Detrimental role of prolonged sleep deprivation on adult neurogenesis

Frontiers in Cellular Neuroscience

Volumn 9, Issue APR, 2015, Pages

  Fernandes, Carina ^a   Rocha, Nuno Barbosa F ^b   Rocha, Susana ^c   Herrera Solís, Andrea ^d   Salas Pacheco, José ^e   García García, Fabio ^f   Murillo Rodríguez, Eric ^g   Yuan, Ti Fei ^h   Machado, Sergio ^i,j   Arias Carrión, Oscar ^d  

^a UNIVERSITY OF PORTO   (Portugal)

^b POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^c POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^d INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^e UNIVERSIDAD JUÁREZ DEL ESTADO DE DURANGO   (Mexico)

^f UNIVERSIDAD VERACRUZANA   (Mexico)

^g Universidad del Mayab   (Mexico)

^h NANJING NORMAL UNIVERSITY   (China)

ⁱ FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^j SALGADO DE OLIVEIRA UNIVERSITY   (Brazil)

more..

Author keywords

Adult neurogenesis; Antidepressants; Circadian rhythms; Hippocampus; Hypnotic drugs; Sleep

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CORTICOSTEROID; CORTICOTROPIN; CYCLINE; DOPAMINE 2 RECEPTOR; ESTROGEN; GROWTH HORMONE; HYPNOTIC AGENT; INTERLEUKIN 6; KI 67 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 7; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SEROTONIN 1A RECEPTOR; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ARTICLE; AUTORADIOGRAPHY; BRAIN FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; DENTATE GYRUS; ELECTRON MICROSCOPY; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOREACTIVITY; LEARNING; MEMORY; MOOD; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; REM SLEEP DEPRIVATION; SLEEP DEPRIVATION; SLEEP WAKING CYCLE; SUBVENTRICULAR ZONE;

EID: 84927610564     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00140     Document Type: Article

References (147)

1. Abrous, D. N., Koehl, M., and Le Moal, M. (2005). Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85, 523-569. doi: 10.1152/physrev.00055.2003
2. Alvarez-Buylla, A., and Lim, D. A. (2004). For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683-686. doi: 10.1016/S0896-6273(04)00111-4
3. Arias-Carrión, O., Freundlieb, N., Oertel, W. H., and Höglinger, G. U. (2007). Adult neurogenesis and Parkinson's disease. CNS Neurol. Disord. Drug Targets 6, 326-335. doi: 10.2174/187152707783220875
4. Arias-Carrión, O., Machado, S., Paes, F., Velasques, B., Teixeira, S., Cardenas-Morales, L., et al. (2011). Is rTMS an effective therapeutic strategy that can be used to treat Parkinson's disease? CNS Neurol. Disord. Drug Targets 10, 693-702. doi: 10.2174/187152711797247821
5. Backhaus, J., Junghanns, K., Born, J., Hohaus, K., Faasch, F., and Hohagen, F. (2006). Impaired declarative memory consolidation during sleep in patients with primary insomnia: influence of sleep architecture and nocturnal cortisol release. Biol. Psychiatry 60, 1324-1330. doi: 10.1016/j.biopsych.2006.03.051
6. Banasr, M., Hery, M., Printemps, R., and Daszuta, A. (2004). Serotonin induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular. Neuropsychopharmacology 29, 450-460. doi: 10.1038/sj.npp.1300320
7. Barnea, A., and Nottebohm, F. (1994). Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl. Acad. Sci. U.S.A. 91, 11217-111221. doi: 10.1073/pnas.91.23.11217
8. Belluzzi, O., Benedusi, M., Ackman, J., and LoTurco, J. J. (2003). Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 23, 10411-10418.
9. Boldrini, M., Underwood, M. D., Hen, R., Rosoklija, G. B., Dwork, A. J., Mann, J. J., et al. (2009). Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34, 2376-2389. doi: 10.1038/npp.2009.75
10. Bolteus, A. J., and Bordey, A. (2004). GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 24, 7623-7631. doi: 10.1523/JNEUROSCI.1999-04.2004
11. Brown, J., Cooper-Kuhn, C. M., Kempermann, G., Praag, H. V., Winkler, J., Gage, F. H., et al. (2003). Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 17, 2041-2046. doi: 10.1046/j.1460-9568.2003.02647.x
12. Buckley, T. M., and Schatzberg, A. F. (2005). Review: on the interactions of the hypothalamic pituitary-adrenal (HPA) axis and sleep: normal HPA axis activity and circadian rhythm, exemplary sleep disorders. J. Clin. Endocrinol. Metab. 90, 3106-3114. doi: 10.1210/jc.2004-1056
13. Burgos, I., Richter, L., Klein, T., Fiebich, B., Feige, B., Lieb, K., et al. (2006). Increased nocturnal interleukin-6 excretion in patients with primary insomnia: a pilot study. Brain Behav. Immun. 20, 246-253. doi: 10.1016/j.bbi.2005.06.007
14. Cameron, A. H., and McKay, R. D. (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435, 406-417. doi: 10.1002/cne.1040
15. Cameron, H. A., and Gould, E. (1994). Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61, 203-209. doi: 10.1016/0306-4522(94)90224-0
16. Cao, L., Jiao, X., Zuzga, D. S., Liu, Y., Fong, D. M., Young, D., et al. (2004). VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36, 827-835. doi: 10.1038/ng1395
17. Cheng, M., Bullock, C. M., Li, C., Lee, A. G., Bermak, J. C., Belluzzi, J., et al. (2002). Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417, 405-410. doi: 10.1038/417405a
18. Claytona, N. S., Reboredab, J. C., and Kacelnikc, A. (1997). Seasonal changes of hippocampus volume in parasitic cowbirds. Behav. Processes 41, 237-243. doi: 10.1016/S0376-6357(97)00050-8
19. Conover, J. C., Doetsch, F., Garcia-Verdugo, J., and Gale, N. W. (2000). Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat. Neurosci. 3, 1091-1097. doi: 10.1038/80606
20. Crews, F. T., Miller, M. W., Ma, W., Nixon, K., Zawada, W. M., and Zakhari, S. (2003). Neural stem cells and alcohol. Alcohol. Clin. Exp. Res. 27, 324-335. doi: 10.1097/01.ALC.0000052581.46630.C5
21. Curtis, M. A., Kam, M., Nannmark, U., Anderson, M. F., Axell, M. Z., Wikkelso, C., et al. (2007). Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315, 1243-1249. doi: 10.1126/science.1136281
22. Daan, S., Beersma, D. G., and Borbély, A. A. (1984). Timing of human sleep: recovery process gated by a circadian pacemaker. Am. J. Physiol. 246, R161-R178. doi: 10.1126/science.1136281
23. Diekelmann, S., and Born, J. (2010). The memory function of sleep. Nat. Rev. Neurosci. 11, 114-126. doi: 10.1038/nrn2762
24. Dobrossy, M. D., Drapeau, E., Aurousseau, C., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2003). Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol. Psychiatry 8, 974-982. doi: 10.1038/sj.mp.4001419
25. Duman, R. S., Heninger, G. R., and Nestler, E. J. (1997). A molecular and cellular theory of depression. Arch. Gen. Psychiatry 54, 597-606. doi: 10.1001/archpsyc.1997.01830190015002
26. Duman, R. S., Malberg, J., and Nakagawa, S. (2001). Regulation of adult neurogenesis by psychotropic drugs and stress. J. Pharmacol. Exp. Ther. 299, 401-407. doi: 10.1177/1073858414561303ů7.62
27. Easton, A., Meerlo, P., Bergmann, B. M., and Turek, W. T. (2004). The suprachiasmatic nucleus regulates sleep timing and amount in mice. Sleep 27, 1307-1318.
28. Eiland, M. M., Eiland, M. M., Ramanathan, L., Gulyani, S., Gilliland, M., Bergmann, B. M., et al. (2002). Increases in amino-cupric-silver staining of the supraoptic nucleus after sleep deprivation. Brain Res. 945, 1-8. doi: 10.1111/j.1365-2869.2012.01023.x
29. Eisch, A. J., Barrot, M., Schad, C. A., Self, D. W., and Nestler, E. J. (2000). Opiates inhibit neurogenesis in the adult rat hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97, 7579-7584. doi: 10.1073/pnas.120552597
30. Enwere, E., Shingo, T., Gregg, C., Fujikawa, H., Ohta, S., and Weiss, S. (2004). Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci. 24, 8354-8365. doi: 10.1523/JNEUROSCI.2751-04.2004
31. Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A., Nordborg, C., Peterson, D. A., et al. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. doi: 10.1038/3305
32. Everson, C. A., and Crowley, W. R. (2004). Reductions in circulating anabolic hormones induced by sustained sleep deprivation in rats. Am. J. Physiol. 286, E1060-E1070. doi: 10.1152/ajpendo.00553.2003
33. Fuchs, E., and Gould, E. (2000). Mini-review: in vivo neurogenesis in the adult brain: regulation and functional implications. Eur. J. Neurosci. 12, 2211-2214. doi: 10.1046/j.1460-9568.2000.00130.x
34. Galea, L. A., and McEwen, B. S. (1999). Sex and seasonal changes in the rate of cell proliferation in the dentate gyrus of adult wild meadow voles. Neuroscience 89, 955-964. doi: 10.1016/S0306-4522(98)00345-5
35. García-García, F., De la Herrán-Arita, A. K., Juárez-Aguilar, E., Regalado-Santiago, C., Millán-Aldaco, D., Blanco-Centurión, C., et al. (2011). Growth hormone improves hippocampal adult cell survival and counteracts the inhibitory effect of prolonged sleep deprivation on cell proliferation. Brain Res. Bull. 84, 252-257. doi: 10.1016/j.brainresbull.2011.01.003
36. Gobes, S. M., Zandbergen, M. A., and Bolhuis, J. J. (2010). Memory in the making: localized brain activation related to song learning in young songbirds. Proc. Biol. Sci. 277, 3343-3351. doi: 10.1098/rspb.2010.0870
37. Goel, N., Rao, H., Durmer, J. S., and Dnges, D. F. (2009). Neurocognitive consequences of sleep deprivation. Semin. Neurol. 29, 320-339. doi: 10.1055/s-0029-1237117
38. Goldman, S. A., and Nottebohm, F. (1983). Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. U.S.A. 80, 2390-2394. doi: 10.1073/pnas.80.8.2390
39. Gould, E., Beylin, A., Tanapat, P., Reeves, A., and Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265.
40. Gould, E., and Tanapat, P. (1999). Stress and hippocampal neurogenesis. Biol. Psychiatry 46, 1472-1479. doi: 10.1016/S0006-3223(99)00247-4
41. Graves, L., Pack, A. L., and Abel, T. (2001). Sleep and memory: a molecular perspective. Trends Neurosci. 24, 237-243. doi: 10.1016/S0166-2236(00)01744-6
42. Gross, C. G. (2000). Neurogenesis in the adult brain: death of a dogma. Neuroscience 1, 67-73. doi: 10.1038/35036235
43. Guzman-Marin, R., Bashir, T., Suntsova, N., Szymusiak, R., and McGinty, D. (2007a). Hippocampal neurogenesis is reduced by sleep fragmentation in the adult rat. Neuroscience 148, 325-333. doi: 10.1016/j.neuroscience.2007.05.030
44. Guzman-Marin, R., Suntsova, N., Bashir, T., Szymusiak, R., and McGinty, D. (2007b). Cell proliferation in the dentate gyrus of the adult rat fluctuates with the light-dark cycle. Neurosci. Lett. 422, 198-201. doi: 10.1016/j.neulet.2007.06.022
45. Guzman-Marin, R., and McGinty, D. (2006). Sleep deprivation suppresses adult neurogenesis: clues to the role of sleep in brain plasticity. Sleep Biol. Rhythms 4, 27-34. doi: 10.1111/j.1479-8425.2006.00203.x
46. Guzman-Marin, R., Suntsova, N., Bashir, T., Nienhuis, R., Szymusiak, R., and McGinty, D. (2008). Rapid eye movement sleep deprivation contributes to reduction of neurogenesis in the hippocampal dentate gyrus of the adult rat. Sleep 31, 167-175.
47. Guzman-Marin, R., Suntsova, N., Methippara, M., Greiffenstein, R., Szymusiak, R., and McGinty, D. (2005). Sleep deprivation suppresses neurogenesis in the adult hippocampus of rats. Eur. J. Neurosci. 22, 2111-2116. doi: 10.1111/j.1460-9568.2005.04376.x
48. Guzmán-Marín, R., Suntsova, N., Stewart, D. R., Gong, H., Szymusiak, R., and McGinty, D. (2003). Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats. J. Physiol. 549, 563-571. doi: 10.1113/jphysiol.2003.041665
49. Guzman-Marin, R., Ying, Z., Suntsova, N., Szymusiak, R., Gomez-Pinilla, F., and McGinty, D. (2006). Suppression of hippocampal plasticity-related gene expression by sleep deprivation. J. Physiol. 575, 807-819. doi: 10.1113/jphysiol.2006.115287
50. Haack, M., Sanchez, E., and Mullington, J. M. (2007). Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers. Sleep 30, 1145-1152.
51. Hairston, H. S., Little, M. T., Scanlon, M. D., Barakat, M. T., Palmer, T. D., and Sapolsky, R. M. (2005). Sleep restriction suppresses neurogenesis induced by hippocampal learning. J. Neurophysiol. 94, 4224-4233. doi: 10.1152/jn.00218.2005
52. Hastings, N. B., and Gould, E. (1999). Rapid extension of axons into the CA3 region by adult-generated granule cells. J. Comp. Neurol. 413, 146-154. doi: 10.1002/(SICI)1096-9861(19991011)413:1<146::AID-CNE10>3.0.CO;2-B
53. Heth, G., Nevo, E., and Todrank, J. (1996). Seasonal changes in urinary odors and in responses to them by blind subterranean mole rats. Physiol. Behav. 60, 963-968. doi: 10.1016/0031-9384(96)00077-7
54. Höglinger, G. U., Huppertz, H. J., Wagenpfeil, S., Andrés, M. V., Belloch, V., León, T., et al. (2014). Tideglusib reduces progression of brain atrophy in progressive supranuclear palsy in a randomized trial. Mov. Disord. 29, 479-487. doi: 10.1002/mds.25815
55. Holmes, M. M., Galea, L. A., Mistlberger, R. E., and Kempermann, G. (2004). Adult hippocampal neurogenesis and voluntary running activity: circadian and dose-dependent effects. J. Neurosci. Res. 76, 216-222. doi: 10.1002/jnr.20039
56. Hu, H., Tomasiewicz, H., Magnuson, T., and Rutishauser, U. (1996). The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16, 735-743. doi: 10.1016/S0896-6273(00)80094-X
57. Imeri, L., and Opp, M. R. (2009). How (and why) the immune system makes us sleep. Nat. Rev. Neurosci. 10, 199-210. doi: 10.1038/nrn2576
58. Irwin, M. R., Wang, M., Campomayor, C. O., Collado-Hidalgo, A., and Cole, S. (2006). Sleep deprivation and activation of morning levels of cellular and genomic markers. Arch. Intern. Med. 166, 1756-1762. doi: 10.1001/archinte.166.16.1756
59. Ishida, A., Mutoh, T., Ueyama, T., Bando, H., Masubuchi, S., Nakahara, D., et al. (2005). Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab. 2, 297-307. doi: 10.1016/j.cmet.2005.09.009
60. Jacobs, B. L., van Praag, H., and Gage, F. H. (2000). Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol. Psychiatry 5, 262-269. doi: 10.1038/sj.mp.4000712
61. Jin, K., Sun, Y., Xie, L., Batteur, S., Mao, X. O., Smelick, C., et al. (2003). Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2, 175-183. doi: 10.1046/j.1474-9728.2003.00046.x
62. Juneka, A., Rusakb, B., and Sembaa, K. (2010). Short-term sleep deprivation may alter the dynamics of hippocampal cell proliferation in adult rats. Neuroscience 170, 1140-1152. doi: 10.1016/j.neuroscience.2010.08.018
63. Kaplan, M. S. (1977). Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197, 1092-1094. doi: 10.1126/science.887941
64. Kaplan, M. S. (1981). Neurogenesis in the 3-month-old rat visual cortex. J. Comp. Neurol. 195, 323-338. doi: 10.1002/cne.901950211
65. Kaplan, M. S. (1984). Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J. Neurosci. 4, 1429-1441.
66. Kaplan, M. S. (1985). Formation and turnover of neurons in young and senescent animals: an electronmicroscopic and morphometric analysis. Ann. N. Y. Acad. Sci. 457, 173-192. doi: 10.1111/j.1749-6632.1985.tb20805.x
67. Keisler, A., and Willingham, J. A. (2007). Time of day accounts for overnight improvement in sequence learning. Learn. Mem. 14, 669-672. doi: 10.1101/lm.751807
68. Kempermann, G. (2002). Regulation of adult hippocampal neurogenesis implications for novel theories of major depression. Bipolar Disord. 4, 17-33. doi: 10.1034/j.1399-5618.2002.40101.x
69. Kempermann, G., and Gage, F. H. (2002). Genetic influence on phenotypic differentiation in adult hippocampal neurogenesis. Brain Res. Dev. Brain Res. 134, 1-12. doi: 10.1016/S0165-3806(01)00224-3
70. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495. doi: 10.1038/386493a0
71. Kochman, L. J., Weber, E. T., Fornal, C. A., and Jacobs, B. L. (2006). Circadian variation in mouse hippocampal cell proliferation. Neurosci. Lett. 406, 256-259. doi: 10.1016/j.neulet.2006.07.058
72. Kornack, D. R., and Rakic, P. (1999). Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl. Acad. Sci. U.S.A. 96, 5768-5773. doi: 10.1073/pnas.96.10.5768
73. Krueger, J. M., Rector, D. M., Roy, S., Van Dongen, H. P., Belenky, G., and Panksepp, J. (2008). Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 9, 910-919. doi: 10.1038/nrn2521
74. Kuhn, H. G., Dickinson-Anson, H., and Gage, F. H. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci. 16, 2027-2033.
75. Lavenex, P., Steele, M. A., and Jacobs, L. F. (2000). The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. Eur. J. Neurosci. 12, 643-648. doi: 10.1046/j.1460-9568.2000.00949.x
76. Leuner, B., Gould, E., and Shors, T. J. (2006). Is there a link between adult neurogenesis and learning?Hippocampus 16, 216-224. doi: 10.1002/hipo.20153
77. Lim, D. A., Tramontin, A. D., Trevejo, J. M., Herrera, D. G., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2000). Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726. doi: 10.1016/S0896-6273(00)00148-3
78. Mahajan, M. A., Das, S., Zhu, H., Tomic-Canic, M., and Samuels, H. H. (2004). The nuclear hormone receptor coactivator NRC is a pleiotropic modulator affecting growth, development, apoptosis, reproduction, and wound repair. Mol. Cell. Biol. 24, 4994-5004. doi: 10.1128/MCB.24.11.4994-5004.2004
79. Malberg, J. E., Eisch, A. J., Nestler, E. J., and Duman, R. S. (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104-9110.
80. Manganas, L. N., Zhang, X., Li, Y., Hazel, R. D., Smith, S. D., Wagshul, M. E., et al. (2007). Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 318, 980-985. doi: 10.1126/science.1147851
81. Maywood, E. S., Reddy, A. B., Wong, G. K., O'Neill, J. S., O'Brien, J. A., McMahon, D. G., et al. (2006). Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr. Biol. 16, 599-605. doi: 10.1016/j.cub.2006.02.023
82. Meerlo, P., Mistlberger, R. E., Jacobs, B. L., Heller, C., and McGinty, D. (2009). New neurons in the adult brain: the role of sleep and consequences of sleep loss. Sleep Med. Rev. 13, 187-194. doi: 10.1016/j.smrv.2008.07.004
83. Ming, G. L., and Song, H. (2005). Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223-250. doi: 10.1146/annurev.neuro.28.051804.101459
84. Mirescu, C., Peters, J. D., Noiman, L., and Gould, E. (2006). Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids. Proc. Natl. Acad. Sci. U.S.A. 103, 19170-19175. doi: 10.1073/pnas.0608644103
85. Monje, M. L., Toda, H., and Palmer, T. D. (2003). Inflammatory blockade restores adult hippocampal neurogenesis. Scienc 302, 1760-1765. doi: 10.1126/science.1088417
86. Moore, R. Y., Speh, J. C., and Leak, R. K. (2002). Suprachiasmatic nucleus organization. Cell Tissue Res. 309, 89-98. doi: 10.1007/s00441-002-0575-2
87. Moser, M. B., and Moser, E. I. (1998). Functional differentiation in the hippocampus. Hippocampus 8, 608-619. doi: 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7
88. Mueller, A. D., Mear, R. J., and Mistlberger, R. E. (2011). Inhibition of hippocampal neurogenesis by sleep deprivation is independent of circadian disruption and melatonin suppression. Neuroscience 193, 170-181. doi: 10.1016/j.neuroscience.2011.07.019
89. Mueller, A. D., Meerlo, P., McGinty, D., and Mistlberger, R. E. (2013). "Sleep and adult neurogenesis: implications for cognition and mood," in Current Topics in Behavioral Neurosciences, eds M. A. Geyer, B. A. Ellenbroek, C. A. Marsden, and Th.R.E. Barnes (Heidelberg: Springer), 1-31.
90. Mueller, A. D., Pollock, M. S., Lieblich, S. E., Epp, J. R., Galea, L. A., and Mistlberger, R. E. (2008). sleep deprivation can inhibit adult hippocampal neurogenesis independent of adrenal stress hormones. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1693-R1703. doi: 10.1152/ajpregu.00858.2007
91. Murase, S., and Horwitz, A. F. (2002). Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J. Neurosci. 22, 3568-3579.
92. Murillo-Rodríguez, E., Arias-Carrión, O., Sanguino-Rodríguez, K., González-Arias, M., and Haro, R. (2009). Mechanisms of sleep-wake cycle modulation. CNS Neurol. Disord. Drug Targets 8, 245-253. doi: 10.1016/j.expneurol.2011.02.020
93. Neylan, T. C., Mueller, S. G., Wang, Z., Metzler, T. J., Lenoci, M., and Truran, D. (2010). Insomnia severity is associated with a decreased volume of the CA3/dentate gyrus hippocampal subfield. Biol. Psychiatry 494-496. doi: 10.1016/j.neuroscience.2011.07.019
94. Nibuya, M., Morinobu, S., and Duman, R. S. (1995). Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 15, 7539-7547.
95. Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O., and Eriksson, P. S. (1999). Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J. Neurobiol. 39, 569-578. doi: 10.1002/(SICI)1097-4695(19990615)39:4<569::AID-NEU10>3.0.CO;2-F
96. Nissen, C., Kloepfer, C., Nofzinger, E., Feige, B., Voderholzer, U., and Riemann, D. (2006). Impaired sleep-related memory consolidation in primary insomnia: a pilot study. Sleep 29, 1068-1073.
97. Nofzinger, E. A., Nissen, C., Germain, A., Moul, D., Hall, M., Price, J. C., et al. (2006). Regional cerebral metabolic correlates of WASO during NREMS sleep in insomnia. J. Clin. Sleep Med. 2, 316-322.
98. Novati, A., Hulshof, H. J., Koolhaas, J. M., Lucassenc, P. J., and Meerlo, P. (2011). Chronic sleep restriction causes a decrease in hippocampal volume in adolescent rats, which is not explained by changes in glucocorticoid levels or neurogenesis. Neuroscience 190, 145-155. doi: 10.1016/j.neuroscience.2011.06.027
99. Novati, A., Roman, V., Cetin, T., Hagewoud, R., Boer, J. A., Luiten, P. G., et al. (2008). Chronically restricted sleep leads to depression-like changes in neurotransmitter receptor sensitivity and neuroendocrine stress reactivity in rats. Sleep 31, 1579-1585.
100. Nowakowski, R. S., Lewin, S. B., and Miller, M. W. (1989). Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol. 18, 311-318. doi: 10.1007/BF01190834
101. Opp, M. R. (2009). Sleeping to fuel the immune system: mammalian sleep and resistance to parasites. BMC Evol. Biol. 9:8. doi: 10.1186/1471-2148-9-8
102. Orban, P., Rauchs, G., Balteau, E., Degueldre, C., Luxen, A., Maquet, P., et al. (2006). Sleep after spatial learning promotes covert reorganization of brain activity. Proc. Natl. Acad. Sci. U.S.A. 103, 7124-7129. doi: 10.1073/pnas.0510198103
103. Ormerod, B. K., and Galea, L. A. (2003). Reproductive status influences the survival of new cells in the dentate gyrus of adult male meadow voles. Neurosci. Lett. 346, 25-28. doi: 10.1016/S0304-3940(03)00546-9
104. Peigneux, P., Laureys, S., Fuchs, S., Collette, F., Perrin, F., Reggers, J., et al. (2004). Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535-545. doi: 10.1016/j.neuron.2004.10.007
105. Price, J., Turner, D., and Cepko, C. (1987). Lineage analysis in the vertebrate nervous system by retrovirus-mediated gene transfer. Proc. Natl. Acad. Sci. U.S.A. 84, 156-160. doi: 10.1073/pnas.84.1.156
106. Radley, J. J., and Jacobs, B. L. (2002). 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res. 955, 264-267. doi: 10.1016/S0006-8993(02)03477-7
107. Rasch, B., Pommer, J., Diekelmann, S., and Born, J. (2008). Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat. Neurosci. 12, 396-397. doi: 10.1038/nn.2206
108. Rector, D. M., Topchiy, I. A., Carter, K. M., and Rojas, M. J. (2005). Local functional state differences between rat cortical. Brain Res. 1047, 45-55. doi: 10.1016/j.brainres.2005.04.002
109. Rickard, T. C., Cai, D. J., Rieth, C. A., Jones, J., and Ard, M. C. (2008). Sleep does not enhance motor sequence learning. J. Exp. Psychol. Learn. Mem. Cogn. 34, 834-842. doi: 10.1037/0278-7393.34.4.834
110. Riemann, D., Voderholzer, U., Spiegelhalder, K., Psych, D., Hornyak, M., Buysse, D. J., et al. (2007). Chronic insomnia and MRI-measured hippocampal volume: a pilot study. Sleep 30, 955-985.
111. Roman, V., van der Borght, K., Leemburg, S., van der Zee, E. A., and Meerlo, P. (2005). Sleep restriction by forced activity reduces hippocampal cell proliferation. Brain Res. 1065, 53-59. doi: 10.1016/j.brainres.2005.10.020
112. Roy, S., Krueger, J. M., Rector, D. M., and Wan, Y. (2008). A Network model for activity-dependent sleep regulation. J. Theor. Biol. 253, 462-468. doi: 10.1016/j.jtbi.2008.03.033
113. Ruehland, W. R., O'Donoghue, F. J., Pierce, R. J., Thornton, A. T., Singh, P., Copland, J. M., et al. (2011). The 2007 AASM recommendations for EEG electrode placement in polysomnography: impact on sleep and cortical arousal scoring. Sleep 34, 73-81.
114. Saghatelyan, A., Chevigny, A., Schachner, M., and Lledo, P. M. (2004). Tenascin-R mediates activitydependent recruitment of neuroblasts in the adult mouse forebrain. Nat. Neurosci. 7, 347-356. doi: 10.1038/nn1211
115. Sahay, A., and Hen, R. (2007). Adult hippocampal neurogenesis in depression. Nat. Neurosci. 10, 1110-1115. doi: 10.1038/nn1969
116. Sahu, S., Kauser, H., Ray, K., Kishore, K., Kumar, S., and Panjwani, U. (2013). Caffeine and modafinil promote adult neuronal cell proliferation during 48 h of total sleep deprivation in rat dentate gyrus. Exp. Neurol. 248, 470-481. doi: 10.1016/j.expneurol.2013.07.021
117. Sakamotoa, M., Imayoshia, I., Ohtsukaa, T., Yamaguchie, M., Morie, K., and Kageyamaa, R. (2011). Continuous neurogenesis in the adult forebrain is required for innate olfactory. Proc. Natl. Acad. Sci. U.S.A. 108, 8479-8484. doi: 10.1073/pnas.1018782108
118. Sanes, J. R., Rubenstein, J. L., and Nicolas, J. F. (1986). Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 5, 3133-3142.
119. Saper, C. B., Chou, T. C., and Scammell, T. E. (2001). The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 24, 726-731. doi: 10.1016/S0166-2236(00)02002-6
120. Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., and Croll, S. (2005). Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192, 348-356. doi: 10.1016/j.expneurol.2004.11.016
121. Shapiro, E. M., Gonzalez-Perez, O., García-Verdugo, J. M., Alvarez-Buylla, A., and Koretsky, A. P. (2006). Magnetic resonance imaging of the migration ofneuronal precursors generated in the adult rodent brain. Neuroimage 32, 1150-1157. doi: 10.1016/j.neuroimage.2006.04.219
122. Sheth, B. R., Nguyen, N., and Janvelyan, D. (2009). Does sleep really influence face recognition memory? PLoS ONE 4:e5496. doi: 10.1371/journal.pone.0005496
123. Sidman, R. L., Miale, I. L., and Feder, N. (1959). Cell proliferation and migration in the primitive ependymal zone; an autoradiographic study of histogenesis in the nervous system. Exp. Neurol. 1, 322-333. doi: 10.1016/0014-4886(59)90024-X
124. Siegel, J. M. (2001). The REM sleep-memory consolidation hypothesis. Science 294, 1058-1063. doi: 10.1126/science.1063049
125. Siegel, J. M. (2009). Sleep viewed as a state of adaptive inactivity. Nat. Rev. Neurosci. 10, 747-753. doi: 10.1038/nrn2697
126. Smulders, T. V., Shiflett, M. W., Sperling, A. J., and DeVoogd, T. J. (2000). Seasonal changes in neuron numbers in the hippocampal formation of a food-hoarding bird: the black-capped chickadee. J. Neurobiol. 44, 414-22. doi: 10.1002/1097-4695(20000915)44
127. Song, S., Howard, J. H., and Howard, D. V. (2007). Sleep does not benefit probabilistic motor sequence learning. J. Neurosci. 27, 12475-12483. doi: 10.1523/JNEUROSCI.2062-07.2007
128. Sportiche, N., Suntsova, N., Methippara, M., Bashir, T., Mitrani, B., Szymusiak, R., et al. (2010). Sustained sleep fragmentation results in delayed changes in hippocampal-dependent cognitive function associated with reduced dentate gyrus neurogenesis. Neuroscience 170, 247-258. doi: 10.1016/j.neuroscience.2010.06.038
129. Stickgold, R. (2005). Sleep-dependent memory consolidation. Nature 437, 1272-1278. doi: 10.1038/nature04286
130. Stickgold, R., and Walker, M. P. (2005). Memory consolidation and reconsolidation: what is the role of sleep?Trends Neurosci. 28, 408-415. doi: 10.1016/j.tins.2005.06.004
131. Takahashi, J., Palmer, T. D., and Gage, F. H. (1998). Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural cell cultures. J. Neurobiol. 38, 65-81. doi: 10.1002/(SICI)1097-4695(199901)38
132. Takase, L. F., Fornal, C. A., and Jacobs, B. L. (2009). Effects of the hypnotic drug zolpidem on cell proliferation and survival in the dentate gyrus of young and old rats. Brain Res. 1259, 26-31. doi: 10.1016/j.brainres.2008.12.049
133. Tamai, S., Sanada, K., and Fukada, Y. (2008). Time-of-Day-Dependent enhancement of adult neurogenesis in the hippocampus. PLoS ONE 3:e3835. doi: 10.1371/journal.pone.0003835
134. Tanapat, P., Hastings, N. B., Reeves, A. J., and Gould, E. (1999). Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19, 5792-5801.
135. Tramontin, A. D., and Brenowitz, E. A. (2000). Seasonal plasticity in the adult brain. Trends Neurosci. 23, 251-258. doi: 10.1016/S0166-2236(00)01558-7
136. Trejo, J. L., Carro, E., and Torres-Aleman, I. (2001). Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J. Neurosci. 21, 1628-1634.
137. Tung, A., Takase, L., Fornal, C., and Jacobs, B. (2005). Effects of sleep deprivation and recovery sleep upon cell proliferation in adult rat dentate gyrus. Neuroscience 134, 721-723. doi: 10.1016/j.neuroscience.2005.06.008
138. van der Borght, K., Ferrari, F., Klauke, K., Roman, V., Havekes, R., Sgoifo, A., et al. (2006). Hippocampal cell proliferation across the day: increase by running wheel activity but no effect of sleep and wakefulness. Behav. Brain Res. 167, 36-41. doi: 10.1016/j.bbr.2005.08.012
139. van Praag, H., Kempermann, G., and Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270. doi: 10.1038/6368
140. van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030-1034. doi: 10.1038/4151030a
141. Walton, J. C., Pyter, L. M., Weil, Z. M., and Nelson, R. J. (2012). Photoperiod mediated changes in olfactory bulb neurogenesis and olfactory behavior in male white-footed mice (Peromyscus leucopus). PLoS ONE 8:e42743. doi: 10.1371/journal.pone.0042743
142. Wang, S., Scott, B. W., and Wojtowicz, J. M. (2000). Heterogenous properties of dentate granule neurons in the adult rat. J. Neurobiol. 42, 248-257. doi: 10.1002/(SICI)1097-4695(20000205)42
143. Wang, W., Pan, Y. W., Wietecha, T., Zou, J., Abel, G. M., Kuo, C. T., et al. (2013). Extracellular signal-regulated kinase 5 (ERK5) mediates prolactin-stimulated adult neurogenesis in the subventricular zone and olfactory bulb. J. Biol. Chem. 288, 2623-2631. doi: 10.1074/jbc.M112.401091
144. Warner-Schmidt, J. L., and Duman, R. S. (2007). VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. U.S.A. 104, 4647-4652. doi: 10.1073/pnas.0610282104
145. Yuan, T. F., and Arias-Carrion, O. (2011). Adult neurogenesis in the hypothalamus: evidence, functions, and implications. CNS Neurol. Disord. Drug Targets 10, 433-439. doi: 10.2174/187152711795563985
146. Yuan, T. F., Li, J., Ding, F., and Arias-Carrion, O. (2014). Evidence of adult neurogenesis in non-human primates and human. Cell Tissue Res. 358, 17-23. doi: 10.1007/s00441-014-1980-z
147. Zucconi, G. G., Cipriani, S., Balgkouranidou, I., and Scattoni, R. (2006). 'One night' sleep deprivation stimulates hippocampal neurogenesis. Brain Res. Bull. 69, 375-381. doi: 10.1016/j.brainresbull.2006.01.009