The effects of hormones and physical exercise on hippocampal structural plasticity

Frontiers in Neuroendocrinology

Volumn 41, Issue , 2016, Pages 23-43

  Triviño Paredes, Juan ^a   Patten, Anna R ^a,b   Gil Mohapel, Joana ^a,b   Christie, Brian R ^a,b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adult neurogenesis; Hippocampus; Hormones; Physical exercise; Stress; Structural plasticity

Indexed keywords

AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ESTRADIOL; ESTRIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTRONE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCAGON LIKE PEPTIDE 1; GLUCOCORTICOID RECEPTOR; INCRETIN; LEPTIN; MINERALOCORTICOID RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NEUROHORMONE; PROGESTERONE; SEX HORMONE; SOMATOMEDIN; STRESS HORMONE; TRANSCRIPTION FACTOR SOX2; HORMONE;

ACUTE STRESS; ANIMAL CELL; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN FUNCTION; BRAIN INJURY; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; COGNITION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; DENTATE GYRUS GRANULAR LAYER; DOWN REGULATION; ESTROGEN SYNTHESIS; ESTRUS CYCLE; EXERCISE; EXERCISE INTENSITY; FEMALE; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; HIPPOCAMPUS; LEARNING; LONG TERM EXPOSURE; LONG TERM POTENTIATION; MALE; MEMORY; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEUROPROTECTION; NEWBORN; NONHUMAN; OVARIECTOMY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROESTRUS; RADIAL ARM MAZE TEST; REVIEW; SPATIAL MEMORY; STRESS; SUBVENTRICULAR ZONE; ANIMAL; ANIMAL EXPERIMENT; GROWTH, DEVELOPMENT AND AGING; MENTAL STRESS; METABOLISM; PHYSIOLOGY;

ANIMALS; FEMALE; HIPPOCAMPUS; HORMONES; MALE; NEUROGENESIS; NEURONAL PLASTICITY; PHYSICAL CONDITIONING, ANIMAL; STRESS, PSYCHOLOGICAL;

EID: 84962140753     PISSN: 00913022     EISSN: 10956808     Source Type: Journal    
DOI: 10.1016/j.yfrne.2016.03.001     Document Type: Review

References (285)

1. Aberg, M.a., Aberg, N.D., Hedbäcker, H., Oscarsson, J., Eriksson, P.S., Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. J. Neurosci. 20 (2000), 2896–2903.
2. Aguiar, A.S., Castro, A.a., Moreira, E.L., Glaser, V., Santos, A.R.S., Tasca, C.I., Latini, A., Prediger, R.D.S., Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling. Mech. Ageing Dev. 132 (2011), 560–567, 10.1016/j.mad.2011.09.005.
3. Alomari, M.a., Khabour, O.F., Alzoubi, K.H., Alzubi, M.a., Combining restricted diet with forced or voluntary exercises improves hippocampal BDNF and cognitive function in rats. Int. J. Neurosci., 2015, 1–8, 10.3109/00207454.2015.1012587.
4. Alomari, M.A., Khabour, O.F., Alzoubi, K.H., Alzubi, M.A., Forced and voluntary exercises equally improve spatial learning and memory and hippocampal BDNF levels. Behav. Brain Res. 247 (2013), 34–39, 10.1016/j.bbr.2013.03.007.
5. Altman, J., Are new neurons formed in the brains of adult mammals?. Science 135 (1962), 1127–1128, 10.1126/science.135.3509.1127.
6. Altman, J., Das, G.D., Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124 (1965), 319–335, 10.1002/cne.901240303.
7. Ambrogini, P., Lattanzi, D., Ciuffoli, S., Agostini, D., Bertini, L., Stocchi, V., Santi, S., Cuppini, R., Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res. 1017 (2004), 21–31, 10.1016/j.brainres.2004.05.039.
8. Amrein, I., Isler, K., Lipp, H.P., Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage. Eur. J. Neurosci. 34 (2011), 978–987, 10.1111/j.1460-9568.2011.07804.x.
9. Anacker, C., Cattaneo, A., Luoni, A., Musaelyan, K., Zunszain, P.A., Milanesi, E., Rybka, J., Berry, A., Cirulli, F., Thuret, S., Price, J., Riva, M.A., Gennarelli, M., Pariante, C.M., Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology 38 (2013), 872–883, 10.1038/npp.2012.253.
10. Anderson, B.J., Rapp, D.N., Baek, D.H., McCloskey, D.P., Coburn-Litvak, P.S., Robinson, J.K., Exercise influences spatial learning in the radial arm maze. Physiol. Behav. 70 (2000), 425–429, 10.1016/S0031-9384(00)00282-1.
11. Anderson, P., Morris, R., Amaral, D., Bliss, T., O'Keefe, J., The Hippocampus Book. 2007, Oxford University Press, 10.1093/acprof:oso/9780195100273.001.0001.
12. Ang, E.T., Dawe, G.S., Wong, P.T.H., Moochhala, S., Ng, Y.K., Alterations in spatial learning and memory after forced exercise. Brain Res. 1113 (2006), 186–193, 10.1016/j.brainres.2006.07.023.
13. Ang, E.T., Gomez-Pinilla, F., Potential therapeutic effects of exercise to the brain. Curr. Med. Chem. 14 (2007), 2564–2571, 10.2174/092986707782023280.
14. Arida, R.M., Scorza, C.A., Da Silva, A.V., Scorza, F.A., Cavalheiro, E.a., Differential effects of spontaneous versus forced exercise in rats on the staining of parvalbumin-positive neurons in the hippocampal formation. Neurosci. Lett. 364 (2004), 135–138, 10.1016/j.neulet.2004.03.086.
15. Arida, R.M., Scorza, C.A., Scorza, F.A., Gomes da Silva, S., da Graça Naffah-Mazzacoratti, M., Cavalheiro, E.a., Effects of different types of physical exercise on the staining of parvalbumin-positive neurons in the hippocampal formation of rats with epilepsy. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 31 (2007), 814–822, 10.1016/j.pnpbp.2007.01.021.
16. Banasr, M., Hery, M., Brezun, J.M., Daszuta, A., Serotonin mediates oestrogen stimulation of cell proliferation in the adult dentate gyrus. Eur. J. Neurosci. 14 (2001), 1417–1424, 10.1046/j.0953-816X.2001.01763.x.
17. Barha, C.K., Lieblich, S.E., Galea, L.A.M., Different forms of oestrogen rapidly upregulate cell proliferation in the dentate gyrus of adult female rats. J. Neuroendocrinol. 21 (2009), 155–166, 10.1111/j.1365-2826.2008.01809.x.
18. Barha, C.K., Pawluski, J.L., Galea, L.A.M., Maternal care affects male and female offspring working memory and stress reactivity. Physiol. Behav. 92 (2007), 939–950, 10.1016/j.physbeh.2007.06.022.
19. Barker, J.M., Galea, L.A.M., Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 152 (2008), 888–902, 10.1016/j.neuroscience.2007.10.071.
20. Barker, J.M., Galea, L.A., Sex and regional differences in estradiol content in the prefrontal cortex, amygdala and hippocampus of adult male and female rats. Gen. Comp. Endocrinol. 164 (2009), 77–84, 10.1016/j.ygcen.2009.05.008.
21. Bayod, S., Menella, I., Sanchez-Roige, S., Lalanza, J.F., Escorihuela, R.M., Camins, A., Pallàs, M., Canudas, A.M., Wnt pathway regulation by long-term moderate exercise in rat hippocampus. Brain Res. 1543 (2014), 38–48, 10.1016/j.brainres.2013.10.048.
22. Beauquis, J., Roig, P., de Nicola, A.F., Saravia, F., Short-term environmental enrichment enhances adult neurogenesis, vascular network and dendritic complexity in the hippocampus of type 1 diabetic mice. PLoS ONE, 5, 2010, 10.1371/journal.pone.0013993.
23. Bednarczyk, M.R., Aumont, A., Décary, S., Bergeron, R., Fernandes, K.J.L., Prolonged voluntary wheel-running stimulates neural precursors in the hippocampus and forebrain of adult CD1 mice. Hippocampus 19 (2009), 913–927, 10.1002/hipo.20621.
24. Bednarczyk, M.R., Hacker, L.C., Fortin-Nunez, S., Aumont, A., Bergeron, R., Fernandes, K.J.L., Distinct stages of adult hippocampal neurogenesis are regulated by running and the running environment. Hippocampus 21 (2011), 1334–1347, 10.1002/hipo.20831.
25. Ben Abdallah, N.M.-B., Slomianka, L., Vyssotski, A.L., Lipp, H.-P., Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol. Aging 31 (2010), 151–161, 10.1016/j.neurobiolaging.2008.03.002.
26. Berchtold, N.C., Castello, N., Cotman, C.W., Exercise and time-dependent benefits to learning and memory. Neuroscience 167 (2010), 588–597, 10.1016/j.neuroscience.2010.02.050.
27. Blumenfeld, H., Neuroanatomy through Clinical Cases. second ed., 2010, Sinauer Associates Inc.
28. Brandt, M.D., Maass, A., Kempermann, G., Storch, A., Physical exercise increases Notch activity, proliferation and cell cycle exit of type-3 progenitor cells in adult hippocampal neurogenesis. Eur. J. Neurosci. 32 (2010), 1256–1264, 10.1111/j.1460-9568.2010.07410.x.
29. Brandt, N., Vierk, R., Rune, G.M., Sexual dimorphism in estrogen-induced synaptogenesis in the adult hippocampus. Int. J. Dev. Biol. 57 (2013), 351–356, 10.1387/ijdb.120217gr.
30. Brannvall, K., Korhonen, L., Lindholm, D., Estrogen-receptor-dependent regulation of neural stem cell proliferation and differentiation. Mol. Cell. Neurosci. 21 (2002), 512–520.
31. Bruel-Jungerman, E., Rampon, C., Laroche, S., Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Rev. Neurosci. 18 (2007), 93–114, 10.1515/REVNEURO.2007.18.2.93.
32. Brummelte, S., Galea, L.A.M., Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 168 (2010), 680–690.
33. Burgess, N., Maguire, E.A., O'Keefe, J., The human hippocampus and spatial and episodic memory. Neuron 35 (2002), 625–641, 10.1016/S0896-6273(02)00830-9.
34. Burghardt, P.R., Fulk, L.J., Hand, G.A., Wilson, M.A., The effects of chronic treadmill and wheel running on behavior in rats. Brain Res. 1019 (2004), 84–96, 10.1016/j.brainres.2004.05.086.
35. Butcher, R.L., Collins, W.E., Fugo, N.W., Virginia, W., Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17/3 throughout the 4-day estrous cycle of the rat. Endocrinology 94 (1973), 1–2, 10.1210/endo-94-6-1704.
36. Cameron, H.A., Gould, E., Adult neurogenesis is regulated by adrenal-steroids in the dentate gyrus. Neuroscience 61 (1994), 203–209.
37. Cameron, H.A., Mckay, R.D.G., Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435 (2001), 406–417, 10.1002/cne.1040.
38. Cameron, H.A., Woolley, C.S., McEwen, B.S., Gould, E., Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56 (1993), 337–344, 10.1016/0306-4522(93)90335-D.
39. Cervero, A., Domínguez, F., Horcajadas, J.A., Quiñonero, A., Pellicer, A., Simón, C., The role of the leptin in reproduction. Curr. Opin. Obstet. Gynecol. 18 (2006), 297–303, 10.1097/01.gco.0000193004.35287.89.
40. Chen, Y., Dubé, C.M., Rice, C.J., Baram, T.Z., Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J. Neurosci. 28 (2008), 2903–2911, 10.1523/JNEUROSCI.0225-08.2008.
41. Choi, J.-H., Kim, T.-S., Park, J.-K., Sim, Y.-J., Kim, K., Lee, S.-J., Short-term treadmill exercise preserves sensory-motor function through inhibiting apoptosis in the hippocampus of hypoxic ischemia injury rat pups. J. Exerc. Rehab. 9 (2013), 457–462, 10.12965/jer.130055.
42. Clelland, C.D., Choi, M., Romberg, C., Clemenson, G.D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L.M., Barker, R.A., Gage, F.H., Bussey, T.J., A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325 (2009), 210–213, 10.1126/science.1173215.
43. Conrad, C.D., LeDoux, J.E., Magariños, A.M., McEwen, B.S., Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 113 (1999), 902–913, 10.1037/0735-7044.113.5.902.
44. Coplan, J.D., Syed, S., Perera, T.D., Fulton, S.L., Banerji, M.A., Dwork, A.J., Kral, J.G., Glucagon-like peptide-1 as predictor of body mass index and dentate gyrus neurogenesis: neuroplasticity and the metabolic milieu. Neural Plast., 2014, 2014, 917981.
45. Corkin, S., What's new with the amnesic patient H.M.?. Nat. Rev. Neurosci. 3 (2002), 153–160, 10.1038/nrn726.
46. Creer, D.J., Romberg, C., Saksida, L.M., van Praag, H., Bussey, T.J., Running enhances spatial pattern separation in mice. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 2367–2372, 10.1073/pnas.0911725107.
47. Czeh, B., Welt, T., Fischer, A.K., Erhardt, A., Schmitt, W., Muller, M.B., Toschi, N., Fuchs, E., Keck, M.E., Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol. Psychiatry 52 (2002), 1057–1065 pii: S0006322302014579.
48. Dalla, C., Whetstone, A.S., Hodes, G.E., Shors, T.J., Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci. Lett. 449 (2009), 52–56, 10.1016/j.neulet.2008.10.051.
49. Dayer, A.G., Ford, A.A., Cleaver, K.M., Yassaee, M., Cameron, H.A., Short-term and long-term survival of new neurons in the rat dentate gyrus. J. Comp. Neurol. 460 (2003), 563–572, 10.1002/cne.10675.
50. de Almeida, A.A., Gomes da Silva, S., Fernandes, J., Peixinho-Pena, L.F., Scorza, F.A., Cavalheiro, E.A., Arida, R.M., Differential effects of exercise intensities in hippocampal BDNF, inflammatory cytokines and cell proliferation in rats during the postnatal brain development. Neurosci. Lett. 553 (2013), 1–6, 10.1016/j.neulet.2013.08.015.
51. Dishman, R.K., Brain monoamines, exercise, and behavioral stress: animal models. Med. Sci. Sports Exerc. 29 (1997), 63–74, 10.1097/00005768-199701000-00010.
52. Dishman, R.K., Dunn, A.L., Youngstedt, S.D., Davis, J.M., Burgess, M.L., Wilson, S.P., Wilson, M.A., Increased open field locomotion and decreased striatal GABA(A) binding after activity wheel running. Physiol. Behav. 60 (1996), 699–705, 10.1016/S0031-9384(96)00102-3.
53. Duan, X., Kang, E., Liu, C.Y., Ming, G.-L., Song, H., Development of neural stem cell in the adult brain. Curr. Opin. Neurobiol. 18 (2008), 108–115, 10.1016/j.conb.2008.04.001.
54. Duarte-Guterman, P., Yagi, S., Chow, C., Galea, L.a.M., Hippocampal learning, memory, and neurogenesis: effects of sex and estrogens across the lifespan in adults. Horm. Behav., 2015, 10.1016/j.yhbeh.2015.05.024.
55. Eckel, R.H., Grundy, S.M., Zimmet, P.Z., The metabolic syndrome. Lancet, 2005, 1415–1428, 10.1016/S0140-6736(05)66378-7.
56. Ekdahl, C.T., Claasen, J.-H., Bonde, S., Kokaia, Z., Lindvall, O., Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. U.S.A. 100 (2003), 13632–13637, 10.1073/pnas.2234031100.
57. Eriksson, P.S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.M., Nordborg, C., Peterson, D.A., Gage, F.H., Neurogenesis in the adult human hippocampus. Nat. Med. 4 (1998), 1313–1317, 10.1038/3305.
58. Espósito, M.S., Piatti, V.C., Laplagne, D.A., Morgenstern, N.A., Ferrari, C.C., Pitossi, F.J., Schinder, A.F., Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J. Neurosci. 25 (2005), 10074–10086, 10.1523/JNEUROSCI.3114-05.2005.
59. Falconer, E.M., Galea, L.A.M., Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res. 975 (2003), 22–36, 10.1016/S0006-8993(03)02542-3.
60. Farinetti, A., Tomasi, S., Foglio, B., Ferraris, A., Ponti, G., Gotti, S., Peretto, P., Panzica, G.C., Testosterone and estradiol differentially affect cell proliferation in the subventricular zone of young adult gonadectomized male and female rats. Neuroscience 286 (2015), 162–170.
61. Farmer, J., Zhao, X., Van Praag, H., Wodtke, K., Gage, F.H., Christie, B.R., Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male sprague-dawley rats in vivo. Neuroscience 124 (2004), 71–79, 10.1016/j.neuroscience.2003.09.029.
62. Farrell, M.R., Gruene, T.M., Shansky, R.M., The influence of stress and gonadal hormones on neuronal structure and function. Horm. Behav., 2015.
63. Farrell, P.A., Garthwaite, T.L., Gustafson, A.B., Plasma adrenocorticotropin and cortisol responses to submaximal and exhaustive exercise. J. Appl. Physiol. 55 (1983), 1441–1444.
64. Fediuc, S., Campbell, J.E., Riddell, M.C., Effect of voluntary wheel running on circadian corticosterone release and on HPA axis responsiveness to restraint stress in Sprague–Dawley rats. J. Appl. Physiol. 100 (2006), 1867–1875, 10.1152/japplphysiol.01416.2005.
65. Ferragud, A., Haro, A., Sylvain, A., Velázquez-Sánchez, C., Hernández-Rabaza, V., Canales, J.J., Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress. Behav. Brain Res. 210 (2010), 134–139, 10.1016/j.bbr.2010.02.013.
66. Ferreira, A.F.B., Real, C.C., Rodrigues, A.C., Alves, A.S., Britto, L.R.G., Short-term, moderate exercise is capable of inducing structural, bdnf-independent hippocampal plasticity. Brain Res. 1425 (2011), 111–122, 10.1016/j.brainres.2011.10.004.
67. Ferri, C.P., Prince, M., Brayne, C., Brodaty, H., Fratiglioni, L., Ganguli, M., Hall, K., Hasegawa, K., Hendrie, H., Huang, Y., Jorm, A., Mathers, C., Menezes, P.R., Rimmer, E., Scazufca, M., Global prevalence of dementia: a Delphi consensus study. Lancet, 2005, 10.1016/S0140-6736(05)67889-0.
68. Fester, L., Prange-Kiel, J., Zhou, L., Blittersdorf, B.V., Böhm, J., Jarry, H., Schumacher, M., Rune, G.M., Estrogen-regulated synaptogenesis in the hippocampus: sexual dimorphism in vivo but not in vitro. J. Steroid Biochem. Mol. Biol., 2012, 10.1016/j.jsbmb.2011.11.010.
69. Fester, L., Ribeiro-Gouveia, V., Prange-Kiel, J., Von Schassen, C., B??ttner, M., Jarry, H., Rune, G.M., Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J. Neurochem. 97 (2006), 1136–1144, 10.1111/j.1471-4159.2006.03809.x.
70. Fuss, J., Ben Abdallah, N.M.B., Vogt, M.a., Touma, C., Pacifici, P.G., Palme, R., Witzemann, V., Hellweg, R., Gass, P., Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 20 (2010), 364–376, 10.1002/hipo.20634.
71. Galea, L.A.M., Leuner, B., Slattery, D.A., Hippocampal plasticity during the peripartum period: influence of sex steroids, stress and ageing. J. Neuroendocrinol. 26 (2014), 641–648.
72. Garza, J.C., Guo, M., Zhang, W., Lu, X.-Y., Leptin restores adult hippocampal neurogenesis in a chronic unpredictable stress model of depression and reverses glucocorticoid-induced inhibition of GSK-3β/β-catenin signaling. Mol. Psychiatry 17 (2012), 790–808.
73. Garza, J.C., Guo, M., Zhang, W., Lu, X.-Y., Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J. Biol. Chem. 283 (2008), 18238–18247.
74. Gil-Mohapel, J., Brocardo, P.S., Choquette, W., Gothard, R., Simpson, J.M., Christie, B.R., Hippocampal neurogenesis levels predict WATERMAZE search strategies in the aging brain. PLoS ONE, 8, 2013, e75125, 10.1371/journal.pone.0075125.
75. Goldman, S.A., Nottebohm, F., Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. U.S.A. 80 (1983), 2390–2394, 10.1073/pnas.80.8.2390.
76. Gómez-Pinilla, F., Brain foods: the effects of nutrients on brain function. Nat. Rev. Neurosci. 9 (2008), 568–578, 10.1038/nrn2421.
77. González-Burgos, I., Alejandre-Gómez, M., Cervantes, M., Spine-type densities of hippocampal CA1 neurons vary in proestrus and estrus rats. Neurosci. Lett. 379 (2005), 52–54, 10.1016/j.neulet.2004.12.043.
78. Gorton, L.M., Vuckovic, M.G., Vertelkina, N., Petzinger, G.M., Jakowec, M.W., Wood, R.I., Exercise effects on motor and affective behavior and catecholamine neurochemistry in the MPTP-lesioned mouse. Behav. Brain Res. 213 (2010), 253–262, 10.1016/j.bbr.2010.05.009.
79. Gould, E., Beylin, A., Tanapat, P., Reeves, A., Shors, T.J., Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2 (1999), 260–265, 10.1038/6365.
80. Gould, E., Daniels, D.C., Cameron, H.a., McEwen, B.S., Expression of adrenal steroid receptors by newly born cells and pyknotic cells in the dentate gyrus of the postnatal rat. Mol. Cell. Neurosci. 3 (1992), 44–48, 10.1016/1044-7431(92)90007-O.
81. Gould, E., Reeves, A.J., Fallah, M., Tanapat, P., Gross, C.G., Fuchs, E., Hippocampal neurogenesis in adult Old World primates. Proc. Natl. Acad. Sci. 96 (1999), 5263–5267, 10.1073/pnas.96.9.5263.
82. Gould, E., Tanapat, P., McEwen, B.S., Flügge, G., Fuchs, E., Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. U.S.A. 95 (1998), 3168–3171, 10.1073/pnas.95.6.3168.
83. Gould, E., Vail, N., Wagers, M., Gross, C.G., Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc. Natl. Acad. Sci. U.S.A. 98 (2001), 10910–10917, 10.1073/pnas.181354698.
84. Gould, E., Woolley, C.S., Frankfurt, M., McEwen, B.S., Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10 (1990), 1286–1291.
85. Greenwood, B.N., Spence, K.G., Crevling, D.M., Clark, P.J., Craig, W.C., Fleshner, M., Exercise-induced stress resistance is independent of exercise controllability and the medial prefrontal cortex. Eur. J. Neurosci. 37 (2013), 469–478, 10.1111/ejn.12044.
86. Haan, M.N., Wallace, R., Can dementia be prevented? Brain aging in a population-based context. Annu. Rev. Publ. Health 25 (2004), 1–24, 10.1146/annurev.publhealth.25.101802.122951.
87. Hajszan, T., MacLusky, N.J., Leranth, C., Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur. J. Neurosci. 21 (2005), 1299–1303, 10.1111/j.1460-9568.2005.03968.x.
88. Hamson, D.K., Wainwright, S.R., Taylor, J.R., Jones, B.A., Watson, N.V., Galea, L.A.M., Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats. Endocrinology 154 (2013), 3294–3304, 10.1210/en.2013-1129.
89. Hare, B.D., Beierle, J.A., Toufexis, D.J., Hammack, S.E., Falls, W.A., Exercise-associated changes in the corticosterone response to acute restraint stress: evidence for increased adrenal sensitivity and reduced corticosterone response duration. Neuropsychopharmacology 39 (2014), 1262–1269, 10.1038/npp.2013.329.
90. Harvey, J., Shanley, L.J., O'Malley, D., Irving, A.J., Leptin: a potential cognitive enhancer?. Biochem. Soc. Trans. 33 (2005), 1029–1032, 10.1042/BST20051029.
91. Haskell, W.L., Lee, I.-M., Pate, R.R., Powell, K.E., Blair, S.N., Franklin, B.A., Macera, C.A., Heath, G.W., Thompson, P.D., Bauman, A., Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med. Sci. Sports Exerc. 39 (2007), 1423–1434, 10.1249/mss.0b013e3180616b27.
92. Hayes, K., Sprague, S., Guo, M., Davis, W., Friedman, A., Kumar, A., Jimenez, D.F., Ding, Y., Forced, not voluntary, exercise effectively induces neuroprotection in stroke. Acta Neuropathol. 115 (2008), 289–296, 10.1007/s00401-008-0340-z.
93. Heine, V.M., Maslam, S., Zareno, J., Joëls, M., Lucassen, P.J., Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur. J. Neurosci. 19 (2004), 131–144, 10.1046/j.1460-9568.2003.03100.x.
94. Hillman, C.H., Erickson, K.I., Kramer, A.F., Be smart, exercise your heart: exercise effects on brain and cognition. Nat. Rev. Neurosci., 2008, 10.1038/nrn2298.
95. Hojo, Y., Hattori, T.-A., Enami, T., Furukawa, A., Suzuki, K., Ishii, H.-T., Mukai, H., Morrison, J.H., Janssen, W.G.M., Kominami, S., Harada, N., Kimoto, T., Kawato, S., Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 865–870, 10.1073/pnas.2630225100.
96. Hojo, Y., Murakami, G., Mukai, H., Higo, S., Hatanaka, Y., Ogiue-Ikeda, M., Ishii, H., Kimoto, T., Kawato, S., Estrogen synthesis in the brain – role in synaptic plasticity and memory. Mol. Cell. Endocrinol. 290 (2008), 31–43, 10.1016/j.mce.2008.04.017.
97. Holmes, M.M., Galea, L.A., Defensive behavior and hippocampal cell proliferation: differential modulation by naltrexone during stress. Behav. Neurosci. 116 (2002), 160–168, 10.1037/0735-7044.116.1.160.
98. Holmes, M.M., Galea, L.aM., Mistlberger, R.E., Kempermann, G., Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J. Neurosci. Res. 76 (2004), 216–222, 10.1002/jnr.20039.
99. Hu, S., Ying, Z., Gomez-Pinilla, F., Frautschy, S.A., Exercise can increase small heat shock proteins (sHSP) and pre- and post-synaptic proteins in the hippocampus. Brain Res. 1249 (2009), 191–201, 10.1016/j.brainres.2008.10.054.
100. Huang, A.M., Jen, C.J., Chen, H.F., Yu, L., Kuo, Y.M., Chen, H.I., Compulsive exercise acutely upregulates rat hippocampal brain-derived neurotrophic factor. J. Neural Transm. 113 (2006), 803–811, 10.1007/s00702-005-0359-4.
101. Hunter, K., Holscher, C., Drugs developed to treat diabetes, liraglutide and lixisenatide, cross the blood brain barrier and enhance neurogenesis. BMC Neurosci., 2012, 10.1186/1471-2202-13-33.
102. Hwang, I.K., Yi, S.S., Yoo, K.Y., Park, O.K., Yan, B., Song, W., Won, M.H., Yoon, Y.S., Seong, J.K., Differential effects of treadmill exercise in early and chronic diabetic stages on parvalbumin immunoreactivity in the hippocampus of a rat model of type 2 diabetes. Neurochem. Res. 36 (2011), 1526–1532, 10.1007/s11064-011-0480-8.
103. Inoue, K., Hanaoka, Y., Nishijima, T., Okamoto, M., Chang, H., Saito, T., Soya, H., Long-term mild exercise training enhances hippocampus-dependent memory in rats. Int. J. Sports Med. 36 (2015), 280–285, 10.1055/s-0034-1390465.
104. Inoue, K., Okamoto, M., Shibato, J., Lee, M.C., Matsui, T., Rakwal, R., Soya, H., Long-term mild, rather than intense, exercise enhances adult hippocampal neurogenesis and greatly changes the transcriptomic profile of the hippocampus. PLoS ONE, 10, 2015, e0128720, 10.1371/journal.pone.0128720.
105. Isgor, C., Watson, S.J., Estrogen receptor alpha and beta mRNA expressions by proliferating and differentiating cells in the adult rat dentate gyrus and subventricular zone. Neuroscience 134 (2005), 847–856, 10.1016/j.neuroscience.2005.05.008.
106. Jessberger, S., Clark, R.E., Broadbent, N.J., Clemenson, G.D., Consiglio, A., Lie, D.C., Squire, L.R., Gage, F.H., Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Memory 16 (2009), 147–154, 10.1101/lm.1172609.
107. Kambo, J.S., Galea, L.A.M., Activational levels of androgens influence risk assessment behaviour but do not influence stress-induced suppression in hippocampal cell proliferation in adult male rats. Behav. Brain Res. 175 (2006), 263–270, 10.1016/j.bbr.2006.08.032.
108. Kaplan, M.S., Hinds, J.W., Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197 (1977), 1092–1094.
109. Karsenty, G., Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab., 2006, 10.1016/j.cmet.2006.10.008.
110. Kato, A., Hojo, Y., Higo, S., Komatsuzaki, Y., Murakami, G., Yoshino, H., Uebayashi, M., Kawato, S., Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines. Front. Neural Circuits, 7, 2013, 149, 10.3389/fncir.2013.00149.
111. Ke, Z., Yip, S.P., Li, L., Zheng, X.X., Tong, K.Y., The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia model. PLoS ONE, 6, 2011, 10.1371/journal.pone.0016643.
112. Kee, N., Teixeira, C.M., Wang, A.H., Frankland, P.W., Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10 (2007), 355–362, 10.1038/nn1847.
113. Kelsch, W., Sim, S., Lois, C., Watching synaptogenesis in the adult brain. Annu. Rev. Neurosci. 33 (2010), 131–149, 10.1146/annurev-neuro-060909-153252.
114. Kempermann, G., Jessberger, S., Steiner, B., Kronenberg, G., Milestones of neuronal development in the adult hippocampus. Trends Neurosci., 2004, 10.1016/j.tins.2004.05.013.
115. Kempermann, G., Kuhn, H.G., Gage, F.H., Experience-induced neurogenesis in the senescent dentate gyrus. J. Neurosci. 18 (1998), 3206–3212, 10.1016/S0149-7634(97)00008-0.
116. Kempermann, G., Kuhn, H.G., Gage, F.H., More hippocampal neurons in adult mice living in an enriched environment. Nature 386 (1997), 493–495, 10.1038/386493a0.
117. Kempermann, G., Wiskott, L., Gage, F.H., Functional significance of adult neurogenesis. Curr. Opin. Neurobiol., 2004, 10.1016/j.conb.2004.03.001.
118. Kesner, R.P., Behavioral functions of the CA3 subregion of the hippocampus. Learn. Memory 14 (2007), 771–781, 10.1101/lm.688207.
119. Kesner, R.P., Lee, I., Gilbert, P., A behavioral assessment of hippocampal function based on a subregional analysis. Rev. Neurosci. 15 (2004), 333–351, 10.1515/REVNEURO.2004.15.5.333.
120. Khabour, O.F., Alzoubi, K.H., Alomari, M.A., Alzubi, M.A., Changes in spatial memory and BDNF expression to concurrent dietary restriction and voluntary exercise. Hippocampus 20 (2010), 637–645, 10.1002/hipo.20657.
121. Kim, J.J., Diamond, D.M., The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3 (2002), 453–462, 10.1038/nrn849.
122. Kim, Y.P., Kim, H., Shin, M.S., Chang, H.K., Jang, M.H., Shin, M.C., Lee, S.J., Lee, H.H., Yoon, J.H., Jeong, I.G., Kim, C.J., Age-dependence of the effect of treadmill exercise on cell proliferation in the dentate gyrus of rats. Neurosci. Lett. 355 (2004), 152–154, 10.1016/j.neulet.2003.11.005.
123. Kinni, H., Guo, M., Ding, J.Y., Konakondla, S., Dornbos, D., Tran, R., Guthikonda, M., Ding, Y., Cerebral metabolism after forced or voluntary physical exercise. Brain Res. 1388 (2011), 48–55, 10.1016/j.brainres.2011.02.076.
124. Kitamura, T., Sun, C., Kitch, L.J., Mark, J., Kitamura, T., Sun, C., Martin, J., Kitch, L.J., Schnitzer, M.J., Tonegawa, S., Entorhinal cortical ocean cells encode specific contexts and drive context-specific fear memory article entorhinal cortical ocean cells encode specific contexts and drive context-specific fear memory. Neuron 87 (2015), 1317–1331, 10.1016/j.neuron.2015.08.036.
125. Klaus, F., Hauser, T., Lindholm, A.K., Cameron, H.A., Slomianka, L., Lipp, H.P., Amrein, I., Different regulation of adult hippocampal neurogenesis in Western house mice (Mus musculus domesticus) and C57BL/6 mice. Behav. Brain Res. 227 (2012), 340–347, 10.1016/j.bbr.2011.07.026.
126. Knoth, R., Singec, I., Ditter, M., Pantazis, G., Capetian, P., Meyer, R.P., Horvat, V., Volk, B., Kempermann, G., Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS ONE, 5, 2010, 10.1371/journal.pone.0008809.
127. Kobilo, T., Liu, Q.-R., Gandhi, K., Mughal, M., Shaham, Y., van Praag, H., Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn. Memory 18 (2011), 605–609, 10.1101/lm.2283011.
128. Kole, M.H.P., Costoli, T., Koolhaas, J.M., Fuchs, E., Bidirectional shift in the cornu ammonis 3 pyramidal dendritic organization following brief stress. Neuroscience 125 (2004), 337–347, 10.1016/j.neuroscience.2004.02.014.
129. Komatsuzaki, Y., Murakami, G., Tsurugizawa, T., Mukai, H., Tanabe, N., Mitsuhashi, K., Kawata, M., Kimoto, T., Ooishi, Y., Kawato, S., Rapid spinogenesis of pyramidal neurons induced by activation of glucocorticoid receptors in adult male rat hippocampus. Biochem. Biophys. Res. Commun. 335 (2005), 1002–1007, 10.1016/j.bbrc.2005.07.173.
130. Kornack, D.R., Rakic, P., Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. U.S.A. 96 (1999), 5768–5773, 10.1073/pnas.96.10.5768.
131. Kronenberg, G., Bick-Sander, A., Bunk, E., Wolf, C., Ehninger, D., Kempermann, G., Physical exercise prevents age-related decline in precursor cell activity in the mouse dentate gyrus. Neurobiol. Aging 27 (2006), 1505–1513, 10.1016/j.neurobiolaging.2005.09.016.
132. Kronenberg, G., Reuter, K., Steiner, B., Brandt, M.D., Jessberger, S., Yamaguchi, M., Kempermann, G., Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467 (2003), 455–463, 10.1002/cne.10945.
133. Kuhn, H.G., Dickinson-Anson, H., Gage, F.H., Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16 (1996), 2027–2033 0270-6474.
134. Kuipers, S.D., Trentani, A., Westenbroek, C., Bramham, C.R., Korf, J., Kema, I.P., Ter Horst, G.J., Den Boer, J.A., Unique patterns of FOS, phospho-CREB and BrdU immunoreactivity in the female rat brain following chronic stress and citalopram treatment. Neuropharmacology 50 (2006), 428–440, 10.1016/j.neuropharm.2005.10.006.
135. Lagace, D.C., Fischer, S.J., Eisch, A.J., Gender and endogenous levels of estradiol do not influence adult hippocampal neurogenesis in mice. Hippocampus 17 (2007), 175–180, 10.1002/hipo.20265.
136. Lassalle, J.M., Bataille, T., Halley, H., Reversible inactivation of the hippocampal mossy fiber synapses in mice impairs spatial learning, but neither consolidation nor memory retrieval, in the Morris navigation task. Neurobiol. Learn. Memory 73 (2000), 243–257, 10.1006/nlme.1999.3931.
137. Le Menuet, D., Lombès, M., The neuronal mineralocorticoid receptor: from cell survival to neurogenesis. Steroids 91 (2014), 11–19, 10.1016/j.steroids.2014.05.018.
138. Leasure, J.L., Jones, M., Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 156 (2008), 456–465, 10.1016/j.neuroscience.2008.07.041.
139. Lee, H., Ohno, M., Ohta, S., Mikami, T., Regular moderate or intense exercise prevents depression-like behavior without change of hippocampal tryptophan content in chronically tryptophan-deficient and stressed mice. PLoS ONE 8 (2013), 1–8, 10.1371/journal.pone.0066996.
140. Lee, J., Duan, W., Long, J.M., Ingram, D.K., Mattson, M.P., Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. J. Mol. Neurosci. 15 (2000), 99–108, 10.1385/JMN:15:2:99.
141. Lee, K.-J., Kim, S.-J., Kim, S.-W., Choi, S.-H., Shin, Y.-C., Park, S.-H., Moon, B.-H., Cho, E., Lee, M.-S., Chun, B.-G., Shin, K.-H., Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp. Mol. Med. 38 (2006), 44–54, 10.1038/emm.2006.6.
142. Leuner, B., Gould, E., Structural plasticity and hippocampal function. Annu. Rev. Psychol. 61:111–140 (2010), C1–C3, 10.1146/annurev.psych.093008.100359.
143. Leuner, B., Gould, E., Shors, T.J., Is there a link between adult neurogenesis and learning?. Hippocampus 16 (2006), 216–224, 10.1002/hipo.20153.
144. Li, X.L., Aou, S., Oomura, Y., Hori, N., Fukunaga, K., Hori, T., Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents. Neuroscience 113 (2002), 607–615, 10.1016/S0306-4522(02)00162-8.
145. Lie, D.C., Song, H., Colamarino, S.A., Ming, G.L., Gage, F.H., Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharmacol. Toxicol. 44 (2004), 399–421, 10.1146/annurev.pharmtox.44.101802.121631.
146. Lin, T.W., Chen, S.J., Huang, T.Y., Chang, C.Y., Chuang, J.I., Wu, F. Sen, Kuo, Y.M., Jen, C.J., Different types of exercise induce differential effects on neuronal adaptations and memory performance. Neurobiol. Learn. Memory 97 (2012), 140–147, 10.1016/j.nlm.2011.10.006.
147. Lin, Y., Dong, J., Yan, T., He, X., Zheng, X., Liang, H., Sui, M., Involuntary, forced and voluntary exercises are equally capable of inducing hippocampal plasticity and the recovery of cognitive function after stroke. Neurol. Res. 37 (2015), 893–901, 10.1179/1743132815Y.0000000074.
148. Lindqvist, A., Mohapel, P., Bouter, B., Frielingsdorf, H., Pizzo, D., Brundin, P., Erlanson-Albertsson, C., High-fat diet impairs hippocampal neurogenesis in male rats. Eur. J. Neurol. 13 (2006), 1385–1388, 10.1111/j.1468-1331.2006.01500.x.
149. Liu, H.-Li, Zhao, G., Cai, K., Zhao, H.-Hua, Shi, L.-de, Treadmill exercise prevents decline in spatial learning and memory in APP/PS1 transgenic mice through improvement of hippocampal long-term potentiation. Behav. Brain Res. 218 (2011), 308–314, 10.1016/j.bbr.2010.12.030.
150. Liu, H.-Li, Zhao, G., Zhang, H., Shi, L.-de, Long-term treadmill exercise inhibits the progression of Alzheimer's disease-like neuropathology in the hippocampus of APP/PS1 transgenic mice. Behav. Brain Res. 256 (2013), 261–272, 10.1016/j.bbr.2013.08.008.
151. Liu, Y.-F., Chen, H., Wu, C.-L., Kuo, Y.-M., Yu, L., Huang, A.-M., Wu, F.-S., Chuang, J.-I., Jen, C.J., Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J. Physiol. 587 (2009), 3221–3231, 10.1113/jphysiol.2009.173088.
152. Lou, S.-jie, Liu, J.-yan, Chang, H., Chen, P.-jie, Hippocampal neurogenesis and gene expression depend on exercise intensity in juvenile rats. Brain Res. 1210 (2008), 48–55, 10.1016/j.brainres.2008.02.080.
153. Maffei, M., Halaas, J., Ravussin, E., Pratley, R.E., Lee, G.H., Zhang, Y., Fei, H., Kim, S., Lallone, R., Ranganathan, S., Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med. 1 (1995), 1155–1161, 10.1038/nm1195-1155.
154. Magariños, A.M., McEwen, B.S., Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69 (1995), 89–98.
155. Malberg, J.E., Eisch, A.J., Nestler, E.J., Duman, R.S., Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20 (2000), 9104–9110.
156. Malendowicz, L.K., Rucinski, M., Belloni, A.S., Ziolkowska, A., Nussdorfer, G.G., Leptin and the regulation of the hypothalamic-pituitary-adrenal axis. Int. Rev. Cytol., 2007, 10.1016/S0074-7696(07)63002-2.
157. Manev, H., Uz, T., Smalheiser, N.R., Manev, R., Antidepressants alter cell proliferation in the adult brain in vivo and in neural cultures in vitro. Eur. J. Pharmacol. 411 (2001), 67–70, 10.1016/S0014-2999(00)00904-3.
158. Marosi, K., Bori, Z., Hart, N., Sárga, L., Koltai, E., Radák, Z., Nyakas, C., Long-term exercise treatment reduces oxidative stress in the hippocampus of aging rats. Neuroscience 226 (2012), 21–28, 10.1016/j.neuroscience.2012.09.001.
159. Mazzucco, C.A., Lieblich, S.E., Bingham, B.I., Williamson, M.A., Viau, V., Galea, L.A.M., Both estrogen receptor alpha and estrogen receptor beta agonists enhance cell proliferation in the dentate gyrus of adult female rats. Neuroscience 141 (2006), 1793–1800, 10.1016/j.neuroscience.2006.05.032 pii: S0306-4522(06)00719-6.
160. McClean, P.L., Parthsarathy, V., Faivre, E., Hölscher, C., The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer's disease. J. Neurosci. 31 (2011), 6587–6594, 10.1523/JNEUROSCI.0529-11.2011.
161. McClure, R.E.S., Barha, C.K., Galea, L.A.M., 17β-Estradiol, but not estrone, increases the survival and activation of new neurons in the hippocampus in response to spatial memory in adult female rats. Horm. Behav. 63 (2013), 144–157, 10.1016/j.yhbeh.2012.09.011.
162. McEwen, B.S., Steroid hormone actions on the brain: when is the genome involved?. Horm. Behav. 28 (1994), 396–405, 10.1006/hbeh.1994.1036.
163. McEwen, B.S., Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain. Exp. Gerontol. 29 (1994), 479–493, 10.1016/0531-5565(94)90022-1.
164. McEwen, B.S., De Kloet, E.R., Rostene, W., Adrenal steroid receptors and actions in the nervous system. Physiol. Rev. 66 (1986), 1121–1188.
165. McEwen, B.S., Krey, L.C., Luine, V.N., Steroid hormone action in the neuroendocrine system: when is the genome involved?. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 56 (1978), 255–268.
166. McEwen, B.S., Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur. J. Pharmacol. 583 (2008), 174–185, 10.1016/j.ejphar.2007.11.071.
167. McKittrick, C.R., Magariños, A.M., Blanchard, D.C., Blanchard, R.J., McEwen, B.S., Sakai, R.R., Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 36 (2000), 85–94, 10.1002/(SICI)1098-2396(200005)36:2<85::AID-SYN1>3.0.CO;2-Y.
168. Melmed, S., Polonsky, K., Larsen, R., Kronenberg, H., Williams Textbook of Endocrinology. 12th ed., 2011, Saunderd Elsevier.
169. Merritt, J.R., Rhodes, J.S., Mouse genetic differences in voluntary wheel running, adult hippocampal neurogenesis and learning on the multi-strain-adapted plus water maze. Behav. Brain Res. 280 (2015), 62–71, 10.1016/j.bbr.2014.11.030.
170. Mojtahedi, S., Kordi, M.R., Hosseini, S.E., Omran, S.F., Soleimani, M., Effect of treadmill running on the expression of genes that are involved in neuronal differentiation in the hippocampus of adult male rats. Cell Biol. Int. 37 (2013), 276–283, 10.1002/cbin.10022.
171. Molteni, R., Ying, Z., Gómez-Pinilla, F., Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. Eur. J. Neurosci. 16 (2002), 1107–1116, 10.1046/j.1460-9568.2002.02158.x.
172. Montaron, M.F., Piazza, P.V., Aurousseau, C., Urani, A., Le Moal, M., Abrous, D.N., Implication of corticosteroid receptors in the regulation of hippocampal structural plasticity. Eur. J. Neurosci. 18 (2003), 3105–3111, 10.1111/j.1460-9568.2003.03048.x.
173. Moraska, a., Deak, T., Spencer, R.L., Roth, D., Fleshner, M., Treadmill running produces both positive and negative physiological adaptations in Sprague–Dawley rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000), R1321–R1329.
174. Morris, R.G., Garrud, P., Rawlins, J.N., O'Keefe, J., Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982), 681–683, 10.1038/297681a0.
175. Morris, R.G.M., Spatial localization does not require the presence of local cues. Learn. Motiv., 1981, 10.1016/0023-9690(81)90020-5.
176. Mukai, H., Tsurugizawa, T., Murakami, G., Kominami, S., Ishii, H., Ogiue-Ikeda, M., Takata, N., Tanabe, N., Furukawa, A., Hojo, Y., Ooishi, Y., Morrison, J.H., Janssen, W.G.M., Rose, J.A., Chambon, P., Kato, S., Izumi, S., Yamazaki, T., Kimoto, T., Kawato, S., Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons. J. Neurochem. 100 (2007), 950–967, 10.1111/j.1471-4159.2006.04264.x.
177. Mukai, H., Tsurugizawa, T., Ogiue-Ikeda, M., Murakami, G., Hojo, Y., Ishii, H., Kimoto, T., Kawato, S., Local neurosteroid production in the hippocampus: influence on synaptic plasticity of memory. Neuroendocrinology, 2007, 255–263, 10.1159/000097747.
178. Mukuda, T., Koyama, Y., Hamasaki, S., Kaidoh, T., Furukawa, Y., Systemic angiotensin II and exercise-induced neurogenesis in adult rat hippocampus. Brain Res. 1588 (2014), 92–103, 10.1016/j.brainres.2014.09.019.
179. Mukuda, T., Sugiyama, H., An angiotensin II receptor antagonist suppresses running-enhanced hippocampal neurogenesis in rat. Neurosci. Res. 58 (2007), 140–144, 10.1016/j.neures.2007.02.005.
180. Murphy, T., Dias, G.P., Thuret, S., Effects of diet on brain plasticity in animal and human studies: mind the gap. Neural Plast., 2014, 10.1155/2014/563160.
181. Murray, F., Smith, D.W., Hutson, P.H., Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. Eur. J. Pharmacol. 583 (2008), 115–127, 10.1016/j.ejphar.2008.01.014.
182. Mustroph, M.L., Chen, S., Desai, S.C., Cay, E.B., DeYoung, E.K., Rhodes, J.S., Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience 219 (2012), 62–71, 10.1016/j.neuroscience.2012.06.007.
183. Nagy, A.I., Ormerod, B.K., Mazzucco, C., Galea, L.A.M., Estradiol-induced enhancement in cell proliferation is mediated through estrogen receptors in the dentate gyrus of adult female rats. Drug Dev. Res. 66 (2005), 142–149, 10.1002/ddr.20053.
184. Nakashiba, T., Cushman, J.D., Pelkey, K.A., Renaudineau, S., Buhl, D.L., McHugh, T.J., Barrera, V.R., Chittajallu, R., Iwamoto, K.S., McBain, C.J., Fanselow, M.S., Tonegawa, S., Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149 (2012), 188–201, 10.1016/j.cell.2012.01.046.
185. Nestler, E.J., Kelz, M.B., Chen, J., ΔFosB: a molecular mediator of long-term neural and behavioral plasticity. Brain Res., 1999, 10–17, 10.1016/S0006-8993(98)01191-3.
186. Ngwenya, L.B., Heyworth, N.C., Shwe, Y., Moore, T.L., Rosene, D.L., Age-related changes in dentate gyrus cell numbers, neurogenesis, and associations with cognitive impairments in the rhesus monkey. Front. Syst. Neurosci., 9, 2015, 102, 10.3389/fnsys.2015.00102.
187. Nishijima, T., Kawakami, M., Kita, I., Long-term exercise is a potent trigger for ΔFosB induction in the hippocampus along the dorso-ventral axis. PLoS ONE, 8, 2013, 10.1371/journal.pone.0081245.
188. O'Keefe, J., Dostrovsky, J., The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34 (1971), 171–175, 10.1016/0006-8993(71)90358-1.
189. O'Malley, D., MacDonald, N., Mizielinska, S., Connolly, C.N., Irving, A.J., Harvey, J., Leptin promotes rapid dynamic changes in hippocampal dendritic morphology. Mol. Cell. Neurosci. 35 (2007), 559–572, 10.1016/j.mcn.2007.05.001.
190. Ohia-Nwoko, O., Montazari, S., Lau, Y., Eriksen, J.L., Long-term treadmill exercise attenuates tau pathology in P301S tau transgenic mice, 2014, 1–17.
191. Okamoto, M., Hojo, Y., Inoue, K., Matsui, T., Kawato, S., McEwen, B.S., Soya, H., Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis. Proc. Natl. Acad. Sci., 2012, 10.1073/pnas.1210023109.
192. Olariu, A., Cleaver, J., Cameron, H., Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J. Comp. Neurol. 504 (2007), 287–297, 10.1002/cne.
193. Ooishi, Y., Kawato, S., Hojo, Y., Hatanaka, Y., Higo, S., Murakami, G., Komatsuzaki, Y., Ogiue-Ikeda, M., Kimoto, T., Mukai, H., Modulation of synaptic plasticity in the hippocampus by hippocampus-derived estrogen and androgen. J. Steroid Biochem. Mol. Biol., 2012, 10.1016/j.jsbmb.2011.10.004.
194. Oomen, C.A., Mayer, J.L., De Kloet, E.R., Joëls, M., Lucassen, P.J., Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur. J. Neurosci. 26 (2007), 3395–3401, 10.1111/j.1460-9568.2007.05972.x.
195. Oomura, Y., Hori, N., Shiraishi, T., Fukunaga, K., Takeda, H., Tsuji, M., Matsumiya, T., Ishibashi, M., Aou, S., Li, X.L., Kohno, D., Uramura, K., Sougawa, H., Yada, T., Wayner, M.J., Sasaki, K., Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides 27 (2006), 2738–2749, 10.1016/j.peptides.2006.07.001.
196. Ormerod, B.K., Lee, T.T.Y., Galea, L.A.M., Estradiol initially enhances but subsequently suppresses (via adrenal steroids) granule cell proliferation in the dentate gyrus of adult female rats. J. Neurobiol. 55 (2003), 247–260, 10.1002/neu.10181.
197. Ortiz, J.B., McLaughlin, K.J., Hamilton, G.F., Baran, S.E., Campbell, A.N., Conrad, C.D., Cholesterol and perhaps estradiol protect against corticosterone-induced hippocampal CA3 dendritic retraction in gonadectomized female and male rats. Neuroscience 246 (2013), 409–421, 10.1016/j.neuroscience.2013.04.027.
198. Park, H.R., Lee, J., Neurogenic contributions made by dietary regulation to hippocampal neurogenesis. Ann. N. Y. Acad. Sci. 1229 (2011), 23–28, 10.1111/j.1749-6632.2011.06089.x.
199. Patten, A.R., Sickmann, H., Hryciw, B.N., Kucharsky, T., Parton, R., Kernick, A., Christie, B.R., Long-term exercise is needed to enhance synaptic plasticity in the hippocampus. Learn. Memory 20 (2013), 642–647, 10.1101/lm.030635.113.
200. Pawluski, J.L., Brummelte, S., Barha, C.K., Crozier, T.M., Galea, L.a.M., Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front. Neuroendocrinol. 30 (2009), 343–357, 10.1016/j.yfrne.2009.03.007.
201. Perez-Martin, M., Cifuentes, M., Grondona, J.M., Bermudez-Silva, F.J., Arrabal, P.M., Perez-Figares, J.M., Jimenez, A.J., Garcia-Segura, L.M., Fernandez-Llebrez, P., Neurogenesis in explants from the walls of the lateral ventricle of adult bovine brain: role of endogenous IGF-1 as a survival factor. Eur. J. Neurosci. 17 (2003), 205–211, 10.1046/j.1460-9568.2003.02432.x.
202. Perl, D.P., Neuropathology of Alzheimer's disease. Mt Sinai J. Med. 77 (2010), 32–42, 10.1002/msj.20157.
203. Pham, K., Nacher, J., Hof, P.R., McEwen, B.S., Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17 (2003), 879–886, 10.1046/j.1460-9568.2003.02513.x.
204. Ploughman, M., Granter-Button, S., Chernenko, G., Attwood, Z., Tucker, B.A., Mearow, K.M., Corbett, D., Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Res. 1150 (2007), 207–216, 10.1016/j.brainres.2007.02.065.
205. Ploughman, M., Granter-Button, S., Chernenko, G., Tucker, B.A., Mearow, K.M., Corbett, D., Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin-I and insulin-like growth factor I after focal ischemia. Neuroscience 136 (2005), 991–1001, 10.1016/j.neuroscience.2005.08.037.
206. Powers, S.K., Ji, L.L., Leeuwenburgh, C., Exercise training-induced alterations in skeletal muscle antioxidant capacity: a brief review. Med. Sci. Sports Exerc. 31 (1999), 987–997, 10.1097/00005768-199907000-00011.
207. Prange-Kiel, J., Wehrenberg, U., Jarry, H., Rune, G.M., Para/autocrine regulation of estrogen receptors in hippocampal neurons. Hippocampus 13 (2003), 226–234, 10.1002/hipo.10075.
208. Prince, M., Bryce, R., Albanese, E., Wimo, A., Ribeiro, W., Ferri, C.P., The global prevalence of dementia: a systematic review and metaanalysis. Alzheimers Dement., 9(63–75), 2013, e2, 10.1016/j.jalz.2012.11.007.
209. Ra, S.M., Kim, H., Jang, M.H., Shin, M.C., Lee, T.H., Lim, B.V., Kim, C.J., Kim, E.H., Kim, K.M., Kim, S.S., Treadmill running and swimming increase cell proliferation in the hippocampal dentate gyrus of rats. Neurosci. Lett. 333 (2002), 123–126, 10.1016/S0304-3940(02)01031-5.
210. Rao, M.S., Hattiangady, B., Shetty, A.K., The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5 (2006), 545–558, 10.1111/j.1474-9726.2006.00243.x.
211. Redila, V.A., Christie, B.R., Exercise-induced changes in dendritic structure and complexity in the adult hippocampal dentate gyrus. Neuroscience 137 (2006), 1299–1307, 10.1016/j.neuroscience.2005.10.050.
212. Ribak, C.E., Shapiro, L.A., Dendritic development of newly generated neurons in the adult brain. Brain Res. Rev., 2007, 10.1016/j.brainresrev.2006.12.005.
213. Rummel, J., Epp, J.R., Galea, L.A.M., Estradiol does not influence strategy choice but place strategy choice is associated with increased cell proliferation in the hippocampus of female rats. Horm. Behav. 58 (2010), 582–590, 10.1016/j.yhbeh.2010.07.009.
214. Sahay, A., Scobie, K.N., Hill, A.S., O'Carroll, C.M., Kheirbek, M.A., Burghardt, N.S., Fenton, A.A., Dranovsky, A., Hen, R., Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472 (2011), 466–470, 10.1038/nature09817.
215. Sahay, A., Wilson, D.A., Hen, R., Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron, 2011, 10.1016/j.neuron.2011.05.012.
216. Scoville, W.B., Milner, B., Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20 (1957), 11–21, 10.1136/jnnp.20.1.11.
217. Sebastian, V., Estil, J.B., Chen, D., Schrott, L.M., Serrano, P.A., Acute physiological stress promotes clustering of synaptic markers and alters spine morphology in the hippocampus. PLoS ONE, 8, 2013, 10.1371/journal.pone.0079077.
218. Sharma, H.S., Cervós-Navarro, J., Dey, P.K., Increased blood-brain barrier permeability following acute short-term swimming exercise in conscious normotensive young rats. Neurosci. Res. 10 (1991), 211–221, 10.1016/0168-0102(91)90058-7.
219. Shen, X., Li, A., Zhang, Y., Dong, X.M., Shan, T., Wu, Y., Jia, J., Hu, Y., The effect of different intensities of treadmill exercise on cognitive function deficit following a severe controlled cortical impact in rats. Int. J. Mol. Sci. 14 (2013), 21598–21612, 10.3390/ijms141021598.
220. Shih, P.C., Yang, Y.R., Wang, R.Y., Effects of exercise intensity on spatial memory performance and hippocampal synaptic plasticity in transient brain ischemic rats. PLoS ONE 8 (2013), 1–8, 10.1371/journal.pone.0078163.
221. Shimada, H., Hamakawa, M., Ishida, A., Tamakoshi, K., Nakashima, H., Ishida, K., Low-speed treadmill running exercise improves memory function after transient middle cerebral artery occlusion in rats. Behav. Brain Res. 243 (2013), 21–27, 10.1016/j.bbr.2012.12.018.
222. Shinohara, Y., Hirase, H., Watanabe, M., Itakura, M., Takahashi, M., Shigemoto, R., Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 19498–19503, 10.1073/pnas.0807461105.
223. Shors, T.J., Stressful experience and learning across the lifespan. Annu. Rev. Psychol. 57 (2006), 55–85, 10.1146/annurev.psych.57.102904.190205.
224. Shors, T.J., Chua, C., Falduto, J., Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 21 (2001), 6292–6297.
225. Shors, T.J., Mathew, J., Sisti, H.M., Edgecomb, C., Beckoff, S., Dalla, C., Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol. Psychiatry 62 (2007), 487–495, 10.1016/j.biopsych.2006.10.033.
226. Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., Gould, E., Neurogenesis in the adult is involved in the formation of trace memories. Nature 410 (2001), 372–376, 10.1038/414938a.
227. Silva-Gómez, A.B., Aguilar-Salgado, Y., Reyes-Hernández, D.O., Flores, G., Dexamethasone induces different morphological changes in the dorsal and ventral hippocampus of rats. J. Chem. Neuroanat. 47 (2013), 71–78, 10.1016/j.jchemneu.2012.12.004.
228. Snyder, J.S., Glover, L.R., Sanzone, K.M., Kamhi, J.F., Cameron, H.A., The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 19 (2009), 898–906, 10.1002/hipo.20552.
229. Snyder, J.S., Kee, N., Wojtowicz, J.M., Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85 (2001), 2423–2431.
230. Sousa, N., Lukoyanov, N.V., Madeira, M.D., Almeida, O.F.X., Paula-Barbosa, M.M., Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97 (2000), 253–266, 10.1016/S0306-4522(00)00050-6.
231. Soya, H., Mukai, A., Deocaris, C.C., Ohiwa, N., Chang, H., Nishijima, T., Fujikawa, T., Togashi, K., Saito, T., Threshold-like pattern of neuronal activation in the hypothalamus during treadmill running: establishment of a minimum running stress (MRS) rat model. Neurosci. Res. 58 (2007), 341–348, 10.1016/j.neures.2007.04.004.
232. Spalding, K.L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H.B., Boström, E., Westerlund, I., Vial, C., Buchholz, B.A., Possnert, G., Mash, D.C., Druid, H., Frisén, J., Dynamics of hippocampal neurogenesis in adult humans. Cell 153 (2013), 1219–1227, 10.1016/j.cell.2013.05.002.
233. Spiegelman, B.M., Flier, J.S., Obesity and the regulation of energy balance. Cell, 2001, 10.1016/S0092-8674(01)00240-9.
234. Spritzer, M.D., Galea, L.A.M., Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev. Neurobiol. 67 (2007), 1321–1333, 10.1002/dneu.20457.
235. Stangl, D., Thuret, S., Impact of diet on adult hippocampal neurogenesis. Genes Nutr., 2009, 10.1007/s12263-009-0134-5.
236. Stranahan, A.M., Lee, K., Martin, B., Maudsley, S., Golden, E., Cutler, R.G., Mattson, M.P., Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19 (2009), 951–961, 10.1002/hipo.20577.
237. Stranahan, A.M., Mattson, M.P., Recruiting adaptive cellular stress responses for successful brain ageing. Nat. Rev. Neurosci., 2012, 10.1038/nrn3151.
238. Surget, A., Saxe, M., Leman, S., Ibarguen-Vargas, Y., Chalon, S., Griebel, G., Hen, R., Belzung, C., Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol. Psychiatry 64 (2008), 293–301, 10.1016/j.biopsych.2008.02.022.
239. Surget, A., Tanti, A., Leonardo, E.D., Laugeray, A., Rainer, Q., Touma, C., Palme, R., Griebel, G., Ibarguen-Vargas, Y., Hen, R., Belzung, C., Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 16 (2011), 1177–1188, 10.1038/mp.2011.48.
240. Swain, R.A., Harris, A.B., Wiener, E.C., Dutka, M.V., Morris, H.D., Theien, B.E., Konda, S., Engberg, K., Lauterbur, P.C., Greenough, W.T., Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 117 (2003), 1037–1046, 10.1016/S0306-4522(02)00664-4.
241. Tajiri, N., Yasuhara, T., Shingo, T., Kondo, A., Yuan, W., Kadota, T., Wang, F., Baba, T., Tayra, J.T., Morimoto, T., Jing, M., Kikuchi, Y., Kuramoto, S., Agari, T., Miyoshi, Y., Fujino, H., Obata, F., Takeda, I., Furuta, T., Date, I., Exercise exerts neuroprotective effects on Parkinson's disease model of rats. Brain Res. 1310 (2010), 200–207, 10.1016/j.brainres.2009.10.075.
242. Tanapat, P., Hastings, N.B., Gould, E., Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J. Comp. Neurol. 481 (2005), 252–265, 10.1002/cne.20385.
243. Tanapat, P., Hastings, N.B., Reeves, A.J., Gould, E., Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 (1999), 5792–5801.
244. Tanapat, P., Hastings, N.B., Rydel, T.A., Galea, L.A.M., Gould, E., Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 437 (2001), 496–504, 10.1002/cne.1297.
245. Thomas, R.M., Hotsenpiller, G., Peterson, D.A., Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J. Neurosci. 27 (2007), 2734–2743, 10.1523/JNEUROSCI.3849-06.2007.
246. Thomas, R.M., Urban, J.H., Peterson, D.A., Acute exposure to predator odor elicits a robust increase in corticosterone and a decrease in activity without altering proliferation in the adult rat hippocampus. Exp. Neurol. 201 (2006), 308–315, 10.1016/j.expneurol.2006.04.010.
247. Thompson, A., Boekhoorn, K., Van Dam, A.-M., Lucassen, P.J., Changes in adult neurogenesis in neurodegenerative diseases: cause or consequence?. Genes Brain Behav. 7:Suppl. 1 (2008), 28–42, 10.1111/j.1601-183X.2007.00379.x.
248. Tong, L., Shen, H., Perreau, V.M., Balazs, R., Cotman, C.W., Effects of exercise on gene-expression profile in the rat hippocampus. Neurobiol. Dis. 8 (2001), 1046–1056, 10.1006/nbdi.2001.0427.
249. Toni, N., Teng, E.M., Bushong, E.A., Aimone, J.B., Zhao, C., Consiglio, A., van Praag, H., Martone, M.E., Ellisman, M.H., Gage, F.H., Synapse formation on neurons born in the adult hippocampus. Nat. Neurosci. 10 (2007), 727–734, 10.1038/nn1908.
250. Toscano-Silva, M., Gomes da Silva, S., Scorza, F.A., Bonvent, J.J., Cavalheiro, E.A., Arida, R.M., Hippocampal mossy fiber sprouting induced by forced and voluntary physical exercise. Physiol. Behav. 101 (2010), 302–308, 10.1016/j.physbeh.2010.05.012.
251. Trejo, J.L., Carro, E., Torres-Aleman, I., Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21 (2001), 1628–1634.
252. Tsurugizawa, T., Mukai, H., Tanabe, N., Murakami, G., Hojo, Y., Kominami, S., Mitsuhashi, K., Komatsuzaki, Y., Morrison, J.H., Janssen, W.G.M., Kimoto, T., Kawato, S., Estrogen induces rapid decrease in dendritic thorns of CA3 pyramidal neurons in adult male rat hippocampus. Biochem. Biophys. Res. Commun. 337 (2005), 1345–1352, 10.1016/j.bbrc.2005.09.188.
253. Tzeng, W.-Y., Chen, L.-H., Cherng, C.G., Tsai, Y.-N., Yu, L., Sex differences and the modulating effects of gonadal hormones on basal and the stressor-decreased newly proliferative cells and neuroblasts in dentate gyrus. Psychoneuroendocrinology 42 (2014), 24–37.
254. Van der Borght, K., Havekes, R., Bos, T., Eggen, B.J.L., Van der Zee, E.A., Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav. Neurosci. 121 (2007), 324–334, 10.1037/0735-7044.121.2.324.
255. van Praag, H., Christie, B.R., Sejnowski, T.J., Gage, F.H., Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96 (1999), 13427–13431, 10.1073/pnas.96.23.13427.
256. van Praag, H., Kempermann, G., Gage, F.H., Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2 (1999), 266–270, 10.1038/6368.
257. van Praag, H., Schinder, A.F., Christie, B.R., Toni, N., Palmer, T.D., Gage, F.H., Functional neurogenesis in the adult hippocampus. Nature 415 (2002), 1030–1034, 10.1038/4151030a.
258. van Praag, H., Shubert, T., Zhao, C., Gage, F.H., Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25 (2005), 8680–8685, 10.1523/JNEUROSCI.1731-05.2005.
259. Vezzoli, A., Pugliese, L., Marzorati, M., Serpiello, F.R., La Torre, A., Porcelli, S., Time-course changes of oxidative stress response to high-intensity discontinuous training versus moderate-intensity continuous training in masters runners. PLoS ONE, 9, 2014, e87506, 10.1371/journal.pone.0087506.
260. Viau, V., Meaney, M.J., Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat. Endocrinology 129 (1991), 2503–2511, 10.1210/endo-129-5-2503.
261. Wang, J.M., Johnston, P.B., Ball, B.G., Brinton, R.D., The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. J. Neurosci. 25 (2005), 4706–4718, 10.1523/JNEUROSCI.4520-04.2005.
262. Watanabe, Y., Gould, E., McEwen, B.S., Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588 (1992), 341–345, 10.1016/0006-8993(92)91597-8.
263. Wayner, M.J., Armstrong, D.L., Phelix, C.F., Oomura, Y., Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo. Peptides 25 (2004), 991–996, 10.1016/j.peptides.2004.03.018.
264. Westenbroek, C., Den Boer, J.A., Veenhuis, M., Ter Horst, G.J., Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res. Bull. 64 (2004), 303–308, 10.1016/j.brainresbull.2004.08.006.
265. Winner, B., Kohl, Z., Gage, F.H., Neurodegenerative disease and adult neurogenesis. Eur. J. Neurosci. 33 (2011), 1139–1151, 10.1111/j.1460-9568.2011.07613.x.
266. Winocur, G., Wojtowicz, J.M., Sekeres, M., Snyder, J.S., Wang, S., Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16 (2006), 296–304, 10.1002/hipo.20163.
267. Wong, E.Y.H., Herbert, J., Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137 (2006), 83–92, 10.1016/j.neuroscience.2005.08.073.
268. Wong, E.Y.H., Herbert, J., The corticoid environment: a determining factor for neural progenitors’ survival in the adult hippocampus. Eur. J. Neurosci. 20 (2004), 2491–2498, 10.1111/j.1460-9568.2004.03717.x.
269. Woolley, C.S., Gould, E., Frankfurt, M., McEwen, B.S., Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10 (1990), 4035–4039.
270. Woolley, C.S., Gould, E., McEwen, B.S., Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531 (1990), 225–231, 10.1016/0006-8993(90)90778-A.
271. Woolley, C.S., McEwen, B.S., Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J. Neurosci. 14 (1994), 7680–7687.
272. Woolley, C.S., McEwen, B.S., Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336 (1993), 293–306, 10.1002/cne.903360210.
273. Yancey, S.L., Overton, J.M., Cardiovascular responses to voluntary and treadmill exercise in rats. J. Appl. Physiol. 75 (1993), 1334–1340.
274. Yap, J.J., Takase, L.F., Kochman, L.J., Fornal, C.A., Miczek, K.A., Jacobs, B.L., Repeated brief social defeat episodes in mice: effects on cell proliferation in the dentate gyrus. Behav. Brain Res. 172 (2006), 344–350, 10.1016/j.bbr.2006.05.027.
275. Yartsev, M.M., Ulanovsky, N., Representation of three-dimensional space in the hippocampus of flying bats. Science 340 (2013), 367–372, 10.1126/science.1235338.
276. Yau, S.Y., Gil-Mohapel, J., Christie, B.R., So, K.F., Physical exercise-induced adult neurogenesis: a good strategy to prevent cognitive decline in neurodegenerative diseases?. Biomed Res. Int., 2014, 2014, 10.1155/2014/403120.
277. Yau, S.Y., Lau, B.W.M., Tong, J. Bin, Wong, R., Ching, Y.P., Qiu, G., Tang, S.W., Lee, T.M.C., So, K.F., Hippocampal neurogenesis and dendritic plasticity support running-improved spatial learning and depression-like behaviour in stressed rats. PLoS One, 6, 2011, 10.1371/journal.pone.0024263.
278. Yau, S.Y., Li, a., Hoo, R.L.C., Ching, Y.P., Christie, B.R., Lee, T.M.C., Xu, a., So, K.-F., Physical exercise-induced hippocampal neurogenesis and antidepressant effects are mediated by the adipocyte hormone adiponectin. Proc. Natl. Acad. Sci. 111 (2014), 15810–15815, 10.1073/pnas.1415219111.
279. Yoshiya, M., Komatsuzaki, Y., Hojo, Y., Ikeda, M., Mukai, H., Hatanaka, Y., Murakami, G., Kawata, M., Kimoto, T., Kawato, S., Corticosterone rapidly increases thorns of CA3 neurons via synaptic/extranuclear glucocorticoid receptor in rat hippocampus. Front. Neural Circuits, 7, 2013, 191, 10.3389/fncir.2013.00191.
280. Zagaar, M., Dao, A., Alhaider, I., Alkadhi, K., Regular treadmill exercise prevents sleep deprivation-induced disruption of synaptic plasticity and associated signaling cascade in the dentate gyrus. Mol. Cell. Neurosci. 56 (2013), 375–383, 10.1016/j.mcn.2013.07.011.
281. Zagaar, M., Dao, A., Levine, A., Alhaider, I., Alkadhi, K., Regular exercise prevents sleep deprivation associated impairment of long-term memory and synaptic plasticity in the CA1 area of the hippocampus. Sleep 36 (2013), 751–761, 10.5665/sleep.2642.
282. Zhang, Z., Yang, R., Zhou, R., Li, L., Sokabe, M., Chen, L., Progesterone promotes the survival of newborn neurons in the dentate gyrus of adult male mice. Hippocampus 20 (2010), 402–412, 10.1002/hipo.20642.
283. Zhao, C., Deng, W., Gage, F.H., Mechanisms and functional implications of adult neurogenesis. Cell 132 (2008), 645–660, 10.1016/j.cell.2008.01.033.
284. Zhao, H., Tian, Z., Hao, J., Chen, B., Extragonadal aromatization increases with time after ovariectomy in rats. Reprod. Biol. Endocrinol., 3, 2005, 6, 10.1186/1477-7827-3-6.
285. Zigova, T., Pencea, V., Wiegand, S.J., Luskin, M.B., Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol. Cell. Neurosci. 11 (1998), 234–245, 10.1006/mcne.1998.0684.