In an awake state, neurons in the cerebral cortex fire irregularly and electroencephalogram (EEG) recordings display low-amplitude, high-frequency fluctuations. During sleep, neurons oscillate between ‘on’ periods, when they fire as in an awake brain, and ‘off’ periods, when they stop firing altogether and the EEG displays high-amplitude slow waves. However, what happens to neuronal firing after a long period of being awake is not known. Here we show that in freely behaving rats after a long period in an awake state, cortical neurons can go briefly ‘offline’ as in sleep, accompanied by slow waves in the local EEG. Neurons often go offline in one cortical area but not in another, and during these periods of ‘local sleep’, the incidence of which increases with the duration of the awake state, rats are active and display an ‘awake’ EEG. However, they are progressively impaired in a sugar pellet reaching task. Thus, although both the EEG and behaviour indicate wakefulness, local populations of neurons in the cortex may be falling asleep, with negative consequences for performance.
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Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969–1985 (2001)
Vyazovskiy, V. V. et al. Cortical firing and sleep homeostasis. Neuron 63, 865–878 (2009)
Dijk, D. J., Duffy, J. F. & Czeisler, C. A. Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J. Sleep Res. 1, 112–117 (1992)
Van Dongen, H. P., Maislin, G., Mullington, J. M. & Dinges, D. F. 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, 117–126 (2003)
Borbély, A. A. & Achermann, P. Sleep homeostasis and models of sleep regulation. In Principles and Practice of Sleep Medicine (eds Kryger, M. H., Roth, T., & Dement, W. C. ) 405–417 (W. B. Saunders, 2005)
Dang-Vu, T. T. et al. Functional neuroimaging insights into the physiology of human sleep. Sleep 33, 1589–1603 (2010)
Diekelmann, S. & Born, J. The memory function of sleep. Nature Rev. Neurosci. 11, 114–126 (2010)
Huber, R., Ghilardi, M. F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78–81 (2004)
Finelli, L. A., Baumann, H., Borbely, A. A. & Achermann, P. Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep. Neuroscience 101, 523–529 (2000)
Vyazovskiy, V. V. & Tobler, I. Theta activity in the waking EEG is a marker of sleep propensity in the rat. Brain Res. 1050, 64–71 (2005)
Leemburg, S. et al. Sleep homeostasis in the rat is preserved during chronic sleep restriction. Proc. Natl Acad. Sci. USA 107, 15939–15944 (2010)
Maquet, P. Functional neuroimaging of normal human sleep by positron emission tomography. J. Sleep Res. 9, 207–231 (2000)
Sejnowski, T. J. & Destexhe, A. Why do we sleep? Brain Res. 886, 208–223 (2000)
Krueger, J. M. et al. Sleep as a fundamental property of neuronal assemblies. Nature Rev. Neurosci. 9, 910–919 (2008)
Riedner, B. A. et al. Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep 30, 1643–1657 (2007)
Esser, S. K., Hill, S. L. & Tononi, G. Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 30, 1617–1630 (2007)
Nir, Y. et al. Regional slow waves and spindles in human sleep. Neuron 10.1016/j.neuron.2011.02.043
Vyazovskiy, V. V., Faraguna, U., Cirelli, C. & Tononi, G. Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: effects of sleep/wake history and background activity. J. Neurophysiol. 101, 1921–1931 (2009)
Tirunahari, V. L., Zaidi, S. A., Sharma, R., Skurnick, J. & Ashtyani, H. Microsleep and sleepiness: a comparison of multiple sleep latency test and scoring of microsleep as a diagnostic test for excessive daytime sleepiness. Sleep Med. 4, 63–67 (2003)
Blaivas, A. J., Patel, R., Hom, D., Antigua, K. & Ashtyani, H. Quantifying microsleep to help assess subjective sleepiness. Sleep Med. 8, 156–159 (2007)
Hanlon, E. C., Faraguna, U., Vyazovskiy, V. V., Tononi, G. & Cirelli, C. Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. Sleep 32, 719–729 (2009)
Rioult-Pedotti, M. S., Friedman, D. & Donoghue, J. P. Learning-induced LTP in neocortex. Science 290, 533–536 (2000)
Vyazovskiy, V. V. & Tobler, I. Handedness leads to interhemispheric EEG asymmetry during sleep in the rat. J. Neurophysiol. 99, 969–975 (2008)
Moruzzi, G. (ed.) The Functional Significance of Sleep with Particular Regard to the Brain Mechanisms Underlying Consciousness. (Springer, 1966)
Killgore, W. D. Effects of sleep deprivation on cognition. Prog. Brain Res. 185, 105–129 (2010)
Ferrillo, F. et al. Sleep-EEG modulation of interictal epileptiform discharges in adult partial epilepsy: a spectral analysis study. Clin. Neurophysiol. 111, 916–923 (2000)
Poulet, J. F. & Petersen, C. C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008)
Hill, S. & Tononi, G. Modeling sleep and wakefulness in the thalamocortical system. J. Neurophysiol. 93, 1671–1698 (2005)
Doran, S. M., Van Dongen, H. P. & Dinges, D. F. Sustained attention performance during sleep deprivation: evidence of state instability. Arch. Ital. Biol. 139, 253–267 (2001)
Chauvette, S., Volgushev, M. & Timofeev, I. Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex 20, 2660–2674 (2010)
Wu, M. F. et al. Locus coeruleus neurons: cessation of activity during cataplexy. Neuroscience 91, 1389–1399 (1999)
Nunez, A. Unit activity of rat basal forebrain neurons: relationship to cortical activity. Neuroscience. 72, 757–766 (1996)
Laplante, F., Morin, Y., Quirion, R. & Vaucher, E. Acetylcholine release is elicited in the visual cortex, but not in the prefrontal cortex, by patterned visual stimulation: a dual in vivo microdialysis study with functional correlates in the rat brain. Neuroscience 132, 501–510 (2005)
Marrocco, R. T., Lane, R. F., McClurkin, J. W., Blaha, C. D. & Alkire, M. F. Release of cortical catecholamines by visual stimulation requires activity in thalamocortical afferents of monkey and cat. J. Neurosci. 7, 2756–2767 (1987)
Cirelli, C. & Tononi, G. Is sleep essential? PLoS Biol. 6, e216 (2008)
Pigarev, I. N., Nothdurft, H. C. & Kastner, S. Evidence for asynchronous development of sleep in cortical areas. Neuroreport 8, 2557–2560 (1997)
Terzaghi, M. et al. Evidence of dissociated arousal states during NREM parasomnia from an intracerebral neurophysiological study. Sleep 32, 409–412 (2009)
Mahowald, M. W. & Schenck, C. H. Insights from studying human sleep disorders. Nature 437, 1279–1285 (2005)
Tononi, G. & Cirelli, C. Sleep function and synaptic homeostasis. Sleep Med. Rev. 10, 49–62 (2006)
Attwell, D. & Laughlin, S. B. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21, 1133–1145 (2001)
This work was supported by NIMH P20 MH077967 (C.C.), NIH Director’s Pioneer award (G.T.) and AFOSR FA9550-08-1-0244 (G.T.). We thank A. Nelson, M. Dash and U. Faraguna for help with the experiments, L. Krugner-Higby for advice about surgical procedures and P. Frumento for advice on statistical procedures.
The authors declare no competing financial interests.
This file contains Supplementary Figures 1-5 with legends, legends for Supplementary Movies 1-2, Supplementary Materials and additional references. (PDF 827 kb)
This movie shows a representative example of a successful reach (hit), where the rat successfully grasps the pellet. (MOV 2742 kb)
This movie shoes a representative example of two consecutive unsuccessful reaches (misses), where the rat fails to grasp the pellets, but knocks them off the shelf. Note that the rat is clearly behaviorally awake throughout both trials. (MOV 3305 kb)
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Vyazovskiy, V., Olcese, U., Hanlon, E. et al. Local sleep in awake rats. Nature 472, 443–447 (2011). https://doi.org/10.1038/nature10009
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