دورية أكاديمية
أعرض في EDS

Impaired Hippocampal-Cortical Interactions during Sleep in a Mouse Model of Alzheimer's Disease.

التفاصيل البيبلوغرافية
العنوان: Impaired Hippocampal-Cortical Interactions during Sleep in a Mouse Model of Alzheimer's Disease.
المؤلفون: Benthem SD; Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA. Electronic address: benthem@psy.fsu.edu., Skelin I; Department of Neurobiology and Behavior, University of California Irvine, Irvine, CA 92697, USA., Moseley SC; Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA., Stimmell AC; Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA., Dixon JR; Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA., Melilli AS; Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA., Molina L; Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada., McNaughton BL; Department of Neurobiology and Behavior, University of California Irvine, Irvine, CA 92697, USA; Department of Neuroscience, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada., Wilber AA; Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306, USA. Electronic address: awilber@fsu.edu.
المصدر: Current biology : CB [Curr Biol] 2020 Jul 06; Vol. 30 (13), pp. 2588-2601.e5. Date of Electronic Publication: 2020 May 28.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.
اللغة: English
بيانات الدورية: Publisher: Cell Press Country of Publication: England NLM ID: 9107782 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1879-0445 (Electronic) Linking ISSN: 09609822 NLM ISO Abbreviation: Curr Biol Subsets: MEDLINE
أسماء مطبوعة: Publication: Cambridge, MA : Cell Press
Original Publication: London, UK : Current Biology Ltd., c1991-
مواضيع طبية MeSH: Memory Consolidation* , Sleep*, Alzheimer Disease/*physiopathology , Hippocampus/*physiopathology , Memory Disorders/*physiopathology , Neocortex/*physiopathology, Animals ; Disease Models, Animal ; Female ; Mice ; Mice, Transgenic ; Spatial Memory
مستخلص: Spatial learning is impaired in humans with preclinical Alzheimer's disease (AD). We reported similar impairments in 3xTg-AD mice learning a spatial reorientation task. Memory reactivation during sleep is critical for learning-related plasticity, and memory consolidation is correlated with hippocampal sharp wave ripple (SWR) density, cortical delta waves (DWs), cortical spindles, and the temporal coupling of these events-postulated as physiological substrates for memory consolidation. Further, hippocampal-cortical discoordination is prevalent in individuals with AD. Thus, we hypothesized that impaired memory consolidation mechanisms in hippocampal-cortical networks could account for spatial memory deficits. We assessed sleep architecture, SWR-DW dynamics, and memory reactivation in a mouse model of tauopathy and amyloidosis implanted with a recording array targeting isocortex and hippocampus. Mice underwent daily recording sessions of rest-task-rest while learning the spatial reorientation task. We assessed memory reactivation by matching activity patterns from the approach to the unmarked reward zone to patterns during slow-wave sleep (SWS). AD mice had more SWS, but reduced SWR density. The increased SWS compensated for reduced SWR density so there was no reduction in SWR number. In control mice, spindles were phase-coupled with DWs, and hippocampal SWR-cortical DW coupling was strengthened in post-task sleep and was correlated with performance on the spatial reorientation task the following day. However, in AD mice, SWR-DW and spindle-DW coupling were impaired. Thus, reduced SWR-DW coupling may cause impaired learning in AD, and spindle-DW coupling during short rest-task-rest sessions may serve as a biomarker for early AD-related changes in these brain dynamics.
Competing Interests: Declaration of Interests The authors declare no competing interests.
(Copyright © 2020 Elsevier Inc. All rights reserved.)
التعليقات: Erratum in: Curr Biol. 2024 Mar 28;:. (PMID: 38552626)
References: J Alzheimers Dis. 2010;22(3):873-87. (PMID: 20858963)
Neurobiol Sleep Circadian Rhythms. 2017 Jan;2:4-14. (PMID: 28217760)
J Alzheimers Dis. 2017;59(1):21-29. (PMID: 28550245)
JAMA Neurol. 2013 May;70(5):587-93. (PMID: 23479184)
Physiol Behav. 2014 Aug;135:25-33. (PMID: 24907698)
Ann Neurol. 1991 Oct;30(4):572-80. (PMID: 1789684)
J Neurosci. 1999 Jul 15;19(14):6191-9. (PMID: 10407055)
J Vis Exp. 2013 Jul 05;(77):e50470. (PMID: 23851569)
Proc Natl Acad Sci U S A. 2008 Jun 3;105(22):7863-8. (PMID: 18505838)
Neuroscience. 2003;116(1):201-11. (PMID: 12535953)
PLoS One. 2013 Nov 13;8(11):e80355. (PMID: 24236177)
Am J Pathol. 2005 Nov;167(5):1361-9. (PMID: 16251420)
Neurobiol Aging. 2012 Nov;33(11):2533-50. (PMID: 22365486)
Cereb Cortex. 2012 Aug;22(8):1813-23. (PMID: 21945849)
Biol Psychiatry. 1989 Feb 1;25(3):320-8. (PMID: 2914155)
Neuron. 2005 Mar 3;45(5):675-88. (PMID: 15748844)
Nat Neurosci. 2009 Jul;12(7):919-26. (PMID: 19483687)
J Neurophysiol. 2000 Jul;84(1):401-14. (PMID: 10899214)
Curr Alzheimer Res. 2013 Jan;10(1):95-103. (PMID: 23036016)
Front Pharmacol. 2019 Jun 20;10:695. (PMID: 31281257)
J Neurosci. 2019 Aug 7;39(32):6315-6324. (PMID: 31209175)
Acta Neuropathol. 1991;82(4):239-59. (PMID: 1759558)
Neuron. 2012 Sep 20;75(6):1001-7. (PMID: 22998869)
J Physiol. 2003 Aug 1;550(Pt 3):873-87. (PMID: 12807984)
Sleep. 2017 May 1;40(5):. (PMID: 28329084)
Nat Rev Neurosci. 2010 Feb;11(2):114-26. (PMID: 20046194)
Psychol Rev. 2007 Apr;114(2):340-75. (PMID: 17500630)
Neurobiol Learn Mem. 2015 Nov;125:152-162. (PMID: 26385257)
J Neurosci. 2014 Apr 9;34(15):5200-10. (PMID: 24719099)
Neurobiol Aging. 2016 May;41:107-114. (PMID: 27103523)
Physiol Rev. 2013 Apr;93(2):681-766. (PMID: 23589831)
Curr Top Behav Neurosci. 2013;15:313-40. (PMID: 23670818)
Ann Neurol. 2002 Feb;51(2):182-9. (PMID: 11835374)
Front Neurorobot. 2017 Feb 07;11:4. (PMID: 28223931)
Nat Neurosci. 2016 Jul;19(7):959-64. (PMID: 27182818)
Exp Mol Med. 2015 Mar 13;47:e148. (PMID: 25766617)
Nature. 1993 Jan 7;361(6407):31-9. (PMID: 8421494)
J Sleep Res. 2005 Sep;14(3):311-7. (PMID: 16120107)
J Alzheimers Dis. 2017;59(3):883-892. (PMID: 28697554)
PLoS One. 2013 Aug 28;8(8):e74070. (PMID: 24015315)
Ann Neurol. 2006 Mar;59(3):512-9. (PMID: 16372280)
Neuron. 1998 Nov;21(5):1123-8. (PMID: 9856467)
Trends Neurosci. 2016 Aug;39(8):552-566. (PMID: 27325209)
Nature. 1982 Jun 24;297(5868):681-3. (PMID: 7088155)
Nat Neurosci. 2015 Nov;18(11):1679-1686. (PMID: 26389842)
Nature. 2006 Mar 30;440(7084):680-3. (PMID: 16474382)
Neuron. 2018 Jan 3;97(1):221-230.e4. (PMID: 29249289)
Science. 2015 Oct 23;350(6259):430-3. (PMID: 26494756)
Neurosci Biobehav Rev. 2012 Jan;36(1):297-309. (PMID: 21741401)
Neuron. 2009 Dec 24;64(6):910-21. (PMID: 20064396)
Neuron. 2016 Apr 6;90(1):113-27. (PMID: 26971950)
J Gerontol. 1990 Jul;45(4):M131-8. (PMID: 2365965)
Neurobiol Dis. 2004 Jul;16(2):291-9. (PMID: 15193286)
Neurology. 2017 Aug 1;89(5):445-453. (PMID: 28679595)
J Alzheimers Dis. 2016 Feb 9;52(1):77-90. (PMID: 26967209)
J Neurosci. 2013 Apr 17;33(16):7027-37. (PMID: 23595760)
Nat Neurosci. 2014 Feb;17(2):304-11. (PMID: 24362760)
Behav Neurosci. 2018 Oct;132(5):416-429. (PMID: 30091619)
Science. 2007 Nov 16;318(5853):1147-50. (PMID: 18006749)
Trends Cogn Sci. 2007 Oct;11(10):442-50. (PMID: 17905642)
Neurobiol Aging. 2015 Sep;36(9):2568-76. (PMID: 26059712)
J Physiol. 2005 Mar 15;563(Pt 3):663-70. (PMID: 15661820)
Brain Res. 2002 Feb 22;928(1-2):126-37. (PMID: 11844479)
Neuron. 1999 Nov;24(3):521-9. (PMID: 10595506)
Neuroimage Clin. 2016 May 26;12:78-84. (PMID: 27408792)
Int J Geriatr Psychiatry. 2000 Nov;15(11):1028-33. (PMID: 11113983)
Neuron. 2017 Sep 13;95(6):1406-1419.e5. (PMID: 28910623)
Neurobiol Learn Mem. 2019 Apr;160:21-31. (PMID: 29660400)
Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):2065-9. (PMID: 12576550)
Neuron. 2016 Sep 21;91(6):1342-1355. (PMID: 27593179)
JAMA Neurol. 2014 Dec;71(12):1498-505. (PMID: 25322206)
J Neurosci Methods. 2003 Nov 30;130(1):93-101. (PMID: 14583408)
J Neurosci. 2010 Feb 17;30(7):2650-61. (PMID: 20164349)
Nat Neurosci. 2003 Jun;6(6):609-15. (PMID: 12717437)
Nat Neurosci. 2012 Oct;15(10):1365-7. (PMID: 22960933)
Brain. 2017 Aug 1;140(8):2066-2069. (PMID: 28899024)
Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):21159-64. (PMID: 24324174)
Neuroscience. 1989;31(3):551-70. (PMID: 2687720)
Neuron. 2016 Dec 7;92(5):968-974. (PMID: 27840002)
Science. 1994 Jul 29;265(5172):676-9. (PMID: 8036517)
JAMA. 2011 Aug 10;306(6):613-9. (PMID: 21828324)
Cereb Cortex. 1994 Nov-Dec;4(6):664-80. (PMID: 7703691)
Behav Brain Res. 2019 Jan 1;356:305-313. (PMID: 30208295)
Brain. 2007 Nov;130(Pt 11):2868-78. (PMID: 17615093)
Sleep. 2013 Jul 1;36(7):1027-1032. (PMID: 23814339)
Sleep Med Rev. 2015 Feb;19:29-38. (PMID: 24846773)
Neurosci Biobehav Rev. 1998 Mar;22(2):275-90. (PMID: 9579318)
Neuromolecular Med. 2012 Sep;14(3):194-204. (PMID: 22552887)
Biol Psychiatry. 2018 Feb 15;83(4):328-336. (PMID: 29279202)
Neuron. 2008 Nov 26;60(4):683-97. (PMID: 19038224)
Brain. 1999 Sep;122 ( Pt 9):1613-28. (PMID: 10468502)
Nat Rev Neurol. 2014 Feb;10(2):115-9. (PMID: 24366271)
Neuron. 2017 Sep 27;96(1):217-227.e4. (PMID: 28957670)
Science. 2012 Jun 15;336(6087):1454-8. (PMID: 22555434)
Arch Neurol. 1989 Apr;46(4):391-4. (PMID: 2705898)
Behav Neurosci. 1986 Apr;100(2):147-54. (PMID: 3008780)
Neurobiol Dis. 2016 Jul;91:105-23. (PMID: 26949217)
J Neurol Neurosurg Psychiatry. 1957 Feb;20(1):11-21. (PMID: 13406589)
J Neurosci. 2004 May 12;24(19):4541-50. (PMID: 15140925)
Behav Neural Biol. 1993 Jul;60(1):9-26. (PMID: 8216164)
Neuron. 2001 Jan;29(1):145-56. (PMID: 11182087)
Wiley Interdiscip Rev Cogn Sci. 2010 Jul;1(4):478-490. (PMID: 26271495)
Nat Neurosci. 2007 Jan;10(1):100-7. (PMID: 17173043)
Nat Neurosci. 2011 Aug 07;14(9):1174-81. (PMID: 21822270)
Nat Rev Neurosci. 2005 Feb;6(2):119-30. (PMID: 15685217)
Neuron. 2016 May 18;90(4):740-51. (PMID: 27161522)
Nat Neurosci. 2017 Jun;20(6):845-853. (PMID: 28394323)
Cold Spring Harb Perspect Med. 2012 Apr;2(4):a006171. (PMID: 22474609)
Nat Neurosci. 2009 Oct;12(10):1222-3. (PMID: 19749750)
J Neurosci. 2015 May 27;35(21):8118-31. (PMID: 26019329)
Hippocampus. 2010 Jan;20(1):1-10. (PMID: 19816984)
Nat Neurosci. 2014 Dec;17(12):1658-60. (PMID: 25326690)
Sci Rep. 2019 Feb 4;9(1):1311. (PMID: 30718609)
Sci Rep. 2017 Jan 03;7:39688. (PMID: 28045040)
Nat Neurosci. 2007 Oct;10(10):1241-2. (PMID: 17828259)
J Neurosci. 2014 Apr 16;34(16):5431-46. (PMID: 24741034)
J Physiol. 2016 Aug 15;594(16):4615-30. (PMID: 25480798)
Behav Brain Res. 2015 Mar 15;281:16-23. (PMID: 25486177)
Nature. 2016 Mar 24;531(7595):508-12. (PMID: 26982728)
Neuron. 2012 Feb 23;73(4):789-802. (PMID: 22365551)
Prog Brain Res. 1990;83:435-43. (PMID: 2203107)
Elife. 2013 Jun 25;2:e00647. (PMID: 23805379)
Neuroscience. 2005;131(2):375-85. (PMID: 15708480)
J Alzheimers Dis. 2018;64(4):1325-1336. (PMID: 29991134)
Neuron. 2005 Mar 3;45(5):667-74. (PMID: 15748843)
Behav Neurosci. 2006 Aug;120(4):852-60. (PMID: 16893291)
Philos Trans R Soc Lond B Biol Sci. 1997 Oct 29;352(1360):1525-33. (PMID: 9368941)
Eur J Neurosci. 2011 Feb;33(3):511-20. (PMID: 21138489)
Sleep. 2016 Nov 01;39(11):2041-2048. (PMID: 27568802)
J Neurosci. 2013 Dec 4;33(49):19304-13. (PMID: 24305826)
Neuron. 2017 Jul 19;95(2):424-435.e6. (PMID: 28689981)
Nature. 2017 Jul 12;547(7662):153-155. (PMID: 28703214)
Brain. 2017 Aug 1;140(8):2104-2111. (PMID: 28899014)
Neuron. 2003 Jul 31;39(3):409-21. (PMID: 12895417)
Sci Transl Med. 2012 Sep 5;4(150):150ra122. (PMID: 22956200)
J Neurosci. 2008 Jun 18;28(25):6372-82. (PMID: 18562607)
Cell Rep. 2019 Nov 19;29(8):2123-2133.e4. (PMID: 31747587)
Behav Brain Res. 2019 Nov 5;373:112089. (PMID: 31325518)
Hippocampus. 2000;10(4):352-68. (PMID: 10985275)
Neuron. 2009 Oct 29;64(2):267-80. (PMID: 19874793)
Ann Neurol. 2018 Jan;83(1):197-204. (PMID: 29220873)
Sleep. 2018 May 1;41(5):. (PMID: 29425372)
معلومات مُعتمدة: K99 AG049090 United States AG NIA NIH HHS; R00 AG049090 United States AG NIA NIH HHS; PJT 156040 Canada CIHR
فهرسة مساهمة: Keywords: Alzheimer's disease; hippocampal-cortical dynamics; hippocampus; memory reactivation; memory replay; parietal cortex; sharp wave ripples; sleep; spatial memory; spatial orientation
تواريخ الأحداث: Date Created: 20200530 Date Completed: 20210809 Latest Revision: 20240329
رمز التحديث: 20240330
مُعرف محوري في PubMed: PMC7356567
DOI: 10.1016/j.cub.2020.04.087
PMID: 32470367
قاعدة البيانات: MEDLINE
الوصف
تدمد:1879-0445
DOI:10.1016/j.cub.2020.04.087