Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation

NeuroImage

Volumn 111, Issue , 2015, Pages 147-158

  Yeo, B T Thomas ^a,b   Tandi, Jesisca ^a   Chee, Michael W L ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Attention networks; Default network; Predictive marker of sleep deprivation vulnerability; Resting state fMRI; Whole brain signal

Indexed keywords

ADULT; ALERTNESS; AMPLITUDE MODULATION; AMYGDALOID NUCLEUS; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FUNCTIONAL CONNECTIVITY; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; NERVE CELL NETWORK; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; PREDICTION; PRIORITY JOURNAL; REST; SLEEP DEPRIVATION; THALAMUS; VULNERABLE POPULATION; WAKEFULNESS; YOUNG ADULT; AROUSAL; BRAIN; BRAIN CORTEX; FUNCTIONAL NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PSYCHOMOTOR PERFORMANCE;

ADULT; AROUSAL; BRAIN; CEREBRAL CORTEX; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PSYCHOMOTOR PERFORMANCE; SLEEP DEPRIVATION; WAKEFULNESS; YOUNG ADULT;

EID: 84923294813     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.02.018     Document Type: Article

References (91)

1. Åkerstedt T., Gillberg M. Subjective and objective sleepiness in the active individual. Int. J. Neurosci. 1990, 52:29-37.
2. Allen E.A., Damaraju E., Plis S.M., Erhardt E.B., Eichele T., Calhoun V.D. Tracking whole-brain connectivity dynamics in the resting state. Cereb. Cortex 2012, 24:663-676.
3. Andrews-Hanna J.R., Reidler J.S., Sepulcre J., Poulin R., Buckner R.L. Functional-anatomic fractionation of the brain's default network. Neuron 2010, 65:550-562.
4. Baker J.T., Holmes A.J., Masters G.A., Yeo B.T.T., Krienen F., Buckner R.L., Öngür D. Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. JAMA Psychiatry 2014, 71:109-118.
5. Basner M., Mollicone D., Dinges D.F. Validity and sensitivity of a brief psychomotor vigilance test (PVT-B) to total and partial sleep deprivation. Acta Astronaut. 2011, 69:949-959.
6. Behzadi Y., Restom K., Liau J., Liu T.T. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 2007, 37:90-101.
7. Bell-McGinty S., Habeck C., Hilton H.J., Rakitin B., Scarmeas N., Zarahn E., Flynn J., DeLaPaz R., Basner R., Stern Y. Identification and differential vulnerability of a neural network in sleep deprivation. Cereb. Cortex 2004, 14:496-502.
8. Betzel R.F., Byrge L., He Y., Goñi J., Zuo X.N., Sporns O. Changes in structural and functional connectivity among resting-state networks across the human lifespan. Neuroimage 2014, 102:345-357.
9. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
10. Bosch O.G., Rihm J.S., Scheidegger M., Landolt H.P., Stampfli P., Brakowski J., Esposito F., Rasch B., Seifritz E. Sleep deprivation increases dorsal nexus connectivity to the dorsolateral prefrontal cortex in humans. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:19597-19602.
11. Buckner R.L. The brain's default network: origins and implications for the study of psychosis. Dialogues Clin. Neurosci. 2013, 15:351-358.
12. Buckner R.L., Krienen F.M., Castellanos A., Diaz J.C., Yeo B.T.T. The organization of the human cerebellum estimated by intrinsic functional connectivity. J. Neurophysiol. 2011, 106:2322-2345.
13. Buckner R.L., Krienen F.M., Yeo B.T.T. Opportunities and limitations of intrinsic functional connectivity MRI. Nat. Neurosci. 2013, 16:832-837.
14. Caldwell L.C., Schweinsburg A.D., Nagel B.J., Barlett V.C., Brown S.A., Tapert S.F. Gender and adolescent alcohol use disorders on BOLD (blood oxygen level dependent) response to spatial working memory. Alcohol Alcohol. 2005, 40:194-200.
15. Chai X.J., Castañón A.N., Öngür D., Whitfield-Gabrieli S. Anticorrelations in resting state networks without global signal regression. Neuroimage 2012, 59:1420-1428.
16. Chee M.W.L., Chuah L.Y.M. Functional neuroimaging and behavioral correlate of capacity decline in visual short-term memory after sleep deprivation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9487-9492.
17. Chee M.W.L., Tan J.C. Lapsing when sleep deprived: neural activation characteristics of resistant and vulnerable individuals. Neuroimage 2010, 51:835-843.
18. Chee M.W.L., Chuah L.Y.M., Venkatraman V., Chan W.Y., Philip P., Dinges D.F. Functional imaging of working memory following normal sleep and after 24 and 35h of sleep deprivation: correlations of fronto-parietal activation with performance. Neuroimage 2006, 31:419-428.
19. Chua E.C.P., Tan W.Q., Yeo S.C., Lau P., Lee I., Mien I.H., Puvanendran K., Gooley J.J. Heart rate variability can be used to estimate sleepiness-related decrements in psychomotor vigilance during total sleep deprivation. Sleep 2012, 35:325-334.
20. Chuah L.Y.M., Chee M.W.L. Cholinergic augmentation modulates visual task performance in sleep-deprived young adults. J. Neurosci. 2008, 28:11369-11377.
21. Chuah L.Y.M., Chong D.L., Chen A.K., Rekshan W.R., Tan J.C., Zheng H., Chee M.W.L. Donepezil improves episodic memory in young individuals vulnerable to the effects of sleep deprivation. Sleep 2009, 32:999-1010.
22. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
23. De Havas J.A., Parimal S., Soon C.S., Chee M.W.L. Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance. Neuroimage 2012, 59:1745-1751.
24. Dinges D., Powell J. Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behav. Res. Methods Instrum. Comput. 1985, 17:652-655.
25. Dinges D.F., Pack F., Williams K., Gillen K.A., Powell J.W., Ott G.E., Aptowicz C., Pack A.I. Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4-5hours per night. Sleep 1997, 20:267-277.
26. Doran S.M., Van Dongen H.P., Dinges D.F. Sustained attention performance during sleep deprivation: evidence of state instability. Arch. Ital. Biol. 2001, 139:253-267.
27. Dorrian J., Rogers N.L., Dinges D.F. Psychomotor vigilance performance: neurocognitive assay sensitive to sleep loss. Sleep Deprivation: Clinical Issues, Pharmacology and Sleep Loss Effects 2005, 39-70. Marcel Dekker, New York. C.A. Kushida (Ed.).
28. Dosenbach N.U.F., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A.T., Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E., Schlaggar B.L., Petersen S.E. Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11073-11078.
29. Drummond S.P.A., Bischoff-Grethe A., Dinges D.F., Ayalon L., Mednick S.C., Meloy M.J. The neural basis of the psychomotor vigilance task. Sleep 2005, 28:1059-1068.
30. Fedorenko E., Duncan J., Kanwisher N. Broad domain generality in focal regions of frontal and parietal cortex. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:16616-16621.
31. Fischl B. FreeSurfer. Neuroimage 2012, 62:774-781.
32. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., van der Kouwe A., Killiany R., Kennedy D., Klaveness S., Montillo A., Makris N., Rosen B., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
33. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Ségonne F., Salat D.H., Busa E., Seidman L.J., Goldstein J., Kennedy D., Caviness V., Makris N., Rosen B., Dale A.M. Automatically parcellating the human cerebral cortex. Cereb. Cortex 2004, 14:11-22.
34. Fornito A., Harrison B.J., Zalesky A., Simons J.S. Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:12788-12793.
35. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
36. Fox M.D., Corbetta M., Snyder A.Z., Vincent J.L., Raichle M.E. Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10046-10051.
37. Fox M.D., Zhang D.Y., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 2009, 101:3270-3283.
38. Giessing C., Thiel C.M., Alexander-Bloch A.F., Patel A.X., Bullmore E.T. Human brain functional network changes associated with enhanced and impaired attentional task performance. J. Neurosci. 2013, 33:5903-5914.
39. Greve D.N., Fischl B. Accurate and robust brain image alignment using boundary-based registration. Neuroimage 2009, 48:63-72.
40. Han X., Fischl B. Atlas renormalization for improved brain MR image segmentation across scanner platforms. IEEE Trans. Med. Imaging 2007, 26:479-486.
41. Horne J.A., Östberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 1976, 4:97-110.
42. Horovitz S.G., Braun A.R., Carr W.S., Picchioni D., Balkin T.J., Fukunaga M., Duyn J.H. Decoupling of the brain's default mode network during deep sleep. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11376-11381.
43. Huber R., Maki H., Rosanova M., Casarotto S., Canali P., Casali A.G., Tononi G., Massimini M. Human cortical excitability increases with time awake. Cereb. Cortex 2013, 23:332-338.
44. Hutchison R.M., Womelsdorf T., Gati J.S., Everling S., Menon R.S. Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum. Brain Mapp. 2013, 34:2154-2177.
45. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
46. Kong D., Asplund C.L., Chee M.W.L. Sleep deprivation reduces the rate of rapid picture processing. Neuroimage 2014, 91:169-176.
47. Krienen F.M., Yeo B.T.T., Buckner R.L. Reconfigurable task-dependent functional coupling modes cluster around a core functional architecture. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369.
48. Laird A.R., Eickhoff S.B., Li K., Robin D.A., Glahn D.C., Fox P.T. Investigating the functional heterogeneity of the default mode network using coordinate-based meta-analytic modeling. J. Neurosci. 2009, 29:14496-14505.
49. Larson-Prior L.J., Zempel J.M., Nolan T.S., Prior F.W., Snyder A.Z., Raichle M.E. Cortical network functional connectivity in the descent to sleep. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4489-4494.
50. Leech R., Kamourieh S., Beckmann C.F., Sharp D.J. Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J. Neurosci. 2011, 31:3217-3224.
51. Lim J., Choo W.C., Chee M.W.L. Reproducibility of changes in behaviour and fMRI activation associated with sleep deprivation in a working memory task. Sleep 2007, 30:61-70.
52. Magnin M., Rey M., Bastuji H., Guillemant P., Mauguiere F., Garcia-Larrea L. Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3829-3833.
53. Mu Q., Mishory A., Johnson K.A., Nahas Z., Kozel F.A., Yamanaka K., Bohning D.E., George M.S. Decreased brain activation during a working memory task at rested baseline is associated with vulnerability to sleep deprivation. Sleep 2005, 28:433-446.
54. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. Neuroimage 2009, 44:893-905.
55. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
56. Ong J.L., Asplund C.L., Chia T.T.Y., Chee M.W.L. Now you hear me, now you don't: eyelid closures as an indicator of auditory task disengagement. Sleep 2013, 36:1867-1874.
57. Patanaik A., Zagorodnov V., Kwoh C.K., Chee M.W.L. Predicting vulnerability to sleep deprivation using diffusion model parameters. J. Sleep Res. 2014, 23:576-584.
58. Picchioni D., Pixa M.L., Fukunaga M., Carr W.S., Horovitz S.G., Braun A.R., Duyn J.H. Decreased connectivity between the thalamus and the neocortex during human nonrapid eye movement sleep. Sleep 2014, 37:387-397.
59. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012, 59:2142-2154.
60. Rechtschaffen A., Hauri P., Zeitlin M. Auditory awakening thresholds in REM and NREM sleep stages. Percept. Mot. Skills 1966, 22:927-942.
61. Rowley J.T., Stickgold R., Hobson J.A. Eyelid movements and mental activity at sleep onset. Conscious. Cogn. 1998, 7:67-84.
62. Rupp T.L., Wesensten N.J., Balkin T.J. Trait-like vulnerability to total and partial sleep loss. Sleep 2012, 35:1163-1172.
63. Russo M.B., Kendall A.P., Johnson D.E., Sing H.C., Thorne D.R., Escolas S.M., Santiago S., Holland D.A., Hall S.W., Redmond D.P. Visual perception, psychomotor performance, and complex motor performance during an overnight air refueling simulated flight. Aviat. Space Environ. Med. 2005, 76:C92-C103.
64. Sämann P.G., Tully C., Spoormaker V.I., Wetter T.C., Holsboer F., Wehrle R., Czisch M. Increased sleep pressure reduces resting state functional connectivity. MAGMA 2010, 23:375-389.
65. Sämann P.G., Wehrle R., Hoehn D., Spoormaker V.I., Peters H., Tully C., Holsboer F., Czisch M. Development of the brain's default mode network from wakefulness to slow wave sleep. Cereb. Cortex 2011, 21:2082-2093.
66. Satterthwaite T.D., Wolf D.H., Loughead J., Ruparel K., Elliott M.A., Hakonarson H., Gur R.E., Gur R.E. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 2012, 60:623-632.
67. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
68. Shao Y., Wang L., Ye E., Jin X., Ni W., Yang Y., Wen B., Hu D., Yang Z. Decreased thalamocortical functional connectivity after 36hours of total sleep deprivation: evidence from resting state FMRI. PLoS One 2013, 8:e78830.
69. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl. 1):S208-S219.
70. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
71. Spoormaker V.I., Schroter M.S., Gleiser P.M., Andrade K.C., Dresler M., Wehrle R., Sämann P.G., Czisch M. Development of a large-scale functional brain network during human non-rapid eye movement sleep. J. Neurosci. 2010, 30:11379-11387.
72. Spreng R.N. The fallacy of a "task-negative" network. Front. Psychol. 2012, 3.
73. Thompson G.J., Magnuson M.E., Merritt M.D., Schwarb H., Pan W.J., McKinley A., Tripp L.D., Schumacher E.H., Keilholz S.D. Short-time windows of correlation between large-scale functional brain networks predict vigilance intraindividually and interindividually. Hum. Brain Mapp. 2013, 34:3280-3298.
74. Tomasi D., Wang R.L., Telang F., Boronikolas V., Jayne M.C., Wang G.J., Fowler J.S., Volkow N.D. Impairment of attentional networks after 1 night of sleep deprivation. Cereb. Cortex 2009, 19:233-240.
75. Tomasi D., Wang R.L., Wang G.J., Volkow N.D. Functional connectivity and brain activation: a synergistic approach. Cereb. Cortex 2014, 24:2619-2629.
76. Uddin L.Q., Kelly A.M., Biswal B.B., Castellanos F.X., Milham M.P. Functional connectivity of default mode network components: correlation, anticorrelation, and causality. Hum. Brain Mapp. 2009, 30:625-637.
77. Van Dijk K.R.A., Hedden T., Venkataraman A., Evans K.C., Lazar S.W., Buckner R.L. Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. J. Neurophysiol. 2010, 103:297-321.
78. Van Dijk K.R.A., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012, 59:431-438.
79. Van Dongen H.P.A., Baynard M.D., Maislin G., Dinges D.F. Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep 2004, 27:423-433.
80. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E., Buckner R.L. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 2006, 96:3517-3531.
81. Vul E., Harris C., Winkielman P., Pashler H. Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect. Psychol. Sci. 2009, 4:274-290.
82. Whitfield-Gabrieli S., Thermenos H.W., Milanovic S., Tsuang M.T., Faraone S.V., McCarley R.W., Shenton M.E., Green A.I., Nieto-Castanon A., LaViolette P., Wojcik J., Gabrieli J.D.E., Seidman L.J. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1279-1284.
83. Wong C.W., Olafsson V., Tal O., Liu T.T. The amplitude of the resting-state fMRI global signal is related to EEG vigilance measures. Neuroimage 2013, 83:983-990.
84. Yan C.-G., Cheung B., Kelly C., Colcombe S., Craddock R.C., Di Martino A., Li Q., Zuo X.-N., Castellanos F.X., Milham M.P. A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 2013, 76:183-201.
85. Yeo B.T.T., Krienen F.M., Sepulcre J., Sabuncu M.R., Lashkari D., Hollinshead M., Roffman J.L., Smoller J.W., Zöllei L., Polimeni J.R., Fischl B., Liu H., Buckner R.L. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 2011, 106:1125-1165.
86. Yeo B.T.T., Krienen F.M., Chee M.W.L., Buckner R.L. Estimates of segregation and overlap of functional connectivity networks in the human cerebral cortex. Neuroimage 2014, 88:212-227.
87. Yeo B.T.T., Krienen F.M., Eickhoff S.B., Yaakub S.N., Fox P.T., Buckner R.L., Asplund C.L., Chee M.W.L. Functional specialization and flexibility in human association cortex. Cereb. Cortex 2015, (in press). 10.1093/cercor/bhu217.
88. Zalesky A., Fornito A., Bullmore E.T. Network-based statistic: identifying differences in brain networks. Neuroimage 2010, 53:1197-1207.
89. Zalesky A., Fornito A., Cocchi L., Gollo L.L., Breakspear M. Time-resolved resting-state brain networks. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:10341-10346.
90. Zeng L.L., Wang D., Fox M.D., Sabuncu M., Hu D., Ge M., Buckner R.L., Liu H. Neurobiological basis of head motion in brain imaging. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:6058-6062.
91. Zhang D., Snyder A.Z., Fox M.D., Sansbury M.W., Shimony J.S., Raichle M.E. Intrinsic functional relations between human cerebral cortex and thalamus. J. Neurophysiol. 2008, 100:1740-1748.