OpenLB
Open Library of Bioscience
Advanced Search
Nature communications
Dec 01, 2023;14 (1): 7927.

Opposing brain signatures of sleep in task-based and resting-state conditions.

Mohamed Abdelhack, Peter Zhukovsky, Milos Milic, Shreyas Harita, Michael Wainberg, Shreejoy J Tripathy, John D Griffiths, Sean L Hill, Daniel Felsky
Author Information
  1. Mohamed Abdelhack: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada. ORCID
  2. Peter Zhukovsky: Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, ON, Canada.
  3. Milos Milic: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada.
  4. Shreyas Harita: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada.
  5. Michael Wainberg: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada.
  6. Shreejoy J Tripathy: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada.
  7. John D Griffiths: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada.
  8. Sean L Hill: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada. ORCID
  9. Daniel Felsky: Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health, Toronto, ON, Canada. daniel.felsky@camh.ca. ORCID
PMID: 38040769 DOI: 10.1038/s41467-023-43737-7

Abstract

Sleep and depression have a complex, bidirectional relationship, with sleep-associated alterations in brain dynamics and structure impacting a range of symptoms and cognitive abilities. Previous work describing these relationships has provided an incomplete picture by investigating only one or two types of sleep measures, depression, or neuroimaging modalities in parallel. We analyze the correlations between brainwide neural signatures of sleep, cognition, and depression in task and resting-state data from over 30,000 individuals from the UK Biobank and Human Connectome Project. Neural signatures of insomnia and depression are negatively correlated with those of sleep duration measured by accelerometer in the task condition but positively correlated in the resting-state condition. Our results show that resting-state neural signatures of insomnia and depression resemble that of rested wakefulness. This is further supported by our finding of hypoconnectivity in task but hyperconnectivity in resting-state data in association with insomnia and depression. These observations dispute conventional assumptions about the neurofunctional manifestations of hyper- and hypo-somnia, and may explain inconsistent findings in the literature.

References

  1. Cereb Cortex. 2008 Sep;18(9):2077-85 [PMID: 18203694]
  2. Sleep Med Rev. 2006 Feb;10(1):49-62 [PMID: 16376591]
  3. J Clin Psychopharmacol. 2018 Oct;38(5):513-519 [PMID: 30124583]
  4. Sleep Med Rev. 2010 Feb;14(1):9-15 [PMID: 19640748]
  5. JAMA Psychiatry. 2018 Oct 1;75(10):1052-1061 [PMID: 30046833]
  6. J Neurophysiol. 2018 Nov 1;120(5):2498-2512 [PMID: 30156458]
  7. Vision Res. 2001;41(10-11):1409-22 [PMID: 11322983]
  8. Eur Neurol. 2016;75(1-2):48-57 [PMID: 26784899]
  9. J Sleep Res. 2000 Dec;9(4):335-52 [PMID: 11123521]
  10. Front Syst Neurosci. 2008 Nov 24;2:4 [PMID: 19104670]
  11. Neuroimage. 2015 May 1;111:147-58 [PMID: 25700949]
  12. BMC Psychiatry. 2023 Sep 15;23(1):671 [PMID: 37715146]
  13. Psychiatry (Edgmont). 2006 Apr;3(4):33-9 [PMID: 21103169]
  14. Neuron. 2011 Apr 14;70(1):153-69 [PMID: 21482364]
  15. Neuroimage. 2011 Sep 15;58(2):595-604 [PMID: 21745579]
  16. Psychiatry Res. 1989 May;28(2):193-213 [PMID: 2748771]
  17. PLoS Med. 2021 Oct 12;18(10):e1003782 [PMID: 34637446]
  18. Sci Rep. 2018 Apr 12;8(1):5891 [PMID: 29651014]
  19. Nature. 2011 Apr 28;472(7344):443-7 [PMID: 21525926]
  20. Neuroimage. 2022 Feb 15;247:118825 [PMID: 34942362]
  21. Neuroimage. 2005 Apr 1;25(2):579-87 [PMID: 15784437]
  22. J Clin Psychiatry. 2017 Sep/Oct;78(8):e1020-e1034 [PMID: 28937707]
  23. Nature. 2022 Mar;603(7902):654-660 [PMID: 35296861]
  24. Psychiatry Res. 2013 Mar 30;206(1):88-97 [PMID: 23083918]
  25. Nat Neurosci. 2016 Nov;19(11):1523-1536 [PMID: 27643430]
  26. Neuropsychiatr Dis Treat. 2019 May 10;15:1249-1258 [PMID: 31190831]
  27. Depress Anxiety. 2015 Sep;32(9):664-70 [PMID: 26047492]
  28. Neuroimage. 2010 Jan 15;49(2):1903-10 [PMID: 19761853]
  29. Sleep Med Rev. 2022 Feb;61:101569 [PMID: 34902821]
  30. Neuropsychiatr Dis Treat. 2017 Jun 06;13:1449-1462 [PMID: 28652745]
  31. Neuroimage. 2018 Feb 1;166:400-424 [PMID: 29079522]
  32. Sleep. 2009 Jun;32(6):767-71 [PMID: 19544753]
  33. Brain Res Cogn Brain Res. 2004 Feb;18(3):306-21 [PMID: 14741317]
  34. Ann N Y Acad Sci. 2013 Aug;1296:108-34 [PMID: 23738883]
  35. Front Neurol. 2012 Apr 27;3:67 [PMID: 22557992]
  36. J Sleep Res. 1997 Sep;6(3):179-88 [PMID: 9358396]
  37. Cochrane Database Syst Rev. 2021 Jul 27;7:CD010783 [PMID: 34313331]
  38. Eur Radiol. 2018 Feb;28(2):664-672 [PMID: 28828546]
  39. Nat Neurosci. 2005 May;8(5):679-85 [PMID: 15852014]
  40. Nat Commun. 2023 Dec 1;14(1):7927 [PMID: 38040769]
  41. Brain Sci. 2017 Feb 23;7(3): [PMID: 28241468]
  42. Neuroimage. 2018 Sep;178:540-551 [PMID: 29860082]
  43. Neuroimage. 2010 Jun;51(2):835-43 [PMID: 20171288]
  44. Neuroimage. 2013 Oct 15;80:105-24 [PMID: 23668970]
  45. Sleep Med Rev. 2012 Feb;16(1):83-94 [PMID: 21636297]
  46. J Affect Disord. 2004 Jul;81(1):61-6 [PMID: 15183601]
  47. Neuroimage. 2012 Aug 15;62(2):782-90 [PMID: 21979382]
  48. JAMA Psychiatry. 2015 Jun;72(6):603-11 [PMID: 25785575]
  49. J Neurophysiol. 2009 Oct;102(4):2096-111 [PMID: 19657080]
  50. Int J Environ Res Public Health. 2021 Jan 26;18(3): [PMID: 33530453]
  51. Sleep Med Rev. 2010 Aug;14(4):227-38 [PMID: 20137989]
  52. Sleep Med Rev. 2016 Feb;25:52-73 [PMID: 26163057]
  53. Sleep. 1992 Aug;15(4):293-301 [PMID: 1519002]
  54. Commun Biol. 2022 Jan 11;5(1):34 [PMID: 35017660]
  55. JAMA. 2020 Jun 9;323(22):2290-2300 [PMID: 32515813]
  56. Dialogues Clin Neurosci. 2008;10(3):329-36 [PMID: 18979946]
  57. Science. 2001 Sep 28;293(5539):2425-30 [PMID: 11577229]
  58. Psychosom Med. 2010 May;72(4):397-403 [PMID: 20368477]
  59. Sleep Med Rev. 2001 Oct;5(5):363-374 [PMID: 12531000]
  60. Cereb Cortex. 2009 Jan;19(1):233-40 [PMID: 18483003]
  61. J Neurosci. 2008 May 21;28(21):5519-28 [PMID: 18495886]
  62. Epidemiology. 2008 Nov;19(6):838-45 [PMID: 18854708]
  63. Neuroimage. 2002 Sep;17(1):317-23 [PMID: 12482086]
  64. Neuroimage. 2013 Oct 15;80:169-89 [PMID: 23684877]
  65. Sleep. 2013 Jun 01;36(6):857-71 [PMID: 23729929]
  66. Hum Brain Mapp. 2009 Jul;30(7):2207-19 [PMID: 18937282]
  67. J Clin Med. 2023 Sep 16;12(18): [PMID: 37762948]
  68. Neuropsychologia. 2012 Mar;50(4):544-52 [PMID: 22100534]
  69. PLoS One. 2014 Apr 23;9(4):e94973 [PMID: 24759619]
  70. Sleep Health. 2015 Sep;1(3):214-220 [PMID: 29073443]
  71. Brain Imaging Behav. 2020 Oct;14(5):1430-1444 [PMID: 31011953]
  72. Medicine (Baltimore). 2018 Aug;97(34):e11944 [PMID: 30142814]
  73. Neuroimage. 2012 Oct 1;62(4):2222-31 [PMID: 22366334]
  74. Neuroimage. 2014 Aug 15;97:271-83 [PMID: 24768930]
  75. Nat Protoc. 2017 Mar;12(3):506-518 [PMID: 28182017]
  76. Nat Rev Neurosci. 2017 Jul;18(7):404-418 [PMID: 28515433]
  77. Lancet Psychiatry. 2016 May;3(5):425-35 [PMID: 26995298]
  78. Brain Imaging Behav. 2022 Aug;16(4):1538-1551 [PMID: 35088354]
  79. Neuropsychiatr Dis Treat. 2015 Dec 16;11:3085-93 [PMID: 26719693]
  80. Psychiatry Res Neuroimaging. 2017 Jul 30;265:26-34 [PMID: 28500965]
  81. Science. 2005 Sep 30;309(5744):2228-32 [PMID: 16195466]
  82. PLoS One. 2013;8(2):e56578 [PMID: 23418586]
  83. Med Care. 2003 Nov;41(11):1284-92 [PMID: 14583691]
  84. Sleep Med Rev. 2010 Feb;14(1):19-31 [PMID: 19481481]
  85. Proc Natl Acad Sci U S A. 2007 May 29;104(22):9487-92 [PMID: 17517619]
  86. Nature. 2016 Aug 11;536(7615):171-178 [PMID: 27437579]
  87. J Sleep Res. 2008 Jun;17(2):180-90 [PMID: 18482106]
  88. Sleep Med. 2023 Mar;103:41-50 [PMID: 36758346]
  89. J Neurophysiol. 2011 Sep;106(3):1125-65 [PMID: 21653723]
  90. J Neurosci. 2021 Sep 22;41(38):8065-8074 [PMID: 34380762]
  91. Neuroimage. 2012 Aug 15;62(2):774-81 [PMID: 22248573]

MeSH Term

Humans
Sleep Initiation and Maintenance Disorders
Magnetic Resonance Imaging
Brain
Sleep
Cognition
Journal Article
Article has an altmetric score of 16

Word Cloud

Created with Highcharts 10.0.0depressionresting-statesleepsignaturestaskinsomniabrainneuraldatacorrelatedconditionSleepcomplexbidirectionalrelationshipsleep-associatedalterationsdynamicsstructureimpactingrangesymptomscognitiveabilitiesPreviousworkdescribingrelationshipsprovidedincompletepictureinvestigatingonetwotypesmeasuresneuroimagingmodalitiesparallelanalyzecorrelationsbrainwidecognition30000individualsUKBiobankHumanConnectomeProjectNeuralnegativelydurationmeasuredaccelerometerpositivelyresultsshowresemblerestedwakefulnesssupportedfindinghypoconnectivityhyperconnectivityassociationobservationsdisputeconventionalassumptionsneurofunctionalmanifestationshyper-hypo-somniamayexplaininconsistentfindingsliteratureOpposingtask-basedconditions

Similar Articles

Cited By