Temporal evolution of neutral activity and connectivity during microsleeps when rested and following sleep restriction

Journal article

Poudel, Govinda, Innes, Carrie R. H. and Jones, Richard. (2018). Temporal evolution of neutral activity and connectivity during microsleeps when rested and following sleep restriction. NeuroImage. 174, pp. 263 - 273. https://doi.org/10.1016/j.neuroimage.2018.03.031
AuthorsPoudel, Govinda, Innes, Carrie R. H. and Jones, Richard
Abstract

Even when it is critical to stay awake, such as when driving, sleep deprivation weakens one's ability to do so by substantially increasing the propensity for microsleeps. Microsleeps are complete lapses of consciousness but, paradoxically, are associated with transient increases in cortical activity. But do microsleeps provide a benefit in terms of attenuating the need for sleep? And is the neural response to microsleeps altered by the degree of homeostatic drive to sleep? In this study, we continuously monitored eye-video, visuomotor responsiveness, and brain activity via fMRI in 20 healthy subjects during a 20-min visuomotor tracking task following a normally-rested night and a sleep-restricted (4-h) night. As expected, sleep restriction led to an increased number of microsleeps and an increased variability in tracking error. Microsleeps exhibited transient increases in regional activity in the fronto-parietal and parahippocampal area. Network analyses revealed divergent transient changes in the right fronto-parietal, dorsal-attention, default-mode, and thalamo-cortical functional networks. In all subjects, tracking error immediately following microsleeps was improved compared to before the microsleeps. Importantly, post-microsleep recovery in tracking response speed was associated with hyperactivation in the thalamo-cortical network. The temporal evolution of functional connectivity within the frontal and posterior nodes of the default-mode network and between the right fronto-parietal and default-mode networks was associated with temporal changes in visuomotor responsiveness. These findings demonstrate distinct brain-network-level changes in brain activity during microsleeps and suggest that neural activity in the thalamo-cortical network may facilitate the transient recovery from microsleeps. The temporal pattern of evolution in brain activity and performance is indicative of dynamic changes in vigilance during the struggle to stay awake following sleep loss.

KeywordsSleep deprivation; Dynamic functional connectivity; fMRI; Microsleeps
Year2018
JournalNeuroImage
Journal citation174, pp. 263 - 273
PublisherElsevier
ISSN1053-8119
Digital Object Identifier (DOI)https://doi.org/10.1016/j.neuroimage.2018.03.031
Scopus EID2-s2.0-85044112757
Page range263 - 273
Research GroupMary MacKillop Institute for Health Research
Publisher's version
File Access Level
Controlled
Place of publicationNetherlands
EditorsM. Breakspear
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Goscinski, Wojtek J., McIntosh, Paul, Felzmann, Ulrich, Maksimenko, Anton, Hall, Christopher J., Gureyev, Timur, Thompson, Darren, Janke, Andrew, Galloway, Graham, Killeen, Neil E. B., Raniga, Parnesh, Kaluza, Owen, Ng, Amanda, Poudel, Govinda, Barnes, David G., Nguyen, Toan, Bonnington, Paul and Egan, Gary F.. (2014). The Multi-modal Australian ScienceS Imaging and Visualization Environment (MASSIVE) high performance computing infrastructure: Applications in neuroscience and neuroinformatics research. Frontiers in Neuroinformatics. 8(March), pp. 1 - 13. https://doi.org/10.3389/fninf.2014.00030
Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study
Georgiou-Karistianis, Nellie, Stout, Julie C., Domínguez, Juan F., Carron, Sarah P., Ando, Ayaka, Churchyard, Andrew, Chua, Phyllis, Bohanna, India, Dymowski, Alicia R., Poudel, Govinda and Egan, Gary F.. (2014). Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study. Human Brain Mapping. 35(5), pp. 1847 - 1864. https://doi.org/10.1002/hbm.22296
Voxel-ICA for reconstruction of source signal time-series and orientation in EEG and MEG
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie and Jones, Richard. (2014). Voxel-ICA for reconstruction of source signal time-series and orientation in EEG and MEG. Australasian Physical and Engineering Sciences in Medicine. 37(2), pp. 457 - 464. https://doi.org/10.1007/s13246-014-0265-x
Multi-modal neuroimaging in premanifest and early Huntington's disease : 18 month longitudinal data from the IMAGE-HD study
Domínguez D, Juan F., Egan, Gary F., Gray, Marcus A., Poudel, Govinda R., Churchyard, Andrew, Chua, Phyllis, Stout, Julie C. and Georgiou-Karistianis, Nellie. (2013). Multi-modal neuroimaging in premanifest and early Huntington's disease : 18 month longitudinal data from the IMAGE-HD study. PLoS ONE. 8(9), pp. 1-10. https://doi.org/10.1371/journal.pone.0074131
Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study
Georgiou-Karistianis, Nellie, Poudel, Govinda R., Domínguez D, Juan F., Langmaid, Rebecca, Gray, Marcus A., Churchyard, Andrew, Chua, Phyllis, Borowsky, Beth, Egan, Gary F. and Stout, Julie C.. (2013). Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study. Brain and Cognition. 83(1), pp. 80-91. https://doi.org/10.1016/j.bandc.2013.07.004
Efficient and regular patterns of nighttime sleep are related to increased vulnerability to microsleeps following a single night of sleep restriction
Innes, Carrie R. H., Poudel, Govinda R. and Jones, Richard D.. (2013). Efficient and regular patterns of nighttime sleep are related to increased vulnerability to microsleeps following a single night of sleep restriction. Chronobiology International. 30(9), pp. 1187-1196. https://doi.org/10.3109/07420528.2013.810222
Distinct neural correlates of time-on-task and transient errors during a visuomotor tracking task after sleep restriction
Poudel, Govinda R., Innes, Carrie R. H. and Jones, Richard D.. (2013). Distinct neural correlates of time-on-task and transient errors during a visuomotor tracking task after sleep restriction. NeuroImage. 77, pp. 105-113. https://doi.org/10.1016/j.neuroimage.2013.03.054
Time-Varying Functional Connectivity for Understanding the Neural Basis of Behavioral Microsleeps
J Toppi, L Astolfi, GR Poudel, F Babiloni, L Macchiusi, D Mattia, S Salinari and RD Jones. (2012). Time-Varying Functional Connectivity for Understanding the Neural Basis of Behavioral Microsleeps. 34th Annual International Conference of the IEEE EMBS. IEEE, Institute of Electrical and Electronics Engineers. pp. 4708-4711 https://doi.org/10.1109/EMBC.2012.6347018
Performance of Beamformers on EEG Source Reconstruction
Yaqub Jon Mohamadi, Govinda Poudel, Carrie R H Innes and Richard Jones. (2012). Performance of Beamformers on EEG Source Reconstruction. 34th Annual International Conference of the IEEE EMBS. IEEE, Institute of Electrical and Electronics Engineers. https://doi.org/10.1109/EMBC.2012.6346476
Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction
Poudel, Govinda R., Innes, Carrie R. H. and Jones, Richard D.. (2012). Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction. Sleep. 35(8), pp. 1085-1096. https://doi.org/10.5665/sleep.1994