[en] The process of neurogenesis has been demonstrated to occur throughout life in the subgranular zone (SGZ) of the hippocampal dentate gyrus of several mammals, including humans. The basal rate of adult hippocampal neurogenesis can be altered by lifestyle and environmental factors. In this perspective review, the evidence for sleep as a modulator of adult hippocampal neurogenesis is first summarized. Following this, the impacts of sleep and sleep disturbances on hippocampal-dependent functions, including learning and memory, and depression are critically evaluated. Finally, we postulate that the effects of sleep on hippocampal-dependent functions may possibly be mediated by a change in adult hippocampal neurogenesis. This could provide a route to new treatments for cognitive impairments and psychiatric disorders.
Abel, T., Havekes, R., Saletin, J. M., and Walker, M. P. (2013). Sleep, plasticity and memory from molecules to whole-brain networks. Curr. Biol. 23, R774-R788. doi: 10.1016/j.cub.2013.07.025
Aimone, J. B., Li, Y., Lee, S. W., Clemenson, G. D., Deng, W., and Gage, F. H. (2014). Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev. 94, 991-1026. doi: 10.1152/physrev.00004.2014
Altman, J. (1969). Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J. Comp. Neurol. 137, 433-457.
Altman, J., and Das, G. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319-335. doi: 10.1002/cne.901240303
Anacker, C., and Hen, R. (2017). Adult hippocampal neurogenesis and cognitive flexibility [mdash] linking memory and mood. Nat. Rev. Neurosci. 18, 335-346. doi: 10.1038/nrn.2017.45
Anacker, C., Zunszain, P. A., Cattaneo, A., Carvalho, L. A., Garabedian, M. J., Thuret, S., et al. (2011). Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol. Psychiatry 16, 738-750. doi: 10.1038/mp.2011.26
Asnis, G. M., Chakraburtty, A., DuBoff, E. A., Krystal, A., Londborg, P. D., Rosenberg, R., et al. (1999). Zolpidem for persistent insomnia in SSRI-treated depressed patients. J. Clin. Psychiatry 60, 668-676. doi: 10.4088/JCP.v60n1005
Aton, S. J., Suresh, A., Broussard, C., and Frank, M. G. (2014). Sleep promotes cortical response potentiation following visual experience. Sleep 37, 1163-1170. doi: 10.5665/sleep.3830
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
Baglioni, C., Nanovska, S., Regen, W., Spiegelhalder, K., Feige, B., Nissen, C., et al. (2016). Sleep and mental disorders: a meta-analysis of polysomnographic research. Psychol. Bull. 142, 969-990. doi: 10.1037/bul0000053
Beason-Held, L. L., Rosene, D. L., Killiany, R. J., and Moss, M. B. (1999). Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 9, 562-574. doi: 10.1002/(SICI)1098-1063(1999)9:5<562::AID-HIPO10>3.0.CO;2-X
Besnard, A., and Sahay, A. (2016). Adult hippocampal neurogenesis, fear generalization, and stress. Neuropsychopharmacology 41, 24-44. doi: 10.1038/npp.2015.167
Boldrini, M., Underwood, M. D., Hen, R., Rosoklija, G. B., Dwork, A. J., John Mann, J., et al. (2009). Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34, 2376-2389. doi: 10.1038/npp.2009.75
Borgs, L., Beukelaers, P., Vandenbosch, R., Nguyen, L., Moonen, G., Maquet, P., et al. (2009). Period 2 regulates neural stem/progenitor cell proliferation in the adult hippocampus. BMC Neurosci. 10:30. doi: 10.1186/1471-2202-10-30
Boyce, R., Glasgow, S. D., Williams, S., and Adamantidis, A. (2016). Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation. Science 352, 812-816. doi: 10.1126/science.aad5252
Bragin, A., Jando, G., Nadasdy, Z., van Landeghem, M., and Buzsaki, G. (1995). Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J. Neurophysiol. 73, 1691-1705.
Bremner, J. D., and Vermetten, E. (2004). Neuroanatomical changes associated with pharmacotherapy in posttraumatic stress disorder. Ann. N. Y. Acad. Sci. 1032, 154-157. doi: 10.1196/annals.1314.012
Brooke, S. M., de Haas-Johnson, A. M., Kaplan, J. R., Manuck, S. B., and Sapolsky, R. M. (1994). Dexamethasone resistance among nonhuman primates associated with a selective decrease of glucocorticoid receptors in the hippocampus and a history of social instability. Neuroendocrinology 60, 134-140. doi: 10.1159/000126743
Brown, J., Cooper-Kuhn, C. M., Kempermann, G., Van Praag, H., Winkler, J., Gage, F. H., et al. (2003). Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 17, 2042-2046. doi: 10.1046/j.1460-9568.2003.02647.x
Buzsaki, G. (1989). Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31, 551-570. doi: 10.1016/0306-4522(89)90423-5
Buzsaki, G., Haas, H. L., and Anderson, E. G. (1987). Long-term potentiation induced by physiologically relevant stimulus patterns. Brain Res. 435, 331-333. doi: 10.1016/0006-8993(87)91618-0
Buzsaki, G., and Silva, F. L. (2012). High frequency oscillations in the intact brain. Progr. Neurobiol. 98, 241-249. doi: 10.1016/j.pneurobio.2012.02.004
Cameron, H. A., 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
Campbell, S., Marriott, M., Nahmias, C., and MacQueen, G. M. (2004). Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am. J. Psychiatry 161, 598-607. doi: 10.1176/appi.ajp.161.4.598
Chen, G., Rajkowska, G., Du, F., Seraji-Bozorgzad, N., and Manji, H. K. (2000). Enhancement of hippocampal neurogenesis by lithium. J. Neurochem. 75, 1729-1734. doi: 10.1046/j.1471-4159.2000.0751729.x
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D. Jr., Fragniere, A., Tyers, P., et al. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213. doi: 10.1126/science.1173215
Coe, C. L., Kramer, M., Czeh, B., Gould, E., Reeves, A. J., Kirschbaum, C., et al. (2003). Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol. Psychiatry 54, 1025-1034. doi: 10.1016/S0006-3223(03)00698-X
Cole, M. G., and Dendukuri, N. (2003). Risk factors for depression among elderly community subjects: a systematic review and meta-analysis. Am. J. Psychiatry 160, 1147-1156. doi: 10.1176/appi.ajp.160.6.1147
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
Czeh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., et al. (2001). Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl. Acad. Sci. U.S.A. 98, 12796-12801. doi: 10.1073/pnas.211427898
Dale, E., Pehrson, A. L., Jeyarajah, T., Li, Y., Leiser, S. C., Smagin, G., et al. (2016). Effects of serotonin in the hippocampus: how SSRIs and multimodal antidepressants might regulate pyramidal cell function. CNS Spectr. 21, 143-161. doi: 10.1017/S1092852915000425
Daumas, S., Halley, H., Frances, B., and Lassalle, J. M. (2005). Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CA1 hippocampal subregions. Learn. Mem. 12, 375-382. doi: 10.1101/lm.81905
David, D. J., Samuels, B. A., Rainer, Q., Wang, J. W., Marsteller, D., Mendez, I., et al. (2009). Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493. doi: 10.1016/j.neuron.2009.04.017
Deng, W., Aimone, J. B., and Gage, F. H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350. doi: 10.1038/nrn2822
Diamond, D. M., Park, C. R., Heman, K. L., and Rose, G. M. (1999). Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9, 542-552. doi: 10.1002/(SICI)1098-1063(1999)9:5<542::AID-HIPO8>3.0.CO;2-N
Diekelmann, S., and Born, J. (2010). The memory function of sleep. Nat. Rev. Neurosci. 11, 114-126. doi: 10.1038/nrn2762
Dijk, D. J. (2009). Regulation and functional correlates of slow wave sleep. J. Clin. Sleep Med. 5, S6-15.
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
Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2003). Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 14385-14390. doi: 10.1073/pnas.2334169100
Dupret, D., Fabre, A., Dobrossy, M. D., Panatier, A., Rodriguez, J. J., Lamarque, S., et al. (2007). Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol. 5:e214. doi: 10.1371/journal.pbio.0050214
Egeland, M., Guinaudie, C., Du Preez, A., Musaelyan, K., Zunszain, P. A., Fernandes, C., et al. (2017). Depletion of adult neurogenesis using the chemotherapy drug temozolomide in mice induces behavioural and biological changes relevant to depression. Transl. Psychiatry 7:e1101. doi: 10.1038/tp.2017.68
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
Eisch, A. J., and Petrik, D. (2012). Depression and hippocampal neurogenesis: a road to remission? Science 338, 72-75. doi: 10.1126/science.1222941
Epp, J. R., Silva Mera, R., Kohler, S., Josselyn, S. A., and Frankland, P. W. (2016). Neurogenesis-mediated forgetting minimizes proactive interference. Nat. Commun. 7:10838. doi: 10.1038/ncomms10838
Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., et al. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317. doi: 10.1038/3305
Ernst, A., Alkass, K., Bernard, S., Salehpour, M., Perl, S., Tisdale, J., et al. (2014). Neurogenesis in the striatum of the adult human brain. Cell 156, 1072-1083. doi: 10.1016/j.cell.2014.01.044
Fernandes, C., Rocha, N. B., Rocha, S., Herrera-Solis, A., Salas-Pacheco, J., Garcia-Garcia, F., et al. (2015). Detrimental role of prolonged sleep deprivation on adult neurogenesis. Front. Cell. Neurosci. 9:140. doi: 10.3389/fncel.2015.00140
Frank, M. G. (2013). “Astroglial regulation of sleep,” in The Genetic Basis of Sleep and Sleep Disorders, eds M. T. Paul Shaw and J. Michael Thorpy (Cambridge, UK: Cambridge University Press), 84-91.
Frank, M. G., and Cantera, R. (2014). Sleep, clocks, and synaptic plasticity. Trends Neurosci. 37, 491-501. doi: 10.1016/j.tins.2014.06.005
Frodl, T., Meisenzahl, E. M., Zetzsche, T., Born, C., Groll, C., Jager, M., et al. (2002). Hippocampal changes in patients with a first episode of major depression. Am. J. Psychiatry 159, 1112-1118. doi: 10.1176/appi.ajp.159.7.1112
Fuss, J., Ben Abdallah, N. M., Hensley, F. W., Weber, K. J., Hellweg, R., and Gass, P. (2010). Deletion of running-induced hippocampal neurogenesis by irradiation prevents development of an anxious phenotype in mice. PLoS ONE 5:e12769. doi: 10.1371/journal.pone.0012769
Garcia-Garcia, F., De la Herran-Arita, A. K., Juarez-Aguilar, E., Regalado-Santiago, C., Millan-Aldaco, D., Blanco-Centurion, 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
Gery, S., Komatsu, N., Baldjyan, L., Yu, A., Koo, D., and Koeffler, H. P. (2006). The circadian gene per1 plays an important role in cell growth and DNA damage control in human cancer cells. Mol. Cell 22, 375-382. doi: 10.1016/j.molcel.2006.03.038
Gibson, E. M., Wang, C., Tjho, S., Khattar, N., and Kriegsfeld, L. J. (2010). Experimental ‘jet lag’ inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters. PLoS ONE 5:e15267. doi: 10.1371/journal.pone.0015267
Giedke, H., and Schwarzler, F. (2002). Therapeutic use of sleep deprivation in depression. Sleep Med. Rev. 6, 361-377. doi: 10.1053/smrv.2002.0235
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsaki, G., and Zugaro, M. B. (2009). Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222-1223. doi: 10.1038/nn.2384
Goergen, E. M., Bagay, L. A., Rehm, K., Benton, J. L., and Beltz, B. S. (2002). Circadian control of neurogenesis. J. Neurobiol. 53, 90-95. doi: 10.1002/neu.10095
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
Gonçalves, J. T., Schafer, S. T., and Gage, F. H. (2016). Adult neurogenesis in the hippocampus: from stem cells to behavior. Cell 167, 897-914. doi: 10.1016/j.cell.2016.10.021
Gould, E., Tanapat, P., Hastings, N. B., and Shors, T. J. (1999). Neurogenesis in adulthood: a possible role in learning. Trends Cogn. Sci. 3, 186-192. doi: 10.1016/S1364-6613(99)01310-8
Grassi Zucconi, 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
Gross, C. G. (2000). Neurogenesis in the adult brain: death of a dogma. Nat. Rev. Neurosci. 1, 67-73. doi: 10.1038/35036235
Guzman-Marin, R., Bashir, T., Suntsova, N., Szymusiak, R., and McGinty, D. (2007). Hippocampal neurogenesis is reduced by sleep fragmentation in the adult rat. Neuroscience 148, 325-333. doi: 10.1016/j.neuroscience.2007.05.030
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. doi: 10.1093/sleep/31.2.167
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
Guzman-Marin, 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
Hagewoud, R., Havekes, R., Novati, A., Keijser, J. N., Van der Zee, E. A., and Meerlo, P. (2010). Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation. J. Sleep Res. 19, 280-288. doi: 10.1111/j.1365-2869.2009.00799.x
Hahn, T. T., Sakmann, B., and Mehta, M. R. (2007). Differential responses of hippocampal subfields to cortical up-down states. Proc. Natl. Acad. Sci. U.S.A. 104, 5169-5174. doi: 10.1073/pnas.0700222104
Hairston, I. S., Little, M. T., Scanlon, M. D., Barakat, M. T., Palmer, T. D., Sapolsky, R. M., et al. (2005). Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J. Neurophysiol. 94, 4224-4233. doi: 10.1152/jn.00218.2005
Hajek, T., Kozeny, J., Kopecek, M., Alda, M., and Hoschl, C. (2008). Reduced subgenual cingulate volumes in mood disorders: a meta-analysis. J. Psychiatry Neurosci. 33, 91-99.
Halassa, M. M., Florian, C., Fellin, T., Munoz, J. R., Lee, S. Y., Abel, T., et al. (2009). Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61, 213-219. doi: 10.1016/j.neuron.2008.11.024
Hamilton, M. (1989). Frequency of symptoms in melancholia (depressive illness). Br. J. Psychiatry 154, 201-206. doi: 10.1192/bjp.154.2.201
Harvey, A. G. (2011). Sleep and circadian functioning: critical mechanisms in the mood disorders? Annu. Rev. Clin. Psychol. 7, 297-319. doi: 10.1146/annurev-clinpsy-032210-104550
Havekes, R., Park, A. J., Tolentino, R. E., Bruinenberg, V. M., Tudor, J. C., Lee, Y., et al. (2016). Compartmentalized PDE4A5 signaling impairs hippocampal synaptic plasticity and long-term memory. J. Neurosci. 36, 8936-8946. doi: 10.1523/JNEUROSCI.0248-16.2016
Havekes, R., and Abel, T. (2017). The tired hippocampus: the molecular impact of sleep deprivation on hippocampal function. Curr. Opin. Neurobiol. 44, 13-19. doi: 10.1016/j.conb.2017.02.005
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
Jayatissa, M. N., Henningsen, K., West, M. J., and 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. doi: 10.1016/j.brainres.2009.07.001
Jilg, A., Lesny, S., Peruzki, N., Schwegler, H., Selbach, O., Dehghani, F., et al. (2010). Temporal dynamics of mouse hippocampal clock gene expression support memory processing. Hippocampus 20, 377-388. doi: 10.1002/hipo.20637
Josselyn, S. A., Kohler, S., and Frankland, P. W. (2015). Finding the engram. Nat. Rev. Neurosci. 16, 521-534. doi: 10.1038/nrn4000
Junek, A., Rusak, B., and Semba, 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
Karlsson, M. P., and Frank, L. M. (2009). Awake replay of remote experiences in the hippocampus. Nat. Neurosci. 12, 913-918. doi: 10.1038/nn.2344
Kee, N., Teixeira, C. M., Wang, A. H., and Frankland, P. W. (2007). Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10, 355-362. doi: 10.1038/nn1847
Kempermann, G. (2008). The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci. 31, 163-169. doi: 10.1016/j.tins.2008.01.002
Kempermann, G., Krebs, J., and Fabel, K. (2008). The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr. Opin. Psychiatry 21, 290-295. doi: 10.1097/YCO.0b013e3282fad375
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
Kodama, M., Fujioka, T., and Duman, R. S. (2004). Chronic olanzapine or fluoxetine administration increases cell proliferation in hippocampus and prefrontal cortex of adult rat. Biol. Psychiatry 56, 570-580. doi: 10.1016/j.biopsych.2004.07.008
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
Kott, J., Leach, G., and Yan, L. (2012). Direction-dependent effects of chronic “jet-lag” on hippocampal neurogenesis. Neurosci. Lett. 515, 177-180. doi: 10.1016/j.neulet.2012.03.048
Krause, A. J., Simon, E. B., Mander, B. A., Greer, S. M., Saletin, J. M., Goldstein-Piekarski, A. N., et al. (2017). The sleep-deprived human brain. Nat. Revi. Neurosci. 8, 404-418. doi: 10.1038/nrn.2017.55
Kreutzmann, J. C., Havekes, R., Abel, T., and Meerlo, P. (2015). Sleep deprivation and hippocampal vulnerability: changes in neuronal plasticity, neurogenesis and cognitive function. Neuroscience 309, 173-190. doi: 10.1016/j.neuroscience.2015.04.053
Krystal, A. D. (2012). Psychiatric disorders and sleep. Neurol. Clin. 30, 1389-1413. doi: 10.1016/j.ncl.2012.08.018
Krystal, A., Fava, M., Rubens, R., Wessel, T., Caron, J., Wilson, P., et al. (2007). Evaluation of eszopiclone discontinuation after cotherapy with fluoxetine for insomnia with coexisting depression. J. Clin. Sleep Med. 3, 48-55.
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.
Lemaire, V., Koehl, M., Le Moal, M., and Abrous, D. N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97, 11032-11037. doi: 10.1073/pnas.97.20.11032
Leuner, B., Mendolia-Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E., and Shors, T. J. (2004). Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J. Neurosci. 24, 7477-7481. doi: 10.1523/JNEUROSCI.0204-04.2004
Levone, B. R., Cryan, J. F., and O'Leary, O. F. (2015). Role of adult hippocampal neurogenesis in stress resilience. Neurobiol. Stress 1, 147-155. doi: 10.1016/j.ynstr.2014.11.003
Li, Y. F., Zhang, Y. Z., Liu, Y. Q., Wang, H. L., Yuan, L., and Luo, Z. P. (2004). Moclobemide up-regulates proliferation of hippocampal progenitor cells in chronically stressed mice. Acta Pharmacol. Sin. 25, 1408-1412.
Lo, J. C., Groeger, J. A., Santhi, N., Arbon, E. L., Lazar, A. S., Hasan, S., et al. (2012). Effects of partial and acute total sleep deprivation on performance across cognitive domains, individuals and circadian phase. PLoS ONE 7:e45987. doi: 10.1371/journal.pone.0045987
Lucassen, P. J., Stumpel, M. W., Wang, Q., and Aronica, E. (2010). Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 58, 940-949. doi: 10.1016/j.neuropharm.2010.01.012
MacQueen, G. M., Campbell, S., McEwen, B. S., Macdonald, K., Amano, S., Joffe, R. T., et al. (2003). Course of illness, hippocampal function, and hippocampal volume in major depression. Proc. Natl. Acad. Sci. U.S.A. 100, 1387-1392. doi: 10.1073/pnas.0337481100
Madeira, M. D., Cadete-Leite, A., Andrade, J. P., and Paula-Barbosa, M. M. (1991). Effects of hypothyroidism upon the granular layer of the dentate gyrus in male and female adult rats: a morphometric study. J. Comp. Neurol. 314, 171-186. doi: 10.1002/cne.903140116
Madsen, T. M., Kristjansen, P. E., Bolwig, T. G., and Wortwein, G. (2003). Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119, 635-642. doi: 10.1016/S0306-4522(03)00199-4
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.
Manber, R., Edinger, J. D., Gress, J. L., San Pedro-Salcedo, M. G., Kuo, T. F., and Kalista, T. (2008). Cognitive behavioral therapy for insomnia enhances depression outcome in patients with comorbid major depressive disorder and insomnia. Sleep 31, 489-495. doi: 10.1093/sleep/31.4.489
Matsuo, T., Yamaguchi, S., Mitsui, S., Emi, A., Shimoda, F., and Okamura, H. (2003). Control mechanism of the circadian clock for timing of cell division in vivo. Science 302, 255-259. doi: 10.1126/science.1086271
McClelland, J. L., McNaughton, B. L., and O'Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419-457. doi: 10.1037/0033-295X.102.3.419
McDermott, C. M., LaHoste, G. J., Chen, C., Musto, A., Bazan, N. G., and Magee, J. C. (2003). Sleep deprivation causes behavioral, synaptic, and membrane excitability alterations in hippocampal neurons. J. Neurosci. 23, 9687-9695.
Meerlo, P., Mistlberger, R. E., Jacobs, B. L., Heller, H. 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
Methippara, M., Bashir, T., Suntsova, N., Szymusiak, R., and McGinty, D. (2010). Hippocampal adult neurogenesis is enhanced by chronic eszopiclone treatment in rats. J. Sleep Res. 19, 384-393. doi: 10.1111/j.1365-2869.2010.00833.x
Miller, B. H., McDearmon, E. L., Panda, S., Hayes, K. R., Zhang, J., Andrews, J. L., et al. (2007). Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 104, 3342-3347. doi: 10.1073/pnas.0611724104
Miller, B. R., and Hen, R. (2015). The current state of the neurogenic theory of depression and anxiety. Curr. Opin. Neurobiol. 30, 51-58. doi: 10.1016/j.conb.2014.08.012
Ming, G. L., and Song, H. (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687-702. doi: 10.1016/j.neuron.2011.05.001
Mirescu, C., and Gould, E. (2006). Stress and adult neurogenesis. Hippocampus 16, 233-238. doi: 10.1002/hipo.20155
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
Molle, M., Yeshenko, O., Marshall, L., Sara, S. J., and Born, J. (2006). Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J. Neurophysiol. 96, 62-70. doi: 10.1152/jn.00014.2006
Mongrain, V., Hernandez, S. A., Pradervand, S., Dorsaz, S., Curie, T., Hagiwara, G., et al. (2010). Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis. Sleep 33, 1147-1157. doi: 10.1093/sleep/33.9.1147
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
Mueller, A. D., Meerlo, P., McGinty, D., and Mistlberger, R. E. (2015). Sleep and adult neurogenesis: implications for cognition and mood. Curr. Top. Behav. Neurosci. 25, 151-181. doi: 10.1007/7854_2013_251
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. Compar. Physiol. 294, R1693-R1703. doi: 10.1152/ajpregu.00858.2007
Mullen, R. J., Buck, C. R., and Smith, A. M. (1992). NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211.
Murphy, T., Dias, G. P., and Thuret, S. (2014). Effects of diet on brain plasticity in animal and human studies: mind the gap. Neural Plast. 2014:563160. doi: 10.1155/2014/563160
Muto, V., Jaspar, M., Meyer, C., Kussé, C., Chellappa, S. L., Degueldre, C., et al. (2016). Local modulation of human brain responses by circadian rhythmicity and sleep debt. Science 353, 687-690. doi: 10.1126/science.aad2993
Nixon, K., and Crews, F. T. (2004). Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J. Neurosci. 24, 9714-9722. doi: 10.1523/JNEUROSCI.3063-04.2004
Nutt, D., Wilson, S., and Paterson, L. (2008). Sleep disorders as core symptoms of depression. Dialogues Clin. Neurosci. 10, 329-336.
Ognjanovski, N., Schaeffer, S., Wu, J., Mofakham, S., Maruyama, D., Zochowski, M., et al. (2017). Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation. Nat. Commun. 8:15039. doi: 10.1038/ncomms15039
Palchykova, S., Winsky-Sommerer, R., Meerlo, P., Durr, R., and Tobler, I. (2006). Sleep deprivation impairs object recognition in mice. Neurobiol. Learn. Mem. 85, 263-271. doi: 10.1016/j.nlm.2005.11.005
Palchykova, S., Winsky-Sommerer, R., and Tobler, I. (2009). Sleep deprivation in the dark period does not impair memory in OF1 mice. Chronobiol. Int. 26, 682-696. doi: 10.1080/07420520902926025
Palmer, C. A., and Alfano, C. A. (2017). Sleep and emotion regulation: an organizing, integrative review. Sleep Med. Rev. 31, 6-16. doi: 10.1016/j.smrv.2015.12.006
Perera, T. D., Coplan, J. D., Lisanby, S. H., Lipira, C. M., Arif, M., Carpio, C., et al. (2007). Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J. Neurosci. 27, 4894-4901. doi: 10.1523/JNEUROSCI.0237-07.2007
Perlis, M. L., Giles, D. E., Buysse, D. J., Tu, X., and Kupfer, D. J. (1997). Self-reported sleep disturbance as a prodromal symptom in recurrent depression. J. Affect. Disord. 42, 209-212. doi: 10.1016/S0165-0327(96)01411-5
Pham, K., Nacher, J., Hof, P. R., and 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, 879-886. doi: 10.1046/j.1460-9568.2003.02513.x
Pillai, V., Kalmbach, D. A., and Ciesla, J. A. (2011). A meta-analysis of electroencephalographic sleep in depression: evidence for genetic biomarkers. Biol. Psychiatry 70, 912-919. doi: 10.1016/j.biopsych.2011.07.016
Pitkanen, A., Pikkarainen, M., Nurminen, N., and Ylinen, A. (2000). Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A Review. Ann. N. Y. Acad. Sci. 911, 369-391. doi: 10.1111/j.1749-6632.2000.tb06738.x
Raber, J., Rola, R., LeFevour, A., Morhardt, D., Curley, J., Mizumatsu, S., et al. (2004). Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 162, 39-47. doi: 10.1667/RR3206
Rakai, B. D., Chrusch, M. J., Spanswick, S. C., Dyck, R. H., and Antle, M. C. (2014). Survival of adult generated hippocampal neurons is altered in circadian arrhythmic mice. PLoS ONE 9:e99527. doi: 10.1371/journal.pone.0099527
Ramirez-Amaya, V., Marrone, D. F., Gage, F. H., Worley, P. F., and Barnes, C. A. (2006). Integration of new neurons into functional neural networks. J. Neurosci. 26, 12237-12241. doi: 10.1523/JNEUROSCI.2195-06.2006
Ramirez-Rodriguez, G., Ortiz-Lopez, L., Dominguez-Alonso, A., Benitez-King, G. A., and Kempermann, G. (2011). Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice. J. Pineal Res. 50, 29-37. doi: 10.1111/j.1600-079X.2010.00802.x
Reif, A., Fritzen, S., Finger, M., Strobel, A., Lauer, M., Schmitt, A., et al. (2006). Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol. Psychiatry 11, 514-522. doi: 10.1038/sj.mp.4001791
Revest, J. M., Dupret, D., Koehl, M., Funk-Reiter, C., Grosjean, N., Piazza, P. V., et al. (2009). Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol. Psychiatry 14, 959-967. doi: 10.1038/mp.2009.15
Riemann, D., Berger, M., and Voderholzer, U. (2001). Sleep and depression-results from psychobiological studies: an overview. Biol. Psychol. 57, 67-103. doi: 10.1016/S0301-0511(01)00090-4
Rolls, A., Colas, D., Adamantidis, A., Carter, M., Lanre-Amos, T., Heller, H. C., et al. (2011). Optogenetic disruption of sleep continuity impairs memory consolidation. Proc. Natl. Acad. Sci. U.S.A. 108, 13305-13310. doi: 10.1073/pnas.1015633108
Roman, V., Van der Borght, K., Leemburg, S. A., 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
Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., et al. (2006). Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24, 1850-1856. doi: 10.1111/j.1460-9568.2006.05059.x
Sahay, A., and Hen, R. (2007). Adult hippocampal neurogenesis in depression. Nat. Neurosci. 10, 1110-1115. doi: 10.1038/nn1969
Sairanen, M., Lucas, G., Ernfors, P., Castren, M., and Castren, E. (2005). Brain-derived neurotrophic factor and antidepressant drugs have different but coordinated effects on neuronal turnover, proliferation, and survival in the adult dentate gyrus. J. Neurosci. 25, 1089-1094. doi: 10.1523/JNEUROSCI.3741-04.2005
Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., et al. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809. doi: 10.1126/science.1083328
Sato, K. (2015). Effects of microglia on neurogenesis. Glia 63, 1394-1405. doi: 10.1002/glia.22858
Scerri, C., Stewart, C. A., Breen, K. C., and Balfour, D. J. (2006). The effects of chronic nicotine on spatial learning and bromodeoxyuridine incorporation into the dentate gyrus of the rat. Psychopharmacology (Berl). 184, 540-546. doi: 10.1007/s00213-005-0086-4
Scherrer, J. F., Salas, J., Copeland, L. A., Stock, E. M., Ahmedani, B. K., Sullivan, M. D., et al. (2016). Prescription opioid duration, dose, and increased risk of depression in 3 large patient populations. Ann. Fam. Med. 14, 54-62. doi: 10.1370/afm.1885
Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184-187. doi: 10.1038/nature02553
Scott, B. W., Wojtowicz, J. M., and Burnham, W. M. (2000). Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp. Neurol. 165, 231-236. doi: 10.1006/exnr.2000.7458
Sheline, Y. I. (2000). 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity. Biol. Psychiatry 48, 791-800. doi: 10.1016/S0006-3223(00)00994-X
Sheline, Y. I., Gado, M. H., and Kraemer, H. C. (2003). Untreated depression and hippocampal volume loss. Am. J. Psychiatry 160, 1516-1518. doi: 10.1176/appi.ajp.160.8.1516
Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., and Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376. doi: 10.1038/35066584
Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12, 578-584. doi: 10.1002/hipo.10103
Siapas, A. G., and Wilson, M. A. (1998). Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 1123-1128. doi: 10.1016/S0896-6273(00)80629-7
Sirota, A., and Buzsaki, G. (2005). Interaction between neocortical and hippocampal networks via slow oscillations. Thalamus Relat. Syst. 3, 245-259. doi: 10.1017/S1472928807000258
Sirota, A., Csicsvari, J., Buhl, D., and Buzsaki, G. (2003). Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U.S.A. 100, 2065-2069. doi: 10.1073/pnas.0437938100
Smith, W. T., Londborg, P. D., Glaudin, V., Painter, J. R., and Summit Research, N. (2002). Is extended clonazepam cotherapy of fluoxetine effective for outpatients with major depression? J. Affect. Disord. 70, 251-259.
Spalding, K. L., Bergmann, O., Alkass, K., Bernard, S., Salehpour, M., Huttner, H. B., et al. (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell 153, 1219-1227. doi: 10.1016/j.cell.2013.05.002
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
Stickgold, R., and Walker, M. P. (2005). Memory consolidation and reconsolidation: what is the role of sleep? Trends Neurosci. 28, 408-415.
Su, X. W., Li, X. Y., Banasr, M., and Duman, R. S. (2009). Eszopiclone and fluoxetine enhance the survival of newborn neurons in the adult rat hippocampus. Int. J. Neuropsychopharmacol. 12, 1421-1428. doi: 10.1017/S1461145709990629
Sullivan, D., Csicsvari, J., Mizuseki, K., Montgomery, S., Diba, K., and Buzsaki, G. (2011). Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J. Neurosci. 31, 8605-8616. doi: 10.1523/JNEUROSCI.0294-11.2011
Surget, A., Saxe, M., Leman, S., Ibarguen-Vargas, Y., Chalon, S., Griebel, G., et al. (2008). Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol. Psychiatry 64, 293-301. doi: 10.1016/j.biopsych.2008.02.022
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
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.
Tartar, J. L., Ward, C. P., Cordeira, J. W., Legare, S. L., Blanchette, A. J., McCarley, R. W., et al. (2009). Experimental sleep fragmentation and sleep deprivation in rats increases exploration in an open field test of anxiety while increasing plasma corticosterone levels. Behav. Brain Res. 197, 450-453. doi: 10.1016/j.bbr.2008.08.035
Thompson, A., Boekhoorn, K., Van Dam, A. M., and Lucassen, P. J. (2008). Changes in adult neurogenesis in neurodegenerative diseases: cause or consequence? Genes Brain Behav. 7(Suppl. 1), 28-42. doi: 10.1111/j.1601-183X.2007.00379.x
Thuret, S., Toni, N., Aigner, S., Yeo, G. W., and Gage, F. H. (2009). Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus 19, 658-669. doi: 10.1002/hipo.20550
Tiba, P. A., Oliveira, M. G., Rossi, V. C., Tufik, S., and Suchecki, D. (2008). Glucocorticoids are not responsible for paradoxical sleep deprivation-induced memory impairments. Sleep 31, 505-515. doi: 10.1093/sleep/31.4.505
Tudor, J. C., Davis, E. J., Peixoto, L., Wimmer, M. E., van Tilborg, E., Park, A. J., et al. (2016). Sleep deprivation impairs memory by attenuating mTORC1-dependent protein synthesis. Sci. Signal. 9:ra41. doi: 10.1126/scisignal.aad4949
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
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
Van Der Werf, Y. D., Van Der Helm, E., Schoonheim, M. M., Ridderikhoff, A., and Van Someren, E. J. (2009). Learning by observation requires an early sleep window. Proc. Natl. Acad. Sci. U.S.A. 106, 18926-18930. doi: 10.1073/pnas.0901320106
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.
van Praag, H., Shubert, T., Zhao, C., and Gage, F. H. (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25, 8680-8685. doi: 10.1523/JNEUROSCI.1731-05.2005
Videbech, P., and Ravnkilde, B. (2004). Hippocampal volume and depression: a meta-analysis of MRI studies. Am. J. Psychiatry 161, 1957-1966. doi: 10.1176/appi.ajp.161.11.1957
Vorster, A. P., and Born, J. (2015). Sleep and memory in mammals, birds and invertebrates. Neurosci. Biobehav. Rev. 50, 103-119. doi: 10.1016/j.neubiorev.2014.09.020
Walker, M. P. (2009). The role of sleep in cognition and emotion. Ann. N. Y. Acad. Sci. 1156, 168-197. doi: 10.1111/j.1749-6632.2009.04416.x
Wang, J. W., David, D. J., Monckton, J. E., Battaglia, F., and Hen, R. (2008). Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J. Neurosci. 28, 1374-1384. doi: 10.1523/JNEUROSCI.3632-07.2008
Watson, B. O., and Buzsaki, G. (2015). Sleep, Memory & Brain Rhythms. Daedalus 144, 67-82. doi: 10.1162/DAED_a_00318
Wilson, M. A., and McNaughton, B. L. (1994). Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679. doi: 10.1126/science.8036517
Xu, H., Chen, Z., He, J., Haimanot, S., Li, X., Dyck, L., et al. (2006). Synergetic effects of quetiapine and venlafaxine in preventing the chronic restraint stress-induced decrease in cell proliferation and BDNF expression in rat hippocampus. Hippocampus 16, 551-559. doi: 10.1002/hipo.20184
Yoo, S. S., Hu, P. T., Gujar, N., Jolesz, F. A., and Walker, M. P. (2007). A deficit in the ability to form new human memories without sleep. Nat. Neurosci. 10, 385-392. doi: 10.1038/nn1851
