Abstract
Recent functional neuroimaging studies have investigated brain activity patterns during sleep in humans, beyond the conventionally defined sleep stages. These works have characterized the neural activations related to the major brain oscillations of sleep, that is, spindles and slow waves during non-rapid-eye-movement sleep and ponto-geniculo-occipital waves during rapid-eye-movement sleep. These phasic events have been found associated with increases of brain activity in specific neural networks, which identify structures involved in the generation of sleep oscillations. Most importantly, these results confirm that, even during the deepest stages of sleep, neuronal network activities are sustained and organized by spontaneous brain oscillations of sleep. The understanding of the neural mechanisms underlying sleep oscillations is fundamental since increasing evidence suggests a pivotal role for these rhythms in the functional properties of sleep. In particular, interactions between the sleeping brain and the surrounding environment are closely modulated by neuronal oscillations of sleep. Functional neuroimaging studies have demonstrated that spindles distort the transmission of auditory information to the cortex, therefore isolating the brain from external disturbances during sleep. In contrast, slow waves evoked by acoustic stimulation—and also termed K-complexes—are associated with larger auditory cortex activation, thus reflecting an enhanced processing of external information during sleep. Future brain imaging studies of sleep should further explore the contribution of neuronal oscillations to the off-line consolidation of memory during sleep.
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References
Achermann, P., & Borbely, A. A. (1997). Low-frequency (<1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience, 81(1), 213–222.
Andersson, J. L., Onoe, H., Hetta, J., Lidstrom, K., Valind, S., Lilja, A., et al. (1998). Brain networks affected by synchronized sleep visualized by positron emission tomography. Journal of Cerebral Blood Flow and Metabolism, 18(7), 701–715.
Andrade, K. C., Spoormaker, V. I., Dresler, M., Wehrle, R., Holsboer, F., Samann, P. G., et al. (2011). Sleep spindles and hippocampal functional connectivity in human NREM sleep. Journal of Neuroscience, 31(28), 10331–10339.
Arieli, A., Sterkin, A., Grinvald, A., & Aertsen, A. (1996). Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science, 273(5283), 1868–1871.
Barakat, M., Doyon, J., Debas, K., Vandewalle, G., Morin, A., Poirier, G., et al. (2011). Fast and slow spindle involvement in the consolidation of a new motor sequence. Behavioural Brain Research, 217(1), 117–121.
Blethyn, K. L., Hughes, S. W., Toth, T. I., Cope, D. W., & Crunelli, V. (2006). Neuronal basis of the slow (<1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. Journal of Neuroscience, 26(9), 2474–2486.
Boly, M., Balteau, E., Schnakers, C., Degueldre, C., Moonen, G., Luxen, A., et al. (2007). Baseline brain activity fluctuations predict somatosensory perception in humans. Proceedings of the National Academy of Sciences of the United States of America, 104(29), 12187–12192.
Bonjean, M., Baker, T., Lemieux, M., Timofeev, I., Sejnowski, T., & Bazhenov, M. (2011). Corticothalamic feedback controls sleep spindle duration in vivo. Journal of Neuroscience, 31(25), 9124–9134.
Born, A. P., Law, I., Lund, T. E., Rostrup, E., Hanson, L. G., Wildschiodtz, G., et al. (2002). Cortical deactivation induced by visual stimulation in human slow-wave sleep. NeuroImage, 17(3), 1325–1335.
Braun, A. R., Balkin, T. J., Wesenten, N. J., Carson, R. E., Varga, M., Baldwin, P., et al. (1997). Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain, 120(Pt 7), 1173–1197.
Cash, S. S., Halgren, E., Dehghani, N., Rossetti, A. O., Thesen, T., Wang, C., et al. (2009). The human K-complex represents an isolated cortical down-state. Science, 324(5930), 1084–1087.
Colrain, I. M. (2005). The K-complex: A 7-decade history. Sleep, 28(2), 255–273.
Contreras, D., & Steriade, M. (1995). Cellular basis of EEG slow rhythms: A study of dynamic corticothalamic relationships. Journal of Neuroscience, 15(1 Pt 2), 604–622.
Cote, K. A., Epps, T. M., & Campbell, K. B. (2000). The role of the spindle in human information processing of high-intensity stimuli during sleep. Journal of Sleep Research, 9(1), 19–26.
Czisch, M., Wehrle, R., Kaufmann, C., Wetter, T. C., Holsboer, F., Pollmacher, T., et al. (2004). Functional MRI during sleep: BOLD signal decreases and their electrophysiological correlates. European Journal of Neuroscience, 20(2), 566–574.
Czisch, M., Wehrle, R., Stiegler, A., Peters, H., Andrade, K., Holsboer, F., et al. (2009). Acoustic oddball during NREM sleep: A combined EEG/fMRI study. PloS One, 4(8), e6749.
Czisch, M., Wetter, T. C., Kaufmann, C., Pollmacher, T., Holsboer, F., & Auer, D. P. (2002). Altered processing of acoustic stimuli during sleep: Reduced auditory activation and visual deactivation detected by a combined fMRI/EEG study. NeuroImage, 16(1), 251–258.
Dang Vu, T. T., Desseilles, M., Peigneux, P., Laureys, S., & Maquet, P. (2009). Sleep and sleep states: PET activation patterns. In L. R. Squire (Ed.), Encyclopedia of neuroscience (Vol. 8, pp. 955–961). Oxford: Academic Press.
Dang-Vu, T. T., Bonjean, M., Schabus, M., Boly, M., Darsaud, A., Desseilles, M., et al. (2011). Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proceedings of the National Academy of Sciences of the United States of America, 108(37), 15438–15443.
Dang-Vu, T. T., Desseilles, M., Laureys, S., Degueldre, C., Perrin, F., Phillips, C., et al. (2005). Cerebral correlates of delta waves during non-REM sleep revisited. NeuroImage, 28(1), 14–21.
Dang-Vu, T. T., McKinney, S. M., Buxton, O. M., Solet, J. M., & Ellenbogen, J. M. (2010). Spontaneous brain rhythms predict sleep stability in the face of noise. Current Biology, 20(15), R626–R627.
Dang-Vu, T. T., Schabus, M., Desseilles, M., Albouy, G., Boly, M., Darsaud, A., et al. (2008). Spontaneous neural activity during human slow wave sleep. Proceedings of the National Academy of Sciences of the United States of America, 105(39), 15160–15165.
Datta, S. (1997). Cellular basis of pontine ponto-geniculo-occipital wave generation and modulation. Cellular and Molecular Neurobiology, 17(3), 341–365.
Datta, S. (1999). PGO wave generation: Mechanism and functional significance. In B. N. Mallick & S. Inoue (Eds.), Rapid eye movement sleep (pp. 91–106). New Dehli: Narosa Publishing House.
Datta, S. (2000). Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity. Journal of Neuroscience, 20(22), 8607–8613.
Davenne, D., & Adrien, J. (1984). Suppression of PGO waves in the kitten: Anatomical effects on the lateral geniculate nucleus. Neuroscience Letters, 45(1), 33–38.
Davenne, D., Fregnac, Y., Imbert, M., & Adrien, J. (1989). Lesion of the PGO pathways in the kitten. II. Impairment of physiological and morphological maturation of the lateral geniculate nucleus. Brain Research, 485(2), 267–277.
De Gennaro, L., & Ferrara, M. (2003). Sleep spindles: An overview. Sleep Medicine Reviews, 7(5), 423–440.
Destexhe, A., Hughes, S. W., Rudolph, M., & Crunelli, V. (2007). Are corticothalamic ‘up’ states fragments of wakefulness? Trends in Neurosciences, 30, 334–342.
Elton, M., Winter, O., Heslenfeld, D., Loewy, D., Campbell, K., & Kok, A. (1997). Event-related potentials to tones in the absence and presence of sleep spindles. Journal of Sleep Research, 6(2), 78–83.
Eschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2011). Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cerebral Cortex (in press). doi:10.1093/cercor/bhr121.
Fernandez-Mendoza, J., Lozano, B., Seijo, F., Santamarta-Liebana, E., Ramos-Platon, M. J., Vela-Bueno, A., et al. (2009). Evidence of subthalamic PGO-like waves during REM sleep in humans: A deep brain polysomnographic study. Sleep, 32(9), 1117–1126.
Ferrarelli, F., Peterson, M. J., Sarasso, S., Riedner, B. A., Murphy, M. J., Benca, R. M., et al. (2010). Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. The American Journal of Psychiatry, 167(11), 1339–1348.
Finelli, L. A., Borbely, A. A., & Achermann, P. (2001). Functional topography of the human nonREM sleep electroencephalogram. European Journal of Neuroscience, 13(12), 2282–2290.
Fogel, S. M., & Smith, C. T. (2011). The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neuroscience and Biobehavioral Reviews, 35(5), 1154–1165.
Gaab, N., Gaser, C., Zaehle, T., Jancke, L., & Schlaug, G. (2003). Functional anatomy of pitch memory—An fMRI study with sparse temporal sampling. NeuroImage, 19(4), 1417–1426.
Gais, S., Molle, M., Helms, K., & Born, J. (2002). Learning-dependent increases in sleep spindle density. Journal of Neuroscience, 22(15), 6830–6834.
Happe, S., Anderer, P., Gruber, G., Klosch, G., Saletu, B., & Zeitlhofer, J. (2002). Scalp topography of the spontaneous K-complex and of delta-waves in human sleep. Brain Topography, 15(1), 43–49.
Hobson, J. A. (1964). L’activité électrique du cortex et du thalamus au cours du sommeil désynchronisé chez le chat. Comptes Rendus de la Société de Biologie (Paris), 158, 2131–2135.
Hofle, N., Paus, T., Reutens, D., Fiset, P., Gotman, J., Evans, A. C., et al. (1997). Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. Journal of Neuroscience, 17(12), 4800–4808.
Holcomb, H. H., Medoff, D. R., Caudill, P. J., Zhao, Z., Lahti, A. C., Dannals, R. F., et al. (1998). Cerebral blood flow relationships associated with a difficult tone recognition task in trained normal volunteers. Cerebral Cortex, 8(6), 534–542.
Iber, C., Ancoli-Israel, S., Chesson, A. L., & Quan, S. F. (2007). The AASM manual for the scoring of sleep and associated events. Westchester: American Academy of Sleep Medicine.
Jouvet, M., & Michel, F. (1959). Corrélations électromyographiques du sommeil chez le Chat décortiqué et mésencéphalique chronique. Comptes Rendus de la Société de Biologie (Paris), 153, 422–425.
Kajimura, N., Uchiyama, M., Takayama, Y., Uchida, S., Uema, T., Kato, M., et al. (1999). Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. Journal of Neuroscience, 19(22), 10065–10073.
Kaufmann, C., Wehrle, R., Wetter, T. C., Holsboer, F., Auer, D. P., Pollmacher, T., et al. (2006). Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: An EEG/fMRI study. Brain, 129(Pt 3), 655–667.
Landsness, E. C., Crupi, D., Hulse, B. K., Peterson, M. J., Huber, R., Ansari, H., et al. (2009). Sleep-dependent improvement in visuomotor learning: A causal role for slow waves. Sleep, 32(10), 1273–1284.
Larson-Prior, L. J., Power, J. D., Vincent, J. L., Nolan, T. S., Coalson, R. S., Zempel, J., et al. (2011). Modulation of the brain’s functional network architecture in the transition from wake to sleep. Progress in Brain Research, 193, 277–294.
Maquet, P. (2000). Functional neuroimaging of normal human sleep by positron emission tomography. Journal of Sleep Research, 9(3), 207–231.
Maquet, P., Degueldre, C., Delfiore, G., Aerts, J., Peters, J. M., Luxen, A., et al. (1997). Functional neuroanatomy of human slow wave sleep. Journal of Neuroscience, 17(8), 2807–2812.
Maquet, P., Dive, D., Salmon, E., Sadzot, B., Franco, G., Poirrier, R., et al. (1990). Cerebral glucose utilization during sleep-wake cycle in man determined by positron emission tomography and [18F]2-fluoro-2-deoxy-d-glucose method. Brain Research, 513(1), 136–143.
Maquet, P., Laureys, S., Peigneux, P., Fuchs, S., Petiau, C., Phillips, C., et al. (2000). Experience-dependent changes in cerebral activation during human REM sleep. Nature Neuroscience, 3(8), 831–836.
Maquet, P., Peters, J., Aerts, J., Delfiore, G., Degueldre, C., Luxen, A., et al. (1996). Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature, 383(6596), 163–166.
Maquet, P., Ruby, P., Maudoux, A., Albouy, G., Sterpenich, V., Dang-Vu, T., et al. (2005). Human cognition during REM sleep and the activity profile within frontal and parietal cortices: A reappraisal of functional neuroimaging data. Progress in Brain Research, 150, 219–227.
Marshall, L., Helgadottir, H., Molle, M., & Born, J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature, 444(7119), 610–613.
Massimini, M., Huber, R., Ferrarelli, F., Hill, S., & Tononi, G. (2004). The sleep slow oscillation as a traveling wave. Journal of Neuroscience, 24(31), 6862–6870.
Massimini, M., Rosanova, M., & Mariotti, M. (2003). EEG slow (approximately 1 Hz) waves are associated with nonstationarity of thalamo-cortical sensory processing in the sleeping human. Journal of Neurophysiology, 89(3), 1205–1213.
Mavanji, V., & Datta, S. (2003). Activation of the phasic pontine-wave generator enhances improvement of learning performance: A mechanism for sleep-dependent plasticity. European Journal of Neuroscience, 17(2), 359–370.
McCarley, R. W., Winkelman, J. W., & Duffy, F. H. (1983). Human cerebral potentials associated with REM sleep rapid eye movements: Links to PGO waves and waking potentials. Brain Research, 274(2), 359–364.
Mikiten, T. H., Niebyl, P. H., & Hendley, C. D. (1961). EEG desynchronization during behavioral sleep associated with spike discharges from the thalamus of the cat. Federation Proceedings, 20, 327.
Milner, C. E., Fogel, S. M., & Cote, K. A. (2006). Habitual napping moderates motor performance improvements following a short daytime nap. Biological Psychology, 73(2), 141–156.
Miyauchi, S., Misaki, M., Kan, S., Fukunaga, T., & Koike, T. (2009). Human brain activity time-locked to rapid eye movements during REM sleep. Experimental Brain Research, 192(4), 657–667.
Molle, M., Bergmann, T. O., Marshall, L., & Born, J. (2011). Fast and slow spindles during the sleep slow oscillation: Disparate coalescence and engagement in memory processing. Sleep, 34(10), 1411–1421.
Molle, M., Marshall, L., Gais, S., & Born, J. (2002). Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. Journal of Neuroscience, 22(24), 10941–10947.
Mouret, J., Jeannerod, M., & Jouvet, M. (1963). L’activite électrique du systeme visuel au cours de la phase paradoxale du sommeil chez le chat. J Physiol (Paris), 55, 305–306.
Murphy, M., Riedner, B. A., Huber, R., Massimini, M., Ferrarelli, F., & Tononi, G. (2009). Source modeling sleep slow waves. Proceedings of the National Academy of Sciences of the United States of America, 106(5), 1608–1613.
Nir, Y., Staba, R. J., Andrillon, T., Vyazovskiy, V. V., Cirelli, C., Fried, I., et al. (2011). Regional slow waves and spindles in human sleep. Neuron, 70(1), 153–169.
Nofzinger, E. A., Buysse, D. J., Miewald, J. M., Meltzer, C. C., Price, J. C., Sembrat, R. C., et al. (2002). Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. Brain, 125(Pt 5), 1105–1115.
Nofzinger, E. A., Mintun, M. A., Wiseman, M., Kupfer, D. J., & Moore, R. Y. (1997). Forebrain activation in REM sleep: An FDG PET study. Brain Research, 770(1–2), 192–201.
Pare, D., Steriade, M., Deschenes, M., & Oakson, G. (1987). Physiological characteristics of anterior thalamic nuclei, a group devoid of inputs from reticular thalamic nucleus. Journal of Neurophysiology, 57(6), 1669–1685.
Peigneux, P., Laureys, S., Fuchs, S., Delbeuck, X., Degueldre, C., Aerts, J., et al. (2001). Generation of rapid eye movements during paradoxical sleep in humans. NeuroImage, 14(3), 701–708.
Portas, C. M., Krakow, K., Allen, P., Josephs, O., Armony, J. L., & Frith, C. D. (2000). Auditory processing across the sleep-wake cycle: Simultaneous EEG and fMRI monitoring in humans. Neuron, 28(3), 991–999.
Salzarule, P., Liary, G. C., Bancaud, J., Munari, C., Barros-Ferreira, M. D., Chodkiewicz, J. P., et al. (1975). Direct depth recording of the striate cortex during REM sleep in man: Are there PGO potentials? Electroencephalography and Clinical Neurophysiology, 38(2), 199–202.
Schabus, M., Dang-Vu, T. T., Albouy, G., Balteau, E., Boly, M., Carrier, J., et al. (2007). Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proceedings of the National Academy of Sciences of the United States of America, 104(32), 13164–13169.
Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klosch, G., Anderer, P., et al. (2004). Sleep spindles and their significance for declarative memory consolidation. Sleep, 27(8), 1479–1485.
Shaffery, J. P., Roffwarg, H. P., Speciale, S. G., & Marks, G. A. (1999). Ponto-geniculo-occipital-wave suppression amplifies lateral geniculate nucleus cell-size changes in monocularly deprived kittens. Developmental Brain Research, 114(1), 109–119.
Spoormaker, V. I., Schroter, M. S., Gleiser, P. M., Andrade, K. C., Dresler, M., Wehrle, R., et al. (2010). Development of a large-scale functional brain network during human non-rapid eye movement sleep. Journal of Neuroscience, 30(34), 11379–11387.
Steriade, M. (2001). Impact of network activities on neuronal properties in corticothalamic systems. Journal of Neurophysiology, 86(1), 1–39.
Steriade, M., Contreras, D., Curro Dossi, R., & Nunez, A. (1993a). The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: Scenario of sleep rhythm generation in interacting thalamic and neocortical networks. Journal of Neuroscience, 13(8), 3284–3299.
Steriade, M., & Deschenes, M. (1984). The thalamus as a neuronal oscillator. Brain Research, 320(1), 1–63.
Steriade, M., Domich, L., Oakson, G., & Deschenes, M. (1987). The deafferented reticular thalamic nucleus generates spindle rhythmicity. Journal of Neurophysiology, 57(1), 260–273.
Steriade, M., & McCarley, R. W. (2005). Brain control of wakefulness and sleep. New York: Springer.
Steriade, M., Nunez, A., & Amzica, F. (1993b). Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. Journal of Neuroscience, 13(8), 3266–3283.
Steriade, M., Nunez, A., & Amzica, F. (1993c). A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components. Journal of Neuroscience, 13(8), 3252–3265.
Steriade, M., & Timofeev, I. (2003). Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron, 37(4), 563–576.
Tamaki, M., Matsuoka, T., Nittono, H., & Hori, T. (2008). Fast sleep spindle (13–15 hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep, 31(2), 204–211.
Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T. J., & Steriade, M. (2000). Origin of slow cortical oscillations in deafferented cortical slabs. Cerebral Cortex, 10(12), 1185–1199.
Timofeev, I., & Steriade, M. (1996). Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. Journal of Neurophysiology, 76(6), 4152–4168.
Wamsley, E. J., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S. K., Ely, A. V., et al. (2011). Reduced sleep spindles and spindle coherence in schizophrenia: Mechanisms of impaired memory consolidation? Biological Psychiatry, 71, 154–161.
Wehrle, R., Czisch, M., Kaufmann, C., Wetter, T. C., Holsboer, F., Auer, D. P., et al. (2005). Rapid eye movement-related brain activation in human sleep: A functional magnetic resonance imaging study. Neuroreport, 16(8), 853–857.
Wehrle, R., Kaufmann, C., Wetter, T. C., Holsboer, F., Auer, D. P., Pollmacher, T., et al. (2007). Functional microstates within human REM sleep: First evidence from fMRI of a thalamocortical network specific for phasic REM periods. European Journal of Neuroscience, 25(3), 863–871.
Zeitlhofer, J., Gruber, G., Anderer, P., Asenbaum, S., Schimicek, P., & Saletu, B. (1997). Topographic distribution of sleep spindles in young healthy subjects. Journal of Sleep Research, 6(3), 149–155.
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This research was supported by the Belgian Fonds National de la Recherche Scientifique (FNRS), Fondation Médicale Reine Elisabeth (FMRE), Research Fund of the University of Liège, the “Interuniversity Attraction Poles Programme—Belgian State—Belgian Science Policy”, the Fonds Léon Frédéricq and the Canadian Institutes of Health Research (CIHR).
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Dang-Vu, T.T. Neuronal Oscillations in Sleep: Insights from Functional Neuroimaging. Neuromol Med 14, 154–167 (2012). https://doi.org/10.1007/s12017-012-8166-1
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DOI: https://doi.org/10.1007/s12017-012-8166-1