Stress, hippocampal neurogenesis and cognition: functional correlations
Received date: 02 Jun 2016
Accepted date: 12 Jun 2016
Published date: 05 Jul 2016
Copyright
The brain of many species including humans, harbors stem cells that continue to generate new neurons up into adulthood. This form of structural plasticity occurs in a limited number of brain regions, i.e. the subventricular zone and the hippocampal dentate gyrus and is regulated by environmental and hormonal factors. In this minireview, we provide an overview of the effects of stress and glucocorticoid hormones on adult hippocampal neurogenesis and discuss how these effects may be relevant for cognitive function and possibly, brain disease. While its exact functional role remains elusive, adult neurogenesis has been implicated in learning and memory, fear and mood regulation and recently, adult-born neurons were found to be involved in specific cognitive functions such as pattern separation (i.e. the ability to form unique memory representations) and cognitive flexibility. The process of adult neurogenesis is influenced by several factors; whereas e.g. exercise stimulates, exposure to stress and stress hormones generally inhibit neurogenesis. Effects of acute, mild stress are generally short-lasting and recover quickly, but chronic or severe forms of stress can induce lasting reductions in adult neurogenesis. Some of the inhibitory effects of stress can be rescued by exercise, by allowing a period of recovery from stress, by drugs that target the stress system, or by some, but not all, antidepressants. Stress may, partly through its effects on adult neurogenesis, alter structure and plasticity of the hippocampal circuit. This can lead to subsequent changes in stress responsivity and aspects of memory processing, which may be particularly relevant for stress related psychopathology or brain diseases that involve perturbed memory processing.
Key words: adult neurogenesis; stem cells; hippocampus; stress; memory; pattern separation; cognition
Paul J. Lucassen , Charlotte A. Oomen . Stress, hippocampal neurogenesis and cognition: functional correlations[J]. Frontiers in Biology, 2016 , 11(3) : 182 -192 . DOI: 10.1007/s11515-016-1412-4
1 |
Abrous D N, Koehl M, Le Moal M (2005). Adult neurogenesis: from precursors to network and physiology. Physiol Rev, 85(2): 523–569
|
2 |
Aimone J B, Deng W, Gage F H (2010). Adult neurogenesis: integrating theories and separating functions. Trends Cogn Sci, 14(7): 325–337
|
3 |
Aimone J B, Wiles J, Gage F H (2009). Computational influence of adult neurogenesis on memory encoding. Neuron, 61(2): 187–202
|
4 |
Alonso R, Griebel G, Pavone G, Stemmelin J, Le Fur G, Soubrié P (2004). Blockade of CRF(1) or V(1b) receptors reverses stress-induced suppression of neurogenesis in a mouse model of depression. Mol Psychiatry, 9(3): 278–286, 224
|
5 |
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 (2013). Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology, 38(5): 872–883
|
6 |
Arruda-Carvalho M, Sakaguchi M, Akers K G, Josselyn S A, Frankland P W (2011). Posttraining ablation of adult-generated neurons degrades previously acquired memories. J Neurosci, 31(42): 15113–15127
|
7 |
Balu D T, Lucki I (2009). Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology. Neurosci Biobehav Rev, 33(3): 232–252
|
8 |
Banasr M, Duman R S (2007). Regulation of neurogenesis and gliogenesis by stress and antidepressant treatment. CNS Neurol Disord Drug Targets, 6(5): 311–320
|
9 |
Becker S (2005). A computational principle for hippocampal learning and neurogenesis. Hippocampus, 15(6): 722–738
|
10 |
Bekinschtein P, Kent B A, Oomen C A, Clemenson G D, Gage F H, Saksida L M, Bussey T J (2014). Brain-derived neurotrophic factor interacts with adult-born immature cells in the dentate gyrus during consolidation of overlapping memories. Hippocampus, 24(8): 905–911
|
11 |
Bekinschtein P, Kent B A, Oomen C A, Clemenson G D, Jr., Gage F H, Saksida L M, Bussey T J (2013). BDNF in the Dentate Gyrus Is Required for Consolidation of “Pattern-Separated” Memories. Cell Reports, 5: 1–10
|
12 |
Bekinschtein P, Oomen C A, Saksida L M, Bussey T J (2011). Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin Cell Dev Biol, 22(5): 536–542
|
13 |
Ben Abdallah N M, Filipkowski R K, Pruschy M, Jaholkowski P, Winkler J, Kaczmarek L, Lipp H P (2013). Impaired long-term memory retention: common denominator for acutely or genetically reduced hippocampal neurogenesis in adult mice. Behav Brain Res, 252: 275–286
|
14 |
Besnard A, Sahay A (2016). Adult Hippocampal Neurogenesis, Fear Generalization, and Stress. Neuropsychopharmacology, 41(1): 24–44
|
15 |
Binder E B, Bradley R G, Liu W, Epstein M P, Deveau T C, Mercer K B, Tang Y, Gillespie C F, Heim C M, Nemeroff C B, Schwartz A C, Cubells J F, Ressler K J (2008). Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. JAMA, 299(11): 1291–1305
|
16 |
Boku S, Toda H, Nakagawa S, Kato A, Inoue T, Koyama T, Hiroi N, Kusumi I (2015). Neonatal maternal separation alters the capacity of adult neural precursor cells to differentiate into neurons via methylation of retinoic acid receptor gene promoter. Biol Psychiatry, 77(4): 335–344
|
17 |
Bruel-Jungerman E, Lucassen P J, Francis F (2011). Cholinergic influences on cortical development and adult neurogenesis. Behav Brain Res, 221(2): 379–388
|
18 |
Burghardt N S, Park E H, Hen R, Fenton A A (2012). Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus, 22(9): 1795–1808
|
19 |
Chetty S, Friedman A R, Taravosh-Lahn K, Kirby E D, Mirescu C, Guo F, Krupik D, Nicholas A, Geraghty A C, Krishnamurthy A, Tsai M K, Covarrubias D, Wong A T, Francis D D, Sapolsky R M, Palmer T D, Pleasure D, Kaufer D (2014). Stress and glucocorticoids promote oligodendrogenesis in the adult hippocampus. Mol Psychiatry, 19(12): 1275–1283
|
20 |
Clelland C D, Choi M, Romberg C, Clemenson G D Jr, Fragniere A, Tyers P, Jessberger S, Saksida L M, Barker R A, Gage F H, Bussey T J (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 325(5937): 210–213
|
21 |
Creer D J, Romberg C, Saksida L M, van Praag H, Bussey T J (2010). Running enhances spatial pattern separation in mice. Proc Natl Acad Sci USA, 107(5): 2367–2372
|
22 |
Czéh B, Lucassen P J (2007). What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci, 257(5): 250–260
|
23 |
Czéh B, Simon M, Schmelting B, Hiemke C, Fuchs E (2006). Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology, 31(8): 1616–1626
|
24 |
Czéh B, Welt T, Fischer A K, Erhardt A, Schmitt W, Müller M B, Toschi N, Fuchs E, Keck M E (2002). Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biol Psychiatry, 52(11): 1057–1065
|
25 |
Dagyte G, Van der Zee E A, Postema F, Luiten P G, Den Boer J A, Trentani A, Meerlo P (2009). Chronic but not acute foot-shock stress leads to temporary suppression of cell proliferation in rat hippocampus. Neuroscience, 162(4): 904–913
|
26 |
Datson N A, Speksnijder N, Mayer J L, Steenbergen P J, Korobko O, Goeman J, de Kloet E R, Joëls M, Lucassen P J (2012). The transcriptional response to chronic stress and glucocorticoid receptor blockade in the hippocampal dentate gyrus. Hippocampus, 22(2): 359–371
|
27 |
de Kloet E R, Joëls M, Holsboer F (2005). Stress and the brain: from adaptation to disease. Nat Rev Neurosci, 6(6): 463–475
|
28 |
Djavadian R L (2004). Serotonin and neurogenesis in the hippocampal dentate gyrus of adult mammals. Acta Neurobiol Exp (Wars), 64(2): 189–200
|
29 |
Domínguez-Escribà L, Hernández-Rabaza V, Soriano-Navarro M, Barcia J A, Romero F J, García-Verdugo J M, Canales J J (2006). Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur J Neurosci, 24(2): 586–594
|
30 |
Dranovsky A, Hen R (2006). Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry, 59(12): 1136–1143
|
31 |
Droste S K, Gesing A, Ulbricht S, Müller M B, Linthorst A C, Reul J M (2003). Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis. Endocrinology, 144(7): 3012–3023
|
32 |
Ehninger D, Kempermann G (2006). Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes Brain Behav, 5(1): 29–39
|
33 |
Erdmann G, Berger S, Schütz G (2008). Genetic dissection of glucocorticoid receptor function in the mouse brain. J Neuroendocrinol, 20(6): 655–659
|
34 |
Fitzsimons C P, Herbert J, Schouten M, Meijer O C, Lucassen P J, Lightman S (2016). Circadian and Ultradian Glucocorticoid Rhythmicity: Implications for the Effects of Glucocorticoids on Neural Stem Cells and Adult Hippocampal Neurogenesis. Front Neuroendocrinol, (In press)
|
35 |
Fitzsimons C P, van Hooijdonk L W, Schouten M, Zalachoras I, Brinks V, Zheng T, Schouten T G, Saaltink D J, Dijkmans T, Steindler D A, Verhaagen J, Verbeek F J, Lucassen P J, de Kloet E R, Meijer O C, Karst H, Joels M, Oitzl M S, Vreugdenhil E (2013). Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol Psychiatry, 18(9): 993–1005
|
36 |
Galea L A (2008). Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Brain Res Rev, 57(2): 332–341
|
37 |
Garcia A, Steiner B, Kronenberg G, Bick-Sander A, Kempermann G (2004). Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell, 3(6): 363–371
|
38 |
Garthe A, Behr J, Kempermann G (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE, 4(5): e5464
|
39 |
Garthe A, Huang Z, Kaczmarek L, Filipkowski R K, Kempermann G (2014). Not all water mazes are created equal: cyclin D2 knockout mice with constitutively suppressed adult hippocampal neurogenesis do show specific spatial learning deficits. Genes Brain Behav, 13(4): 357–364
|
40 |
Ge S, Yang C H, Hsu K S, Ming G L, Song H (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron, 54(4): 559–566
|
41 |
Gould E (2007). How widespread is adult neurogenesis in mammals? Nat Rev Neurosci, 8(6): 481–488
|
42 |
Gould E, Beylin A, Tanapat P, Reeves A, Shors T J (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci, 2(3): 260–265
|
43 |
Gould E, McEwen B S, Tanapat P, Galea L A, 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(7): 2492–2498
|
44 |
Groves J O, Leslie I, Huang G J, McHugh S B, Taylor A, Mott R, Munafò M, Bannerman D M, Flint J (2013). Ablating adult neurogenesis in the rat has no effect on spatial processing: evidence from a novel pharmacogenetic model. PLoS Genet, 9(9): e1003718
|
44a |
Gu Y, Arruda-Carvalho M, Wang J, Janoschka S R, Josselyn S A, Frankland P W, Ge S (2012). Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci, 36(15): 1700–1706
|
45 |
Guadagno J, Swan P, Shaikh R, Cregan S P (2015). Microglia-derived IL-1beta triggers p53-mediated cell cycle arrest and apoptosis in neural precursor cells. Cell death & disease, 6: e1779
|
46 |
Hanson N D, Owens M J, Boss-Williams K A, Weiss J M, Nemeroff C B (2011a). Several stressors fail to reduce adult hippocampal neurogenesis. Psychoneuroendocrinology, 36(10): 1520–1529
|
47 |
Hanson N D, Owens M J, Nemeroff C B (2011b). Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology, 36(13): 2589–2602
|
48 |
Harris A P, Holmes M C, de Kloet E R, Chapman K E, Seckl J R (2013). Mineralocorticoid and glucocorticoid receptor balance in control of HPA axis and behaviour. Psychoneuroendocrinology, 38(5): 648–658
|
49 |
Heine V M, Maslam S, Joëls M, Lucassen P J (2004a). Increased P27KIP1 protein expression in the dentate gyrus of chronically stressed rats indicates G1 arrest involvement. Neuroscience, 129(3): 593–601
|
50 |
Heine V M, Maslam S, Joëls M, Lucassen P J (2004b). 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(3): 361–375
|
51 |
Heine V M, Maslam S, Zareno J, Joëls M, Lucassen P J (2004c). Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci, 19(1): 131–144
|
52 |
Heine V M, Zareno J, Maslam S, Joëls M, Lucassen P J (2005). Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur J Neurosci, 21(5): 1304–1314
|
53 |
Hill A S, Sahay A, Hen R (2015). Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors. Neuropsychopharmacology, 40(10): 2368–2378
|
54 |
Hinwood M, Morandini J, Day T A, Walker F R (2012). Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb Cortex, 22(6): 1442–1454
|
55 |
Holmes M M, Galea L A, Mistlberger R E, Kempermann G (2004). Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J Neurosci Res, 76(2): 216–222
|
56 |
Hu P, Oomen C, van Dam A M, Wester J, Zhou J N, Joëls M, Lucassen P J (2012). A single-day treatment with mifepristone is sufficient to normalize chronic glucocorticoid induced suppression of hippocampal cell proliferation. PLoS ONE, 7(9): e46224
|
57 |
Hu P, Wang Y, Liu J, Meng F T, Qi X R, Chen L, van Dam A M, Joëls M, Lucassen P J, Zhou J N (2016). Chronic retinoic acid treatment suppresses adult hippocampal neurogenesis, in close correlation with depressive-like behavior. Hippocampus: n/a
|
58 |
Jayatissa M N, Bisgaard C, Tingström A, Papp M, Wiborg O (2006). Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology, 31(11): 2395–2404
|
59 |
Jayatissa M N, Henningsen K, West M J, Wiborg O (2009). Decreased cell proliferation in the dentate gyrus does not associate with development of anhedonic-like symptoms in rats. Brain Res, 1290: 133–141
|
60 |
Jessberger S, Gage F H (2014). Adult neurogenesis: bridging the gap between mice and humans. Trends Cell Biol, 24(10): 558–563
|
61 |
Joca S R, Ferreira F R, Guimarães F S (2007). Modulation of stress consequences by hippocampal monoaminergic, glutamatergic and nitrergic neurotransmitter systems. Stress, 10(3): 227–249
|
62 |
Joëls M, Baram T Z (2009). The neuro-symphony of stress. Nat Rev Neurosci, 10(6): 459–466
|
63 |
Joëls M, Pu Z, Wiegert O, Oitzl M S, Krugers H J (2006). Learning under stress: how does it work? Trends Cogn Sci, 10(4): 152–158
|
64 |
Joëls M, Sarabdjitsingh R A, Karst H (2012). Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol Rev, 64(4): 901–938
|
65 |
Kanatsou S, Fearey B C, Kuil L E, Lucassen P J, Harris A P, Seckl J R, Krugers H, Joels M (2015). Overexpression of Mineralocorticoid Receptors Partially Prevents Chronic Stress-Induced Reductions in Hippocampal Memory and Structural Plasticity. PLoS ONE, 10(11): e0142012
|
66 |
Kannangara T S, Lucero M J, Gil-Mohapel J, Drapala R J, Simpson J M, Christie B R, van Praag H (2011). Running reduces stress and enhances cell genesis in aged mice. Neurobiol Aging, 32(12): 2279–2286
|
67 |
Karst H, Berger S, Erdmann G, Schütz G, Joëls M (2010). Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc Natl Acad Sci USA, 107(32): 14449–14454
|
68 |
Kempermann G (2012). New neurons for ‘survival of the fittest’. Nat Rev Neurosci, 13(10): 727–736
|
69 |
Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, Wolf S A (2010). Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci, 4: 189
|
70 |
Kheirbek M A, Klemenhagen K C, Sahay A, Hen R (2012a). Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci, 15(12): 1613–1620
|
71 |
Kheirbek M A, Tannenholz L, Hen R (2012b). NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J Neurosci, 32(25): 8696–8702
|
72 |
Koolhaas J M, Bartolomucci A, Buwalda B, de Boer S F, Flügge G, Korte S M, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E (2011). Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev, 35(5): 1291–1301
|
73 |
Kreisel T, Frank M G, Licht T, Reshef R, Ben-Menachem-Zidon O, Baratta M V, Maier S F, Yirmiya R (2014). Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis. Mol Psychiatry, 19(6): 699–709
|
74 |
Kretz O, Reichardt H M, Schütz G, Bock R (1999). Corticotropin-releasing hormone expression is the major target for glucocorticoid feedback-control at the hypothalamic level. Brain Res, 818(2): 488–491
|
75 |
Krugers H J, Goltstein P M, van der Linden S, Joëls M (2006). Blockade of glucocorticoid receptors rapidly restores hippocampal CA1 synaptic plasticity after exposure to chronic stress. Eur J Neurosci, 23(11): 3051–3055
|
76 |
Kuhn H G, Dickinson-Anson H, Gage F H (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci, 16(6): 2027–2033
|
77 |
Lagace D C, Donovan M H, DeCarolis N A, Farnbauch L A, Malhotra S, Berton O, Nestler E J, Krishnan V, Eisch A J (2010). Adult hippocampal neurogenesis is functionally important for stress-induced social avoidance. Proc Natl Acad Sci USA, 107(9): 4436–4441
|
78 |
Lehmann M L, Brachman R A, Martinowich K, Schloesser R J, Herkenham M (2013). Glucocorticoids orchestrate divergent effects on mood through adult neurogenesis. J Neurosci, 33(7): 2961–2972
|
79 |
Lemaire V, Koehl M, Le Moal M, Abrous D N (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA, 97(20): 11032–11037
|
80 |
Levine S (2005). Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology, 30(10): 939–946
|
81 |
Levone B R, Cryan J F, O'Leary O F (2015). Role of adult hippocampal neurogenesis in stress resilience. Neurobiology of Stress 1. Neurobiol Stress, 1: 147–155
|
82 |
Liston C, Cichon J M, Jeanneteau F, Jia Z, Chao M V, Gan W B (2013). Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance. Nat Neurosci, 16(6): 698–705
|
83 |
Llorens-Martín M, Jurado-Arjona J, Bolós M, Pallas-Bazarra N, Ávila J (2016). Forced swimming sabotages the morphological and synaptic maturation of newborn granule neurons and triggers a unique pro-inflammatory milieu in the hippocampus. Brain Behav Immun, 53: 242–254
|
84 |
Lucassen P J, Fitzsimons C P, Korosi A, Joels M, Belzung C, Abrous D N (2013a). Stressing new neurons into depression? Mol Psychiatry, 18(4): 396–397
|
85 |
Lucassen P J, Meerlo P, Naylor A S, van Dam A M, Dayer A G, Fuchs E, Oomen C A, Czéh B (2010). Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: Implications for depression and antidepressant action. Eur Neuropsychopharmacol, 20(1): 1–17
|
86 |
Lucassen P J, Naninck E F, van Goudoever J B, Fitzsimons C, Joels M, Korosi A (2013b). Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci, 36(11): 621–631
|
87 |
Lucassen P J, Pruessner J, Sousa N, Almeida O F, Van Dam A M, Rajkowska G, Swaab D F, Czéh B (2014). Neuropathology of stress. Acta Neuropathol, 127(1): 109–135
|
88 |
Lyons D M, Buckmaster P S, Lee A G, Wu C, Mitra R, Duffey L M, Buckmaster C L, Her S, Patel P D, Schatzberg A F (2010). Stress coping stimulates hippocampal neurogenesis in adult monkeys. Proc Natl Acad Sci USA, 107(33): 14823–14827
|
89 |
Mahmoud R, Wainwright S R, Galea L A (2016). Sex hormones and adult hippocampal neurogenesis: Regulation, implications, and potential mechanisms. Front Neuroendocrinol,
|
90 |
Mak G K, Weiss S (2010). Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci, 13: 753–758
|
91 |
Malberg J E, Duman R S (2003). Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology, 28(9): 1562–1571
|
92 |
Marlatt M W, Potter M C, Lucassen P J, van Praag H (2012). Running throughout middle-age improves memory function, hippocampal neurogenesis, and BDNF levels in female C57BL/6J mice. Dev Neurobiol, 72(6): 943–952
|
93 |
Mayer J L, Klumpers L, Maslam S, de Kloet E R, Joëls M, Lucassen P J (2006). Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol, 18(8): 629–631
|
94 |
Meaney M J, Szyf M, Seckl J R (2007). Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med, 13(7): 269–277
|
95 |
Medina A, Seasholtz A F, Sharma V, Burke S, Bunney W Jr, Myers R M, Schatzberg A, Akil H, Watson S J (2013). Glucocorticoid and mineralocorticoid receptor expression in the human hippocampus in major depressive disorder. J Psychiatr Res, 47(3): 307–314
|
96 |
Miller J A, Nathanson J, Franjic D, Shim S, Dalley R A, Shapouri S, Smith K A, Sunkin S M, Bernard A, Bennett J L, Lee C K, Hawrylycz M J, Jones A R, Amaral D G, Šestan N, Gage F H, Lein E S (2013). Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. Development, 140(22): 4633–4644
|
97 |
Mirescu C, Gould E (2006). Stress and adult neurogenesis. Hippocampus, 16(3): 233–238
|
98 |
Mitra R, Sundlass K, Parker K J, Schatzberg A F, Lyons D M (2006). Social stress-related behavior affects hippocampal cell proliferation in mice. Physiol Behav, 89(2): 123–127
|
99 |
Montaron M F, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M, Piazza P V, Abrous D N (2006). Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol Aging, 27(4): 645–654
|
100 |
Montaron M F, Koehl M, Lemaire V, Drapeau E, Abrous D N, Le Moal M (2004). Environmentally induced long-term structural changes: cues for functional orientation and vulnerabilities. Neurotox Res, 6(7-8): 571–580
|
101 |
Montaron M F, Piazza P V, Aurousseau C, Urani A, Le Moal M, Abrous D N (2003). Implication of corticosteroid receptors in the regulation of hippocampal structural plasticity. Eur J Neurosci, 18(11): 3105–3111
|
102 |
Morris G P, Clark I A, Zinn R, Vissel B (2013). Microglia: a new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research. Neurobiol Learn Mem, 105: 40–53
|
103 |
Nacher J, McEwen B S (2006). The role of N-methyl-D-asparate receptors in neurogenesis. Hippocampus, 16(3): 267–270
|
104 |
Nishijima T, Llorens-Martín M, Tejeda G S, Inoue K, Yamamura Y, Soya H, Trejo J L, Torres-Alemán I (2013). Cessation of voluntary wheel running increases anxiety-like behavior and impairs adult hippocampal neurogenesis in mice. Behav Brain Res, 245: 34–41
|
105 |
O’Leary O F, Cryan J F (2014). A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharmacol Sci, 35(12): 675–687
|
106 |
O’Leary O F, O’Connor R M, Cryan J F (2012). Lithium-induced effects on adult hippocampal neurogenesis are topographically segregated along the dorso-ventral axis of stressed mice. Neuropharmacology, 62(1): 247–255
|
107 |
Oomen C A, Bekinschtein P, Kent B A, Saksida L M, Bussey T J (2014). Adult hippocampal neurogenesis and its role in cognition. Wiley Interdiscip Rev Cogn Sci, 5(5): 573–587
|
108 |
Oomen C A, Girardi C E, Cahyadi R, Verbeek E C, Krugers H, Joëls M, Lucassen P J (2009). Opposite effects of early maternal deprivation on neurogenesis in male versus female rats. PLoS ONE, 4(1): e3675
|
109 |
Oomen C A, Mayer J L, de Kloet E R, Joëls M, Lucassen P J (2007). Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci, 26(12): 3395–3401
|
110 |
Palmer T D, Willhoite A R, Gage F H (2000). Vascular niche for adult hippocampal neurogenesis. J Comp Neurol, 425(4): 479–494
|
111 |
Parihar V K, Hattiangady B, Kuruba R, Shuai B, Shetty A K (2011). Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol Psychiatry, 16(2): 171–183
|
112 |
Perera T D, Dwork A J, Keegan K A, Thirumangalakudi L, Lipira C M, Joyce N, Lange C, Higley J D, Rosoklija G, Hen R, Sackeim H A, Coplan J D (2011). Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS ONE, 6(4): e17600
|
113 |
Pham K, McEwen B S, Ledoux J E, Nader K (2005). Fear learning transiently impairs hippocampal cell proliferation. Neuroscience, 130(1): 17–24
|
114 |
Pham K, Nacher J, Hof P R, McEwen B S (2003). Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci, 17(4): 879–886
|
115 |
Qi X R, Kamphuis W, Wang S, Wang Q, Lucassen P J, Zhou J N, Swaab D F (2013). Aberrant stress hormone receptor balance in the human prefrontal cortex and hypothalamic paraventricular nucleus of depressed patients. Psychoneuroendocrinology, 38(6): 863–870
|
116 |
Qian X, Droste S K, Lightman S L, Reul J M, Linthorst A C (2012). Circadian and ultradian rhythms of free glucocorticoid hormone are highly synchronized between the blood, the subcutaneous tissue, and the brain. Endocrinology, 153(9): 4346–4353
|
117 |
Revest J M, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza P V, Abrous D N (2009). Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry, 14(10): 959–967
|
118 |
Ridder S, Chourbaji S, Hellweg R, Urani A, Zacher C, Schmid W, Zink M, Hörtnagl H, Flor H, Henn F A, Schütz G, Gass P (2005). Mice with genetically altered glucocorticoid receptor expression show altered sensitivity for stress-induced depressive reactions. J Neurosci, 25(26): 6243–6250
|
119 |
Sahay A, Hen R (2007). Adult hippocampal neurogenesis in depression. Nat Neurosci, 10(9): 1110–1115
|
120 |
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 (2011a). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature, 472(7344): 466–470
|
121 |
Sahay A, Wilson D A, Hen R (2011b). Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron, 70(4): 582–588
|
122 |
Sampedro-Piquero P, Begega A, Arias J L (2014). Increase of glucocorticoid receptor expression after environmental enrichment: relations to spatial memory, exploration and anxiety-related behaviors. Physiol Behav, 129: 118–129
|
123 |
Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 301(5634): 805–809
|
124 |
Sapolsky R M, Uno H, Rebert C S, Finch C E (1990). Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J Neurosci, 10(9): 2897–2902
|
125 |
Sarabdjitsingh R A, Conway-Campbell B L, Leggett J D, Waite E J, Meijer O C, de Kloet E R, Lightman S L (2010). Stress responsiveness varies over the ultradian glucocorticoid cycle in a brain-region-specific manner. Endocrinology, 151(11): 5369–5379
|
126 |
Sarabdjitsingh R A, Jezequel J, Pasricha N, Mikasova L, Kerkhofs A, Karst H, Groc L, Joëls M (2014). Ultradian corticosterone pulses balance glutamatergic transmission and synaptic plasticity. Proc Natl Acad Sci USA, 111(39): 14265–14270
|
127 |
Sarabdjitsingh R A, Joëls M, de Kloet E R (2012). Glucocorticoid pulsatility and rapid corticosteroid actions in the central stress response. Physiol Behav, 106(1): 73–80
|
128 |
Saxe M D, Battaglia F, Wang J W, Malleret G, David D J, Monckton J E, Garcia A D, Sofroniew M V, Kandel E R, Santarelli L, Hen R, Drew M R (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA, 103(46): 17501–17506
|
129 |
Schloesser R J, Lehmann M, Martinowich K, Manji H K, Herkenham M (2010). Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol Psychiatry, 15(12): 1152–1163
|
130 |
Schmidt H D, Duman R S (2007). The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav Pharmacol, 18(5-6): 391–418
|
131 |
Schoenfeld T J, Cameron H A (2015). Adult neurogenesis and mental illness. Neuropsychopharmacology, 40(1): 113–128
|
132 |
Schoenfeld T J, Gould E (2013). Differential effects of stress and glucocorticoids on adult neurogenesis. Curr Top Behav Neurosci, 15: 139–164
|
133 |
Schouten M, Buijink M R, Lucassen P J, Fitzsimons C P (2012). New Neurons in Aging Brains: Molecular Control by Small Non-Coding RNAs. Front Neurosci, 6: 25
|
134 |
Schwabe L, Joëls M, Roozendaal B, Wolf O T, Oitzl M S (2012). Stress effects on memory: an update and integration. Neurosci Biobehav Rev, 36(7): 1740–1749
|
135 |
Seo D O, Carillo M A, Chih-Hsiung Lim S, Tanaka K F, Drew M R (2015). Adult Hippocampal Neurogenesis Modulates Fear Learning through Associative and Nonassociative Mechanisms. J Neurosci, 35(32): 11330–11345
|
136 |
Shors T J, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410(6826): 372–376
|
137 |
Shors T J, Townsend D A, Zhao M, Kozorovitskiy Y, Gould E (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus, 12(5): 578–584
|
138 |
Sierra A, Beccari S, Diaz-Aparicio I, Encinas J M, Comeau S, Tremblay M E (2014). Surveillance, phagocytosis, and inflammation: how never-resting microglia influence adult hippocampal neurogenesis. Neural Plast, 2014: 610343
|
139 |
Sierra A, Encinas J M, Deudero J J, Chancey J H, Enikolopov G, Overstreet-Wadiche L S, Tsirka S E, Maletic-Savatic M (2010). Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell, 7(4): 483–495
|
140 |
Simon M, Czéh B, Fuchs E (2005). Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res, 1049(2): 244–248
|
141 |
Snyder J S, Glover L R, Sanzone K M, Kamhi J F, Cameron H A (2009). The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus, 19(10): 898–906
|
142 |
Snyder J S, Grigereit L, Russo A, Seib D R, Brewer M, Pickel J, Cameron H A (2016). A Transgenic Rat for Specifically Inhibiting Adult Neurogenesis. eNeuro, 3(3): e0064-16.2016 1–13
|
143 |
Snyder J S, Hong N S, McDonald R J, Wojtowicz J M (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience, 130(4): 843–852
|
144 |
Snyder J S, Soumier A, Brewer M, Pickel J, Cameron H A (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature, 476(7361): 458–461
|
145 |
Sousa N (2016). The dynamics of the stress neuromatrix. Mol Psychiatry, 21(3): 302–312
|
146 |
Sultan S, Li L, Moss J, Petrelli F, Cassé F, Gebara E, Lopatar J, Pfrieger F W, Bezzi P, Bischofberger J, Toni N (2015). Synaptic Integration of Adult-Born Hippocampal Neurons Is Locally Controlled by Astrocytes. Neuron, 88(5): 957–972
|
147 |
Surget A, Tanti A, Leonardo E D, Laugeray A, Rainer Q, Touma C, Palme R, Griebel G, Ibarguen-Vargas Y, Hen R, Belzung C (2011). Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry, 16(12): 1177–1188
|
148 |
Swaab D F, Bao A M, Lucassen P J (2005). The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev, 4(2): 141–194
|
149 |
Takamura N, Nakagawa S, Masuda T, Boku S, Kato A, Song N, An Y, Kitaichi Y, Inoue T, Koyama T, Kusumi I (2014). The effect of dopamine on adult hippocampal neurogenesis. Prog Neuropsychopharmacol Biol Psychiatry, 50: 116–124
|
150 |
Tanapat P, Galea L A, Gould E (1998). Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int J Dev Neurosci, 16(3-4): 235–239
|
151 |
Tanti A, Belzung C (2013). Neurogenesis along the septo-temporal axis of the hippocampus: are depression and the action of antidepressants region-specific? Neuroscience, 252: 234–252
|
152 |
Tanti A, Rainer Q, Minier F, Surget A, Belzung C (2012). Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology, 63(3): 374–384
|
153 |
Tasker J G (2006). Rapid glucocorticoid actions in the hypothalamus as a mechanism of homeostatic integration. Obesity (Silver Spring), 14(Suppl 5): 259S–265S
|
154 |
Toni N, Laplagne D A, Zhao C, Lombardi G, Ribak C E, Gage F H, Schinder A F (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci, 11(8): 901–907
|
155 |
Tronel S, Belnoue L, Grosjean N, Revest J M, Piazza P V, Koehl M, Abrous D N (2012). Adult-born neurons are necessary for extended contextual discrimination. Hippocampus, 22(2): 292–298
|
156 |
Ursin H, Eriksen H R (2004). The cognitive activation theory of stress. Psychoneuroendocrinology, 29(5): 567–592
|
157 |
Vallières L, Campbell I L, Gage F H, Sawchenko P E (2002). Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci, 22(2): 486–492
|
158 |
Van Bokhoven P, Oomen C A, Hoogendijk W J, Smit A B, Lucassen P J, Spijker S (2011). Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur J Neurosci, 33(10): 1833–1840
|
159 |
Van der Borght K, Meerlo P, Luiten P G, Eggen B J, Van der Zee E A (2005). Effects of active shock avoidance learning on hippocampal neurogenesis and plasma levels of corticosterone. Behav Brain Res, 157(1): 23–30
|
160 |
van Praag H, Christie B R, Sejnowski T J, Gage F H (1999a). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA, 96(23): 13427–13431
|
161 |
van Praag H, Kempermann G, Gage F H (1999b). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci, 2(3): 266–270
|
162 |
Veena J, Srikumar B N, Mahati K, Bhagya V, Raju T R, Shankaranarayana Rao B S (2009). Enriched environment restores hippocampal cell proliferation and ameliorates cognitive deficits in chronically stressed rats. J Neurosci Res, 87(4): 831–843
|
163 |
Vinkers C H, Joëls M, Milaneschi Y, Kahn R S, Penninx B W, Boks M P (2014). Stress exposure across the life span cumulatively increases depression risk and is moderated by neuroticism. Depress Anxiety, 31(9): 737–745
|
164 |
Vivar C, Potter M C, Choi J, Lee J Y, Stringer T P, Callaway E M, Gage F H, Suh H, van Praag H (2012). Monosynaptic inputs to new neurons in the dentate gyrus. Nat Commun, 3: 1107
|
165 |
Vivar C, Potter M C, van Praag H (2013). All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci, 15: 189–210
|
166 |
Vivinetto A L, Suárez M M, Rivarola M A (2013). Neurobiological effects of neonatal maternal separation and post-weaning environmental enrichment. Behav Brain Res, 240: 110–118
|
167 |
Vollmayr B, Simonis C, Weber S, Gass P, Henn F (2003). Reduced cell proliferation in the dentate gyrus is not correlated with the development of learned helplessness. Biol Psychiatry, 54(10): 1035–1040
|
168 |
Wang Q, Joels M, Swaab D F, Lucassen P J (2012). Hippocampal GR expression is increased in elderly depressed females. Neuropharmacology, 62(1): 527–533
|
169 |
Wang Q, Van Heerikhuize J, Aronica E, Kawata M, Seress L, Joels M, Swaab D F, Lucassen P J (2013). Glucocorticoid receptor protein expression in human hippocampus; stability with age. Neurobiol Aging, 34(6): 1662–1673
|
170 |
Wei Q, Hebda-Bauer E K, Pletsch A, Luo J, Hoversten M T, Osetek A J, Evans S J, Watson S J, Seasholtz A F, Akil H (2007). Overexpressing the glucocorticoid receptor in forebrain causes an aging-like neuroendocrine phenotype and mild cognitive dysfunction. J Neurosci, 27(33): 8836–8844
|
171 |
Westenbroek C, Den Boer J A, Veenhuis M, Ter Horst G J (2004). Chronic stress and social housing differentially affect neurogenesis in male and female rats. Brain Res Bull, 64(4): 303–308
|
172 |
Wilson C B, Ebenezer P J, McLaughlin L D, Francis J (2014). Predator exposure/psychosocial stress animal model of post-traumatic stress disorder modulates neurotransmitters in the rat hippocampus and prefrontal cortex. PLoS ONE, 9(2): e89104
|
173 |
Winocur G, Wojtowicz J M, Sekeres M, Snyder J S, Wang S (2006). Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus, 16(3): 296–304
|
174 |
Wojtowicz J M, Askew M L, Winocur G (2008). The effects of running and of inhibiting adult neurogenesis on learning and memory in rats. Eur J Neurosci, 27(6): 1494–1502
|
175 |
Wong E Y, Herbert J (2004). The corticoid environment: a determining factor for neural progenitors’ survival in the adult hippocampus. Eur J Neurosci, 20(10): 2491–2498
|
176 |
Wong E Y, Herbert J (2005). Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci, 22(4): 785–792
|
177 |
Wong E Y, Herbert J (2006). Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience, 137(1): 83–92
|
178 |
Wu M V, Shamy J L, Bedi G, Choi C W, Wall M M, Arango V, Boldrini M, Foltin R W, Hen R (2014). Impact of social status and antidepressant treatment on neurogenesis in the baboon hippocampus. Neuropsychopharmacology, 39(8): 1861–1871
|
179 |
Yu S, Patchev A V, Wu Y, Lu J, Holsboer F, Zhang J Z, Sousa N, Almeida O F (2010). Depletion of the neural precursor cell pool by glucocorticoids. Ann Neurol, 67(1): 21–30
|
180 |
Yun S, Donovan M H, Ross M N, Richardson D R, Reister R, Farnbauch L A, Fischer S J, Riethmacher D, Gershenfeld H K, Lagace D C, Eisch A J (2016). Stress-Induced Anxiety- and Depressive-Like Phenotype Associated with Transient Reduction in Neurogenesis in Adult Nestin-CreERT2/Diphtheria Toxin Fragment A Transgenic Mice. PLoS ONE, 11(1): e0147256
|
181 |
Zhang C L, Zou Y, He W, Gage F H, Evans R M (2008). A role for adult TLX-positive neural stem cells in learning and behaviour. Nature, 451(7181): 1004–1007
|
182 |
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660
|
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