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Hypothetical neurochemical mechanisms of paradoxical sleep deficiency in Alzheimer’s disease

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Abstract

Based on the known experimental data on the specific morphological and neurochemical changes in the neural circuits involved in the occurrence of paradoxical sleep (REM sleep) that are observed in Alzheimer’s disease (AD) and our analysis of the effects of neuromodulators on the functioning of these circuits we propose that REM sleep deficiency in AD is caused by the following mechanisms: (1) the activity of the lateral geniculate body and occipital cortex is not sufficient to generate the ponto-geniculo-occipital (PGO) waves that are specific for REM sleep due to lower activity of cholinergic cells of the pedunculopontine and laterodorsal tegmental nuclei (PPN and LDTN) and lower density of cholinergic receptors; (2) because of reduced activity of cholinergic neurons of the PPN and LDN on GABAergic interneurons projecting to noradrenergic and serotonergic cells, the activity of the latter cannot be completely inhibited, as should occur during REM sleep; (3) the concentration of melanin-concentrating hormone is not sufficient for sleep due to the decreased activity of cholinergic cells of the basal forebrain nucleus, which excite neurons that produce this hormone; and (4) the activity of histaminergic cells increases and the activity of neurons that release melanin-concentrating hormone decreases due to the increased orexin level. Our analysis shows that common use of drugs that increase the acetylcholine concentration in patients with AD may result in increased activity of orexinergic cells and this must prevent the occurrence of REM sleep. We hypothesize that microstimulation of PPN may improve the occurrence of REM sleep because it should decrease the activity of serotoninergic, noradrenergic, and histaminergic cells and promote the generation of PGO waves and hippocampal theta activity. This treatment may improve the conditions for memory consolidation in patients with AD. Such microstimulation should be applied at night according to a special protocol.

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Abbreviations

AD:

Alzheimer’s disease

EPSP:

excitatory postsynaptic potential

DRN:

dorsal raphe nucleus

LDTN:

laterodorsal tegmental nucleus

SWS:

slow-wave sleep

MCH:

melanin-concentrating hormone

MCHN:

melaninconcentrating hormone expressing neuron

LGB:

lateral geniculate body

PPN:

pedunculopontine nucleus

REM sleep:

paradoxical sleep

IPSC:

inhibitory postsynaptic current

AChN:

cholinergic neuron

PGO waves:

ponto-geniculooccipital waves

References

  1. Hauw, J.J., Hausser-Hauw, C., De Girolami, U., Hasboun, D., and Seilhean, D., J. Neuropathol. Exp. Neurol., 2011, vol. 70, no. 4, pp. 243–252.

    Article  PubMed  Google Scholar 

  2. Busche, M.A., Kekus, M., and Förstl, H., Nervenarzt, 2017, vol. 88, no. 3, pp. 215–221.

    Article  CAS  PubMed  Google Scholar 

  3. Cipriani, G., Lucetti, C., Danti, S., and Nuti, A., Psychogeriatrics, 2015, vol. 15, no. 1, pp. 65–74.

    Article  PubMed  Google Scholar 

  4. Moran, M., Lynch, C.A., Walsh, C., Coen, R., Coakley, D., and Lawlor, B.A., Sleep Med., 2005, vol. 6, no. 4, pp. 347–352.

    Article  PubMed  Google Scholar 

  5. Vecchierini, M.F., Psychol. Neuropsychiatr. Vieil., 2010, vol. 8, no. 1, pp. 15–23.

    PubMed  Google Scholar 

  6. Hot, P., Rauchs, G., Bertran, F., Denise, P., Desgranges, B., Clochon, P., and Eustache, F., Biol. Psychol., 2011, vol. 87, no. 3, pp. 334–339.

    Article  PubMed  Google Scholar 

  7. Savaskan, E., Z. Gerontol. Geriatr., 2015, vol. 48, no. 4, pp. 312–317.

    Article  CAS  PubMed  Google Scholar 

  8. Cooke, J.R., Liu, L., Natarajan, L., He, F., Marler, M., Loredo, J.S., Corey-Bloom, J., Palmer, B.W., Greenfield, D., and Ancoli-Israel, S., Behav. Sleep Med., 2006, vol. 4, no. 4, pp. 219–227.

    Article  PubMed  Google Scholar 

  9. Liguori, C., Nuccetelli, M., Izzi, F., Sancesario, G., Romigi, A., Martorana, A., Amoroso, C., Bernardini, S., Marciani, M.G., Mercuri, N.B., and Placidi, F., Neurobiol. Aging, 2016, vol. 40, pp. 120–126.

    Article  CAS  PubMed  Google Scholar 

  10. Vitiello, M.V. and Borson, S., CNS Drugs, 2001, vol. 15, no. 10, pp. 777–796.

    Article  CAS  PubMed  Google Scholar 

  11. Zhang, B., Veasey, S.C., Wood, M.A., Leng, L.Z., Kaminski, C., Leight, S., Abel, T., Lee, V.M., and Trojanowski, J.Q., Am. J. Pathol., 2005, vol. 167, no. 5, pp. 1361–1369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Urrestarazu, E. and Iriarte, J., Nat. Sci. Sleep, vol. 14, no. 8, pp. 21–33.

  13. Zeitzer, J.M., Prog. Mol. Biol. Transl. Sci., 2013, vol. 119, pp. 137–154.

    Article  PubMed  Google Scholar 

  14. O’Malley, M.W. and Datta, S., Indian J. Sleep Med., 2013, vol. 8, no. 2, pp. 58–66.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Datta, S., Spoley, E.E., Mavanji, V.K., and Patterson, E.H., Neuroscience, 2002, vol. 114, no. 1, pp. 157–164.

    Article  CAS  PubMed  Google Scholar 

  16. Sil’kis, I.G., Neirokhimiya, 2006, vol. 23, no. 4, pp. 283–293.

    Google Scholar 

  17. Sil’kis, I.G., Neurochem. J., 2009, vol. 3, no. 3, pp. 221–231.

    Article  Google Scholar 

  18. Hernández-Vázquez, F., Chavarría, K., Garduno, J., Hérnandez-Lopez, S., and Mihailescu, S.P., J. Neurophysiol., 2014, vol. 112, no. 12, pp. 3154–3163.

    Article  PubMed  CAS  Google Scholar 

  19. Yang, C. and Brown, R.E., Neuroscience, 2014, vol. 258, no. 1, pp. 62–73.

    Article  CAS  PubMed  Google Scholar 

  20. Lykhmus, O., Koval, L., Skok, M., Zouridakis, M., Zisimopoulou, P., Tzartos, S., Tsetlin, V., Granon, S., Changeux, J.P., Komisarenko, S., and Cloëz-Tayarani, I., J. Alzheimer’s Dis., vol. 24, no. 4, pp. 693–704.

  21. Mallick, B.N., Kaur, S., and Saxena, R.N., Neuroscience, 2001, vol. 104, no. 2, pp. 467–485.

    Article  CAS  PubMed  Google Scholar 

  22. Gervasoni, D., Darracq, L., Fort, P., Souliere, F., Chouvet, G., and Luppi, P.H., Eur. J. Neurosci., 1998, vol. 10, no. 3, pp. 964–970.

    Article  CAS  PubMed  Google Scholar 

  23. McDuff, T. and Sumi, S.M., Neurology, 1985, vol. 35, no. 1, pp. 123–126.

    Article  CAS  PubMed  Google Scholar 

  24. Ogomori, K., Kitamoto, T., Tateishi, J., Sato, Y., and Suetsugu, M., Am. J. Pathol., 1989, vol. 134, no. 2, pp. 243–251.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Garcia, A.P., Aitta-aho, T., Schaaf, L., Heeley, N., Heuschmid, L., Bai, Y., Barrantes, F.J., and Apergis-Schoute, J., PLoS One, 2015, vol. 10, no. 8: e0133327.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Yeomans, J.S., Handb. Exp. Pharmacol., 2012, vol. 208, pp. 243–259.

    Article  CAS  Google Scholar 

  27. Bayer, L., Eggermann, E., Serafin, M., Grivel, J., Machard, D., Muhlethaler, M., and Jones, B.E., Neuroscience, 2005, vol. 130, no. 4, pp. 807–811.

    Article  CAS  PubMed  Google Scholar 

  28. Willie, J.T., Sinton, C.M., Maratos-Flier, E., and Yanagisawa, M., Neuroscience, 2008, vol. 156, no. 4, pp. 819–829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Losier, B.J. and Semba, K., Brain Res., 1993, vol. 604, nos. 1–2, pp. 41–52.

    Article  CAS  PubMed  Google Scholar 

  30. Adamantidis, A. and de Lecea, L., Peptides, 2009, vol. 30, no. 11, pp. 2066–2070.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Hassani, O.K., Lee, M.G., and Jones, B.E., Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 7, pp. 2418–2422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Hervieu, G.J., Cluderay, J.E., Harrison, D., Meakin, J., Maycox, P., Nasir, S., and Leslie, R.A., Eur. J. Neurosci., 2000, vol. 12, no. 4, pp. 1194–1216.

    Article  CAS  PubMed  Google Scholar 

  33. Gao, X.B. and Pol, A.N., J. Physiol., 2001, vol. 533, pt. 1, pp. 237–252.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rao, Y., Lu, M., Ge, F., Marsh, D.J., Qian, S., Wang, A.H., Picciotto, M.R., and Gao, X.B., J. Neurosci., 2008, vol. 28, no. 37, pp. 9101–9110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Dell, L.A., Kruger, J.L., Pettigrew, J.D., and Manger, P.R., J. Chem. Neuroanat., 2013, vol. 53, pp. 64–71.

    Article  CAS  PubMed  Google Scholar 

  36. Hong, E.Y., Yoon, Y.S., and Lee, H.S., Brain Res., 2011, vol. 1424, pp. 20–31.

    Article  CAS  PubMed  Google Scholar 

  37. Papp, R.S. and Palkovits, M., Front. Neuroanat., 2014, vol. 8: 34.

    Google Scholar 

  38. Takahashi, K., Koyama, Y., Kayama, Y., and Yamamoto, M., Psychiatry. Clin. Neurosci., 2002, vol. 56, no. 3, pp. 335–336.

    Article  CAS  PubMed  Google Scholar 

  39. Xi, M.C., Morales, F.R., and Chase, M.H., Brain Res., 2001, vol. 901, nos. 1–2, pp. 259–264.

    Article  CAS  PubMed  Google Scholar 

  40. Hong, E.Y. and Lee, H.S., Brain Res., 2011, vol. 1383, pp. 169–178.

    Article  CAS  PubMed  Google Scholar 

  41. Khateb, A., Serafin, M., and Muhlethaler, M., Neurosci. Let., 1990, vol. 112, nos. 2–3, pp. 257–262.

    Article  CAS  Google Scholar 

  42. Mufson, E.J., Mash, D.C., and Hersh, L.B., Neurol., 1988, vol. 24, no. 5, pp. 623–629.

    CAS  Google Scholar 

  43. Rüb, U., Stratmann, K., Heinsen, H., Turco, D.D., Seidel, K., Dunnen, W., and Korf, H.W., Curr. Alzheimer Res., 2016, vol. 13, no. 10, pp. 1178–1197.

    Article  PubMed  CAS  Google Scholar 

  44. Steckler, T., Inglis, W., Winn, P., and Sahgal, A., Brain Res. Rev., 1994, vol. 19, no. 3, pp. 298–318.

    Article  CAS  PubMed  Google Scholar 

  45. Xuereb, J.H., Perry, E.K., Candy, J.M., Bonham, J.R., Perry, R.H., and Marshall, E., J. Neurol. Sci., 1990, vol. 99, nos. 2–3, pp. 185–197.

    Article  CAS  PubMed  Google Scholar 

  46. Ransmayr, G., Faucheux, B., Nowakowski, C., Kubis, N., Federspiel, S., Kaufmann, W., Henin, D., Hauw, J.J., Agid, Y., and Hirsch, E.C., Neurosci. Let., 2000, vol. 288, no. 3, pp. 195–198.

    Article  CAS  Google Scholar 

  47. Barrantes, F.J. and Borroni, V., FEBS Lett., 2010, vol. 584, no. 9, pp. 1856–1863.

    Article  CAS  PubMed  Google Scholar 

  48. Medeiros, R., Kitazawa, M., Caccamo, A., Baglietto-Vargas, D., Estrada-Hernandez, T., Cribbs, D.H., Fisher, A., and Laferla, F.M., Am. J. Pathol., 2011, vol. 179, no. 2, pp. 980–991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Paterson, D. and Nordberg, A., Prog. Neurobiol., 2000, vol. 61, no. 1, pp. 75–111.

    Article  CAS  PubMed  Google Scholar 

  50. Perry, E.K., Perry, R.H., Smith, C.J., Purohit, D., Bonham, J., Dick, D.J., Candy, J.M., Edwardson, J.A., and Fairbairn, A., Can. J. Neurol. Sci., 1986, vol. 13, suppl. 4, pp. 521–527.

    Article  CAS  PubMed  Google Scholar 

  51. Rinne, J.O., Myllykyla, T., Lonnberg, P., and Marjamaki, P., Brain Res., 1991, vol. 547, no. 1, pp. 167–170.

    Article  CAS  PubMed  Google Scholar 

  52. Court, J., Martin-Ruiz, C., Piggott, M., Spurden, D., Griffiths, M., and Perry, E., Biol. Psychiatry, 2001, vol. 49, no. 3, pp. 175–184.

    Article  CAS  PubMed  Google Scholar 

  53. Dijk, S.N., Francis, P.T., Stratmann, G.C., and Bowen, D.M., J. Neurochem., 1995, vol. 65, no. 5, pp. 2165–2169.

    Article  CAS  PubMed  Google Scholar 

  54. Liguori, C., Romigi, A., Nuccetelli, M., Zannino, S., Sancesario, G., Martorana, A., Albanese, M., Mercuri, N.B., Izzi, F., Bernardini, S., Nitti, A., Sancesario, G.M., Sica, F., Marciani, M.G., and Placidi, F., JAMA Neurol., 2014, vol. 71, no. 12, pp. 1498–1505.

    Article  PubMed  Google Scholar 

  55. Malkki, H., Nat. Rev. Neurol., 2014, vol. 10, no. 12, p. 672.

    Article  PubMed  Google Scholar 

  56. Dauvilliers, Y.A., Lehmann, S., Jaussent, I., and Gabelle, A., Front. Aging Neurosci., 2014, vol. 6: 119.

    Google Scholar 

  57. Alam, M.N., Kumar, S., Bashir, T., Suntsova, N., Methippara, M.M., Szymusiak, R., and McGinty, D., J. Physiol., 2005, vol. 563, pt. 2, pp. 569–582.

    Article  CAS  PubMed  Google Scholar 

  58. Stanley, E.M. and Fadel, J., Synapse, 2012, vol. 66, no. 5, pp. 445–452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Fronczek, R., van Geest, S., Frölich, M., Overeem, S., Roelandse, F.W., Lammers, G.J., and Swaab, D.F., Neurobiol. Aging, 2012, vol. 33, no. 8, pp. 1642–1650.

    Article  CAS  PubMed  Google Scholar 

  60. Friedman, L.F., Zeitzer, J.M., Lin, L., Hoff, D., Mignot, E., Peskind, E.R., and Yesavage, J.A., Neurology, 2007, vol. 68, no. 10, pp. 793–794.

    Article  CAS  PubMed  Google Scholar 

  61. Schmidt, F.M., Kratzsch, J., Gertz, H.J., Tittmann, M., Jahn, I., Pietsch, U.C., Kaisers, U.X., Thiery, J., Hegerl, U., and Schonknecht, P., PLoS One, 2013, vol. 8, no. 5: e63136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Konadhode, R.R., Pelluru, D., Blanco-Centurion, C., Zayachkivsky, A., Liu, M., Uhde, T., Glen, W.B.Jr., Pol, A.N., Mulholland, P.J., and Shiromani, P.J., J. Neurosci., 2013, vol. 33, no. 25, pp. 10257–10263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lu, Z.H., Fukuda, S., Minakawa, Y., Yasuda, A., Sakamoto, H., Sawamura, S., Takahashi, H., and Ishii, N., Peptides, 2013, vol. 44, pp. 32–39.

    Article  CAS  PubMed  Google Scholar 

  64. Jego, S., Glasgow, S.D., Herrera, C.G., Ekstrand, M., Reed, S.J., Boyce, R., Friedman, J., Burdakov, D., and Adamantidis, A.R., Nat. Neurosci., 2013, vol. 16, no. 11, pp. 1637–1643.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Jones, B.E. and Hassani, O.K., Sleep, vol. 36, no. 12, pp. 1769–1772.

  66. Del Cid-Pellitero, E. and Jones, B.E., Neuroscience, 2012, vol. 223, pp. 269–276.

    Article  PubMed  CAS  Google Scholar 

  67. Henny, P., Brischoux, F., Mainville, L., Stroh, T., and Jones, B.E., Neuroscience, 2010, vol. 169, pp. 1150–1157.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Adamantidis, A.R., Zhang, F., Aravanis, A.M., Deisseroth, K., and de Lecea, L., Nature, 2007, vol. 450, no. 7168, pp. 420–424.

    Article  CAS  PubMed  Google Scholar 

  69. Apergis-Schoute, J., Iordanidou, P., Faure, C., Jego, S., Schöne, C., Aitta-Aho, T., Adamantidis, A., and Burdakov, D., J. Neurosci., 2015, vol. 35, no. 14, pp. 5435–5441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Shan, L., Dauvilliers, Y., and Siegel, J.M., Nat. Rev. Neurol., 2015, vol. 11, no. 7, pp. 401–413.

    Article  CAS  PubMed  Google Scholar 

  71. Zlomuzica, A., Dere, D., Binder, S., De Souza, Silva M.A., Huston, J.P., and Dere, E., Neuropharmacology, 2016, vol. 106, pp. 135–145.

    Article  CAS  PubMed  Google Scholar 

  72. Slats, D., Claassen, J.A., Verbeek, M.M., and Overeem, S., Ageing Res. Rev., 2013, vol. 12, no. 1, pp. 188–200.

    Article  CAS  PubMed  Google Scholar 

  73. Mishima, K., Tozawa, T., Satoh, K., Matsumoto, Y., Hishikawa, Y., and Okawa, M., Biol. Psychiatry, 1999, vol. 45, no. 4, pp. 417–421.

    Article  CAS  PubMed  Google Scholar 

  74. Wu, Y.H. and Swaab, D.F., J. Pineal Res., 2005, vol. 38, no. 3, pp. 145–152.

    Article  CAS  PubMed  Google Scholar 

  75. Zhou, J.N., Liu, R.Y., Kamphorst, W., Hofman, M.A., and Swaab, D.F., J. Pineal Res., 2003, vol. 35, no. 2, pp. 125–130.

    Article  CAS  PubMed  Google Scholar 

  76. Lim, A.S., Lozano, A.M., Moro, E., Hamani, C., Hutchison, W.D., Dostrovsky, J.O., Lang, A.E., Wennberg, R.A., and Murray, B.J., Sleep, vol. 30, no. 7, pp. 823–827.

  77. Sil’kis, I.G., Neurochem. J., 2010, vol. 4, no. 3, pp. 170–177.

    Article  Google Scholar 

  78. Koyama, Y. and Sakai, K., Neuroscience, 2000, vol. 96, no. 4, pp. 723–733.

    Article  CAS  PubMed  Google Scholar 

  79. Hu, B., Bouhassira, D., Steriade, M., and Deschenes, M., Brain Res., 1988, vol. 473, no. 2, pp. 394–397.

    Article  CAS  PubMed  Google Scholar 

  80. Armstrong, R. and Kergoat, H., Ophthalmic Physiol. Opt., 2015, vol. 35, no. 4, pp. 352–576.

    Article  PubMed  Google Scholar 

  81. Okada, K. and Kobayashi, Y., Eur. J. Neurosci., 2014, vol. 40, no. 4, pp. 2641–2651.

    Article  PubMed  Google Scholar 

  82. Hu, B., Steriade, M., and Deschênes, M., Neuroscience, 1989, vol. 31, no. 1, pp. 25–35.

    Article  CAS  PubMed  Google Scholar 

  83. Sato, H., Hata, Y., Masui, H., and Tsumoto, T., J. Neurophysiol., 1987, vol. 58, no. 4, pp. 765–780.

    CAS  PubMed  Google Scholar 

  84. Anderson, K.N., Jamieson, S., Graham, A.J., and Shneerson, J.M., Clin. Neurol. Neurosurg., 2008, vol. 110, no. 5, pp. 492–495.

    Article  PubMed  Google Scholar 

  85. Cardinali, D.P., Vigo, D.E., Olivar, N., Vidal, M.F., Furio, A.M., and Brusco, L.I., Am. J. Neurodegener. Dis., vol. 1, no. 3, pp. 280–291.

  86. Furio, A.M., Brusco, L.I., and Cardinali, D.P., J. Pineal Res., 2007, vol. 43, no. 4, pp. 404–409.

    Article  CAS  PubMed  Google Scholar 

  87. Zhang, W., Chen, X.Y., Su, S.W., Jia, Q.Z., Ding, T., Zhu, Z.N., and Zhang, T., Neurol. Sci., 2016, vol. 37, no. 1, pp. 57–65.

    Article  PubMed  Google Scholar 

  88. Boeve, B.F., Silber, M.H., and Ferman, T.J., Sleep Med., 2003, vol. 4, no. 4, pp. 281–284.

    Article  PubMed  Google Scholar 

  89. McCleery, J., Cohen, D.A., and Sharpley, A.L., Cochrane Database Syst. Rev., 2014, vol. 21, no. 3: CD009178.

    Google Scholar 

  90. Baronio, D., Gonchoroski, T., Castro, K., Zanatta, G., Gottfried, C., and Riesgo, R., Ann. Gen. Psychiatry, 2014, vol. 13, no. 1, p. 34.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Shan, L., Bao, A.M., and Swaab, D.F., Trends Neurosci., 2015, vol. 38, no. 3, pp. 167–177.

    Article  CAS  PubMed  Google Scholar 

  92. Scammell, T.E., Matheson, J.K., Honda, M., Thannickal, T.C., and Siegel, J.M., Neurobiol. Aging, 2012, vol. 33, no. 7, pp. 1318–1319.

    Article  CAS  PubMed  Google Scholar 

  93. Peyron, C., Sapin, E., Leger, L., Luppi, P.H., and Fort, P., Peptides, 2009, vol. 30, no. 11, pp. 2052–2059.

    Article  CAS  PubMed  Google Scholar 

  94. Verret, L., Goutagny, R., Fort, P., Cagnon, L., Salvert, D., Leger, L., Boissard, R., Salin, P., Peyron, C., and Luppi, P.H., BMC Neurosci., 2003, vol. 4: 19.

    Google Scholar 

  95. Cooke, J.R., Loredo, J.S., Liu, L., Marler, M., Corey-Bloom, J., Fiorentino, L., Harrison, T., and Ancoli-Israel, S., Drugs Aging, 2006, vol. 23, no. 6, pp. 503–511.

    Article  CAS  PubMed  Google Scholar 

  96. Moraes, WdosS., Poyares, D.R., Guilleminault, C., Ramos, L.R., Bertolucci, P.H., and Tufik, S., Sleep, vol. 29, no. 2, pp. 199–205.

  97. Schredl, M., Hornung, O., Regen, F., Albrecht, N., Danker-Hopfe, H., and Heuser, I., Pharmacopsychiatry, 2006, vol. 39, no. 6, pp. 205–208.

    Article  CAS  PubMed  Google Scholar 

  98. Yeh, S.B., Yeh, P.Y., and Schenck, C.H., J. Clin. Sleep Med., 2010, vol. 6, no. 2, pp. 192–195.

    PubMed  PubMed Central  Google Scholar 

  99. Wu, T.Y., Chen, C.P., and Jinn, T.R., Taiwan J. Obstet. Gynecol., 2010, vol. 49, no. 4, pp. 468–472.

    Article  PubMed  Google Scholar 

  100. Van Dort, C.J., Zachs, D.P., Kenny, J.D., Zheng, S., Goldblum, R.R., Gelwan, N.A., Ramos, D.M., Nolan, M.A., Wang, K., Weng, F.J., Lin, Y., Wilson, M.A., and Brown, E.N., Proc. Natl. Acad. Sci. USA, 2015, vol. 112, no. 2, pp. 584–589.

    Article  PubMed  CAS  Google Scholar 

  101. Bick, S.K. and Eskandar, E.N., Neurosurg. Focus, 2016, vol. 40, no. 5: E5.

    Article  PubMed  Google Scholar 

  102. Garcia-Rill, E., Luster, B., D’Onofrio, S., Mahaffey, S., Bisagno, V., and Urbano, F.J., Sleep Sci., 2015, vol. 8, no. 3, pp. 153–161.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Morita, H., Hass, C.J., Moro, E., Sudhyadhom, A., Kumar, R., and Okun, M.S., Front. Neurol., 2014, vol. 5: 243.

    Article  PubMed  PubMed Central  Google Scholar 

  104. Amara, A.W., Watts, R.L., and Walker, H.C., Ther. Adv. Neurol. Disord., 2011, vol. 4, no. 1, pp. 15–24.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Romigi, A., Placidi, F., Peppe, A., Pierantozzi, M., Izzi, F., Brusa, L., Galati, S., Moschella, V., Marciani, M.G., Mazzone, P., Stanzione, P., and Stefani, A., Eur. J. Neurol., 2008, vol. 15, no. 7, pp. e64–e65.

    Article  CAS  PubMed  Google Scholar 

  106. Lim, A.S., Moro, E., Lozano, A.M., Hamani, C., Dostrovsky, J.O., Hutchison, W.D., Lang, A.E., Wennberg, R.A., and Murray, B.J., Ann. Neurol., 2009, vol. 66, no. 1, pp. 110–114.

    Article  PubMed  Google Scholar 

  107. Peppe, A., Pierantozzi, M., Baiamonte, V., Moschella, V., Caltagirone, C., Stanzione, P., and Stefani, A., Sleep, vol. 35, no. 12, pp. 1637–1642.

  108. Datta, S. and Siwek, D.F., J. Neurophysiol., 1997, vol. 77, no. 6, pp. 2975–2988.

    CAS  PubMed  Google Scholar 

  109. Datta, S., Spoley, E.E., and Patterson, E.H., Am. J. Physiol. Regul. Integr. Comp. Physiol., 2001, vol. 280, no. 3, pp. R752–R759.

    CAS  PubMed  Google Scholar 

  110. Thakkar, M., Portas, C., and McCarley, R.W., Brain Res., 1996, vol. 723, nos. 1–2, pp. 223–227.

    Article  CAS  PubMed  Google Scholar 

  111. Shouse, M.N. and Siegel, J.M., Brain Res., 1992, vol. 571, no. 1, pp. 50–63.

    Article  CAS  PubMed  Google Scholar 

  112. Webster, H.H. and Jones, B.E., Brain Res., 1988, vol. 458, no. 2, pp. 285–302.

    Article  CAS  PubMed  Google Scholar 

  113. Moe, K.E., Vitiello, M.V., Larsen, L.H., and Prinz, P.N., J. Sleep Res., 1995, vol. 4, no. 1, pp. 15–20.

    Article  CAS  PubMed  Google Scholar 

  114. Boyce, R., Glasgow, S.D., Williams, S., and Adamantidis, A., Science, 2016, vol. 352, no. 6287, pp. 812–816.

    Article  CAS  PubMed  Google Scholar 

  115. Dasari, S. and Gulledge, A.T., J. Neurophysiol., 2011, vol. 105, no. 2, pp. 779–792.

    Article  PubMed  Google Scholar 

  116. Szabó, G.G., Holderith, N., Gulyás, A.I., Freund, T.F., and Hajos, N., Eur. J. Neurosci., 2010, vol. 31, no. 12, pp. 2234–2246.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Lu, C.B. and Henderson, Z., Neuroscience, 2010, vol. 166, no. 1, pp. 84–93.

    Article  CAS  PubMed  Google Scholar 

  118. McKenna, J.T. and Vertes, R.P., J. Comp. Neurol., 2004, vol. 480, no. 2, pp. 115–142.

    Article  PubMed  Google Scholar 

  119. Bokor, H., Csáki, A., Kocsis, K., and Kiss, J., Eur. J. Neurosci., 2002, vol. 16, no. 7, pp. 1227–1239.

    Article  PubMed  Google Scholar 

  120. Vertes, R.P., Colom, L.V., Fortin, W.J., and Bland, B.H., Exp. Brain Res., 1993, vol. 96, no. 3, pp. 419–429.

    Article  CAS  PubMed  Google Scholar 

  121. Takano, Y. and Hanada, Y., Neurosci. Let., 2009, vol. 455, no. 1, pp. 65–69.

    Article  CAS  Google Scholar 

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  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

    I. G. Silkis

  2. ul. Butlerova, 5a, 117485, Moscow, Russia

    I. G. Silkis

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Original Russian Text © I.G. Silkis, 2017, published in Neirokhimiya, 2017, Vol. 34, No. 2, pp. 118–128.

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Silkis, I.G. Hypothetical neurochemical mechanisms of paradoxical sleep deficiency in Alzheimer’s disease. Neurochem. J. 11, 138–148 (2017). https://doi.org/10.1134/S181971241702012X

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