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Decreased cortical and subcortical response to inhibition control after sleep deprivation

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Abstract

The effects of sleep deprivation (SD) on the neural substrates of inhibition control are poorly understood. Here we used functional magnetic resonance imaging to examine the effects of 24 h of SD on cerebral activation during a stop-signal task in 20 normal young subjects. Behaviorally, subjects showed significantly delayed stop-signal reaction time (SSRT) following SD. In addition, reduced cerebral activation was found in the “stopping network” (including the inferior frontal gyrus [IFG], supplementary motor area, subthalamic nucleus [STN] and insula) and vision-related regions (occipital cortex, lingual gyrus and fusiform gyrus) after SD. These findings support the hypothesis that task-related activation in prefrontal cortex is particularly vulnerable to SD. After rested wakefulness (RW), significant negative correlations were found between SSRT and cerebral activation in left IFG, right hippocampus, right lingual gyrus, left STN and bilateral fusiform gyrus, with activation in left IFG making the most contribution. After SD, significant negative correlations were found between SSRT and activation in right middle frontal cortex, right IFG and left lingual gyrus, with the activation in right IFG making the most contribution. Furthermore, we observed significant interaction effects of state (SD or RW) with activation in bilateral IFG, left STN and left lingual gyrus on SSRT. In conclusion, sleep deprivation is associated with the deficits in inhibition-related neural activation and the altered correlation between SSRT and cerebral activation, especially in the bilateral IFG, left STN and left lingual gyrus.

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References

  • Almklov, E. L., Drummond, S. P., Orff, H., & Alhassoon, O. M. (2015). The effects of sleep deprivation on brain functioning in older adults. Behavioral Sleep Medicine, 13(4), 324–345. https://doi.org/10.1080/15402002.2014.905474.

    Article  PubMed  Google Scholar 

  • Aron, A. R., & Poldrack, R. A. (2006). Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. The Journal of Neuroscience, 26(9), 2424–2433. https://doi.org/10.1523/JNEUROSCI.4682-05.2006.

    Article  CAS  PubMed  Google Scholar 

  • Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6(2), 115–116. https://doi.org/10.1038/nn1003.

    Article  CAS  PubMed  Google Scholar 

  • Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., & Poldrack, R. A. (2007). Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 27(14), 3743–3752.

    Article  CAS  Google Scholar 

  • Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2014a). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8(4), 170–177.

    Article  Google Scholar 

  • Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2014b). Inhibition and the right inferior frontal cortex: one decade on. Trends in Cognitive Sciences, 18(4), 177–185. https://doi.org/10.1016/j.tics.2013.12.003.

    Article  PubMed  Google Scholar 

  • Asplund, C. L., & Chee, M. W. (2013). Time-on-task and sleep deprivation effects are evidenced in overlapping brain areas. NeuroImage, 82(2), 326–335.

    Article  PubMed  Google Scholar 

  • Band, G. P., van der Molen, M. W., & Logan, G. D. (2003). Horse-race model simulations of the stop-signal procedure. Acta Psychologica, 112(2), 105–142.

    Article  PubMed  Google Scholar 

  • Basner, M., Rao, H., Goel, N., & Dinges, D. F. (2013). Sleep deprivation and neurobehavioral dynamics. Current Opinion in Neurobiology, 23(5), 854–863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell-McGinty, S., Habeck, C., Hilton, H. J., Rakitin, B., Scarmeas, N., Zarahn, E., et al. (2004). Identification and differential vulnerability of a neural network in sleep deprivation. Cerebral Cortex, 14(5), 496–502. https://doi.org/10.1093/cercor/bhh011.

    Article  PubMed  Google Scholar 

  • Bogousslavsky, J., Miklossy, J., Deruaz, J. P., Assal, G., & Regli, F. (1987). Lingual and fusiform gyri in visual processing: a clinico-pathologic study of superior altitudinal hemianopia. Journal of Neurology, Neurosurgery, and Psychiatry, 50(5), 607–614.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunge, S. A., Dudukovic, N. M., Thomason, M. E., Vaidya, C. J., & Gabrieli, J. D. (2002). Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron, 33(2), 301–311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai, W., Cannistraci, C. J., Gore, J. C., & Leung, H. C. (2014). Sensorimotor-independent prefrontal activity during response inhibition. Human Brain Mapping, 35(5), 2119–2136.

    Article  PubMed  Google Scholar 

  • Chambers, C. D., Bellgrove, M. A., Stokes, M. G., Henderson, T. R., Garavan, H., Robertson, I. H., et al. (2006). Executive "Brake Failure" following Deactivation of Human Frontal Lobe. Journal of Cognitive Neuroscience, 18(3), 444–455.

    PubMed  Google Scholar 

  • Chambers, C. D., Bellgrove, M. A., Gould, I. C., English, T., Garavan, H., Mcnaught, E., et al. (2007). Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. Journal of Neurophysiology, 98(6), 3638.

    Article  PubMed  Google Scholar 

  • Chambers, C. D., Garavan, H., & Bellgrove, M. A. (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience & Biobehavioral Reviews, 33(5), 631.

    Article  Google Scholar 

  • Chee, M. W., & Choo, W. C. (2004). Functional imaging of working memory after 24 hr of total sleep deprivation. The Journal of Neuroscience, 24(19), 4560–4567. https://doi.org/10.1523/JNEUROSCI.0007-04.2004.

    Article  CAS  PubMed  Google Scholar 

  • Chee, M. W., Chuah, L. Y., Venkatraman, V., Chan, W. Y., Philip, P., & Dinges, D. F. (2006). Functional imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation: Correlations of fronto-parietal activation with performance. NeuroImage, 31(1), 419–428. https://doi.org/10.1016/j.neuroimage.2005.12.001.

    Article  PubMed  Google Scholar 

  • Chuah, Y. M., Venkatraman, V., Dinges, D. F., & Chee, M. W. (2006). The neural basis of interindividual variability in inhibitory efficiency after sleep deprivation. Journal of Neuroscience, 26(27), 7156–7162.

    Article  CAS  PubMed  Google Scholar 

  • Cohen, J. R., Asarnow, R. F., Sabb, F. W., Bilder, R. M., Bookheimer, S. Y., Knowlton, B. J., et al. (2010). Decoding Developmental Differences and Individual Variability in Response Inhibition Through Predictive Analyses Across Individuals. Frontiers in Human Neuroscience, 4(5), 47.

    PubMed  PubMed Central  Google Scholar 

  • Congdon, E., Mumford, J. A., Cohen, J. R., Galvan, A., Aron, A. R., Xue, G., et al. (2010). Engagement of large-scale networks is related to individual differences in inhibitory control. NeuroImage, 53(2), 653–663.

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond, S. P., Brown, G. G., Gillin, J. C., Stricker, J. L., Wong, E. C., & Buxton, R. B. (2000). Altered brain response to verbal learning following sleep deprivation. Nature, 403(6770), 655–657. https://doi.org/10.1038/35001068.

    Article  CAS  PubMed  Google Scholar 

  • Durmer, J. S., & Dinges, D. F. (2005). Neurocognitive consequences of sleep deprivation. Seminars in Neurology, 25(1), 117–129.

    Article  PubMed  Google Scholar 

  • Floden, D., & Stuss, D. T. (2006). Inhibitory control is slowed in patients with right superior medial frontal damage. Cognitive Neuroscience Journal of, 18(11), 1843–1849.

    Article  Google Scholar 

  • Galván, A., Poldrack, R. A., Baker, C. M., Mcglennen, K. M., & London, E. D. (2011). Neural Correlates of Response Inhibition and Cigarette Smoking in Late Adolescence. Neuropsychopharmacology Official Publication of the American College of Neuropsychopharmacology, 36(5), 970.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghahremani, D. G., Lee, B., Robertson, C. L., Tabibnia, G., Morgan, A. T., Shetler, N. D., et al. (2012). Striatal Dopamine D2/D3 Receptors Mediate Response Inhibition and Related Activity in Frontostriatal Neural Circuitry in Humans. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 32(21), 7316–7324.

    Article  CAS  Google Scholar 

  • Gusnard, D. A., Akbudak, E., Shulman, G. L., & Raichle, M. E. (2001). Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(7), 4259–4264. https://doi.org/10.1073/pnas.071043098.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horne, J. A. (1993). Human sleep, sleep loss and behaviour. Implications for the prefrontal cortex and psychiatric disorder. The British Journal of Psychiatry: the Journal of Mental Science, 162(162), 413–419.

    Article  CAS  Google Scholar 

  • Horne, J. A., & Ostberg, O. (1976). A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. International Journal of Chronobiology, 4(2), 97–110.

    CAS  PubMed  Google Scholar 

  • Huang, C. C., Liu, M. E., Chou, K. H., Yang, A. C., Hung, C. C., Hong, C. J., et al. (2014). Effect of BDNF Val66Met polymorphism on regional white matter hyperintensities and cognitive function in elderly males without dementia. Psychoneuroendocrinology, 39(1), 94.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, J. W. (2004). Factors Affecting Relative Weights: The Influence of Sampling and Measurement Error. Organizational Research Methods, 7(3), 283–299.

    Article  Google Scholar 

  • Johnson, J. W., & Lebreton, J. M. (2004). History and Use of Relative Importance Indices in Organizational Research. Organizational Research Methods, 7(3), 238–257.

    Article  Google Scholar 

  • Kanwisher, N., Mcdermott, J., & Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 17(11), 4302–4311.

    Article  CAS  Google Scholar 

  • Killgore, W. D. S. (2010). Effects of sleep deprivation on cognition. Progress in Brain Research, 185(1), 105–129.

    Article  PubMed  Google Scholar 

  • Kong, D., Soon, C. S., & Chee, M. W. (2011). Reduced visual processing capacity in sleep deprived persons. NeuroImage, 55(2), 629–634.

    Article  PubMed  Google Scholar 

  • Lebreton, J. M., & Tonidandel, S. (2008). Multivariate relative importance: Extending relative weight analysis to multivariate criterion spaces. Journal of Applied Psychology, 93(2), 329–345.

    Article  PubMed  Google Scholar 

  • Lee, H. H., & Hsieh, S. (2017). Resting-State fMRI Associated with Stop-Signal Task Performance in Healthy Middle-Aged and Elderly People. Frontiers in Psychology, 8.

  • Li, C. S., Huang, C., Constable, R. T., & Sinha, R. (2006). Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26(1), 186–192.

    Article  CAS  Google Scholar 

  • Lim, J., Choo, W. C., & Chee, M. W. (2007). Reproducibility of changes in behaviour and fMRI activation associated with sleep deprivation in a working memory task. Sleep, 30(1), 61–70.

    Article  PubMed  Google Scholar 

  • Logan, G. D. (1994). On the ability to inhibit thought and action: A users' guide to the stop signal paradigm. Inhibitory Processes in Attention Memory & Language, 189–239.

  • Lucerna, S., Salpietro, F. M., Alafaci, C., & Tomasello, F. (2002). In Vivo Atlas of Deep Brain Structures: Springer Berlin Heidelberg.

    Book  Google Scholar 

  • Ma, N., Dinges, D. F., Basner, M., & Rao, H. (2014). How Acute Total Sleep Loss Affects the Attending Brain: A Meta-analysis of Neuroimaging Studies. Sleep, 38(2), 233.

    Article  Google Scholar 

  • Mu, Q., Mishory, A., Johnson, K. A., Nahas, Z., Kozel, F. A., Yamanaka, K., et al. (2005a). Decreased brain activation during a working memory task at rested baseline is associated with vulnerability to sleep deprivation. Sleep, 28(4), 433.

    Article  PubMed  Google Scholar 

  • Mu, Q., Nahas, Z., Johnson, K. A., Yamanaka, K., Mishory, A., Koola, J., et al. (2005b). Decreased cortical response to verbal working memory following sleep deprivation. Sleep, 28(1), 55–67.

    Article  PubMed  Google Scholar 

  • Picton, T. W., Stuss, D. T., Alexander, M. P., Shallice, T., Binns, M. A., & Gillingham, S. (2007). Effects of focal frontal lesions on response inhibition. Cerebral Cortex, 17(4), 826.

    Article  PubMed  Google Scholar 

  • Rubia, K., Smith, A. B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., et al. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27(12), 973–993. https://doi.org/10.1002/hbm.20237.

    Article  PubMed  Google Scholar 

  • Suh, S., Kim, H., Dang-Vu, T. T., Joo, E., & Shin, C. (2016). Cortical Thinning and Altered Cortico-Cortical Structural Covariance of the Default Mode Network in Patients with Persistent Insomnia Symptoms. Sleep, 39(1), 161–171. https://doi.org/10.5665/sleep.5340.

    Article  PubMed  PubMed Central  Google Scholar 

  • Swick, D., Ashley, V., & Turken, U. (2011). Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. NeuroImage, 56(3), 1655–1665.

    Article  PubMed  Google Scholar 

  • Tomasi, D., Wang, R. L., Telang, F., Boronikolas, V., Jayne, M. C., Wang, G. J., et al. (2009). Impairment of attentional networks after 1 night of sleep deprivation. Cerebral Cortex, 19(1), 233–240.

    Article  CAS  PubMed  Google Scholar 

  • Van Dongen, H. P., Maislin, G., Mullington, J. M., & Dinges, D. F. (2003). The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep, 26(2), 117–126.

    Article  PubMed  Google Scholar 

  • Wager, T. D., Sylvester, C. Y., Lacey, S. C., Nee, D. E., Franklin, M., & Jonides, J. (2005). Common and unique components of response inhibition revealed by fMRI. NeuroImage, 27(2), 323–340.

    Article  PubMed  Google Scholar 

  • White, C. N., Congdon, E., Mumford, J. A., Karlsgodt, K. H., Sabb, F. W., Freimer, N. B., et al. (2014). Decomposing decision components in the stop-signal task: A model-based approach to individual differences in inhibitory control. Journal of Cognitive Neuroscience, 26(8), 1601.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xue, G., Aron, A. R., & Poldrack, R. A. (2008). Common neural substrates for inhibition of spoken and manual responses. Cerebral Cortex, 18(8), 1923–1932.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the subjects whose participation enabled this work. This study was funded by National Basic Research Program of China under Grant Nos. 2015CB856403 and 2014CB543203; the National Natural Science Foundation of China under Grant Nos. 81471811, 81471738 and 61401346; and the Fundamental Research Funds for the Central Universities.

Funding

This study was funded by National Basic Research Program of China under Grant Nos. 2015CB856403 and 2014CB543203; the National Natural Science Foundation of China under Grant Nos. 81471811, 81471738 and 61401346; and the Fundamental Research Funds for the Central Universities.

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Correspondence to Wei Qin.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research ethics committee of the Xijing Hospital of the Fourth Military Medical University and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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This was not an industry supportd study. The authors have indicated no financial conflicts of interest.

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Zhao, R., Zhang, X., Fei, N. et al. Decreased cortical and subcortical response to inhibition control after sleep deprivation. Brain Imaging and Behavior 13, 638–650 (2019). https://doi.org/10.1007/s11682-018-9868-2

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