Sleep is related to neuron numbers in the ventrolateral preoptic/intermediate nucleus in older adults with and without Alzheimer's disease

Brain

Volumn 137, Issue 10, 2014, Pages 2847-2861

  Lim, Andrew S P ^a,b,c   Ellison, Brian A ^b,c   Wang, Joshua L ^b,c   Yu, Lei ^d   Schneider, Julie A ^d   Buchman, Aron S ^d   Bennett, David A ^d   Saper, Clifford B ^b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; human; hypothalamus; intermediate nucleus; sleep

Indexed keywords

GALANIN;

ACTIMETRY; AGING; ALZHEIMER DISEASE; ARTICLE; CELL COUNT; COHORT ANALYSIS; FEMALE; GROWTH, DEVELOPMENT AND AGING; HUMAN; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INTERMEDIATE NUCLEUS; MALE; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREOPTIC AREA; REST; SLEEP; SLEEP DEPRIVATION; SLEEP DISORDER; STATISTICAL ANALYSIS; SUPRACHIASMATIC NUCLEUS; VERY ELDERLY;

ALZHEIMER'S DISEASE; HUMAN; HYPOTHALAMUS; INTERMEDIATE NUCLEUS; SLEEP;

ACTIGRAPHY; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; CELL COUNT; COHORT STUDIES; DATA INTERPRETATION, STATISTICAL; FEMALE; GALANIN; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PREOPTIC AREA; REST; SLEEP; SLEEP DEPRIVATION; SLEEP DISORDERS; SUPRACHIASMATIC NUCLEUS;

EID: 84908374081     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awu222     Document Type: Article

References (66)

1. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 2007; 450: 420-4.
2. Allen LS, Hines M, Shryne JE, Gorski RA. Two sexually dimorphic cell groups in the human brain. J Neurosci 1989; 9: 497-506.
3. Allen SR, Seiler WO, Stahelin HB, Spiegel R. Seventy-Two hour polygraphic and behavioral recordings of wakefulness and sleep in a hospital geriatric unit: comparison between demented and nondemented patients. Sleep 1987; 10: 143-59.
4. Ancoli-Israel S, Kripke DF, Klauber MR, Mason WJ, Fell R, Kaplan O. Sleep-disordered breathing in community-dwelling elderly. Sleep 1991; 14: 486-95.
5. Bennett DA, Schneider JA, Buchman AS, Barnes LL, Boyle PA, Wilson RS. Overview and findings from the rush Memory and Aging Project. Curr Alzheimer Res 2012; 9: 646-63.
6. Bennett DA, Schneider JA, Aggarwal NT, Arvanitakis Z, Shah RC, Kelly JF, et al. Decision rules guiding the clinical diagnosis of Alzheimer's disease in two community-based cohort studies compared to standard practice in a clinic-based cohort study. Neuroepidemiology 2006a; 27: 169-76.
7. Bennett DA, Schneider JA, Arvanitakis Z, Kelly JF, Aggarwal NT, Shah RC, et al. Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology 2006b; 66: 1837-44.
8. Bero AW, Yan P, Roh JH, Cirrito JR, Stewart FR, Raichle ME, et al. Neuronal activity regulates the regional vulnerability to amyloid-b deposition. Nat Neurosci 2011; 16: 750-6.
9. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-59.
10. Brockhaus H. Beitrag zur normalen Anatomie des Hypothalamus und der Zona incerta beim Menschen. J Psychol Neurol 1942; 51: 96-196.
11. Chawla MK, Gutierrez GM, Young WS 3rd, McMullen NT, Rance NE. Localization of neurons expressing substance P and neurokinin B gene transcripts in the human hypothalamus and basal forebrain. J Comp Neurol 1997; 384: 429-42.
12. Chou TC, Bjorkum AA, Gaus SE, Lu J, Scammell TE, Saper CB. Afferents to the ventrolateral preoptic nucleus. J Neurosci 2002; 22: 977-90.
13. Clark CN, Warren JD. A hypnic hypothesis of Alzheimer's disease. Neurodegener Dis 2013; 12: 165-76.
14. Cole MG, Dendukuri N. Risk factors for depression among elderly community subjects: A systematic review and meta-Analysis. Am J Psychiatry 2003; 160: 1147-56.
15. Cole RJ, Kripke DF, Gruen W, Mullaney DJ, Gillin JC. Automatic sleep/wake identification from wrist activity. Sleep 1992; 15: 461-9.
16. Dai J, Swaab DF, Buijs RM. Distribution of vasopressin and vasoactive intestinal polypeptide (VIP) fibers in the human hypothalamus with special emphasis on suprachiasmatic nucleus efferent projections. J Comp Neurol 1997; 1997: 397-414.
17. Fernandez-Guasti A, Kruijver FP, Fodor M, Swaab DF. Sex differences in the distribution of androgen receptors in the human hypothalamus. J Comp Neurol 2000; 425: 422-35.
18. Fliers E, Noppen NW, Wiersinga WM, Visser TJ, Swaab DF. Distribution of thyrotropin-releasing hormone (TRH)-containing cells and fibers in the human hypothalamus. J Comp Neurol 1994; 350: 311-23.
19. Gai WP, Geffen LB, Blessing WW. Galanin immunoreactive neurons in the human hypothalamus: colocalization with vasopressin-containing neurons. J Comp Neurol 1990; 298: 265-80.
20. Gao B, Moore RY. The sexually dimorphic nucleus of the hypothalamus contains GABA neurons in rat and man. Brain Res 1996; 742: 163-71.
21. Garcia-Falgueras A, Ligtenberg L, Kruijver FP, Swaab DF. Galanin neurons in the intermediate nucleus (InM) of the human hypothalamus in relation to sex, age, and gender identity. J Comp Neurol 2011; 519: 3061-84.
22. Gaus SE, Strecker RE, Tate BA, Parker RA, Saper CB. Ventrolateral preoptic nucleus contains sleep-Active, galaninergic neurons in multiple mammalian species. Neuroscience 2002; 115: 285-94.
23. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in sterology and its prediction. J Microsc 1987; 147 (Pt 3): 229-63.
24. Harper DG, Stopa EG, Kuo-Leblanc V, McKee AC, Asayama K, Volicer L, et al. Dorsomedial SCN neuronal subpopulations subserve different functions in human dementia. Brain 2008; 131 (Pt 6): 1609-17.
25. Harris JA, Devidze N, Verret L, Ho K, Halabisky B, Thwin MT, et al. Transsynaptic progression of amyloid-b-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 2010; 2010: 428-41.
26. Hidalgo JL, Gras CB, Garcia YD, Lapeira JT, del Campo del Campo JM, Verdejo MA. Functional status in the elderly with insomnia. Qual Life Res 2007; 16: 279-86.
27. Hofman MA, Swaab DF. The sexually dimorphic nucleus of the preoptic area in the human brain: A comparative morphometric study. J Anat 1989; 164: 55-72.
28. Hu K, Scheer FA, Ivanov P, Buijs RM, Shea SA. The suprachiasmatic nucleus functions beyond circadian rhythm generation. Neuroscience 2007; 149: 508-17.
29. Hu K, Van Someren EJ, Shea SA, Scheer FA. Reduction of scale invariance of activity fluctuations with aging and Alzheimer's disease: involvement of the circadian pacemaker. Proc Natl Acad Sci USA 2009; 106: 2490-4.
30. Ishunina TA, Swaab DF. Neurohypophyseal peptides in aging and Alzheimer's disease. Ageing Res Rev 2002; 1: 537-58.
31. Kang JE, Lim MM, Bateman RJ, Lee JJ, Smyth LP, Cirrito JR, et al. Amyloid-beta dynamics are regulated by orexin and the sleep-wake cycle. Science 2009; 326: 1005-7.
32. Koutcherov Y, Paxinos G, Mai JK. Organization of the human medial preoptic nucleus. J Comp Neurol 2007; 503: 392-406.
33. Kruijver FP, Balesar R, Espila AM, Unmehopa UA, Swaab DF. Estrogenreceptor-beta distribution in the human hypothalamus: similarities and differences with ER alpha distribution. J Comp Neurol 2003; 466: 251-77.
34. Lauderdale DS, Knutson KL, Yan LL, Liu K, Rathouz PJ. Self-reported and measured sleep duration: how similar are they? Epidemiology 2008; 19: 838-45.
35. Lee HM, Giguere PM, Roth BL. DREADDs: novel tools for drug discovery and development. Drug Discov Today 2013; 19: 469-73.
36. Lim AS, Kowgier M, Yu L, Buchman AS, Bennett DA. Sleep fragmentation and the risk of incident alzheimer's disease and cognitive decline in older persons. Sleep 2013; 36: 1027-32.
37. Lim AS, Moro E, Lozano AM, Hamani C, Dostrovsky JO, Hutchison WD, et al. Selective enhancement of rapid eye movement sleep by deep brain stimulation of the human pons. Ann Neurol 2009; 66: 110-4.
38. Lim AS, Yu L, Costa MD, Buchman AS, Bennett DA, Leurgans SE, et al. Quantification of the fragmentation of rest-Activity patterns in elderly individuals using a state transition analysis. Sleep 2011; 34: 1569-81.
39. Lim AS, Yu L, Costa MD, Leurgans SE, Buchman AS, Bennett DA, et al. Increased fragmentation of rest-Activity patterns is associated with a characteristic pattern of cognitive impairment in older individuals. Sleep 2012; 35: 633-40.
40. Liu RY, Zhou JN, Hoogendijk WJ, van Heerikhuize J, Kamphorst W, Unmehopa UA, et al. Decreased vasopressin gene expression in the biological clock of Alzheimer disease patients with and without depression. J Neuropathol Exp Neurol 2000; 59: 314-22.
41. Lu J, Greco MA, Shiromani P, Saper CB. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 2000; 20: 3830-42.
42. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDSADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 1984; 34: 939-44.
43. National Institute on Aging and Reagan Institute Working Group of Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. Neurobiol Aging 1997; 18 (Suppl 4): S1-S2.
44. Oosterman JM, van Someren EJ, Vogels RL, Van Harten B, Scherder EJ. Fragmentation of the rest-Activity rhythm correlates with age-related cognitive deficits. J Sleep Res 2009; 18: 129-35.
45. Pollak CP, Perlick D. Sleep problems and institutionalization of the elderly. J Geriatr Psychiatry Neurol 1991; 4: 204-10.
46. R Development Core Team. R: A language and environment for statistical computing. Vienne, Austria: R Foundation for Statistical Computing; 2008.
47. Roh JH, Huang Y, Bero AW, Kasten T, Stewart FR, Bateman RJ, et al. Disruption of the sleep-wake cycle and diurnal fluctuation of b-Amyloid in mice with Alzheimer's disease pathology. Sci Transl Med 2012; 4: 150ra22.
48. Saper CB. A guide to the perplexed on the specificity of antibodies. J Histochem Cytochem 2009; 57: 1-5.
49. Saper CB. An open letter to our readers on the use of antibodies. J Comp Neurol 2005; 493: 477-8.
50. Saper CB, German DC. Hypothalamic pathology in Alzheimer's disease. Neurosci Lett 1987; 74: 364-70.
51. Sherin JE, Elmquist JK, Torrealba F, Saper CB. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 1998; 18: 4705-21.
52. Sherin JE, Shiromani PJ, McCarley RW, Saper CB. Activation of ventrolateral preoptic neurons during sleep. Science 1996; 271: 216-9.
53. Stone KL, Ancoli-Israel S, Blackwell T, Ensrud KE, Cauley JA, Redline S, et al. Actigraphy-measured sleep characteristics and risk of falls in older women. Arch Intern Med 2008; 168: 1768-75.
54. Swaab DF, Fliers E. A sexually dimorphic nucleus in the human brain. Science 1985; 228: 1112-5.
55. Swaab DF, Fliers E, Partiman TS. The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia. Brain Res 1985; 342: 37-44.
56. Swaab DF, Hofman MA, Lucassen PJ, Purba JS, Raadsheer FC, Van de Nes JA. Functional neuroanatomy and neuropathology of the human hypothalamus. Anat Embryol (Berl) 1993; 187: 317-30.
57. Szymusiak R, Alam N, Steininger TL, McGinty D. Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res 1998; 803: 178-88.
58. van de Nes JA, Kamphorst W, Ravid R, Swaab DF. Comparison of betaprotein/A4 deposits and Alz-50-stained cytoskeletal changes in the hypothalamus and adjoining areas of Alzheimer's disease patients: Amorphic plaques and cytoskeletal changes occur independently. Acta Neuropathol 1998; 96: 129-38.
59. Van der Woude PF, Goudsmit E, Wierda M, Purba JS, Hofman MA, Bogte H, et al. No vasopressin cell loss in the human hypothalamus in aging and Alzheimer's disease. Neurobiol Aging 1995; 16: 11-8.
60. West MJ. Stereological methods for estimating the total number of neurons and synapses: isues of precision and bias. Trends Neurosci 1999; 22: 51-61.
61. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991; 231: 482-97.
62. Wilson RS, Barnes LL, Krueger KR, Hoganson G, Bienias JL, Bennett DA. Early and late life cognitive activity and cognitive systems in old age. J Int Neuropsychol Soc 2005; 11: 400-7.
63. Wu YH, Fischer DF, Kalsbeek A, Garidou-Boof ML, van der Vliet J, van Heijningen C, et al. Pineal clock gene oscillation is disturbed in Alzheimer's disease, due to functional disconnection from the "master clock". FASEB J 2006; 20: 1874-6.
64. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, et al. Sleep drives metabolite clearance from the adult brain. Science 2013; 342: 373-7.
65. Yamada K, Holth JK, Liao F, Stewart FR, Mahan TE, Jiang H, et al. Neuronal activity regulates extracellular tau in vivo. J Exp Med 2014; 211: 387-93.
66. Zhou JN, Hofman MA, Swaab DF. VIP neurons in the human SCN in relation to sex, age, and Alzheimer's disease. Neurobiol Aging 1995; 16: 571-6