Abstract
The effects of sleep deprivation on the neural substrates of cognition are poorly understood. Here we used functional magnetic resonance imaging to measure the effects of 35 hours of sleep deprivation on cerebral activation during verbal learning in normal young volunteers. On the basis of a previous hypothesis1, we predicted that the prefrontal cortex (PFC) would be less responsive to cognitive demands following sleep deprivation. Contrary to our expectations, however, the PFC was more responsive after one night of sleep deprivation than after normal sleep. Increased subjective sleepiness in sleep-deprived subjects correlated significantly with activation of the PFC. The temporal lobe was activated after normal sleep but not after sleep deprivation; in contrast, the parietal lobes were not activated after normal sleep but were activated after sleep deprivation. Although sleep deprivation significantly impaired free recall compared with the rested state, better free recall in sleep-deprived subjects was associated with greater parietal lobe activation. These findings show that there are dynamic, compensatory changes in cerebral activation during verbal learning after sleep deprivation and implicate the PFC and parietal lobes in this compensation.
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References
Horne, J. A. Human sleep, sleep loss, and behaviour: Implications for the prefrontal cortex and psychiatric disorder. Br. J. Psychiat. 162, 413–419 (1993).
Pilcher, J. L. & Huffcutt, A. I. Effects of sleep deprivation on performance: A meta-analysis. Sleep 19, 318–326 (1996).
Dinges, D. F. & Kribbs, N. B. in Sleep, Sleepiness and Performance (ed. Monk, T. H. ) 97–128 (Wiley, New York, 1991).
Harrison, Y. & Horne, J. A. Sleep deprivation affects speech. Sleep 20, 871–877 (1997).
Harrison, Y. & Horne, J. A. Sleep loss impairs short and novel language tasks having a prefrontal focus. J. Sleep Res. 7, 95–100 (1998).
Horne, J. A. Sleep loss and divergent thinking ability. Sleep 11 , 528–536 (1988).
Lubin, A., Hord, D. J., Tracy, M. L. & Johnson, L. C. Effects of exercise, bedrest, and napping on performance decrement during 40 hours. Psychophysiology 13, 334–339 (1976).
Polzella, D. J. Effects of sleep deprivation on short term recognition memory. J. Exp. Psychol. Hum. Learn. Mem. 104, 194– 200 (1975).
Williams, H. L., Gieseking, C. F. & Lubin, A. Some effects of sleep loss on memory. Percept. Mot. Skills, 23, 1287–1293 (1966).
Wu, J. et al. The effect of sleep deprivation on cerebral glucose metabolic rate in normal humans assessed with Positron Emission Tomography. Sleep , 14, 155–162 ( 1991).
Portas, C. M. et al. A specific role for the thalamus in mediating the interaction of attention and arousal in humans. J. Neurosci., 18 , 8979–8989 (1998).
Thomas, M. et al. Cerebral glucose utilization during task performance and prolonged sleep loss. J. Cereb. Blood Flow Metab. 13, S531 (abstr.) (1993).
Petiau, C. et al. Modification of fronto-temporal connectivity during a verb generation task after a 30-hour total sleep deprivation: A PET study. J. Sleep Res. 7, 208 (abstr. ) (1998).
Bandettini, P. A., Jesmanowicz, A., Wong, E. C. & Hyde, J. S. Processing strategies for time-course data sets in functional MRI of the human brain. Magn. Reson. Med. 30, 161– 173. (1993).
Forman, S. D. et al. Improved assessment of significant activation in Functional Magnetic Resonance Imaging (fMRI): Use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647. (1995).
Hoddes, E., Zarcone, V., Smythe, H., Phillips, R. & Dement, W. Quantification of sleepiness: A new approach. Psychophysiology 10, 431–436 (1973).
Buckner, R. L., Kelley, W. M. & Petersen, S. E. Frontal cortex contributes to human memory formation. Nature Neurosci. 2, 311– 314 (1999).
Smith, E. E. & Jonides, J. Storage and executive processes in the frontal lobes. Science 283, 1657– 1661 (1999).
Brown, G. G. et al. Brain activation and pupil response during covert performance of the Stroop color word task. J. Int. Neuropsychol. Soc. 5, 308–319 (1999).
Smith, E. E. & Jonides, J. Working memory: A view from neuroimaging. Cogn. Psychol. 33, 5–42 (1997).
Frackowiak, R. S. J. Functional mapping of verbal memory and language. Trends Neurosci. 17, 109–114 ( 1994).
Hockey, G. R. J. Compensatory control in the regulation of human performance under stress and high workload: A cognitive–energetical framework. Biol. Psychol. 45, 73–93 ( 1997).
Werth, E., Achermann, P. & Borbély, A. A. Brain topography of the human sleep EEG: antero–posterior shifts of spectral power. NeuroReport 8, 123–127 (1996).
Porkka-Heiskanen, T. et al. Adenosine: A mediator of the sleep-inducing effects of prolonged wakefulness. Science 276, 1265– 1268 (1997).
Drummond, S. P. A. et al. Sleep deprivation-induced reduction in cortical functional response to serial subtraction. NeuroReport 10, 3745–3748 (1999).
Wolfe, N., Reed, B. R., Eberling, J. L. & Jagust, W. J. Temporal lobe perfusion on single photon emission computed tomography predicts the rate of cognitive decline in Alzheimer's disease. Arch. Neurol. 52, 257–262 ( 1995).
Wong, E. C., Bandettini, P. A. & Hyde, J. S. Echo-planar imaging of the human brain using a three axis local gradient coil. Abstr. Proc. 11th Annual Meeting of the Society of Magnetic Resonance in Medicine 1, 105 (Abstr.) (1992).
Cox, R. W. AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162 –173 (1996).
Cohen, M. S. Parametric analysis of fMRI data using linear systems methods. Neuroimage 6, 93–103 ( 1997).
Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme Medical, New York, 1988).
Acknowledgements
This research was supported by an individual NRSA to S.P.A.D., a Mental Health Clinical Research Center grant from NIMH (J.C.G.), the UCSD General Clinical Research Center, the Department of Veterans Affairs research service, and the VA Desert-Pacific Healthcare Network Mental Illness Research, Education, and Clinical Center (MIRECC).
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Drummond, S., Brown, G., Gillin, J. et al. Altered brain response to verbal learning following sleep deprivation . Nature 403, 655–657 (2000). https://doi.org/10.1038/35001068
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DOI: https://doi.org/10.1038/35001068
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