Oxotremorine treatment restores hippocampal neurogenesis and ameliorates depression-like behaviour in chronically stressed rats

Psychopharmacology

Volumn 217, Issue 2, 2011, Pages 239-253

  Veena, J ^a,b   Srikumar, B N ^a,c   Mahati, K ^a   Raju, T R ^a   Shankaranarayana Rao, B S ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

^b NutriNeuro Bordeaux University   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Adult neurogenesis; Cholinergic activity; Depression; Forced swim test; Hippocampal volume; Oxotremorine; Stress; Sucrose consumption test

Indexed keywords

ACETYLCHOLINE; BROMODEOXYCYTIDINE; OXOTREMORINE; SUCROSE;

ANALYTIC METHOD; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHOLINERGIC ACTIVITY; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; DEPRESSION; EMOTIONAL STRESS; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; STEM CELL; SUCROSE CONSUMPTION TEST;

ANIMALS; BEHAVIOR, ANIMAL; CELL PROLIFERATION; CELL SURVIVAL; DEPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MUSCARINIC AGONISTS; NEUROGENESIS; NEURONS; ORGAN SIZE; OXOTREMORINE; RATS; RATS, WISTAR; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 82955167844     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2279-3     Document Type: Article

References (116)

1. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523-569 (Pubitemid 40404636)
2. Ashkenazi A, Ramachandran J, Capon DJ (1989) Acetylcholine analogue stimulates DNA synthesis in brain-derived cells via specific muscarinic receptor subtypes. Nature 340:146-150 (Pubitemid 19175366)
3. Balu DT, Lucki I (2009) Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev 33:232-252
4. Banasr M, Duman RS (2007) Regulation of neurogenesis and gliogenesis by stress and antidepressant treatment. CNS Neurol Disord Drug Targets 6:311-320 (Pubitemid 351492092)
5. Banasr M, Valentine GW, Li XY, Gourley SL, Taylor JR, Duman RS (2007) Chronic unpredictable stress decreases cell proliferation in the cerebral cortex of the adult rat. Biol Psychiatry 62:496-504 (Pubitemid 47284039)
6. Bartus RT, Dean RL 3rd, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414
7. Bhagya V, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2008) Neonatal clomipramine induced endogenous depression in rats is associated with learning impairment in adulthood. Behav Brain Res 187:190-194 (Pubitemid 350225612)
8. Bhagya V, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2011) Chronic escitalopram treatment restores spatial learning, monoamine levels, and hippocampal long-term potentiation in an animal model of depression. Psychopharmacology (Berl) 214(2):477-494
9. 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
10. Burgard EC, Sarvey JM (1990) Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci Lett 116:34-39 (Pubitemid 20237132)
11. Cameron HA, McKay RD (1999) Restoring production of hippocampal neurons in old age. Nat Neurosci 2:894-897 (Pubitemid 30602603)
12. 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 (Pubitemid 36877077)
13. 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 (Pubitemid 32607430)
14. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210-213
15. Cobb SR, Davies CH (2005) Cholinergic modulation of hippocampal cells and circuits. J Physiol 562:81-88 (Pubitemid 40207787)
16. Cohen JE, Zimmerman G, Melamed-Book N, Friedman A, Dori A, Soreq H (2008) Transgenic inactivation of acetylcholinesterase impairs homeostasis in mouse hippocampal granule cells. Hippocampus 18:182-192 (Pubitemid 351413484)
17. Cooper-Kuhn CM, Winkler J, Kuhn HG (2004) Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J Neurosci Res 77:155-165 (Pubitemid 38859401)
18. Coskun V, Luskin MB (2002) Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J Neurosci Res 69:795-802 (Pubitemid 34984697)
19. Czeh B, Lucassen PJ (2007) What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci 257:250-260 (Pubitemid 47301403)
20. Czeh B, Welt T, Fischer AK, Erhardt A, Schmitt W, Muller MB, Toschi N, Fuchs E, Keck ME (2002) Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry 52:1057-1065 (Pubitemid 35379963)
21. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572 (Pubitemid 36528662)
22. Dori A, Cohen J, Silverman WF, Pollack Y, Soreq H (2005) Functional manipulations of acetylcholinesterase splice variants highlight alternative splicing contributions to murine neocortical development. Cereb Cortex 15:419-430 (Pubitemid 40388243)
23. Duman RS, Monteggia LM (2006) A neurotrophic model for stressrelated mood disorders. Biol Psychiatry 59:1116-1127
24. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317 (Pubitemid 28512114)
25. Forette F, Hauw JJ (2008) Alzheimer;s disease: from brain lesions to new drugs. Bull Acad Natl Med 192:363-378, discussion 378-380
26. Frodl T, Meisenzahl EM, Zetzsche T, Born C, Groll C, Jager M, Leinsinger G, Bottlender R, Hahn K, Moller HJ (2002) Hippocampal changes in patients with a first episode of major depression. Am J Psychiatry 159:1112-1118 (Pubitemid 34743250)
27. Fuchs E, Czeh B, Michaelis T, de Biurrun G, Watanabe T, Frahm J (2002) Synaptic plasticity and tianeptine: structural regulation. Eur Psychiatry 17(Suppl 3):311-317 (Pubitemid 34839394)
28. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438 (Pubitemid 30127128)
29. Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4:e5464
30. 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
31. Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492-2498 (Pubitemid 27137415)
32. Gould E, Tanapat P, Hastings NB, Shors TJ (1999) Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 3:186-192 (Pubitemid 29215058)
33. Govindarajan A, Shankaranarayana 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 (Pubitemid 44338941)
34. Gronier B, Rasmussen K (1998) Activation of midbrain presumed dopaminergic neurones by muscarinic cholinergic receptors: an in vivo electrophysiological study in the rat. Br J Pharmacol 124:455-464 (Pubitemid 28254500)
35. Gronier B, Perry KW, Rasmussen K (2000) Activation of the mesocorticolimbic dopaminergic system by stimulation of muscarinic cholinergic receptors in the ventral tegmental area. Psychopharmacol Berl 147:347-355 (Pubitemid 30048481)
36. Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16:710-715 (Pubitemid 44791918)
37. Hasselmo ME, Giocomo LM (2006) Cholinergic modulation of cortical function. J Mol Neurosci 30:133-135 (Pubitemid 46035351)
38. Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146-154 (Pubitemid 29409757)
39. Heine VM, Maslam S, Joels M, Lucassen PJ (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol Aging 25:361-375 (Pubitemid 38220972)
40. Ho NF, Han SP, Dawe GS (2009) Effect of voluntary running on adult hippocampal neurogenesis in cholinergic lesioned mice. BMC Neurosci 10:57
41. Janowsky DS, el-Yousef MK, Davis JM (1974) Acetylcholine and depression. Psychosom Med 36:248-257
42. Janowsky DS, el-Yousef MK, Davis JM, Sekerke HJ (1972) A cholinergic-adrenergic hypothesis of mania and depression. Lancet 2:632-635
43. Janowsky DS, el-Yousel MK, Davis JM, Sekerke HJ (1973) Provocation of schizophrenic symptoms by intravenous administration of methylphenidate. Arch Gen Psychiatry 28:185-191
44. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16:147-154
45. Joca SR, Ferreira FR, Guimaraes FS (2007) Modulation of stress consequences by hippocampal monoaminergic, glutamatergic and nitrergic neurotransmitter systems. Stress 10:227-249 (Pubitemid 47037199)
46. Kaneko N, Okano H, Sawamoto K (2006) Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 11:1145-1159 (Pubitemid 44426205)
47. Kempermann G, Gage FH (2002) Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16:129-136 (Pubitemid 35463603)
48. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adultgenerated new neurons in the hippocampus of mice. Development 130:391-399 (Pubitemid 36175935)
49. Kendler KS, Karkowski LM, Prescott CA (1999) Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 156:837-841 (Pubitemid 29260336)
50. Kotani S, Yamauchi T, Teramoto T, Ogura H (2006) Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142:505-514 (Pubitemid 44415335)
51. Kotani S, Yamauchi T, Teramoto T, Ogura H (2008) Donepezil, an acetylcholinesterase inhibitor, enhances adult hippocampal neurogenesis. Chem Biol Interact 175:227-230
52. Krishnan KR, Charles HC, Doraiswamy PM, Mintzer J, Weisler R, Yu X, Perdomo C, Ieni JR, Rogers S (2003) Randomized, placebo-controlled trial of the effects of donepezil on neuronal markers and hippocampal volumes in Alzheimer's disease. Am J Psychiatry 160: 2003-2011 (Pubitemid 39619638)
53. Laviola G, Hannan AJ, Macri S, Solinas M, Jaber M (2008) Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol Dis 31:159-168
54. Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, Kang DW, Jahng JW (2007) Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58:32-39 (Pubitemid 46678488)
55. Lehmann K, Butz M, Teuchert-Noodt G (2005) Offer and demand: proliferation and survival of neurons in the dentate gyrus. Eur J Neurosci 21:3205-3216 (Pubitemid 40961416)
56. Leuner B, Gould E, Shors TJ (2006) Is there a link between adult neurogenesis and learning? Hippocampus 16:216-224
57. Lisman J, Spruston N (2005) Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat Neurosci 8:839-841
58. Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS (1996) Restraint stress reversibly enhances spatial memory performance. Physiol Behav 59:27-32 (Pubitemid 26008202)
59. Ma W, Maric D, Li BS, Hu Q, Andreadis JD, Grant GM, Liu QY, Shaffer KM, Chang YH, Zhang L, Pancrazio JJ, Pant HC, Stenger DA, Barker JL (2000) Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur J Neurosci 12:1227-1240 (Pubitemid 30224227)
60. 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 (Pubitemid 36184011)
61. Magarinos AM, McEwen BS, Flugge G, Fuchs E (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16:3534-3540 (Pubitemid 26142382)
62. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:1562-1571 (Pubitemid 41070856)
63. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104-9110 (Pubitemid 32042912)
64. 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 (Pubitemid 28529507)
65. 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 (Pubitemid 36535389)
66. Mayer JL, Klumpers L, Maslam S, de Kloet ER, Joels M, Lucassen PJ (2006) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol 18:629-631
67. McEwen BS, Magarinos AM, Reagan LP (2002) Structural plasticity and tianeptine: cellular and molecular targets. Eur Psychiatry 17 (Suppl 3):318-330 (Pubitemid 34839395)
68. McGurk SR, Levin ED, Butcher LL (1991) Impairment of radial-arm maze performance in rats following lesions involving the cholinergic medial pathway: reversal by arecoline and differential effects of muscarinic and nicotinic antagonists. Neuroscience 44:137-147
69. Mervaala E, Fohr J, Kononen M, Valkonen-Korhonen M, Vainio P, Partanen K, Partanen J, Tiihonen J, Viinamaki H, Karjalainen AK, Lehtonen J (2000) Quantitative MRI of the hippocampus and amygdala in severe depression. Psychol Med 30:117-125 (Pubitemid 30099124)
70. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250 (Pubitemid 41098905)
71. Mirescu C, Gould E (2006) Stress and adult neurogenesis. Hippocampus 16:233-238
72. Mohapel P, Leanza G, Kokaia M, Lindvall O (2005) Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging 26:939-946 (Pubitemid 40249497)
73. Nijholt I, Farchi N, Kye M, Sklan EH, Shoham S, Verbeure B, Owen D, Hochner B, Spiess J, Soreq H, Blank T (2004) Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation. Mol Psychiatry 9:174-183 (Pubitemid 38299531)
74. Oomen CA, Mayer JL, de Kloet ER, Joels M, Lucassen PJ (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 26:3395-3401 (Pubitemid 350243543)
75. Packard DS Jr, Menzies RA, Skalko RG (1973) Incorportaiton of thymidine and its analogue, bromodeoxyuridine, into embryos and maternal tissues of the mouse. Differentiation 1:397-404
76. Pathania M, Yan LD, Bordey A (2010) A symphony of signals conducts early and late stages of adult neurogenesis. Neuropharmacology 58:865-876
77. Pawlak R, Shankaranarayana Rao BS, Melchor JP, Chattarji S, McEwen B, Strickland S (2005) Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc Natl Acad Sci USA 102:18201-18206 (Pubitemid 41798525)
78. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic, San Diego
79. Pepeu G, Giovannini MG (2004) Changes in acetylcholine extracellular levels during cognitive processes. Learn Mem 11:21-27 (Pubitemid 38167054)
80. Perry KW, Nisenbaum LK, George CA, Shannon HE, Felder CC, Bymaster FP (2001) The muscarinic agonist xanomeline increases monoamine release and immediate early gene expression in the rat prefrontal cortex. Biol Psychiatry 49:716-725 (Pubitemid 32328121)
81. Peterson D (2004) The use of fluorescent probes in cell counting procedures. In: Evans S, Jansen AM, Nyengaard JR (eds) Quantitative methods in neuroscience. Oxford University Press, Oxford
82. Pham K, Nacher J, Hof PR, McEwen BS (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17:879-886 (Pubitemid 36315258)
83. Pittenger C, Duman RS (2008) Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33:88-109 (Pubitemid 350191319)
84. Ramkumar K, Srikumar BN, Shankaranarayana Rao BS, Raju TR (2008) Self-stimulation rewarding experience restores stressinduced CA3 dendritic atrophy, spatial memory deficits and alterations in the levels of neurotransmitters in the hippocampus. Neurochem Res 33:1651-1662
85. 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 (Pubitemid 39576070)
86. Sahay A, Hen R (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115 (Pubitemid 47339960)
87. Sahay A, Drew MR, Hen R (2007) Dentate gyrus neurogenesis and depression. Prog Brain Res 163:697-722
88. Sapolsky RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57:925-935
89. Shankaranarayana Rao BS, Madhavi R, Sunanda Raju TR (2001) Complete reversal of dendritic atrophy in CA3 neurons of the hippocampus by rehabilitation in restraint stressed rats. Curr Sci 80:653-659 (Pubitemid 33616280)
90. 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 (Pubitemid 26144221)
91. Slotkin TA, Seidler FJ (2006) Cholinergic receptor subtypes in the olfactory bulbectomy model of depression. Brain Res Bull 68:341-345 (Pubitemid 41827716)
92. Srikumar BN, Raju TR, Shankaranarayana Rao BS (2006) The involvement of cholinergic and noradrenergic systems in behav-ioral recovery following oxotremorine treatment to chronically stressed rats. Neuroscience 143:679-688 (Pubitemid 44781287)
93. Srikumar BN, Raju TR, Shankaranarayana Rao BS (2007) Contrasting effects of bromocriptine on learning of a partially baited radial arm maze task in the presence and absence of restraint stress. Psychopharmacol Berl 193:363-374 (Pubitemid 47063517)
94. Srikumar BN, Priya V, Bhagya V, Veena J, Raju TR, Shankaranarayana Rao BS (2008) Chronic oxotremorine treatment reverses stressinduced impairment of hippocampal long-term potentiation and spatial learning in rats. Society for Neuroscience Abstracts 38:282-314.
95. Srikumar BN, Priya V, Bhagya V, Veena J, Raju TR, Shankaranarayana Rao BS (2011) Chronic oxotremorine treatment reverses stressinduced impairment of hippocampal long-term potentiation and spatial learning in rats. Soc Neurosci
96. Steffens DC, Byrum CE, McQuoid DR, Greenberg DL, Payne ME, Blitchington TF, MacFall JR, Krishnan KR (2000) Hippocampal volume in geriatric depression. Biol Psychiatry 48:301-309 (Pubitemid 30645800)
97. Stockmeier CA, Mahajan GJ, Konick LC, Overholser JC, Jurjus GJ, Meltzer HY, Uylings HB, Friedman L, Rajkowska G (2004) Cellular changes in the postmortem hippocampus in major depression. Biol Psychiatry 56:640-650 (Pubitemid 39446845)
98. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P (2004) Stressinduced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29:2007-2017 (Pubitemid 39486552)
99. Sunanda, Rao MS, Raju TR (1995) Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons - a quantitative study. Brain Res 694:312-317
100. Sunanda, Meti BL, Raju TR (1997) Entorhinal cortex lesioning protects hippocampal CA3 neurons from stress-induced damage. Brain Res 770:302-306 (Pubitemid 27468082)
101. Sunanda, Shankaranarayana Rao BS, Raju TR (2000a) Chronic restraint stress impairs acquisition and retention of spatial memory task in rats. Curr Sci 79:1581-1584
102. Sunanda, Shankaranarayana Rao BS, Raju TR (2000b) Restraint stressinduced alterations in the levels of biogenic amines, amino acids, and AChE activity in the hippocampus. Neurochem Res 25:1547-1552 (Pubitemid 32052015)
103. Thomas RM, Peterson DA (2008) Even neural stem cells get the blues: evidence for a molecular link between modulation of adult neurogenesis and depression. Gene Expr 14:183-193 (Pubitemid 351959722)
104. Thuret S, Toni N, Aigner S, Yeo GW, Gage FH (2009) Hippocampusdependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 19:658-669
105. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10:727-734 (Pubitemid 46828514)
106. Van der Borght K, Mulder J, Keijser JN, Eggen BJ, Luiten PG, Van der Zee EA (2005) Input from the medial septum regulates adult hippocampal neurogenesis. Brain Res Bull 67:117-125 (Pubitemid 41225325)
107. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034 (Pubitemid 34193451)
108. Veena J, Srikumar BN, Mahati K, Bhagya V, Raju TR, Shankaranarayana Rao BS (2009a) Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. J Neurosci Res 87:831-843
109. Veena J, Srikumar BN, Raju TR, Shankaranarayana Rao BS (2009b) Exposure to enriched environment restores the survival and differentiation of new born cells in the hippocampus and ameliorates depressive symptoms in chronically stressed rats. Neurosci Lett 455:178-182
110. Vermetten E, Vythilingam M, Southwick SM, Charney DS, Bremner JD (2003) Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry 54:693-702 (Pubitemid 37281385)
111. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810-6818 (Pubitemid 35386438)
112. Watanabe Y, Gould E, Cameron HA, Daniels DC, McEwen BS (1992) Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2:431-435
113. Williams BP, Milligan CJ, Street M, Hornby FM, Deuchars J, Buckley NJ (2004) Transcription of the M1 muscarinic receptor gene in neurons and neuronal progenitors of the embryonic rat forebrain. J Neurochem 88:70-77 (Pubitemid 38030210)
114. 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. Psychopharmacol Berl 93:358-364 (Pubitemid 17160661)
115. Winkler J, Thal LJ, Gage FH, Fisher LJ (1998) Cholinergic strategies for Alzheimer's disease. J Mol Med 76: 555-567 (Pubitemid 28332724)
116. Wuppen K, Oesterle D, Lewicka S, Kopitz J, Plaschke K (2010) A subchronic application period of glucocorticoids leads to rat cognitive dysfunction whereas physostigmine induces a mild neuroprotection. J Neural Transm 117:1055-1065