635
43. Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ (2007) Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci 27:8877–8884. doi:10.1523/JNEUROSCI.2063-07.2007
44. Karege F, Vaudan G, Schwald M, Perroud N, La HR (2005) Neurotrophin levels in postmortem brains of suicide victims and the effects of antemortem diagnosis and psychotropic drugs. Brain Res Mol Brain Res. 136:29–37. doi:10.1016/j.molbrainres.2004.12.020
45. Kokras N, Antoniou K, Mikail HG, Kafetzopoulos V, Papadopoulou-Daifoti Z, Dalla C (2015) Forced swim test: what about females? Neuropharmacology 99:408–421. doi:10.1016/j.neuropharm.2015.03.016
46. Kuroda Y, McEwen BS (1998) Effect of chronic restraint stress and tianeptine on growth factors, growth-associated protein-43 and microtubule-associated protein 2 mRNA expression in the rat hippocampus. Brain Res Mol Brain Res 59:35–39
47. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15:4077–4092
48. Lindholm D, da Penha BM, Cooper J, Thoenen H, Castren E (1994) Brain-derived neurotrophic factor and neurotrophin-4 increase neurotrophin-3 expression in the rat hippocampus. Int J Dev Neurosci 12:745–751
49. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci. 26:7870–7874. doi:10.1523/JNEUROSCI.1184-06.2006
50. Liu RJ, Aghajanian GK (2008) Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc Natl Acad Sci USA 105:359–364. doi:10.1073/pnas.0706679105
51. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
52. Luchicchi A, Bloem B, Viana JN, Mansvelder HD, Role LW (2014) Illuminating the role of cholinergic signaling in circuits of attention and emotionally salient behaviors. Front Synaptic Neurosci 6:24. doi:10.3389/fnsyn.2014.00024
53. MacQueen GM, Campbell S, McEwen BS, Macdonald K, Amano S, Joffe RT, Nahmias C, Young LT (2003) Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci USA 100:1387–1392. doi:10.1073/pnas.0337481100
54. Mallei A, Shi B, Mocchetti I (2002) Antidepressant treatments induce the expression of basic fibroblast growth factor in cortical and hippocampal neurons. Mol Pharmacol 61:1017–1024
55. Maragnoli ME, Fumagalli F, Gennarelli M, Racagni G, Riva MA (2004) Fluoxetine and olanzapine have synergistic effects in the modulation of fibroblast growth factor 2 expression within the rat brain. Biol Psychiatry 55:1095–1102. doi:10.1016/j.biopsych.2004.02.003
56. Marinho MM, de Sousa FC, de Bruin VM, Vale MR, Viana GS (1998) Effects of lithium, alone or associated with pilocarpine, on muscarinic and dopaminergic receptors and on phosphoinositide metabolism in rat hippocampus and striatum. Neurochem Int 33:299–306
57. Martinowich K, Manji H, Lu B (2007) New insights into BDNF function in depression and anxiety. Nat Neurosci 10:1089–1093. doi:10.1038/nn1971
58. Matthews K, Robbins TW (2003) Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neurosci Biobehav Rev 27:45–55
59. Maurer AP, Vanrhoads SR, Sutherland GR, Lipa P, McNaughton BL (2005) Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus 15:841–852. doi:10.1002/hipo.20114
60. McEwen BS (2005) Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54:20–23. doi:10.1016/j.metabol.2005.01.008
61. Mitsushima D, Sano A, Takahashi T (2013) A cholinergic trigger drives learning-induced plasticity at hippocampal synapses. Nat Commun 4:2760. doi:10.1038/ncomms3760
62. Monteggia LM, Luikart B, Barrot M, Theobold D, Malkovska I, Nef S, Parada LF, Nestler EJ (2007) Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors. Biol Psychiatry 61:187–197. doi:10.1016/j.biopsych.2006.03.021
63. Mudo G, Jiang XH, Timmusk T, Bindoni M, Belluardo N (1996) Change in neurotrophins and their receptor mRNAs in the rat forebrain after status epilepticus induced by pilocarpine. Epilepsia 37:198–207
64. Murakami S, Imbe H, Morikawa Y, Kubo C, Senba E (2005) Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci Res 53:129–139. doi:10.1016/j.neures.2005.06.008
65. Navakkode S, Korte M (2012) Cooperation between cholinergic and glutamatergic receptors are essential to induce BDNF-dependent long-lasting memory storage. Hippocampus 22:335–346. doi:10.1002/hipo.20902
66. Neto FL, Borges G, Torres-Sanchez S, Mico JA, Berrocoso E (2011) Neurotrophins role in depression neurobiology: a review of basic and clinical evidence. Curr Neuropharmacol 9:530–552. doi:10.2174/157015911798376262
67. Neves-Pereira M, Mundo E, Muglia P, King N, Macciardi F, Kennedy JL (2002) The brain-derived neurotrophic factor gene confers susceptibility to bipolar disorder: evidence from a family-based association study. Am J Hum Genet 71:651–655. doi:10.1086/342288
68. Nibuya M, Morinobu S, Duman RS (1995) Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 15:7539–7547
69. 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. doi:10.1016/j.tips.2014.09.011
70. Orlovsky MA, Dosenko VE, Spiga F, Skibo GG, Lightman SL (2014) Hippocampus remodeling by chronic stress accompanied by GR, proteasome and caspase-3 overexpression. Brain Res 1593:83–94. doi:10.1016/j.brainres.2014.09.059
71. Padilla-Coreano N, Bolkan SS, Pierce GM, Blackman DR, Hardin WD, Garcia-Garcia AL, Spellman TJ, Gordon JA (2016) Direct ventral hippocampal-prefrontal input is required for anxiety-related neural activity and behavior. Neuron. doi:10.1016/j.neuron.2016.01.011
72. Paxinos G, Watson C (2014) The Rat Brain in Stereotaxic Coordinates, 7th edn. San Diego, CA, Academic Press
73. Perez JA, Clinton SM, Turner CA, Watson SJ, Akil H (2009) A new role for FGF2 as an endogenous inhibitor of anxiety. J Neurosci 29:6379–6387. doi:10.1523/JNEUROSCI.4829-08.2009
74. Ruedi-Bettschen D, Pedersen EM, Feldon J, Pryce CR (2005) Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats. Behav Brain Res 156:297–310. doi:10.1016/j.bbr.2004.06.001
75. Russo-Neustadt A, Ha T, Ramirez R, Kesslak JP (2001) Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model. Behav Brain Res 120:87–95
76. Saarelainen T, Hendolin P, Lucas G, Koponen E, Sairanen M, MacDonald E, Agerman K, Haapasalo A, Nawa H, Aloyz R, Ernfors P, Castren E (2003) Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J Neurosci 23:349–357
77. Sairanen M, Lucas G, Ernfors P, Castren M, Castren E (2005) Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J Neurosci 25:1089–1094. doi:10.1523/JNEUROSCI.3741-04.2005
78. Santos AR, Comprido D, Duarte CB (2010) Regulation of local translation at the synapse by BDNF. Prog Neurobiol 92:505–516. doi:10.1016/j.pneurobio.2010.08.004
79. Schaaf MJ, De Kloet ER, Vreugdenhil E (2000) Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation. Stress 3:201–208
80. Sen S, Nesse RM, Stoltenberg SF, Li S, Gleiberman L, Chakravarti A, Weder AB, Burmeister M (2003) A BDNF coding variant is associated with the NEO personality inventory domain neuroticism, a risk factor for depression. Neuropsychopharmacology 28:397–401. doi:10.1038/sj.npp.1300053
81. Shansky RM, Hamo C, Hof PR, McEwen BS, Morrison JH (2009) Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cereb Cortex 19:2479–2484. doi:10.1093/cercor/bhp003
82. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 93:3908–3913
83. Sheline YI, Gado MH, Kraemer HC (2003) Untreated depression and hippocampal volume loss. Am J Psychiatry 160:1516–1518. doi:10.1176/appi.ajp.160.8.1516
84. Shi SS, Shao SH, Yuan BP, Pan F, Li ZL (2010) Acute stress and chronic stress change brain-derived neurotrophic factor (BDNF) and tyrosine kinase-coupled receptor (TrkB) expression in both young and aged rat hippocampus. Yonsei Med J 51:661–671. doi:10.3349/ymj.2010.51.5.661
85. Shirayama Y, Chen AC, Nakagawa S, Russell DS, Duman RS (2002) Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 22:3251–3261
86. Siuciak JA, Lewis DR, Wiegand SJ, Lindsay RM (1997) Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav 56:131–137. doi:10.1016/S0091-3057(96)00169-4
87. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12:585–601. doi:10.1038/nrn3085
88. Smith MA, Makino S, Kvetnansky R, Post RM (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1768–1777
89. Srikumar BN, Raju TR, Shankaranarayana Rao BS (2006) The involvement of cholinergic and noradrenergic systems in behavioral recovery following oxotremorine treatment to chronically stressed rats. Neuroscience 143:679–688. doi:10.1016/j.neuroscience.2006.08.041
90. Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655–669. doi:10.1038/nrn3785
91. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P (2004) Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29:2007–2017. doi:10.1038/sj.npp.1300532
92. Turner CA, Akil H, Watson SJ, Evans SJ (2006) The fibroblast growth factor system and mood disorders. Biol Psychiatry 59:1128–1135. doi:10.1016/j.biopsych.2006.02.026
93. Turner CA, Calvo N, Frost DO, Akil H, Watson SJ (2008a) The fibroblast growth factor system is downregulated following social defeat. Neurosci Lett 430:147–150. doi:10.1016/j.neulet.2007.10.041
94. Turner CA, Gula EL, Taylor LP, Watson SJ, Akil H (2008b) Antidepressant-like effects of intracerebroventricular FGF2 in rats. Brain Res 1224:63–68. doi:10.1016/j.brainres.2008.05.088
95. Veena J, Srikumar BN, Mahati K, Raju TR, Shankaranarayana Rao BS (2011) Oxotremorine treatment restores hippocampal neurogenesis and ameliorates depression-like behaviour in chronically stressed rats. Psychopharmacology 217:239–253. doi:10.1007/s00213-011-2279-3
96. Warner-Schmidt JL, Duman RS (2007) VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc Natl Acad Sci USA 104:4647–4652. doi:10.1073/pnas.0610282104
97. 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
98. Xu H, Qing H, Lu W, Keegan D, Richardson JS, Chlan-Fourney J, Li XM (2002) Quetiapine attenuates the immobilization stress-induced decrease of brain-derived neurotrophic factor expression in rat hippocampus. Neurosci Lett 321:65–68
99. Yamaura K, Tanaka R, Bi Y, Fukata H, Oishi N, Sato H, Mori C, Ueno K (2015) Protective effect of young green barley leaf (Hordeum vulgare L.) on restraint stress-induced decrease in hippocampal brain-derived neurotrophic factor in mice. Pharmacogn Mag 11:S86–S92. doi:10.4103/0973-1296.157702
100. Yulug B, Ozan E, Gonul AS, Kilic E (2009) Brain-derived neurotrophic factor, stress and depression: a mini review. Brain Res Bull 78:267–269. doi:10.1016/j.brainresbull.2008.12.002
101. Zimmerman M, Mattia JI, Posternak MA (2002) Are subjects in pharmacological treatment trials of depression representative of patients in routine clinical practice? Am J Psychiatry 159:469–473. doi:10.1176/appi.ajp.159.3.469